Indian J Otolaryngol Head Neck Surg
https://doi.org/10.1007/s12070-021-02470-7
    ORIGINAL ARTICLE
Role of Neck Dissection in Organ-Preservation for Glottic
Squamous Cell Carcinoma
Kuauhyama Luna-Ortiz1,2 • Nancy Reynoso-Noverón3 • Luis C. Zacarı́as-Ramón1                   •
Zelik Luna-Peteuil4 • Dorian Y. Garcı́a-Ortega5
Received: 18 January 2021 / Accepted: 16 February 2021
Ó Association of Otolaryngologists of India 2021
Abstract The surgical approach to the neck in laryngeal             87.3%. The 60-month disease-specific survival was 97.1%.
cancer depends on the tumor site and stage. Clinical                Bilateral neck dissection and Delphian node dissection
practice guidelines recommend elective neck dissection              showed a low rate of metastasis (2.8%). Radical neck
in C T2 N0 and all supraglottic cancers; however, there is          dissection may thus represent overtreatment; however, this
no evidence supporting these recommendations. The                   surgical procedure could be justified to prevent regional
objective is to evaluate the results of bilateral elective neck     recurrences.
dissection in patients with glottic cancer who underwent
supracricoid partial laryngectomy (SCPL) with cricohyoi-            Keywords Glottis  Organ preservation  Neck dissection 
doepiglottopexy (CHEP). Thirty-five patients diagnosed              Supracricoid partial laryngectomy 
with C T2 N0 laryngeal squamous cell carcinoma (LSCC)               Cricohyoidoepiglottopexy  Cancer  Delphian lymph node
in a single-center retrospective study. Right-sided neck
dissections yielded 900 lymph nodes, none of which were
positive for metastatic disease. Left-sided neck dissections        Introduction
yielded 949 lymph nodes, one of which was positive for
malignancy. Prelaryngeal (Delphian) neck dissection was             The surgical approach to the neck in laryngeal cancer
performed in all patients. Out of 50 lymph nodes removed;           depends on the tumor site and stage. Accurate staging in
one was positive for malignancy. Median overall survival            cN0 patients leads to appropriate management of early
was 172 months, and the 60-month overall survival was               supraglottic cancer (which has a 30% chance of spreading
                                                                    to the lymph nodes) or advanced glottic cancer. For
                                                                    cN ? patients, neck management depends on the treatment
& Kuauhyama Luna-Ortiz
  kuauhyama@yahoo.com.mx
                                                                    used for the primary tumor, especially in larynx-preserva-
                                                                    tion strategies. Organ preservation treatment includes open
1
     Department of Head and Neck Surgery, Instituto Nacional de     or transoral laser microsurgery, radiotherapy, chemora-
     Cancerologia (Mexico), Av. San Fernando # 22, Col. Sección    diotherapy, or induction chemotherapy followed by surgi-
     XVI, 14080 Tlalpan Mexico CDMX, Mexico
                                                                    cal resection [1, 2]. Out of 500 patients with laryngeal
2
     Department of Surgery (Head and Neck Surgey), Hospital         cancer at different sites and stages that we identified in our
     General Manuel Gea Gonzalez (Mexico), Mexico City,
     Mexico
                                                                    cancer center, 66% were cN0 [3].
3
                                                                       Clinical practice guidelines recommend elective neck
     Basic and Clinical Research, Instituto Nacional de
     Cancerologı́a (Mexico), Av. San Fernando #22, Col. Sección
                                                                    dissection in C T2 cN0 cases and all supraglottic cancers.
     XVI, 14080 Tlalpan, Mexico City, Mexico                        However, these recommendations arise from studies
4                                                                   assessing total laryngectomy as the surgical procedure
     Universitatea de Medicinâ Si Farmacie Grigorie T. Popa IASI
     (visitor medical student), Mexico City, Mexico                 [1, 4–6]. The extent of neck dissection includes levels II–
5                                                                   VI; however, some authors have suggested a less extensive
     Surgical Oncology, Instituto Nacional de Cancerologı́a
     (Mexico), Av. San Fernando #22, Col. Sección XVI, 14080       surgery of just II–IV [7–10]. Even though bilateral or
     Tlalpan, Mexico City, Mexico                                   central neck dissection in patients with laryngeal cancer
                                                                                                                       123
                                                                                          Indian J Otolaryngol Head Neck Surg
has not been thoroughly studied, some guidelines recom-         Statistical Analysis
mend procedures that are yet to be fully supported by
evidence from clinical trials [11, 12]. We aimed to evaluate    We performed a descriptive analysis of demographic and
the results of elective neck dissection in glottic cancer       clinical characteristics. We used measures of central ten-
patients treated with larynx-preservation surgery, specifi-     dency and dispersion to perform an inferential analysis and
cally supracricoid partial laryngectomy (SCPL) with             determine the overall and disease-specific survival
cricohyoidoepiglottopexy (CHEP).                                according to the Kaplan–Meier estimator. We used STATA
                                                                v14.2 for statistical analysis.
Material and Methods
                                                                Results
A single-center, retrospective, cohort study was conducted
by identifying all consecutive patients treated with SCPL-      Cohort of Patients
CHEP during a 20-year period (January 2000–December
2019). This study was reviewed and approved by the              Demographic and clinicopathological data of all 35
Institutional Review Board and registered under the num-        patients are shown in Table 1.
ber IRB 2019/0116.
   A total of 85 patients were identified, and 35 were          Neck Dissection
included for final assessment. All patients included were
diagnosed with laryngeal squamous cell carcinoma                Right-sided dissection yielded 900 lymph nodes; none of
(LSCC). Staging was determined with physical examina-           which was positive for metastasis. Left-sided dissection
tion and nasolaryngoscopy before treatment. A computed          yielded 949 lymph nodes; one of them had metastasis (no
tomography scan was performed in most patients. Patients        extranodal extension was found). Fifty Delphian lymph
with C T2 and cN0 were included in the study. At the            nodes were dissected, and one of them had metastasis. Two
beginning of the period covered in the study, laser surgery     patients (5.7%) at high risk of recurrence (surgical margin
was not available at our cancer center, which is the current    close to malignancy and a sarcomatoid variant of SCC)
treatment of choice; therefore, some T2 patients were           received adjuvant treatment. No patient reported lymph
treated with SCPL-CHEP (our procedure of choice for T2          node recurrence during follow-up. Five patients (14.3%)
glottic cancer at the time). Another criterion for choosing     experienced local recurrence, three (8.6%) underwent total
this surgical procedure was poor visualization during direct    laryngectomy, and two received radiotherapy. Thirty-two
laryngoscopy. All 35 patients included were treated with        patients (91.4%) preserved their larynx throughout follow-
either SCPL-CHEP, bilateral, radical, or modified neck          up. Three deaths (8.6%) were attributable to laryngeal
dissection including levels II–V. Delphian lymph nodes          cancer. Median follow-up was 89.6 months (1.4 – 202).
were deliberately dissected in all patients because this is     Median overall survival was 172 months. The probability
the standard management of laryngeal cancer patients            of survival at 60, 120, and 180 months was, respectively,
treated with SCPL at our center. Head and neck cancer           87.3%, 72%, and, 40.6%. Additionally, the disease-specific
specialists evaluated the surgical specimens and defined        survival was 97.1% at 60 months and 83.7% at both 120
positive lymph nodes as those where neoplastic cells were       and 180 months. Overall and disease-specific survival are
found.                                                          shown (Kaplan–Meier plot) in Figs. 1 and 2.
   We excluded patients who had a histologic diagnosis
other than SCC in the final pathology report, supraglottic or
subglottic epicenters, T1 tumors, or who had previously         Discussion
received other treatment (e.g., radiotherapy, chemoradio-
therapy, neoadjuvant/induction chemotherapy). Patients          SCPL-CHEP is an open larynx-preserving surgery recom-
who had undergone radiotherapy limited to the larynx were       mended by several clinical practice guidelines as the pre-
not excluded. The results of bilateral neck dissection and      ferred organ-preserving surgery for some T3 tumors [1, 13]
Delphian lymph node dissection were analyzed. Dissected         and T2 laryngeal tumors unsuitable for laser resection. Our
lymph nodes and positive lymph nodes were reported.             study only included C T2 glottic tumors; therefore, it can
                                                                be assumed that surgery was appropriate and adhered to
                                                                international guidelines. Most patients with T1–T2 laryn-
                                                                geal cancer are currently treated with laser transoral sur-
                                                                gery at our center. Patients deemed unsuitable for laser
123
Indian J Otolaryngol Head Neck Surg
Table 1 Clinical and follow-up data                   Table 1 continued
n = 35                                   N (%)        n = 35                                            N (%)
Age (mean)                               56 (50–65)   Total lymph nodes dissected                       900
Sex                                                   Mean lymph nodes dissected                        25.7
Male                                     33 (94.3)    Range                                             12–57
Female                                   2 (5.7)      Positive lymph nodes                              0
Comorbidities                                         Left neck dissection
None                                     34 (97.14)   Neck dissections                                  35 (100)
Diabetes mellitus                        0 (0)        Total lymph nodes dissected                       949
Thyroid cancer                           1 (2.86)     Mean lymph nodes dissected                        27.1
Previous treatment                                    Range                                             9–61
Induction chemotherapy                   0 (0)        Positive lymph nodes                              1 (2.8%)
None                                     32 (92.8)    Delphian node dissection
Radiotherapy                             1 (2.86)     Delphian node dissections                         35 (100)
Transoral laser surgery                  2 (5.7)      Patients with identifiable Delphian lymph nodes   30 (85.7)
Site                                                  Number of patients according to                   22 (62.9)
Glottis                                  31 (88.6)    Delphian nodes resected
Glottis ? supraglottis                   1 (2. 9)     1 LN                                              3 (8.6)
Glottis ? subglottis                     3 (8.6)      2 LN                                              1 (2.9)
Histology                                             3 LN                                              2 (5.7)
Conventional squamous cell carcinoma     33 (94.29)   4 LN                                              1 (2.9)
Sarcomatoid carcinoma                    2 (5.71)     5 LN                                              1 (2.9)
(spindle cell squamous cell carcinoma)                Total Delphian nodes dissected                    50
Histologic grade                                      Mean Delphian nodes dissected                     1.4
GX                                       0 (0)        Range                                             0–6
G1                                       19 (54.3)    Positive Delphian nodes                           1 (2.9)
G2                                       13 (37.1)    Tracheostomy (days)                               8.8 (6–8)
G3                                       3 (8.6)      NGT (days)                                        18.2 (13–19)
cT                                                    Hospital stay (days)                              10.1 (3–45)
T2                                       14 (40)      Adjuvant treatment
T3                                       17 (48.6)    None                                              31 (88.5)
T4                                       4 (11.4)     Radiotherapy                                      4 (11.4)
cN                                                    Follow-up
N0                                       35 (100)     Alive and recurrence-free                         11 (31.43)
cM                                                    Lost and recurrence-free                          12 (34.29)
M0                                       35 (100)     Lost with recurrence                              0 (0)
Clinical stage                                        Deceased and recurrence-free                      9 (25. 7)
I                                        0(0)         Deceased with recurrence                          3 (8.6)
II                                       13 (37.1)    Recurrence
III                                      19 (54.3)    No                                                30 (85.71)
IV                                       3 (8.6)      Local recurrence                                  5 (14.29)
pN                                                    Survival
N0                                       33 (94.3)    Yes                                               23 (65.71)
N1                                       1 (2.86)     No                                                12 (34.29)
N2                                       1 (2.86)
Preserved arytenoids
1                                        9 (25.7)     resection, often due to inadequate exposure, are advised to
2                                        26 (74.3)    undergo cordectomy through laryngofissure or SCPL-
Right neck dissection                                 CHEP.
Neck dissections                         35 (100)        International guidelines have yet to standardize elective
                                                      neck dissection for laryngeal cancer. Our case series of 500
                                                                                                            123
                                                                                          Indian J Otolaryngol Head Neck Surg
                                                               fully agree given that in our study only 3.4% of early
                                                               glottic tumors (T1–T2) had lymph node metastasis [3].
                                                               Based on the Brazilian Head and Neck Cancer Study
                                                               Group (BHNCSG), neck dissection is recommended in [
                                                               T2 glottic cancer and all tumors with supraglottic exten-
                                                               sion, even without clinical lymph node disease. In 1999,
                                                               the BHNCSG described 26% of occult lymph node disease
                                                               in supraglottic and transglottic cancers [8]. In our study,
                                                               only three cases out of 35 showed invasion of other
                                                               laryngeal sites. UK guidelines [5] suggest elective neck
                                                               dissection in C T2b tumors but with no supporting clinical
                                                               data. In our study, no T2 patients showed metastatic lymph
                                                               nodes. Shi et al. [15] reported occult lymph node disease in
                                                               15% of glottic cancer patients, while Riviere et al. [16]
Fig. 1 Overall survival according to Kaplan–Meier              found occult lymph node disease in 14% of patients with
                                                               T3 laryngeal cancer who underwent total laryngectomy and
                                                               in 70% of T4 patients; however, they included patients
                                                               with supraglottic tumors. Our cancer center previously
                                                               reported 75% and 50% of pN0 after neck dissection in T3
                                                               and T4 glottic cancer patients, respectively [3]. The present
                                                               study shows an incidence of nodal metastatic disease of
                                                               only 2.8% for T2–T4 tumors.
                                                                  Neck dissection should be ipsilateral for primary glottic
                                                               tumors, limiting a bilateral approach to larger glottic
                                                               tumors. The management of supraglottic tumors has
                                                               apparently been established. Weber et al. [17] suggested
                                                               bilateral neck dissection in patients with supraglottic can-
                                                               cer, based on their results of decreasing lymph node
                                                               recurrence by 11% when compared with unilateral neck
                                                               dissection. Since the introduction of SCPL-CHEP, bilateral
Fig. 2 Disease-specific survival according to Kaplan–Meier
                                                               neck dissection has been the standard procedure at our
                                                               center. We follow Prof. Laccourreye’s instructions, who
laryngeal cancer patients included 308 glottic tumors, of
                                                               promotes this procedure to avoid technical difficulties in
which 242 (78.5%) were classified as cN0. The proportion
                                                               case of recurrence. Furthermore, high-volume centers
of cN0 cases to their respective T status was: 51/55 (92%)
                                                               agree that neck dissection has become a relatively safe
for T2, 91/132 (75%) for T3, and 29/58 (50%) for T4.
                                                               procedure with low morbidity. [18] Contralateral elective
Some studies clearly indicate neck dissection in T3 and T4
                                                               neck dissection is less frequently justified in patients with
patients [3]; however, they are retrospective studies.
                                                               glottic cancer, and its performance depends on the degree
Moreover, not all patients underwent imaging studies (ul-
                                                               of local extension and Delphian node status [19]. Our
trasound, CT scan, MRI), which could have led to over-
                                                               findings could result in two distinct clinical approaches: a
staging. Myers et al. [13] stated that even with these
                                                               conservative ‘‘watch and wait’’ approach restraining from
imaging studies added to the work-up, the size threshold
                                                               performing contralateral neck dissection while considering
for considering a lymph node as suspicious for malignancy
                                                               that neck recurrence will significantly affect prognosis;
is 10 mm. Gallo et al. [14] reported that despite using fine
                                                               conversely, bilateral neck dissection could be justified
needle aspiration cytology, 7–10% of cases may have
                                                               based on the absence of recurrence during follow-up and
occult lymph node metastasis. The National Comprehen-
                                                               that only 2.8% of patients were pN ? (one T4 patient who
sive Cancer Network (NCCN) guidelines [4] suggest
                                                               did not meet the criteria for postsurgical radiotherapy). All
against neck dissection in T1 glottic cancer, but they state
                                                               recurrences were local. The five-year overall survival was
that neck dissection in glottic cancer should be done at the
                                                               100% and the larynx-preservation rate was 91%. The latter
surgeon’s discretion; and if performed, neck dissection
                                                               approach including bilateral neck dissection would be more
should include level VI when appropriate. The American
                                                               appropriate for the population at our center due to their
Society of Clinical Oncology (ASCO) [1] advice against
                                                               demographic and cultural characteristics.
elective neck dissection in T1–T2 tumors, with which we
123
Indian J Otolaryngol Head Neck Surg
   US guidelines [1] recommend level VI neck dissection                References
[13]. However, this recommendation is not widely reported
in the literature. According to Som et al. [20] level VI                1. Forastiere AA, Ismaila N, Lewin JS et al (2018) Use of larynx-
                                                                           preservation strategies in the treatment of laryngeal cancer:
dissection is indicated on glottic carcinoma are C T3
                                                                           american society of clinical oncology clinical practice guideline
tumors and either subglottic or if there is extension to the               update. J ClinOncol 10(36):1143–1169
anterior commissure. Full level VI dissection is not com-               2. Luna-Ortiz K, Villavicencio-Valencia V, Rodrı́guez-Falconi A
monly performed in our center; Delphian node dissection is                 et al (2016) Induction chemotherapy followed by supracricoid
                                                                           partial laryngectomy (SCPL) with cricohyoidoepiglottopexy
performed instead [19]. In the present study, only one
                                                                           (CHEP) in T3NO arytenoid fixation-related glottic cancer.
patient (2.8%) had a metastatic Delphian lymph node, and                   B-ENT 12:271–277
no recurrence was observed during follow-up. Our surgical               3. Herrera-Gómez A, Villavicencio-Valencia V, Rascón-Ortiz M,
approach is based on the risk of hypoparathyroidism [21],                  Luna-Ortiz K (2009) Demographic data of laryngeal cancer at the
                                                                           InstitutoNacional de Cancerologı́a in Mexico City. Cir Cir
whose rates are reported in the literature between 12 and
                                                                           77:353–357
33%, [22] and on the risk of recurrent laryngeal nerve                  4. National Comprehensive Cancer Network. Head and Neck Can-
injury, which is essential for recovery after SCPL. The                    cers (Version 3.2019). Accessed April 1st, 2020.
main limitation of our study is its retrospective nature.               5. Jones TM, De M, Foran B, Harrington K, Mortimore S (2016)
                                                                           Laryngeal cancer: United Kingdom national multidisciplinary
Even though our results seem encouraging, it is clear that
                                                                           guidelines. J LaryngolOtol 130:S75–S82
the clinical advantages offered by this approach need to be             6. Ahn SH, Hong HJ et al (2017) Guidelines for the Surgical
reproduced in different groups of patients before it                       Management of Laryngeal Cancer: Korean Society of Thyroid-
becomes a standard recommendation.                                         Head and Neck Surgery. ClinExpOtorhinolaryngol 10:1–43
                                                                        7. Cayonu M, Tuna EU, Acar A et al (2019) Lymph node yield and
                                                                           lymph node density for elective level II-IV neck dissections in
                                                                           laryngeal squamous cell carcinoma patients. Eur Arch Otorhi-
Conclusion                                                                 nolaryngol 276:2923–2927
                                                                        8. Brazilian Head and Neck Cancer Study Group (1999) End results
                                                                           of a prospective trial on elective lateral neck dissection vs type III
Only 2.8% of cN0 patients with locally advanced glottic
                                                                           modified radical neck dissection in the management of supra-
cancer (T2–T4) treated with SCPL-CHEP had occult                           glottic and transglottic carcinomas. Head Neck 21:694–702
lymph node metastasis. Likewise, 2.8% of Delphian nodes                 9. Chone CT, Kohler HF, Magalhães R, Navarro M, Altemani A,
were positive for SCC metastasis. Bilateral neck dissection                Crespo AN (2012) Levels II and III neck dissection for larynx
                                                                           cancer with N0 neck. Braz J Otorhinolaryngol 78:59–63
and Delphian node dissection demonstrated that metastasis
                                                                       10. Diaz FL, Lima RA, Manfro G et al (2009) Management of the N0
is low in this clinical scenario, and radical bilateral neck               neck in moderately advance squamous carcinoma of the larynx.
dissection could thus be considered as overtreatment.                      Otolaryngol Head Neck Surg 141:59–65
Postoperative radiotherapy will only be justified in                   11. Amar A, Chedid HM, Franzi SA, Rapoport A (2012) Neck dis-
                                                                           section in squamous cell carcinoma of the larynx: indication of
N ? patients with capsule rupture or more than three
                                                                           elective contralateral neck dissection. Braz J Otorhinolaryngol
positive nodes.                                                            78:7–10
                                                                       12. Laccourreye H, Ménard M, Fabre A, Brasnu D, Janot F (1987)
                                                                           Partial supracricoidlaryngectomy. Technics indications and
Data Availability Yes.                                                     results. Ann OtolaryngolChirCervicofac. 104:163–173
                                                                       13. Myers EN, Fagan JF (1999) Management of the neck in cancer of
Declarations                                                               the larynx. Ann Otol Rhinol Laryngol 108:828–832
                                                                       14. Gallo O, Boddi V, Bottai GV, Parrella F, Storchi OF (1996)
Conflict of interest The authors declare that they have no competing       Treatment of the clinically negative neck in laryngeal cancer
interests.                                                                 patients. Head Neck 18:566–572
                                                                       15. Shi Y, Zhou L, Tao L et al (2019) Management of the N0 neck in
Ethical Approval This study was reviewed and approved by the               patients with laryngeal squamous cell carcinoma. Acta Oto-
Institutional Review Board and registered under the number IRB             laryngol 139:908–912
2019/0116.                                                             16. Riviere D, Mancini J, Santini L et al (2019) Nodal metastases
                                                                           distribution in laryngeal cancer requiring total laryngectomy:
Consent for Publication All authors consent for publication.               therapeutic implications for the N0 Neck. Eur Ann Otorhino-
                                                                           laryngol Head Neck Dis 136:S35–S38
Informed Consent Informed consent was done for treatment               17. Weber PC, Johnson JT, Myers EN (1993) Impact of bilateral neck
according to the Mexican law.                                              dissection on recovery following supraglottic laryngectomy. Arch
                                                                           Otolaryngol Head Neck Surg 119:61–64
Employement Any organization gain or lose financially trough           18. Xiao CC, Imam SA, Nguyen SA et al (2019) Neck dissection
publication of this manuscript.                                            does not add to morbidity or mortality of laryngectomy. World J
                                                                           Otorhinolaryngol Head Neck Surg 5:215–221
                                                                       19. Luna-Ortiz K, Mosqueda-Taylor A (2005) Delphian lymph node
                                                                           in glottic carcinoma subjected to supracricoid partial laryngec-
                                                                           tomy with cricohyoidoepiglottopexy. Cir Cir 73:7–10
                                                                                                                                    123
                                                                                                        Indian J Otolaryngol Head Neck Surg
20. Som PM, Curtin HD, Mancuso AA (2000) Imaging-based nodal                 thyroid dysfunction in patients undergoing laryngectomy. Eur
    classification for evaluation of neck metastatic adenopathy. AJR         Arch Otorhinolaryngol 267:807–810
    Am J Roentgenol 174:837–844
21. Geminiani M, Aimoni C, Scanelli G, Pastore A (2007) Parathy-
                                                                         Publisher’s Note Springer Nature remains neutral with regard to
    roid function study in patients submitted to laryngeal surgery for
                                                                         jurisdictional claims in published maps and institutional affiliations.
    squamous cell carcinoma. Acta Otorhinolaryngol Ital 27:123–125
22. Lo Galbo AM, de Bree R, Kuik DJ, Lips P, Leemans CR (2010)
    Paratracheal lymph node dissection does not negatively affect
123