The removal of level II, III, and IV metastases has gained importance in the treatment of squamous cell carcinomas (SCC) of the neck and larynx. This study assessed the possibility of removing level II and level III metastases only, given the low likelihood of occurrence of metastatic lymph nodes on level IV in SCCs of the larynx. Objective: This study aimed to analyze the prevalence rates of metastatic lymph nodes on level IV in laryngeal SCC patients. Methods: This prospective study enrolled consecutive patients with laryngeal SCC submitted to neck lymph node dissection. Neck levels were identified and marked for future histopathology testing. Results: Six percent (3/54) of the necks had level IV metastatic lymph nodes. All cN0 necks (42) were free from level IV metastasis. Histopathology testing done in the cN (+) necks (12) revealed that 25% of the level IV specimens were positive for SCC. The difference between cN0 and cN (+) necks was statistically significant (p = 0.009). Level IV metastases never occurred in isolation, and were always associated with level II or level III involvement (p = 0.002). Conclusion: The prevalence rate for lymph node metastasis in cN0 necks was 0%. Level IV metastatic lymph nodes were correlated to cN (+) necks. Level IV metastasis was associated with the presence of metastatic lymph nodes in levels II or III.785596

Altemani, A

Chone, CT

Crespo, AN

Kohler, HF

Magalhaes, R

Navarro, M

Brazilian Journal of Otorhinolaryngology

Repositorio da Producao Cientifica e Intelectual da Unicamp

59
Brazilian Journal of otorhinolaryngology 78 (5) SeptemBer/octoBer 2012
http://www.bjorl.org  /  e-mail: revista@aborlccf.org.br
Levels II and III neck dissection for larynx cancer with N0 neck
Carlos Takahiro Chone1, Hugo Fontana Kohler2, Rodrigo Magalhães2, Marcos Navarro2, Albina Altemani3, 
Agricio Nubiato Crespo4
1 MD, PhD (Professor, Department of Otolaryngology Head and Neck, University of Campinas).
2 MD (Department of Otolaryngology Head and Neck, University of Campinas).
3 MD, PhD (Professor, Department of Surgical Pathology, University of Campinas).
4 MD, PhD (Professor, Department of Otolaryngology Head and Neck, University of Campinas).
Department Otolaryngology Head and Neck, University of Campinas, Brazil.
Send correspondence to: Carlos Takahiro Chone. Av. Dr. Heitor Penteado, nº 1541, Taquaral. Campinas - SP. Brazil. CEP: 13087-000.
E-mail: carloschone@uol.com.br
Paper submitted to the BJORL-SGP (Publishing Management System - Brazilian Journal of Otorhinolaryngology) on January 18, 2009;
and accepted on July 7, 2012. cod. 9002.
ORIGINAL ARTICLE
Braz J Otorhinolaryngol.
2012;78(5):59-63. BJORL
Keywords:
laryngeal neoplasms,
lymph nodes, 
lymphatic metastasis,
neck dissection.
.org
Abstract
The removal of level II, III, and IV metastases has gained importance in the treatment of squamous 
cell carcinomas (SCC) of the neck and larynx. This study assessed the possibility of removing level 
II and level III metastases only, given the low likelihood of occurrence of metastatic lymph nodes 
on level IV in SCCs of the larynx.
Objective: This study aimed to analyze the prevalence rates of metastatic lymph nodes on level IV 
in laryngeal SCC patients.
Methods: This prospective study enrolled consecutive patients with laryngeal SCC submitted to neck 
lymph node dissection. Neck levels were identified and marked for future histopathology testing.
Results: Six percent (3/54) of the necks had level IV metastatic lymph nodes. All cN0 necks (42) 
were free from level IV metastasis. Histopathology testing done in the cN (+) necks (12) revealed 
that 25% of the level IV specimens were positive for SCC. The difference between cN0 and cN (+) 
necks was statistically significant (p = 0.009). Level IV metastases never occurred in isolation, and 
were always associated with level II or level III involvement (p = 0.002).
Conclusion: The prevalence rate for lymph node metastasis in cN0 necks was 0%. Level IV metastatic 
lymph nodes were correlated to cN (+) necks. Level IV metastasis was associated with the presence 
of metastatic lymph nodes in levels II or III.
78(5) - inglês.indb   59 17/10/2012   15:04:04
60
Brazilian Journal of otorhinolaryngology 78 (5) SeptemBer/octoBer 2012
http://www.bjorl.org  /  e-mail: revista@aborlccf.org.br
INTRODUCTION
The proposal of radical neck dissection for 
treatment of patients with head and neck squa-
mous cell carcinoma (HNSCC) began with Crile 
in 19061. Its routine use declined with time and 
modified procedures gained wider popularity. 
Based in the predictable pattern of neck metas-
tasis for HNSCC2,3, selective neck dissection was 
developed, with dissection of most affected levels 
of neck. If these nodes bear no metastatic disease, 
the incidence of metastases in other levels is low 
and its elective removal is of questionable value.
Regarding laryngeal cancer, a study of 262 
radical neck dissections2,3, observed that metastat-
ic disease occurred at levels II to IV, with sporadic 
metastasis to level I or V. Based on this findings, 
they proposed as elective treatment for these pa-
tients the dissection of levels II to IV. In a study 
of 384 neck dissections by serial sections4, the 
main sites of metastatic disease were levels II-IV. 
The occurrence of metastatic disease in levels I or 
V was associated usually with enlarged nodes at 
levels II to IV2,3. Furthermore, the Brazilian Head 
and Neck Cancer Study Group5 demonstrated no 
difference in outcome between patients submitted 
to a modified neck dissection or a lateral neck 
dissection in the elective treatment of patients 
with laryngeal cancer. Nowadays, dissection 
of levels II to IV is considered the treatment of 
choice for N0 laryngeal neoplasms6 because the 
low probability of metastases to level V ranging 
between 0% and 7% in glottic SCC and 5% to 9% 
for supraglottic SCC1-5,7-11.
The aim of this study was to determine the 
incidence of level IV metastasis in patients with 
laryngeal squamous cell carcinoma (SCC) correlat-
ing it to clinical nodal status of neck.
METHOD
Consecutive patients with laryngeal SCC 
were prospectively evaluated between 2007 and 
2011. For each patient, demographic, clinical 
and pathological data were recorded. Clinical 
and pathological staging was recorded according 
to 2006 AJCC staging system12. The local Institu-
tional Review Board approved the study protocol 
under code CAAE 0020.0.146.000-07. Informed 
consent was obtained from all patients submitted 
to this study. All patients had histopathological 
confirmation of SCC. All patients were staged at 
neck and primary site with computer tomography 
scan before treatment. Only patients submitted to 
surgical treatment with simultaneous neck dissec-
tion were included. Patients with cN0 necks with 
supraglottic cancer were submitted to bilateral 
neck dissection in stages T1 to T4, but in glottic 
cancer through T3, with dissection of levels II to 
IV, ipsilaterally. In cases with cN (+) necks it was 
performed modified or radical neck dissection 
through levels I to V and contralateral dissection 
of levels II, III and IV. Each level was removed in 
a separate fashion, respecting the surgical land-
marks intraoperatively, unless in cN2a disease, 
where some levels was put together as the mes-
tastasis was removed in block and detachment of 
levels means disruption of mass and in this case 
the levels was noted together.
The surgical specimen of neck levels was 
evaluated by conventional hystopathological 
analysis with hematoxilin and esosin (HE). It was 
obtained three slices from each lymph node for 
HE standard evaluation, one from the middle of 
lymph node and other from the center of each 
half of original lymph node.
Patients with previous treatment, pharyn-
geal extension of lesion or N3 necks or without 
inclusion criteria were excluded from the study.
Patients submitted to non-surgical treatment were 
also excluded from the study.
In presence of positive margins or extra-
capsular spread of lymphatic metastases, patient 
was submitted to adjuvant chemoradiotherapy 
with cisplatin at the dose of 100 mg per square 
meter of body surface on day 1, 22 and 43 in-
travenously with conventional fractionation of 2 
Gy per fraction per day to 66 Gy of treatment. 
Otherwise, patients without the features but with 
perineural invasion, angiolymphatic embolus, 
multiple metastases, stage III or IV disease were 
submitted to adjuvant radiation therapy of 60 Gy 
in 30 fractions. Patient not submitted to postopera-
78(5) - inglês.indb   60 17/10/2012   15:04:04
61
Brazilian Journal of otorhinolaryngology 78 (5) SeptemBer/octoBer 2012
http://www.bjorl.org  /  e-mail: revista@aborlccf.org.br
the compromise of level IV when levels II or III 
were also positive on pathological evaluation (p 
= 0.02). Five neck specimens (12%) that were 
clinically negative converted to pathologically 
positive, only at level II, without metastases to 
level IV. Of eleven clinically positive necks, all 
were pathologically positive on levels II or III.
DISCUSSION
The routine inclusion of level IV in elec-
tive neck dissection for laryngeal SCC has been 
questioned due to the low incidence of metastasis 
and the potential complications associated with 
this procedure, particularly on left side due to 
thoracic duct.
Tu13 studied 142 patients with supraglottic 
laryngeal SCC submitted to dissection of levels II 
and III with no pathologically neck metastases. 
The neck dissection specimens of 142 patients 
were negative for metastasis. Fifteen of the 142 
patients (10.6%) had neck recurrences during the 
follow-up of 5 years. The recurrence rate of this 
Table 1. Distribution of patients according to staging.
Clinical tumor staging
Glottic cancer
T1 T2 T3 T4
- 5 10 -
Total 15
Supraglottic câncer
T1 T2 T3 T4
- - 7 9
Total 16
Pathological tumor staging
T1 T2 T3 T4
0 3 7 21
Total 31
Clinical neck staging
cN0 cN1 cN2a cN3
20 6 5 -
Total 31
Pathological neck staging
pN0 pN1 pN2a pN3
15 11 5 -
Total 31
tive adjuvant treatment were excluded of study.
It was compared the rate of metastatic dis-
ease between cN (0) and cN (+) necks.
Statistical analysis was performed using the 
Fisher test with statistical significance at 0.05 level.
RESULTS
Thirty one patients met the inclusion and 
exclusion criteria. There were 26 males and five 
females, with a median age of 64 years at the 
time of diagnosis. Fifteen patients presented 
advanced glottic cancer and 16 supraglottic can-
cers. The distribution of theses tumors by clinical 
and pathological stage was shown in Table 1. 
Twenty-five were submitted to total laryngec-
tomy (all T3 and T4 lesions) and six to partial 
horizontal laryngectomy(T2 supraglottic cancer). 
Twenty-three patients were submitted to bilateral 
neck dissection and eight to unilateral neck dis-
section. Bilateral neck dissection was done in 16 
supraglottic ones, four of these with clinically 
and radiologically positive unilateral necks, and 
in seven glottic cases with positive necks. No bi-
lateral positive necks were observed on clinical 
and radiological evaluation.
Twenty patients were cN (0) and eleven had 
palpable lymph nodes only at the same side of 
the lesion cN (+). Patients were staged as cN0 in 
20 patients, cN1 in six patients(level II) and cN2a 
in five patients(levels II and III).
Fifty-four neck dissections were obtained. 
There were 43 cN0 neck dissections and eleven 
cN+ neck dissections. Of selective neck dissec-
tions, 34 to 47 lymph nodes were harvested from 
surgical specimen (mean = 39) and from radical or 
modified neck dissections 61 to 84 lymph nodes 
(mean = 67).
No patients staged as cN0 presented histo-
pathological metastasis at level IV. Among those 
patients with clinically positive neck nodes, the-
re was a 25% (3/11) incidence of metastasis to 
level IV at histopathological evaluation. There 
was a significant difference in rate of metastases 
at level IV among patients cN0 and cN+ (p = 
0.009). No patient presented isolated metastasis 
to level IV. There was a significant difference in 
78(5) - inglês.indb   61 17/10/2012   15:04:04
62
Brazilian Journal of otorhinolaryngology 78 (5) SeptemBer/octoBer 2012
http://www.bjorl.org  /  e-mail: revista@aborlccf.org.br
series with limited dissection on the neck was 
comparable with those reported in the literature 
after radical or modified neck dissection14. In a 
recent study, the rate of occult positive lymph 
node metastasis at level IV, with no evidence of 
disease at levels II and III was 1.4%, in patients 
with endolaryngeal SCC15.
Ambrosch et al.16 published a study with 
503 patients with HNSCC treated with elective 
dissection including only levels II and III and 
recurrences were not observed at level IV with 
a mean follow-up of 41 months. In this same 
study, level IV was dissected only in patients with 
suspicious or pathologically positive (by frozen 
section analysis) nodes at level II or III. The au-
thors conclude that elective dissection of level IV 
is not necessary in oropharyngeal, laryngeal and 
hypopharyngeal SCC.
León et al.8 in a study with similar design 
included 79 patients with endolaryngeal SCC. 
Neck dissection included only levels II and III 
with frozen section analysis of these levels and 
level IV and V were removed only when posi-
tive nodes at levels II or III were found. After a 
minimum follow-up of 24 months, there were no 
regional recurrences in this series without dissec-
tion of level IV. Khafif et al.11 studied 71 patients 
with larynx cancer submitted to elective neck 
dissection. The rate of metastases on level IV was 
2.6%, with no differences between transglottic 
and supraglottic carcinomas. Among the patients 
with clinically enlarged lymph nodes, the rate of 
level IV compromise was 32% in the ipsilateral 
neck and 0% at the contralateral side. Other study, 
collected the data of three prospective multi in-
stitutional trial. Pathologic and molecular studies 
of neck dissection specimens in 175 patients with 
larynx cancer with cN0 necks found only 3,4% of 
occult metastases in level IV17.
CONCLUSION
The results of these studies support that 
dissection of level IV is not mandatory in patients 
with cN0 laryngeal SCC.
The results of our study agree with those 
previously presented. The rate of metastasis to 
level IV was 0% in cN (0) necks despite 12% 
were histopathologically positive in level II , but 
without metastases at level IV and its dissection 
should not be considered in the cN0 neck.
REFERENCES
 1. Byers RM, Wolf PF, Ballantyne AJ. Rationale for elec-
tive modified neck dissection. Head Neck Surg. 
1988;10(3):160-7.
 2. Candela CC, Shah J, Jaques DP, Shah JP. Patterns of cervical 
node metastases from squamous carcinoma of the larynx. 
Arch Otolaryngol Head Neck Surg. 1990;116(4):432-5.
 3. Shah JP. Patterns of cervical lymph node metastasis from 
squamous carcinomas of the upper aerodigestive tract. 
Am J Surg. 1990;160(4):405-9.
 4. Lindberg R. Distribution of cervical lymph node metastases 
from squamous cell carcinoma of the upper respiratory 
and digestive tracts. Cancer. 1972;29(6):1446-9.
 5. End results of a prospective trial on elective lateral neck 
dissection vs type III modified radical neck dissection 
in the management of supraglottic and transglottic car-
cinomas. Brazilian Head and Neck Cancer Study Group. 
Head Neck. 1999;21(8):694-702.
 6. Ferlito A, Silver CE, Rinaldo A, Smith RV. Surgical treat-
ment of the neck in cancer of the larynx. ORL J Otorhi-
nolaryngol Relat Spec. 2000;62(4):217-25.
 7. Yang CY, Andersen PE, Everts EC, Cohen JI. Nodal disease 
in purely glottic carcinoma: is elective neck treatment 
worthwhile? Laryngoscope. 1998;108(7):1006-8.
 8. León X, Quer M, Orús C, Sancho FJ, Bagué S, Burgués J. 
Selective dissection of levels II-III with intraoperative con-
trol of the upper and middle jugular nodes: a therapeutic 
option for the N0 neck. Head Neck. 2001;23(6):441-6.
 9. Redaelli de Zinis LO, Nicolai P, Tomenzoli D, Ghizzardi D, 
Trimarchi M, Cappiello J, et al. The distribution of lymph 
node metastases in supraglottic squamous cell carcinoma: 
therapeutic implications. Head Neck. 2002;24(10):913-20.
10. Spriano G, Piantanida R, Pellini R, Muscatello L. Elective 
treatment of the neck in squamous cell carcinoma of the 
larynx: clinical experience. Head Neck. 2003;25(2):97-102.
11. Khafif A, Fliss DM, Gil Z, Medina JE. Routine inclusion of 
level IV in neck dissection for squamous cell carcinoma 
of the larynx: is it justified? Head Neck. 2004;26(4):309-12.
12. American Joint Committee on Cancer. In: Cancer staging 
Handbook from the AJCC Cancer Staging Manual, 6th ed. 
Philadelphia: Springer; 2006. p.27-98.
13. Tu GY. Upper neck (level II) dissection for N0 neck su-
praglottic carcinoma. Laryngoscope. 1999;109(3):467-70.
14. Strong EW. Preoperative radiation and radical neck dis-
section. Surg Clin North Am. 1969;49(2):271-6.
15. Lim YC, Choi EC, Lee JS, Koo BS, Song MH, Shin HA. 
Is dissection of level IV absolutely necessary in elective 
lateral neck dissection for clinically N0 laryngeal carci-
noma? Oral Oncol. 2006;42(1):102-7.
78(5) - inglês.indb   62 17/10/2012   15:04:04
63
Brazilian Journal of otorhinolaryngology 78 (5) SeptemBer/octoBer 2012
http://www.bjorl.org  /  e-mail: revista@aborlccf.org.br
16. Ambrosch P, Kron M, Pradier O, Steiner W. Efficacy of 
selective neck dissection: a review of 503 cases of elective 
and therapeutic treatment of the neck in squamous cell 
carcinoma of the upper aerodigestive tract. Otolaryngol 
Head Neck Surg. 2001;124(2):180-7.
17. Ferlito A, Silver CE, Rinaldo A. Selective neck dissection 
(IIA, III): a rational replacement for complete functional 
neck dissection in patients with N0 supraglottic and glottic 
squamous carcinoma. Laryngoscope. 2008;118(4):676-9.
78(5) - inglês.indb   63 17/10/2012   15:04:04


Levels II and III neck dissection for larynx cancer with N0 neck

http://repositorio.unicamp.br/jspui/bitstream/REPOSIP/80878/1/WOS000310714500009_I.pdf

Levels II and III neck dissection for larynx cancer with N0 neck

Abstract

Similar works

Full text

Available Versions

Repositorio da Producao Cientifica e Intelectual da Unicamp