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Results of Selective Neck Dissection in Management of the Node-Positive Neck
Peter E. Andersen, MD;
Frank Warren, MD;
Jeffrey Spiro, MD;
Alan Burningham, MD;
Richard Wong, MD;
Mark K. Wax, MD;
Jatin P. Shah, MD;
James I. Cohen, MD, PhD
Arch Otolaryngol Head Neck Surg. 2002;128:1180-1184.
ABSTRACT
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Background Although increasingly accepted in treatment of the N0 neck, use of selective
neck dissection in patients with node-positive squamous cell carcinoma of
the head and neck remains controversial.
Objective To determine the oncologic efficacy of selective node dissection in
patients with node-positive squamous carcinoma of the head and neck.
Setting Three tertiary care academic/Veterans Affairs medical centers.
Methods Ten-year retrospective medical chart review of 106 previously untreated
clinically and pathologically node-positive patients undergoing 129 selective
neck dissections and followed for a minimum of 2 years or until patient death.
Results Regional metastasis was clinically staged as N1 in 58 patients (54.7%),
N2a in 5 (4.7%), N2b in 28 (26.4%), N2c in 14 (13.2%), and N3 in 1 (0.9%).
Extracapsular extension of tumor was present in 36 patients (34.0%), and postoperative
radiation therapy was administered to 76 patients (71.7%). Overall, 9 patients
experienced disease recurrence in the neck. Six of these recurrences were
in the side of the neck that had undergone selective neck dissection, for
a regional control rate of 94.3%.
Conclusions These results support the use of selective neck dissection in carefully
selected patients with clinically node-positive squamous cell carcinoma of
the head and neck region. Regional control rates comparable to those achieved
with comprehensive operations can be achieved in appropriately selected patients.
INTRODUCTION
THE PRIMARY goal in the treatment of patients with head and neck cancer
is control of the disease. However, with increasing recognition of the substantial
morbidity of radical surgical treatment, more emphasis is being placed on
surgical conservatism if it does not negatively impact disease control and
if it offers improved posttreatment function and cosmesis. The evolution of
neck dissection is representative of this trend. Radical neck dissection,
first described by Crile1 in 1906, has served
as the standard method of managing cervical metastases in patients with head
and neck cancer for most of the century. Radical neck dissection accomplishes
en bloc removal of all cervical lymphatic contents believed to be involved
with or at risk for metastatic disease from head and neck malignancy and includes
removal of the sternocleidomastoid muscle, internal jugular vein, submandibular
gland, and spinal accessory nerve. This operation produces substantial postoperative
morbidity from cosmetic and functional standpoints, with typical shoulder
dysfunction seen after this surgery.2 With
time, surgeons have challenged the necessity of such radical neck surgery
and have explored the feasibility of modifications to it.
The rationale for such modifications is based on the finding that modified
radical neck dissection (especially modifications that preserve the spinal
accessory nerve) results in improved postoperative shoulder function3 and on the realization that neck recurrence is still
a significant problem despite the extensiveness of radical neck dissection.
Improved understanding of lymph node drainage patterns4-5 and
fascial compartments of the neck6 and better
understanding of the indications for adjuvant postoperative radiation therapy7-8 have given further impetus to the trend
away from the routine use of radical neck dissection in all patients.
Selective neck dissection (SND), which involves selective removal of
nodal groups most at risk for metastasis with preservation of all nonlymphatic
structures, has gradually gained acceptance in the clinically N0 neck and
has demonstrated regional control and survival rates similar to those of more
extensive neck dissections.8-11
Although SND has been accepted by many as appropriate for use in the
clinically node-negative neck, its use in patients with clinically obvious
(palpable) metastatic disease remains extremely controversial; however, extension
of the indications for its use in this setting seems logical. In the absence
of factors that would alter normal lymphatic flow in the neck, such as previous
neck surgery, radiotherapy, or the presence of massive obstructive adenopathy,
the rationale behind the operation, which like its more radical counterpart
seeks to remove the lymph nodes involved by or at risk for involvement by
head and neck cancer, remains valid. The finding of equivalent disease control
rates in clinically N0 but pathologically node-positive patients undergoing
surgery helped encourage this approach.12
Traynor et al13 previously published
a smaller study describing the use of SND in patients with known cervical
metastases, which showed that in selected patients with N1 or N2 neck staging,
SND gave results comparable to those of more extensive neck dissections. The
present study is an extension of that previous experience involving increased
numbers of patients, increased follow-up time, and involvement of other institutions.
MATERIALS AND METHODS
The medical records of all patients who underwent neck dissection at
Oregon Health Sciences University and the University of Connecticut Health
Center between January 1989 and December 1998 and at Memorial Sloan-Kettering
Cancer Center between January 1995 and December 1998 were reviewed. Patients
undergoing SND who had clinically obvious metastatic disease and pathologically
proven regional metastases were included in the analyzed sample. Patients
with nonsquamous head and neck cancers; a history of head and neck malignancy;
previous treatment with chemotherapy, radiation, or surgery; or less than
2 years of follow-up were excluded. American Joint Committee on Cancer staging
criteria were used.14
The extent of SND performed was at the discretion of the surgeon; in
general, for primary sites involving the oral cavity and oropharynx, a supraomohyoid
neck dissection removing nodal levels I through III was performed. For primary
tumors of the larynx and hypopharynx, a lateral neck dissection involving
removal of levels II through IV was performed.
Patients were considered for SND only in the setting of no previous
treatment to the head and neck for this malignancy. Only patients with freely
mobile metastatic disease in the neck were eligible. These criteria generally
restricted the use of SND to patients with nodal disease less than N3 in stage.
Patients whose operations were extended owing to intraoperative findings to
include resection of nonlymphatic structures usually preserved during SND
(ie, the spinal accessory nerve, internal jugular vein, or sternocleidomastoid
muscle) were not included in this study.
All neck dissection specimens were reviewed by a staff pathologist.
Patients in whom evidence of extracapsular spread (ECS) or multiple levels
of nodal involvement were identified received postoperative radiotherapy on
this basis. In addition, other patients received postoperative radiotherapy
for indications outside of the neck dissection, such as extensive primary
disease or positive margins at the primary resection site. Actuarial disease-specific
survival rates and rates of local regional and distant recurrence were determined
using the Kaplan-Meier method.
RESULTS
Using the patient selection criteria outlined previously, 106 patients
were identified who had undergone SND in a clinically and pathologically node-positive
neck.
Thirty patients (28.3%) were women and 76 (71.7%) were men; mean ±
SD age at the time of treatment was 61.0 ± 11.1 years (range, 35-92
years), and mean ± SD follow-up was 3.4 ± 2.6 years (range,
0.2-10.4 years). Primary site and regional metastatic characteristics are
given in Table 1. Most patients
had advanced disease at the primary site staged T3 or greater. The regional
staging of patients is given in Table 2. Patients were relatively equally divided between N1 and N2 staging,
with most N2-staged patients being so classified because of multiple nodal
metastases either in the ipsilateral (28 patients) or in the bilateral or
contralateral (14 patients) sides of the neck. All of these patients' nodal
metastases were located in levels I through IV of the neck. No patient had
clinical evidence of nodal disease at level V.
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Table 1. Primary Site Location and Stage of Squamous Cell Carcinoma
in 106 Patients Who Underwent Selective Neck Dissection
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Table 2. Nodal Stage Characteristics of 106 Patients Who Underwent
Selective Neck Dissection
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One hundred twenty-nine neck dissections were performed in 106 patients;
31 patients (29.2%) underwent bilateral neck dissection and 75 (70.8%) underwent
unilateral dissection. The types of neck dissection performed are given in Table 3. Extracapsular spread of disease
was noted in 36 patients (34.0%). Postoperative radiation therapy to the neck
was administered to 76 patients (71.7%); the mean dose administered was 6729
rad (6729 cGy).
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Table 3. Types of Neck Dissection Performed in 106 Patients Who Underwent
Selective Neck Dissection (SND)*
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Actuarial disease-specific survival at 5 years was 68.8%. Disease-specific
survival correlated with nodal status. Five-year actuarial disease-specific
survival was 88.1% in N1 patients, 40.0% in N2a patients, 50.1% in N2b patients,
and 30.0% in N2c patients (Figure 1).
Six patients experienced disease recurrence in the surgical neck (5.7%). Five-year
actuarial disease control in the surgical neck was 92.2%. Recurrence in the
surgical neck correlated with nodal stage at presentation early in follow-up;
however, by 5 years, the recurrence rate was similar for patients staged N1,
N2b, and N2c. Five-year actuarial failure rates in the neck were 6.7% in N1
patients, 22.0% in N2a patients, 6.7% in N2b patients, and 7.7% in N2c patients
(Figure 2). Extracapsular spread
of disease correlated with recurrence in the neck. Patients without ECS of
disease had a 5-year actuarial failure rate in the neck of 2.4%, whereas those
with ECS of disease had a 21.9% failure rate (P =
.05) (Figure 3). Patients with and
without ECS of disease had disease-specific survival at 4 years of 55.8% and
75.3%, respectively (P = .02) (Figure 4). Of patients with recurrence in the surgical neck, all
6 had recurrence in the field of the previous neck dissection. Four patients
had recurrence at level I, 2 at level II, 1 at level III, and 1 at levels
I, II, and III (some patients had recurrence at multiple sites in the surgical
neck). In no patient was neck recurrence noted outside of the expected area
of lymphatic drainage based on its primary site, and no patient had recurrence
in the posterior triangle.
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Figure 1. Disease-specific survival by clinical
node staging in 106 patients who underwent selective neck dissection.
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Figure 2. Neck recurrence by clinical node
staging in 106 patients who underwent selective neck dissection.
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Figure 3. Neck failure by extracapsular
spread of disease status in 106 patients who underwent selective neck dissection; P = .05.
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Figure 4. Disease-specific survival by extracapsular
spread of disease status in 106 patients who underwent selective neck dissection; P = .02.
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In contrast to the low regional recurrence rate (4.3%) reported in this
patient group, at 5 years' follow-up, 12.3% of patients had experienced local
recurrence, and 28.9% had developed distant metastasis.
COMMENT
Traditionally, the treatment of patients with clinically palpable metastatic
disease in the neck has been radical neck dissection.1 Modifications
of the radical neck dissection over time have been made in a logical manner
based on firm anatomic and oncologic principles. Radical neck dissection,
which was first conceived of as an en bloc resection of the lymphatic structures
of the neck, is, in fact, not a complete en bloc resection; other structures
in the "bloc," such as the hypoglossal and vagus nerves and the carotid artery,
have never been routinely removed with this operation. Furthermore, results
of anatomic studies6 confirm that the lymphatic
structures of the neck lie within a system of aponeurotic compartments that
envelop the muscles and vessels of the neck but, aside from close anatomic
proximity, have no relationship to the lymphatic structures of the neck. It
therefore seemed logical that preservation of other structures usually removed
during radical neck dissection, and, in fact, enveloped by these same fascial
planes enveloping structures usually preserved during radical neck dissections,
would be equally feasible. Recognition of the significant morbidity of accessory
nerve sacrifice lead early investigators15 to
turn their initial attention to modification of the radical neck dissection
with preservation of this nerve alone. Such modifications, even in selected
patients with node-positive disease, have been shown to be as effective as
radical neck dissection.16 Bocca et al15 also described a "functional" neck dissection in
which all 5 nodal groups of the neck are removed and all nonlymphatic structures
are preserved. In the series by Bocca et al,15 regional
recurrence rates in patients with N0 necks were 2.4%, and recurrence rates
of 30% were noted for N1 and N2 necks. These rates compared favorably with
those in similar patients who had undergone radical neck dissection by the
same surgeon.15
Several studies4-5,17 have
demonstrated that lymphatic flow in the neck occurs in a predictable pattern.
Flow to the nodes of the posterior cervical triangle does not occur from nodes
in the jugular chain. The lack of drainage to the posterior cervical triangle
has been postulated to be due to the presence of lymphatic valves in the cervical
lymphatics. Further evidence of the lack of flow to the posterior cervical
triangle is demonstrated in a study by Davidson et al18 of
more than 1000 comprehensive neck dissections in patients with squamous cancer
of the head and neck that identified metastases to the posterior triangle
in only 3% of patients. There was a slight increase of metastases to level
V when clinically positive nodes were evident in other levels (5%). These
results have been confirmed by other investigators.19
Other studies have demonstrated that metastases to the neck from cancers
of the upper aerodigestive tract occur in a predictable pattern. Studies by
Shah5 show a predominance of metastases to
certain regions based on the primary site. Most oral cavity cancers metastasize
to the lymph nodes at levels I through III. Oropharyngeal, hypopharyngeal,
and laryngeal lesions demonstrated a predilection for metastatic disease to
levels II through IV. Metastatic nodal disease outside of the predominant
regions of spread has been shown in this study to be unusual in the absence
of involvement of the expected regions.
The evidence of compartmentalization of the cervical lymphatics and
the findings of predictable lymphatic flow in the neck do not support the
routine removal of all cervical lymph node groups or the routine sacrifice
of nonlymphatic structures such as the sternocleidomastoid muscle, internal
jugular vein, or spinal accessory nerve in neck dissection. This type of neck
dissection (SND) represents the next logical step in the modification of radical
neck dissection. Selective neck dissection has been extensively used in patients
with a clinically node-negative neck, and treatment results have been shown
to be comparable to those of more extensive lymphadenectomies in a similar
setting. Selective neck dissection, as a result, has become accepted as a
treatment modality for patients without clinical evidence of cervical nodal
metastasis.9-11
Use of SND in the clinically positive neck has been controversial. Our
unusual selection criteria for patients analyzed in this study, that is, those
with clinically and pathologically node-positive neck dissection, was intended
to emphasize that these operations were purposefully performed on patients
with known cervical metastases, not those who were clinically node-negative
at presentation and were later found to have pathologic evidence of nodal
metastases. The inclusion of only patients who were clinically and pathologically
node-positive in the neck was also done to exclude the small, but definite,
incidence of patients who have clinically palpable adenopathy that turns out
to be pathologically node negative on postoperative examination. Other researchers
have reported series of patients undergoing SND in the clinically node-positive
setting. Medina and Byers11 reported a series
that included 114 patients who were clinically node positive, with most being
staged N1. Of these patients, 91 (79.8%) had pathologic evidence of metastasis
to the cervical lymphatics. When only surgical therapy was performed, regional
recurrence of 10% for pathologic N1 disease without ECS and 24% when multiple
nodes or ECS was present were described. Postoperative radiotherapy decreased
recurrence to 15% in patients with multiple positive nodes or ECS. Byers12 reported similar recurrence rates in patients undergoing
planned therapeutic supraomohyoid neck dissection with and without postoperative
radiotherapy. Seventy percent of these patients had either ECS of disease
or multiple levels of involvement. Based on these results, Byers12 suggested
that SND has a role in selected patients with early-stage metastatic disease
in the neck and that the addition of postoperative adjuvant radiotherapy can
improve the disease control rates when ECS, multiple levels of disease, or
both are identified. The results reported herein are consistent with those
of these other researchers and are comparable to the results reported for
more comprehensive operations.16
Based on the aforementioned anatomic and clinical data, it is reasonable
to extend the indications for SND to patients with a higher stage of disease,
that is, N2, but with smaller, nonfixed nodes. The results of our study support
this contention. However, important caveats deserve emphasis. We do not advocate
the use of SND in all patients with clinically positive adenopathy. Specifically,
SND, we believe, should be applied only in patients without massive adenopathy.
Evidence of nodal fixation or obvious gross ECS, a history of neck surgery,
and radiotherapy are believed to be relative contraindications to this approach
until further information is gathered. The small number of patients in this
study with N2a and N3 disease reflects this philosophy.In addition,
the surgeon must be prepared to modify the treatment plan during surgery for
metastatic disease in the neck. If during the operation unexpected findings,
such as adhesion to the jugular vein, sternocleidomastoid muscle, or spinal
accessory nerve, are encountered, then those structures should be resected
to completely remove all gross disease. In addition, when a suspicious lymph
node is encountered at the lowest planned level of the dissection, we believe
that it is prudent to extend the operation to include the next nodal group.
This principle, however, does not apply when suspicious lymph nodes are encountered
at level IV. We do not believe that it is necessary to extend the operation
to level V because of the strong evidence that lymphatic flow does not occur
from the jugular chain to the posterior triangle; however, when nodal metastasis
is encountered at level IV, the surgeon may consider elective treatment of
the ipsilateral paratracheal and upper mediastinal nodes. When the surgical
procedure planned includes total laryngectomy, this treatment should include
surgical removal of the nodes in question. However, when total laryngectomy
is not planned, the risk of injury to the recurrent laryngeal nerve inherent
to lymphadenectomy in this area should be considered.
In conclusion, SND can be applied safely and effectively to appropriately
chosen patients with clinically node-positive metastasis in the neck from
squamous cell carcinoma of the upper aerodigestive tract. Regional control
rates comparable to those achieved with more comprehensive operations can
be achieved in appropriately selected patients.
AUTHOR INFORMATION
Accepted for publication April 26, 2002.
This study was presented at the Fifth International Conference on Head
and Neck Cancer, San Francisco, Calif, August 2, 2000.
Corresponding author and reprints: Peter E. Andersen, MD, Department
of Otolaryngology/Head and Neck Surgery, Oregon Health Sciences University,
PV-01, 3181 SW Sam Jackson Park Rd, Portland, OR 97201.
From the Department of Otolaryngology/Head and Neck Surgery, Oregon
Health Sciences University, Portland (Drs Andersen, Warren, Burningham, Wax,
and Cohen); University of Connecticut Health Center, Farmington (Dr Spiro);
and the Memorial Sloan-Kettering Cancer Center, New York, NY (Drs Wong and
Shah).
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ABSTRACT
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