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Recurrence Rates After Selective Neck Dissection in the N0 Irradiated Neck
Michael A. Fritz, MD;
Ramon M. Esclamado, MD;
Robert R. Lorenz, MD;
Benjamin G. Wood, MD;
Pierre Lavertu, MD;
Marshall Strome, MD
Arch Otolaryngol Head Neck Surg. 2002;128:292-295.
ABSTRACT
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Objectives To define patterns of subclinical metastases in irradiated N0 necks
with recurrent or persistent primary site disease and to determine the regional
control rate when selective neck dissection (SND) is used in this setting.
Patients and Intervention Individuals included were previously treated for head and neck squamous
cell carcinoma with primary radiation therapy or chemoradiotherapy. All had
recurrent or persistent disease at the primary site, with no clinical or radiographic
evidence of nodal disease. The patients underwent surgical treatment of the
primary site along with site-specific SND and were required to undergo at
least 1 year of follow-up. Subsequent recurrence at the primary site disqualified
the patient from further evaluation.
Main Outcome Measure Regional tumor control.
Results Forty-three patients meeting the inclusion criteria underwent 59 SNDs
(levels dissected: I-IV [n = 22], II-IV [n = 34], and I-III [n = 3]). Sixteen
specimens were positive for nodal disease. The charts of 26 patients, who
underwent a total of 35 SNDs, were available for review after 1 year (none
of the patients involved died of disease in the neck). There were no neck
recurrences (mean follow-up, 25 months; median, 21 months). All patients with
more than 2 occult nodal metastases experienced primary site recurrence or
distant metastases.
Conclusions In this small cohort, SND in previously irradiated patients with recurrent
primary disease but clinically negative necks has resulted in excellent tumor
control in the neck. The usual patterns of nodal spread do not appear to be
significantly altered with primary site recurrence after radiation therapy.
The presence of more than 2 positive nodes in the neck specimen correlates
with poor prognosis.
INTRODUCTION
INCREASED UNDERSTANDING of the regional spread of head and neck tumors
and a desire to minimize operative morbidity have led to the widespread use
of selective neck dissection (SND) in the management of the clinically negative
neck. Studies have shown this technique to be oncologically safe in this setting,
with patient survival and regional control comparable to those of more extensive
neck dissections.1-3
However, in the case of multiple subclinical metastases or histologic evidence
of tumor spread beyond the lymph node capsule, most authors recommend adjuvant
radiation therapy to improve regional tumor control.4-7
The literature is replete with reviews concerning the use of SND in
the initial management of head and neck tumors, and the use of planned SND
following radiation or chemoradiation therapy has also been addressed.8-10 However, little information
exists concerning the management of an undissected, previously irradiated,
clinically negative neck following primary site recurrence. The few references
that address this issue advocate therapy ranging from observation to radical
neck dissection.1, 11
Several sources have demonstrated higher rates of wound complications
after head and neck oncologic surgery in patients who were previously treated
with radiotherapy or chemoradiotherapy.12-14
Irrespective of previous adjuvant treatment, SND has been shown to cause less
patient morbidity than modified radical neck dissection.2, 15
For these reasons, a protocol that minimizes the extent of surgery without
compromising tumor control would be beneficial in previously irradiated patients.
The oncologic efficacy of SND in previously irradiated N0 necks requires
further examination for several reasons: (1) patterns of regional metastases
may be affected by radiation-induced lymphatic changes; (2) the frequency
of subclinical metastases in irradiated necks has not been established; (3)
the option of effective postoperative radiation therapy has been exhausted;
and (4) regional control achieved by SND has not been defined in this population.
This retrospective analysis examines the recent experience at The Cleveland
Clinic Foundation, Cleveland, Ohio, in treating patients with primary site
recurrence and clinically N0 necks after previous irradiation. All patients
underwent appropriate resection of the primary tumor and SND. The primary
goals of this study were to examine the frequency and patterns of subclinical
neck node metastases and to determine the regional control achieved with SND
in this setting.
PATIENTS AND METHODS
A retrospective chart review was performed from January 1997 to May
2000 at the Department of Otolaryngology and Communicative Disorders, The
Cleveland Clinic Foundation. Forty-three individuals who met the inclusion
criteria had been previously treated for head and neck squamous cell carcinoma
with daily or twice-daily radiation therapy or with chemoradiotherapy (concurrent
irradiation with 3 courses of fluorouracil and cisplatin). Radiation doses
to neck fields ranged from 5000 to 6400 rads (standard paractice at our institution
is to treat at-risk clinically negative necks with 5200-5400 rads and clinically
positive necks with 6200-6400 rads coned to 7000-7200 rads over clinically
positive nodes). The stages of neck disease before primary therapy were as
follows: N0 (n = 37), N1 (n = 5), and N2c (n = 1). All patients had either
recurrent or persistent disease at the primary site (35 patients) or a metachronous
second primary tumor (8 patients). The patients had no clinical or radiographic
evidence of nodal disease and underwent surgical treatment of the primary
lesion along with site-specific SND. All patients with previously N-positive
necks were assessed with both high-contrast computed tomography and clinical
examination. Fifty-nine SNDs were performed (levels dissected: I-IV [n = 22],
II-IV [n = 34], and I-III [n = 3]). Individuals who received a "planned" salvage
neck dissection after radiotherapy or chemoradiotherapy were excluded from
this study.
A chart review of the cases in which these criteria were met documented
initial tumor site and stage, the location of active primary site disease,
and the elapsed interval between the completion of radiation therapy and surgical
salvage. Surgical procedures, perioperative complications, and pathologic
findings were reviewed. Pathologic analysis included documentation of number
and anatomical location of occult nodal metastases, as well as the presence
of nodal extracapsular spread.
The patients were required to have at least 1 year of follow-up examinations
for evaluation of regional control after SND. Recurrence at the primary site
after surgical intervention disqualified the patient from further observation
for long-term tumor control in the neck. In addition to documentation of the
status of the neck, primary site control and metastatic disease were recorded.
RESULTS
Forty-three patients underwent resection of their recurrent primary
site tumors accompanied by unilateral or bilateral elective SND. The nodal
levels that were dissected depended on the primary tumor location. The mean
interval between the completion of radiotherapy and salvage surgery was 13
months, with a median interval of 7 months. In addition to 59 SNDs, surgical
procedures included 26 total and 5 partial laryngectomies as well as 3 regional
and 16 free-flap reconstructions. Twelve patients (28%) and 16 SND specimens
(28%) harbored occult nodal disease. Two specimens (17%) had pathologic evidence
of extracapsular tumor spread. The neck dissection specimens contained 0 positive
nodes in 47 patients, 1 positive node in 5 patients, 2 positive nodes in 1
patient, and 3 positive nodes in 2 patients. Four patients had more than 3
positive nodes; 4, 5, 6, and 7 tumor-containing lymph nodes were each present
in 1 patient. The frequency of cervical metastases nodes was not higher in
the 6 individuals whose disease was initially staged either N1 or N2 (1 of
6 patients, or 17%).
Regional metastatic rates varied with primary site, with supraglottic
and hypopharyngeal cancers spreading most readily to the neck (Table 1). Despite advanced primary site lesions requiring 15 total
laryngectomies and 2 supracricoid laryngectomies in 17 patients, glottic cancers
metastasized to the neck in only 2 of 24 specimens. All nodal metastases were
found in levels II-IV. Seven specimens revealed tumor in levels III and IV,
without involving level II. Supraglottic, advanced glottic, and hypopharyngeal
lesions metastasized to both sides of the neck.
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Table 1. Subclinical Metastases by Primary Site*
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Surgical complications included 2 pharyngocutaneous fistulas, 2 hematomas,
and 2 infections. One patient suffered from exposed bone as a result of partial
flap breakdown, and another experienced actinomycosis of the mandible after
a mandibulotomy was performed for surgical access. There were no perioperative
deaths.
Seventeen patients were not followed up for a full year. Five patients
died of uncontrolled local disease, 5 of distant metastatic disease, and 3
of unrelated causes. There was an insufficient time interval after surgery
in 2 cases, and 2 patients were unavailable for follow-up. No patients died
of disease in the neck.
Twenty-six patients who underwent 35 SNDs completed more than 1 year
of follow-up. The mean follow-up period was 25 months, and the median was
21 months. Of these 26 patients, 3 had a recurrence at the primary site and
6 developed distant metastatic disease. No patients had a recurrence in the
neck (Table 2).
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Table 2. Patient Outcomes by Primary Site*
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Patient survival correlated with the number of occult cervical metastases.
Despite small patient numbers, a statistically significant difference in survival
was seen between those patients with more than 2 positive lymph nodes and
those with 2 or fewer regional metastases (P = .006,
Fisher exact test comparison) (Table 3).
All patients in the group with 2 or more positive nodes died of either primary
site recurrence or distant metastatic disease. Twelve (38%) of 32 patients
without evidence of tumor in SND specimens suffered similar outcomes. Disease
recurrence in 1 (17%) of 6 patients with 1 or 2 nodal metastases was not significantly
different from those with no pathologic findings (P
= .64).
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Table 3. Outcomes Based on Number of Occult-Positive Nodes
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COMMENT
The most important findings of this study are as follows:
- Selective neck dissection provides excellent regional control
in the previously irradiated, clinically N0 neck.
- The incidence and patterns of subclinical neck metastases are
not significantly altered after radiation therapy.
- The finding of more than 2 occult positive nodes correlates with
poor prognosis.
The utility of SND has been demonstrated in various clinical settings.
Its use in the elective management of the previously untreated, clinically
N0 neck is supported by many authors.1-7
In such a setting, site-specific neck dissections can result in regional control
and patient survival rates comparable to those of more extensive neck dissections.
In addition, SND has been effective for surgical salvage after radiation therapy
or chemoradiotherapy. Stenson et al8 and Robbins
et al,9 using planned SND after chemoradiotherapy
for N2 to N3 disease, demonstrated both low neck recurrence rates (1 of 69
patients and 1 of 52 patients, respectively) and low complication rates. They
concluded that SND, rather than a more extensive neck procedure, was therapeutically
appropriate in this setting. Boyd et al,10
reviewing salvage neck dissection after radiotherapy alone, also endorsed
the use of SND.
Despite many clinical studies of elective SND, its oncologic efficacy
in the previously irradiated N0 neck with recurrent or persistent primary
site disease is not well established. As a result, few authors have recommended
its use in this setting. Goodwin and Chandler11
reviewed the pathologic findings in elective radical neck dissections in 22
patients who had received prior neck irradiation for N0 or N1 disease. Four
(18%) of 22 specimens demonstrated neck metastases and 9 of 12 patients were
without evidence of disease at 2 years. Nodal echelons involved, site and
status of primary disease, and neck control rates were not addressed. Because
of the low yield of subclinical disease and increased morbidity associated
with radical neck dissection after radiation therapy, the authors recommended
observation over elective neck dissection. In contrast, the possibility of
altered lymphatic drainage patterns prompted Shah and Andersen1
to advocate modified radical neck dissection or radical neck dissection for
recurrent disease after radiotherapy.
In our study, 26 patients underwent 36 site-specific SNDs and experienced
no neck recurrences (mean follow-up, 25 months). This finding supports the
ongoing use of SND to manage clinically negative necks in this specific patient
population.
The incidence and patterns of occult regional tumor spread in previously
irradiated necks have not been well defined. While the short-term disturbance
of lymphatic flow is clearly demonstrated by the edema that has been observed
at the primary site in many patients who undergo irradiation of the head and
neck, to our knowl edge no studies to date have demonstrated permanent alterations
in the patterns of lymphatic metastases after therapeutic radiation doses.
Despite previous radiotherapy, the patients in our study experienced a frequency
and an anatomical distribution of occult neck metastases similar to those
reported in previous articles on untreated N0 necks.7, 16-17
The 28% incidence of subclinical neck tumor is similar to the generally reported
rate of 30% in the nonirradiated neck and supports the use of elective neck
dissection in the specific patient population in this study. The nodal levels
involved as a function of primary site closely resemble the results of Shah17; the absence of neck failures in undissected, previously
irradiated levels excludes occult regional metastases beyond the range of
the SNDs performed.
The most important factor in the prognosis of squamous carcinomas of
the head and neck is the status of the cervical lymph nodes.18-19
The presence of clinical neck metastases decreases overall survival by at
least half, and the number of positive nodes relates to the frequency of distant
metastases.20 In nonirradiated N0 necks, Alvi
and Johnson21 found that occult cervical metastases
also carried grave prognostic significance, with disease recurrence occurring
in 60% of patients with histologically positive nodes, compared with 18% of
those with negative nodes. Viani et al,22-23
reporting on glottic and oropharyngeal recurrence after radiotherapy, analyzed
the specimens from neck dissections that were performed for clinically positive
disease. In these cases, regional lymphatic metastases corresponded with a
dismal survival rate: 16% for glottic cancer and 19% for oropharyngeal cancer.
However, the authors reported that neither the number of positive lymphatic
metastases nor the presence of extracapsular spread affected patient outcomes.
Occult neck metastases in the previously irradiated neck appear to carry
different prognostic significance. In contrast to Alvi and Johnson's21 findings in nonirradiated necks, the presence of
1 or 2 subclinical neck metastases did not result in a significantly worse
outcome than did pathologically negative necks (P
= .64). However, all patients with more than 2 histologically positive nodes
had disease recurrence. Although patient numbers are small, the difference
in survival was statistically significant (Table 3).
Alvi and Johnson21 observed a 49% incidence
of extracapsular tumor spread in occult neck metastases. The results in our
patient population differ considerably, with only 2 (17%) of 12 patients having
extracapsular spread. This contrast may indicate a possible mitigating effect
of radiation-induced lymphatic changes and, if so, may suggest an increased
likelihood of regional control in these patients with nodal foci removed by
elective neck dissection. This possibility may be reflected in the similar
outcomes observed between patients with 2 or fewer occult metastases and those
with clinically negative necks.
CONCLUSIONS
Selective neck dissection in previously irradiated patients with recurrent
primary disease but clinically negative necks results in excellent regional
tumor control. The usual patterns of nodal spread are not significantly altered
with primary site recurrence after radiation therapy. The presence of more
than 2 positive nodes in the neck specimen correlates with poor prognosis.
The findings and conclusions of this study must be tempered by its small patient
numbers, mean follow-up of 25 months, and varied primary sites of recurrent
disease. Despite these limitations, we believe that these preliminary data
justify continued study of SND in this setting.
AUTHOR INFORMATION
Accepted for publication November 15, 2001.
This study was presented as a poster at the annual meeting of the American
Head and Neck Society, Palm Desert, Calif, May 15, 2001.
Corresponding author: Ramon M. Esclamado, MD, The Cleveland Clinic
Foundation, Desk A71, 9500 Euclid Ave, Cleveland, OH 44195 (e-mail: esclamr{at}ccf.org).
From the Department of Otolaryngology and Communicative Disorders,
Cleveland Clinic Foundation(Drs Fritz, Esclamado, Lorenz, Wood and Strome),
and the Department of Otolaryngology, University Hospitals of Cleveland (Dr
Lavertu), Cleveland, Ohio.
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