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Ann Thorac Surg 1996;62:338-341
© 1996 The Society of Thoracic Surgeons
Abstract of this Article
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Original Articles: General Thoracic
Lung Cancer Staging: The Value of
Ipsilateral Scalene Lymph Node
Biopsy Performed at Mediastinoscopy
Jeffrey D. Lee, MD, Robert J. Ginsberg, MD
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Author Home Page(s):
Robert J. Ginsberg
Department of Surgery, Thoracic Service, Memorial Sloan-Kettering
Cancer Center, New York, New York
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Footnotes
Abstract
Introduction
Material and Methods
Results
Comment
References
Abstract
Background. The accurate preoperative staging of lung cancer remains an essential
element in its proper treatment. In most centers, N3 disease contraindicates an operative
approach, despite the advent of combined modality therapy. Although it is used to
confirm palpable supraclavicular disease, routine scalene lymph node biopsy to stage
nonpalpable disease has been abandoned.
Methods. From January 1991 to July 1995, 408 cervical mediastinoscopies were
performed by a single surgeon for the staging of lung cancer. In those patients eligible for
induction therapy, when N2 or N3 disease was strongly suspected or identified, ipsilateral
scalene lymph node biopsy was performed through the same cervical incision using the
mediastinoscope to reach the scalene fat pad.
Results. Eighty-one patients underwent this additional staging procedure. There was
minimal morbidit y and no deaths. Of these 81 fully staged patients, primary tumor
histology was non-small cell in 95.1%. Thirty-nine patients were staged as N2 after
standard mediastinoscopy. Of these, 6 (15.4%) harbored occult nonpalpable
supraclavicular lymph node disease as well. Nineteen patients were staged as N3contralateral after standard mediastinoscopy. Of these, 13 (68.4%) had occult
supraclavicular disease as well. Of all 58 patients with superior mediastinal nodal
involvement identified by standard mediastinoscopy, 19 (32.8%) also harbored occult
scalene lymph node disease, rendering them ineligible for our induction therapy
protocols. Scalene positive primary tumors were all centrally located (visualizable by
flexible bronchoscopy) (19 of 19) and were uniformly of nonsquamous origin.
Conclusions. We believe that this technique is a valuable extension to standard cervical
mediastinoscopy and can be used in N2 or N3 staged patients with central, nonsquamous
tumors before considering a combined modality therapeut ic approach that includes
operation. Through its use, more accurate staging before initiation of therapy and
elimination of those patients who may derive no benefit from an aggressive surgical
approach may be possible.
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Footnotes
Abstract
Introduction
Material and Methods
Results
Comment
References
Introduction
Despite the advent of combined modality therapy, the identification of N3 disease
(contralateral- mediastinal or supraclavicular lymph node involvement) may
contraindicate a surgical approach. Although invaluable in staging the superior
mediastinum, standard cervical mediastinoscopy will not routinely evaluate the status of
the supraclavicular scalene lymph nodes. Although initially used to confirm palpable
supraclavicular disease, the routine use of scalene lymph node biopsy in nonpalpable
disease has been abandoned.
In a series of 81 patients undergoing mediastinoscopy, when N2 or N3 disease was
strongly suspected or identified and a combined modality approach including operation
was being considered, we performed ipsilateral scalene lymph node biopsies through the
same cervical incision using the mediastinoscope to reach the scalene fat pad.
Top
Footnotes
Abstract
Introduction
Material and Methods
Results
Comment
References
Material and Methods
In our clinic, most patients undergo an extensive metastatic survey and mediastinoscopy
before definitive treatment planning. Needle biopsy of any palpable supraclavicular
abnormalities is performed in the clinic, and if the results are inconclusive, open scalene
lymph node biopsy is performed. Only those without evidence of extrathoracic metastasis
are staged invasively with cervical mediastinoscopy. For this study, when N2 or N3contralateral disease was discovered by frozen section at mediastinoscopy or strongly
suspected because of lymph node appearance, and a multimodality treatment regimen
including surgical resection was being considered, we used the mediastinoscope to obtain
ipsilateral scalene lymph node biopsy specimens as well.
Technique
Through a 2- to 3-cm transverse suprasternal incision, sharp dissection in the midline was
performed, separating the cervical strap muscles and incising the pretracheal fascia.
Digital dissection into the superior mediastinum and a standard cervical mediastinoscopy
were then completed [1]. Routinely, biopsy was performed of two ipsilateral mediastinal,
one contralateral mediastinal, and the subcarinal nodal stations. Through the same
incision, the mediastinoscope was then withdrawn along the anterior tracheal wall to the
thoracic inlet. Posterolateral and superior rotation of the mediastinoscope tip behind the
ipsilateral carotid sheath and into the supraclavicular fossa was then performed. By gentle
dissection of the medial aspect of the scalene fat pad through the mediastinoscope, a
single ipsilateral scalene lymph node was teased free and then removed (Fig 1 ).
Fig 1. . Technique of mediastinoscopic scalene lymph
node biopsy (see text).
View larger version
(38K):
[in this window]
[in a new window]
Statistical Methods
Statistical analysis was performed using the software package Statview 4.0 (Abacus
Concepts, Berkeley, CA). The paired Student's t test was used to compare variables of
continuous numeric type (age and tumor size). The 2 test was used for nominal variables
(sex, tumor laterality, location, and histology).
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Abstract
Introduction
Material and Methods
Results
Comment
References
Results
Morbidity and Mortality
This additional staging procedure was associated with very limited morbidity (one
superficial wound infection, one wound hematoma) and no mortality. It required only a
few additional minutes of operative time.
Patient and Primary Tumor Characteristics
Of 408 cervical mediastinoscopies performed by a single surgeon (R.J.G.), 81 were in
patients (50 male, 31 female) who also underwent mediastinoscopic ipsilateral scalene
lymph node biopsies. These patients represented a heterogeneous population with a mean
age of 60.5 ± 10.3 years (range, 40 to 82 years). Smoking history was 40.3 ± 30.8 packyears. Tumor size averaged 5.3 ± 2.9 cm (range, 0.9 to 15 cm). Right-sided primary
tumors (70 of 81, 86.4%) were more common than left-sided ones (11 of 81, 13.6%)
because left-sided primary tumors with superior mediastinal-paratracheal lymph node
involvement were usually deemed inoperable, and therefore were not considered for this
additional staging procedure. On final pathologic review, primary tumor histology was
non-small cell in 95.1% (adenocarcinoma in 48, squamous in 14, large cell in 12, and
poorly differentiated in 3). The remainder were small cell (4 patients).
Results of Combined Staging Procedures
Of the 81 patients undergoing the combined procedure, 23 had negative standard cervical
mediastinoscopy results (staged N0-N1). Of these, none had occult scalene lymph node
involvement. Fifty-eight of the 81 patients undergoing the combined procedure were
ultimately proven to have superior mediastinal nodal involvement (N2, n = 39, N3contralateral, n = 19) by standard mediastinoscopy. Of these, 19 (32.8%) had occult
nonpalpable scalene lymph node metastasis. Of 39 patients identified to have ipsilateral
mediastinal nodal involvement (N2), 6 (15.4%) harbored occult ipsilateral scalene nodal
disease. Of 19 patients with both ipsilateral (N2) and contralateral (N3) mediastinal nodal
involvement documented by standard mediastinoscopy, 13 (68.4%) also harbored occult
ipsilateral scalene lymph node metastasis.
Examination of the patterns of lymph node involvement revealed that of the patients with
occult scalene lymph node disease, 14 of 19 (73.7%) had upper paratracheal lymph node
involvement (level 2) as well. Of the 6 N2-staged patients, 2 exhibited a "skip pattern"
(involvement of the ipsilateral scalene fat pad without documented level 2 involvement).
Comparison of Scalene -Negative and Scalene -Positive Patients
We compared the demographics and tumor characteristics of the scalene- negative group
(n = 62) and the scalene-positive group (n = 19) (Table 1 ). There were no statistically
significant differences in patient age (p = 0.533), sex predominance (p = 0.141), or
primary tumor size (p = 0.657). There were more right-sided primary tumors in the
scalene-negative group (p = 0.0187). There were also differences in location and
histologic origin of the primary tumors. When one defines central lesions as those within
the view of a flexible bronchoscope, the scalene-negative group comprised both central
(37 of 62, 59.7%) and peripheral lesions (25 of 62, 40.3%). Conversely, all scalenepositive tumors were central lesions (19 of 19, 100%) (p = 0.001). The histologic origin
of scalene- negative tumors was either squamous (14 of 62, 22.6%) or nonsquamous (48
of 62, 77.4%), whereas all scalene-positive tumors were nonsquamous (19 of 19, 100%; p
= 0.0001).
View this table: Table 1. . Comparison of Scalene-Negative and Scalene-Positive
[in this window] Patients
[in a new
window]
Evaluating only centrally located, nonsquamous tumors (Table 2 ), 8 were staged N0-N1
by standard mediastinoscopy; none had positive scalene nodes. Of those staged N2 by
standard mediastinoscopy (n = 20), 6 (30%) had occult scalene nodal involvement.
Similarly, 16 patients had centrally located nonsquamous primaries that were staged N3contralateral by standard mediastinoscopy. Ofthese, 13 (81.3%) had occult scalene nodal
involvement as well. Hence, of all patients with a centrally located nonsquamous primary
tumor who had positive standard mediastinoscopy results (n = 36), 19 (52.8%) harbored
microscopic, occult, nonpalpable supraclavicular disease as well.
View this table: Table 2. . Central Nonsquamous Tumorsa
[in this window]
[in a new window]
On final pathologic review, 4 patients were classified as having small cell lung cancer.
These were equally distributed between the scalene-negative and scalene-positive groups,
with 2 patients in each.
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Footnotes
Abstract
Introduction
Material and Methods
Results
Comment
References
Comment
Increasingly, multidisciplinary treatment protocols are being used for the treatment of
locally advanced lung cancer. Recent phase II and phase III treatment protocols [2–9]
extensively screened potential patients for metastatic disease and used cervical
mediastinoscopy to stage the mediastinal lymph nodes. We describe a technique for
improving the staging accuracy of standard cervical mediastinoscopy. In our experience,
ipsilateral scalene lymph node biopsies performed in the same setting as standard cervical
mediastinoscopy can greatly expand the findings of the standard approach and identify
those patients with supraclavicular N3 disease.
Excision of the scalene lymph nodes as an aid in diagnosing intrathoracic lesions was
reported by Daniels in 1949 [10]. Others adopted this technique widely for the staging of
lung cancer [11], as well as for a variety of other malignancies [12, 13]. In an autopsy
study, Agliozzo and Reingold [14] documented scalene lymph node metastasis in 18 of
49 patients (37.5%) with lung carcinoma. Of these, 10 lesions (55.6%) were less than 1.0
cm in size and nonpalpable. Others attempted to define the incidence of occult
malignancy in nonpalpable scalene lymph nodes. Palumbo and Sharpe [15] reported
occult malignancy in 11% of nonpalpable scalene nodes, whereas Brantigan and
colleagues [16] found a 23.8% positivity rate. In a recent study, Bernstein and associates
[17] detected only a 3.5% incidence. These wide-ranging results may be due to
differences in patient population, primary tumor stage, location or histology, and surgical
technique. Few studies have assessed both supraclavicular and superior mediastinal nodal
involvement. We have shown a strong positive correlation between superior mediastinal
and scalene lymph node involvement. All patients with negative standard cervical
mediastinoscopy results (staged N0-N1) when evaluated for scalene nodal involvement
were found to be free of occult cervical metastasis. Of those with N2 involvement by
standard cervical mediastinoscopy, 15.4% harbored nonpalpable microscopic scalene
nodal disease. In most cases, N3-contralateral involvement foreboded scalene nodal
involvement as well (68.4%).
Primary tumor location and histologic type were important factors. All of the tumors
associated with occult scalene nodal disease were centrally located (p = 0.001) and of
nonsquamous histology (p = 0.0001). Over 50% of centrally placed, nonsquamous
primary tumors with mediastinal involvement demonstrated occult supraclavicular
disease. Schatzlein and co-workers [18] also found that central tumor location and
nonsquamous histology were important factors in scalene nodal involvement. Hence, the
low 3.5% incidence of involvement reported by Bernstein and associates [17] may be due
to the preponderence of early-stage tumors in this study (only 10 patients [19.2%] had N2
disease documented by preoperative mediastinoscopy or Chamberlain procedure) and the
relatively high percentage of patients (41.1%) with squamous histology. In our series,
biopsy was only performed on single scalene lymph nodes. It is possible that one could
further increase diagnostic yield by performing bilateral scalene lymph node biopsies or
complete scalene fat pad excisions. The higher incidence of positive nodes (23.8%)
reported by Brantigan and colleagues [16] may be attributable in part to the routine
performance in that study of bilateral open scalene fat pad excisions. They found that in
nonpalpable scalene lymph nodes, ipsilateral biopsy detected 73% of occult metastases,
whereas contralateral biopsy identified an additional 27%.
Numerous phase II and a few phase III trials have evaluated a multimodality approach
that includes operation to treat locally advanced lung cancer [2–9]. A few [5–8] have
included IIIb patients (T4 with or without N3-contralateral or N3-scalene) in aggressive
neoadjuvant treatment protocols. Some encouraging early results have been demonstrated
for both the IIIa and IIIb subgroups, with apparently little survival difference between
these groups (3-year survival 27% and 24%, respectively; p = 0.81) [7]. Subset analysis
of the IIIb subgroup, however, seems to highlight important prognostic factors. Those
staged IIIb on the basis of T4 involvement and who were non-N2 had a more favorable
median survival compared with all others in the IIIb subgroup (28 months versus 13
months). Conversely, among 27 patients with N3 disease, none of the patients with N3contralateral disease were alive at 2 years. The vast majority (89%) of recurrences in this
study [7] involved distant metastasis. Our finding that the majority (68.4%) of those with
N3-contralateral disease also harbor occult supraclavicular metastasis, and presumably
other unidentified sites of disease, may help explain their poor survival. These patients
clearly represent a much poorer prognostic group without evidence of benefit from a
surgical approach.
Recent results of positron emission tomography staging suggest that this new noninvasive
modality may identify those patients with superior mediastinal and supraclavicular
involvement [19–21]. Histologic confirmation of these findings should be sought. The
combined modalities of standard cervical mediastinoscopy, extended cervical
mediastinoscopy [22], and mediastinoscopic scalene lymph node biopsy seem well suited
for this role.
When N2 or N3 disease is encountered at mediastinoscopy, scalene lymph node biopsy
will identify occult supraclavicular disease in a substantial proportion of patients with
central, nonsquamous tumors and may be of value before considering such patients for a
combined modality approach that includes operation.
Addendum
Since the presentation of this report, 2 patients have suffered transient bilateral vocal cord
paresis, presumably due to intraoperative injury to both recurrent laryngeal nerves during
mediastinoscopy and scalene lymph node biopsy. Neither patient required further therapy
(eg, tracheostomy), but a 48-hour hospital admission was necessary in each case. Close
attention to anatomic details as depicted in Figure 1 is essential.
Top
Footnotes
Abstract
Introduction
Material and Methods
Results
Comment
References
Footnotes
Presented at the Poster Session of the Thirty-second Annual Meeting of The Society of
Thoracic Surgeons, Orlando, FL, Jan 29–31, 1996.
Address reprint requests to Dr Ginsberg, Department of Surgery, Thoracic Service,
Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021.
Top
Footnotes
Abstract
Introduction
Material and Methods
Results
Comment
References
References
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1987;4:673–5.
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Abstract of this Article
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PubMed Citation
Deslauriers, J., Grégoire, J. (2000). Clinical and
This Article has been cited by:
Surgical Staging of Non-Small Cell Lung Cancer.
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Lee, J. D. || Ginsberg, R. J.
Chest 117: 96S-103 [Abstract] [Full Text]
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Deslauriers, J., Grégoire, J. (2000). Clinical and
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Surgical Staging of Non-Small Cell Lung Cancer.
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Chest 117: 96S-103 [Abstract] [Full Text]
Author Home Page(s):
Marom, E. M., McAdams, H. P., Erasmus, J. J.,
Robert J. Ginsberg
Goodman, P. C., Culhane, D. K., Coleman, R. E.,
Herndon, J. E., Patz, E. F. Jr (1999). Staging Non-Small Cell Lung Cancer with
Whole-Body PET. Radiology 212: 803-809 [Abstract] [Full Text]
Fultz, P. J., Feins, R. H., Strang, J. G., Wandtke, J. C., Johnstone, D. W., Watson,
T. J., Gottlieb, R. H., Voci, S. L., Rubens, D. J. (2002). Detection and Diagnosis
of Nonpalpable Supraclavicular Lymph Nodes in Lung Cancer at CT and US.
Radiology 222: 245-251 [Abstract] [Full Text]
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