Literature
首页医源资料库在线期刊放射学杂志2003年1月第226卷第1期

Detection and Diagnosis of Nonpalpable Supraclavicular Lymph Nodes in Lung Cancer at CT and US1

来源:放射学杂志
摘要:(e-mail:patrick_fultz@urmc。ABSTRACTTopABSTRACTINTRODUCTIONMATERIALSANDMETHODSRESULTSDISCUSSIONREFERENCESPURPOSE:Toassessfrequencyandsignificanceofenlargednonpalpablesupraclavicularlymphnodesbyusingchestcomputedtomography(CT)andsupraclavicularultrasonography(US)inpatie......

点击显示 收起

1 From the Departments of Radiology (P.J.F., J.G.S., J.C.W., R.H.G., S.L.V., D.J.R.) and Surgery (R.H.F., D.W.J., T.J.W.), University of Rochester Medical Center, 601 Elmwood Ave, Rochester, NY 14642. Received February 8, 2001; revision requested March 12; revision received April 30; accepted May 25. Address correspondence to P.J.F. (e-mail: patrick_fultz@urmc.rochester.edu).


     ABSTRACT

Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
PURPOSE: To assess frequency and significance of enlarged nonpalpable supraclavicular lymph nodes by using chest computed tomography (CT) and supraclavicular ultrasonography (US) in patients at initial diagnosis of lung cancer.

MATERIALS AND METHODS: Fifty-five patients with no prior malignancy who presented with suspected and subsequently proven lung cancer of any stage or a proven but potentially resectable lung cancer were prospectively selected after chest CT. Chest CT and other radiologic findings were reviewed and tabulated. Standardized US technique was used to identify and guide needle biopsy of enlarged supraclavicular lymph nodes (0.5 cm short axis).

RESULTS: Twenty-two (40%) of 55 patients had supraclavicular abnormalities detected at CT and/or US. In 18 (82%) of the 22 patients, supraclavicular abnormalities were recognizable at CT. Seventeen of 22 patients had malignant nodes, and five patients had benign nodes (n = 3), a cyst (n = 1), or an indeterminate lesion (n = 1) at US-guided supraclavicular needle sampling. There were no complications. Supraclavicular metastases (31% of patients) were about as common as the combined number of patients with indeterminate (n = 13) and probably or proven malignant (n = 6) adrenal nodules (35% of patients). Supraclavicular metastases were often associated with mediastinal adenopathy or suspected extrapulmonary nonnodal metastases (P < .05).

CONCLUSION: In many patients with lung cancer, chest CT that includes the neck base followed by US-guided sampling of enlarged supraclavicular lymph nodes is a simple and safe method for simultaneously establishing a tissue diagnosis and tumor nonresectability.

 

Index terms: Lung, CT, 60.12112, 60.12115 • Lung, US, 60.12985 • Lung neoplasms, 60.321 • Lymphatic system, abnormalities, 997.31, 997.33


     INTRODUCTION

Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
Lung cancer is one of the most common cancers, and it is the leading cause of cancer mortality in the United States (l). The need for diagnosis and staging of cancer in patients with a suspected lung cancer is a frequent occurrence in medical practice. Guidelines have been published by national and international organizations to assist physicians in the overall evaluation of patients with suspected or known lung cancer, with an emphasis on non–small cell lung cancer (2,3). A variety of noninvasive and invasive nonradiologic and radiologic procedures can be used for the diagnosis of lung cancer and/or its metastases. These procedures include sputum analysis, thoracentesis, palpation-guided needle biopsy, imaging-guided percutaneous needle biopsy (transthoracic or at other sites), bronchoscopy, mediastinoscopy, thoracoscopy, and thoracotomy.

Currently, the best chance for a cure of lung cancer is surgical therapy. Lung cancer metastases to supraclavicular lymph nodes are an indicator of unresectable disease (3). In the current TNM system (24) of lung cancer staging, metastatic tumor in this nodal group is considered N3 disease. Patients with stage IIIB (any T, N3, M0) non–small cell lung cancer have a 3% 5-year survival rate compared with a 14% 5-year overall survival rate in patients with lung cancer (1,4).

The need to include the adrenal glands on the inferior chest computed tomographic (CT) images at initial examination of patients with suspected lung cancer has been emphasized in the literature because of the possibility of adrenal metastases (2,3). There have also been numerous articles that focused on detection and/or characterization of adrenal lesions in these patients to attempt to distinguish incidental benign adrenal lesions from possible metastases. There has been much less published information on the role of imaging of the supraclavicular area in lung cancer.

In patients with lung cancer, palpable supraclavicular lymph nodes are usually involved by metastatic disease (5) and can be sampled with palpation-guided needle biopsy. In surgical series obtained from the era before CT (68), nonpalpable supraclavicular lymph nodes with malignancy were reported in as many as 41%–51% of patients with lung cancer. A retrospective review of chest CT studies that included some patients with lung cancer indicated a role for CT in the assessment of this area (9). Furthermore, authors of some ultrasonographic (US) studies (1012) have indicated that imaging can play a role in the examination of patients with lung cancer and with nonpalpable cervical and supraclavicular adenopathy.

The purpose of our study was to assess the frequency and significance of enlarged but nonpalpable supraclavicular lymph nodes by using chest CT and US in patients with lung cancer.


     MATERIALS AND METHODS

Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
Patient Selection
From December 1998 to July 2000, consecutive patients with suspected lung cancer were prospectively enrolled after chest CT examinations. The study design was approved by our institutional review board, and informed consents were obtained. Patients were recruited from thoracic surgery, pulmonary and inpatient services, as well as from outpatient referrals from primary care physicians.

The inclusion criteria were adult patients without palpable supraclavicular lymph nodes but with a suspected and subsequently proven lung cancer of any stage or a known potentially resectable lung cancer at enrollment. Proof of lung cancer was defined as an intrathoracic pathologic diagnosis or a pathologic diagnosis of an extrathoracic metastasis with typical chest CT findings of lung cancer. In conjunction with chest CT findings typical of a primary lung cancer, the histopathologic cell types from extrathoracic metastases that were considered consistent with metastatic lung cancer included adenocarcinoma, squamous cell carcinoma, adenosquamous carcinoma, large cell carcinoma, poorly differentiated non–small cell carcinoma, and small cell carcinoma. Patients with potentially resectable non–small cell lung cancer were defined by using standard criteria as those fit for thoracic surgery who had a dominant lung lesion with no contralateral intrathoracic nodal disease, no cytologically proven malignant pleural effusion, no gross invasion of vital thoracic structures, and no extrathoracic disease. Chest CT examinations were performed no more than 6 weeks before US examinations.

We excluded patients with palpable supraclavicular lymph nodes or pleural effusions amenable to thoracentesis, patients with pathologically proven small cell lung cancers, nonsurgical candidates with pathologically proven non–small cell lung cancer, and patients with a prior history of malignancy other than nonmelanomatous skin cancer.

Twenty-four patients who consented to participate in this study were excluded because they had final diagnoses other than primary lung cancer, such as infection, sarcoidosis, bronchiolitis obliterans organizing pneumonia, hamartoma, or other malignancies. Nine patients with a final diagnosis of lung cancer declined participation in this study. Six patients who were later proven to have lung cancer were not asked to enroll because of either a markedly impaired mental status (n = 5) or logistical issues (n = 1).

The final study group consisted of 55 patients who were nonconsecutive due to the exclusions mentioned.

Patient Demographics and Tumor Characteristics
Of the 55 patients, 27 were women and 28 were men. Mean patient age was 65.9 years (age range, 41–86 years). Fifty-one patients had non–small cell carcinoma that comprised 30 adenocarcinomas (five of which had bronchioloalveolar features), eight squamous cell carcinomas, five adenosquamous carcinomas, two large cell carcinomas, and six poorly differentiated non–small cell carcinomas. Four patients had small cell carcinomas.

At CT, the average maximal dimension of the dominant lung lesion was 5.9 cm (range, 1.2–14.0 cm). Forty-six (84%) of 55 patients had a dominant lung lesion larger than 3 cm (T2).

Definition of Supraclavicular Lymph Nodes
In the TNM system of lung cancer staging, supraclavicular or scalene lymph nodes are considered a regional lymph node group (potential N3 disease), lying above the mediastinal pleural envelope (13). The term scalene lymph node is used for a supraclavicular lymph node that is in proximity to the scalene muscles. The fat pad containing nodes in the scalene area is sampled during open surgical biopsies. Cervical lymph nodes above the supraclavicular area are considered distant metastases—M1 disease (13).

At CT, the supraclavicular lymph nodes are above the manubrium and on the same image as the clavicle. They lie lateral to the medial edge of the common carotid artery and medial to the lateral rib margin (14). The cervical lymph nodes that are in between the common carotid arteries are referred to as level 6 (visceral) nodes according to the cervical lymph node classification system (14). At US, we defined supraclavicular lymph nodes as those above the manubrium and in immediate proximity to the clavicle. Other CT and US landmarks for the central supraclavicular area include the area at or just above the junction of the internal jugular and subclavian veins in proximity to the lower scalene muscles and posterolateral to or just below the thyroid gland (Figs 1, 2).


fig.ommitted Figure 1a. Images obtained in a 43-year-old woman with poorly differentiated carcinoma with squamous cell features who presented with chest pain. (a) Transverse contrast material-enhanced CT scan of a 3.5-cm left upper lobe lung tumor (arrow) with some peripheral atelectasis. (b) Transverse contrast-enhanced CT scan shows multiple enlarged left supraclavicular lymph nodes (arrows) posterior to the left lobe of the thyroid gland, common carotid artery, and internal jugular vein. The anterior scalene muscle (arrowhead), as seen on the right, can mimic a node when viewed on a single image. (c) Transverse US image shows the metastatic left supraclavicular lymph nodes (straight arrows) posterior and lateral to the common carotid artery (arrowhead) and the internal jugular vein (curved arrow). The internal jugular vein is compressed by the lymph nodes.

 

 

fig.ommitted Figure 1b. Images obtained in a 43-year-old woman with poorly differentiated carcinoma with squamous cell features who presented with chest pain. (a) Transverse contrast material-enhanced CT scan of a 3.5-cm left upper lobe lung tumor (arrow) with some peripheral atelectasis. (b) Transverse contrast-enhanced CT scan shows multiple enlarged left supraclavicular lymph nodes (arrows) posterior to the left lobe of the thyroid gland, common carotid artery, and internal jugular vein. The anterior scalene muscle (arrowhead), as seen on the right, can mimic a node when viewed on a single image. (c) Transverse US image shows the metastatic left supraclavicular lymph nodes (straight arrows) posterior and lateral to the common carotid artery (arrowhead) and the internal jugular vein (curved arrow). The internal jugular vein is compressed by the lymph nodes.

 

 

fig.ommitted
 
Figure 1c. Images obtained in a 43-year-old woman with poorly differentiated carcinoma with squamous cell features who presented with chest pain. (a) Transverse contrast material-enhanced CT scan of a 3.5-cm left upper lobe lung tumor (arrow) with some peripheral atelectasis. (b) Transverse contrast-enhanced CT scan shows multiple enlarged left supraclavicular lymph nodes (arrows) posterior to the left lobe of the thyroid gland, common carotid artery, and internal jugular vein. The anterior scalene muscle (arrowhead), as seen on the right, can mimic a node when viewed on a single image. (c) Transverse US image shows the metastatic left supraclavicular lymph nodes (straight arrows) posterior and lateral to the common carotid artery (arrowhead) and the internal jugular vein (curved arrow). The internal jugular vein is compressed by the lymph nodes.

 

 

fig.ommitted Figure 2a. Images obtained in a 61-year-old woman with an adenosquamous carcinoma who presented with hemiparesis and aphasia from brain metastases. (a) Transverse contrast-enhanced CT scan of the left upper lobe tumor (arrow). (b) Transverse contrast-enhanced CT scan obtained just below the right thyroid margin and just above the internal jugular-subclavian vein junction shows a contralateral right supraclavicular lymph node (arrow). (c) Transverse US image of the 0.9-cm short-axis right supraclavicular lymph node metastasis (straight arrow) posterior to the common carotid artery (arrowhead) and the compressed internal jugular vein (curved arrow).

 

 

fig.ommitted Figure 2b. Images obtained in a 61-year-old woman with an adenosquamous carcinoma who presented with hemiparesis and aphasia from brain metastases. (a) Transverse contrast-enhanced CT scan of the left upper lobe tumor (arrow). (b) Transverse contrast-enhanced CT scan obtained just below the right thyroid margin and just above the internal jugular-subclavian vein junction shows a contralateral right supraclavicular lymph node (arrow). (c) Transverse US image of the 0.9-cm short-axis right supraclavicular lymph node metastasis (straight arrow) posterior to the common carotid artery (arrowhead) and the compressed internal jugular vein (curved arrow).

 

 

fig.ommitted Figure 2c. Images obtained in a 61-year-old woman with an adenosquamous carcinoma who presented with hemiparesis and aphasia from brain metastases. (a) Transverse contrast-enhanced CT scan of the left upper lobe tumor (arrow). (b) Transverse contrast-enhanced CT scan obtained just below the right thyroid margin and just above the internal jugular-subclavian vein junction shows a contralateral right supraclavicular lymph node (arrow). (c) Transverse US image of the 0.9-cm short-axis right supraclavicular lymph node metastasis (straight arrow) posterior to the common carotid artery (arrowhead) and the compressed internal jugular vein (curved arrow).

 

 
We acknowledge that anatomic boundaries of the supraclavicular fossa are likely depicted better at neck US (usually performed with the patient supine with arms down) than at chest CT. During chest CT, patients typically are supine, with their head, neck, and sometimes upper chest propped up on a pillow and their arms raised overhead.

At CT and US, enlarged supraclavicular lymph nodes were defined as those with a short-axis measurement greater than or equal to 0.5 cm. The diagnostic standards of reference to validate supraclavicular lesions were the cytopathologic results of the guided needle aspiration biopsies in all patients except one. In that patient, the biopsy finding was inconclusive, and we categorized it as benign, but CT clearly depicted an abnormality that we believed to be an enlarged node. This was likely a false-negative fine-needle aspiration biopsy finding, but we have no pathologic proof to confirm our suspicion for that particular site. The patient’s tumor was diagnosed as unresectable at subsequent bronchoscopy because of central airway involvement.

CT Examinations
Chest CT was performed at several sites with a variety of protocols. At our hospital, 19 patients underwent helical chest CT (HiSpeed Advantage or CT/i; GE Medical Systems, Milwaukee, Wis). A 3–7-mm section thickness and 100–150 mL of iodinated intravenous contrast material were used for CT (precontrast images also obtained in two patients). Generally, the scans began at least 2 cm above the lung apices and extended through the adrenal glands.

Chest CT studies in the other 36 patients came from 17 facilities. The chest CT section thickness varied from 5 to 10 mm, and a mix of helical and conventional CT scanners was used. Thirty-two of the 36 chest CT studies were performed with iodinated intravenous contrast material (precontrast images were obtained in 18 patients).

In 44 of the 55 patients, the chest CT studies included all of both adrenal glands. In the remaining 11 patients, either one or both glands were partly included, but at least 3 cm of craniocaudal adrenal coverage was obtained in each gland in these instances.

In most patients, the chest CT was prospectively assessed by an observer (P.J.F.) for the presence of supraclavicular adenopathy. The chest CT studies were retrospectively assessed in conjunction with the US studies performed at our hospital in all patients with supraclavicular lesions by the single observer with more than 10 years of body cross-sectional imaging experience.

Various clinical, chest CT, and other radiologic findings were retrospectively tabulated by the aforementioned single observer for correlation with presence versus absence of cytologically proven malignant supraclavicular lymph nodes. The items tabulated included patient age, sex, tumor cell type, maximum dimension of dominant lung lesion and its lobar location, mediastinal and/or chest wall invasion, central versus peripheral versus both for lesion location, number of additional lung lesions (and number 1 cm), pleural effusion, hilar N stage, locations of mediastinal nodes greater than or equal to 1 cm, mediastinal N stage, adrenal gland status, and presence of known or possible extrapulmonary nonnodal metastases at chest CT or at any other modality. The size criterion for significant mediastinal lymph nodes was considered greater than or equal to 1-cm short axis and for the supraclavicular area, greater than or equal to 0.5-cm short axis.

US Examinations and Biopsy Techniques
All patients underwent mid to lower cervical and supraclavicular US examinations at our hospital with 5- and/or 7-MHz linear transducers (Acuson, Mountain View, Calif). Scanning was initially performed by our sonographers, with the patient supine, without a pillow if tolerated, and with arms down. Transverse and sagittal images were obtained from the carotid bifurcation to the sternoclavicular area inferiorly and laterally to the acromioclavicular joint. Location (including whether they were ipsilateral, contralateral, or bilateral with respect to the dominant lung lesion), short- and long-axis transverse node dimensions, and number of enlarged lymph nodes were documented. After reviewing these images, an attending radiologist (P.J.F., J.G.S., R.H.G., S.L.V., or D.J.R.) selectively imaged the areas of interest.

An additional informed consent was obtained for lymph node biopsy of the enlarged supraclavicular lesions. US biopsies were performed by an attending radiologist (P.J.F., J.G.S., R.H.G., S.L.V., D.J.R.) either alone or in conjunction with a radiology fellow or resident. By using a sterile technique and local anesthesia, US-guided fine-needle aspiration biopsy of the enlarged lymph nodes was performed in the majority of instances. When the needle aspirates were bloody, additional samples were sometimes obtained with a nonaspiration technique. US transducer biopsy guides were used.

Generally, the dominant lymph node ipsilateral to the tumor (if supraclavicular nodes were bilateral) was initially sampled by using 22-gauge spinal needles. A minimum of two samples were obtained, as is our usual practice (mean, 3.3; range, 2–5). The number of passes beyond the two was determined by means of physician preference, as influenced by a qualitative visual inspection of material as it was sprayed onto the slides. Preliminary cytopathologic interpretations were then provided.

Patients without enlarged lymph nodes and those with nondiagnostic lymph node aspirates proceeded to other invasive procedures for tissue diagnosis, if a diagnosis of malignancy had not been established previously. We assessed the final disposition of our study patients (those with surgical vs nonsurgical therapy), as well as percutaneous biopsy–related complications.

Statistical Methods
Statistical analysis was performed with a software package (S-Plus 3.4; MathSoft, Seattle, Wash). Ninety-five percent CIs were calculated for the prevalence of malignant and benign and/or indeterminate supraclavicular lymph nodes (15).

The Mann-Whitney test was used for numeric variables, and a Fisher exact test was used for the nonnumeric variables when associations of various clinical and radiologic findings were assessed with presence versus absence of supraclavicular nodal metastases. P values of less than .05 were considered to indicate statistically significant differences. Sensitivity and specificity were calculated for any parameters with statistically significant associations with nonpalpable malignant supraclavicular lymph nodes.


     RESULTS

Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
Supraclavicular Abnormalities
Twenty-two (40%) of 55 patients had supraclavicular lesions at CT and/or US. For the purpose of this discussion, the 22 patients who were considered to have enlarged lymph nodes included one patient with a metastasis to a lymph node at the thyroid margin or to the thyroid margin itself. In 18 (82%) of the 22 patients, the supraclavicular lymph node enlargement was prospectively recognized (n = 14) or retrospectively recognizable (n = 4) at CT. In the remaining four patients, the lymph nodes were not recognizable on CT scans, even in retrospect.

Seventeen (77%) of the 22 patients with enlarged supraclavicular lymph nodes had supraclavicular metastases (31% of the 55 patients, 95% CI: 19.1%, 44.1%). Fifteen (88%) of the 17 patients had supraclavicular metastases that were recognizable at CT. The types of malignancy in the 17 patients with metastatic supraclavicular adenopathy included 11 adenocarcinomas, three adenosquamous carcinomas, two poorly differentiated non–small cell carcinomas, and one small cell carcinoma. Five patients had nonmalignant supraclavicular lesions, three of whom had benign supraclavicular lymph nodes, one had cytologic findings suggesting cyst contents, and one had insufficient cytologic material as determined at US-guided biopsy. The lesion with the cytologic findings suggestive of cyst contents may have been a lymphocele or lymphangioma. The five cytopathologically benign and indeterminate supraclavicular lesions constituted 9% of the 55 patients (95% CI: 3.6%, 19.1%).

The mean short-axis dimension of the 17 malignant supraclavicular lymph nodes was 1.3 cm ± 0.43 (SD) (range, 0.7–2.0 cm). The five nonmalignant supraclavicular lesions had a mean short-axis dimension of 0.72 cm ± 0.26 (range, 0.5–1.1 cm). The mean short-axis dimension difference between the malignant and benign and/or indeterminate lesions was statistically significant (P < .012). However, four of the 17 malignant supraclavicular nodes proven at biopsy had dominant lymph node short-axis dimensions ranging from 0.7 to 1.0 cm.

In the 17 patients with malignant supraclavicular findings, the total number of enlarged supraclavicular lymph nodes at US ranged from one (n = 3) to more than 10 (n = 2) nodes. Ten of these 17 patients had bilateral supraclavicular adenopathy, and the remaining seven had unilateral adenopathy. In six of the seven patients with unilateral malignant adenopathy, the dominant lung lesion was ipsilateral to the adenopathy. Four of the five patients with benign or indeterminate supraclavicular needle biopsy results had a single lesion, and one patient had two enlarged lymph nodes. All five patients had unilateral supraclavicular findings at US. In three of the five patients with nonmalignant supraclavicular biopsy results, the dominant lung lesion was ipsilateral to the biopsy site.

Other Clinical, CT, and Radiologic Findings
The Table provides a statistical assessment of the potential associations of malignant supraclavicular lymph nodes with various clinical, chest CT, and other radiologic findings in patients with lung cancer in our study. Sensitivities and specificities were calculated for those parameters with statistically significant associations with malignant supraclavicular lymph nodes.


fig.ommitted Occurrence of Supraclavicular Metastases: Correlation Analysis, Sensitivities, and Specificities for Clinical, Chest CT, and Radiologic Parameters

 

 
Thirteen patients had small indeterminate nodular adrenal abnormalities. We took a worst-case scenario approach to these indeterminate lesions, and they were all assumed to be adrenal metastases, as listed in the last three rows of the Table.

Sixteen (46%) of the 35 patients with mediastinal adenopathy at CT had malignant supraclavicular lymph nodes. This mediastinal adenopathy was as likely to be unilateral (n = 8) as bilateral (n = 8) in the patients with supraclavicular metastases. Five of the patients with supraclavicular metastases and mediastinal adenopathy had T1 lung lesions (3 cm) at CT. The only patient with a supraclavicular metastasis without recognizable mediastinal adenopathy had a 7.7-cm right lung tumor that abutted and may have invaded the upper mediastinum and had right hilar adenopathy at CT. Furthermore, 48% of patients with known or possible extrapulmonary nonnodal metastases at chest CT (12 of 25 patients) or at any modality (13 of 27 patients) had malignant supraclavicular lymph nodes.

All four of the enrolled patients admitted to our hospital with a chief complaint relating to symptoms of brain metastases had malignant supraclavicular adenopathy. There were 26 patients without pathologic proof of a malignant supraclavicular lymph node in whom the final assessment indicated the presence of an unresectable lung cancer (n = 19) or who were not surgical candidates because of their medical circumstances (n = 7).

Other Primary Diagnostic and Surgical Procedures
Five of 17 patients with supraclavicular metastases underwent other invasive procedures before their supraclavicular lymph node biopsies. Two of the five patients underwent diagnostic bronchoscopies and were being considered for surgery until the supraclavicular biopsies were performed. The remaining three patients underwent nondiagnostic bronchoscopies. In addition, one of five patients with a nonmalignant result at supraclavicular biopsy underwent a nondiagnostic bronchoscopy before enrolling in our study.

Thirty-eight of 55 patients did not have enlarged malignant supraclavicular lymph nodes (n = 33) or had benign or indeterminate supraclavicular biopsy results (n = 5), and their malignancy was diagnosed with other methods. These methods included percutaneous transthoracic fine-needle aspiration biopsy with fluoroscopic (n = 17), US (n = 7), or CT (n = 4) guidance; percutaneous US-guided fine-needle biopsy of abdominal metastatic disease (n = 5); percutaneous US-guided fine-needle biopsy of a skeletal metastasis (n = 1); bronchoscopy (n = 3), and sputum cytology (n = 1). Sixteen of these 38 patients subsequently underwent an intraoperative procedure. These 16 patients comprised 29% of the original 55 patients (31% of the 51 patients with non–small cell carcinoma). Twelve of the 16 patients underwent lobectomy or pneumonectomy, and four were found to have unresectable disease intraoperatively. The 12 patients who underwent lobectomy or pneumonectomy comprised 22% of the original 55 patients (24% of the 51 patients with non–small cell carcinomas).

Percutaneous Biopsy Complications
There were no complications from the US-guided supraclavicular lymph node fine-needle biopsies (n = 22) or in those patients who underwent US-guided abdominal (n = 5) or skeletal (n = 1) metastasis biopsies.

Of the 28 patients undergoing percutaneous transthoracic needle biopsy with various methods (fluoroscopy, US, or CT), eight (29%) patients had a pneumothorax as a complication of the procedure and four (14%) required chest tube placement.


     DISCUSSION

Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 
Lymph node status has an important role in defining lung cancer treatment options. The supraclavicular lymph nodes are an important component of the lymphatic drainage of the chest and are usually superficially located. Supraclavicular lymph node metastases in lung cancer indicate at least stage IIIB disease; and metastatic cervical lymph nodes above the supraclavicular level, stage IV disease (13). Nonsurgical therapy is usually chosen for stages IIIB and IV lung cancer. Therefore, assessment of supraclavicular and adjacent cervical lymph nodes at chest CT combined with US and guided fine-needle biopsies can be of value in establishing both a diagnosis and a critical stage threshold for defining therapeutic options.

Supraclavicular and cervical lymph node metastases (combined palpable and nonpalpable) from lung cancer have been reported with variable frequencies, even in up to 75% of patients, in the surgical literature (8). Most palpable supraclavicular lymph nodes will usually yield a diagnosis of malignancy (5) and can initially be sampled with palpation-guided needle biopsy (16). The results of one study (16) showed that 51 (13%) of approximately 400 patients presenting with lung cancer had palpable supraclavicular or cervical metastases diagnosed with palpation-guided needle sampling.

In the past, nonpalpable supraclavicular lymph nodes have been sampled with open surgical biopsy and also with US guidance (58,10,11,1720). Conclusions regarding surgical biopsies of nonpalpable supraclavicular lymph nodes in patients with lung cancer have varied, from suggestions that biopsy be performed in this area in all patients with primary lung lesions over 3 cm who are being considered for thoracotomy (5) to suggestions that biopsy not be performed in this area because of a low diagnostic yield (18,19).

Some investigations performed in the era of CT indicate that surgically directed supraclavicular biopsies may be of value in certain circumstances for patients for whom resection of the primary tumor is being strongly considered (17,20). One group advocated surgical biopsy of nonpalpable supraclavicular nodes for potentially resectable lung cancers larger than 3 cm when the cell type is adenocarcinoma or an unknown malignancy (20). Other investigators concluded that an ipsilateral scalene node biopsy with the mediastinoscope is useful for patients with N2 or N3 lymph node metastases proven at mediastinoscopy and a central nonsquamous cell primary tumor who are being considered for surgical resections (17).

As was determined at the end of the clinical and radiologic assessments, our study population was a mixture of patients who were surgical (29%) and nonsurgical (71%) candidates. We found nonpalpable metastatic supraclavicular lymph node involvement in 31% of patients with lung cancer (Figs 1, 2). Of patients with malignant and benign supraclavicular findings, 82% had at least a portion of their supraclavicular abnormalities recognizable at chest CT. When considering only patients with malignant supraclavicular findings, 88% of the findings were recognizable at chest CT. Other chest CT findings associated with malignant supraclavicular nodes that had statistical significance included enlarged mediastinal lymph nodes and nonnodal extrapulmonary lesions that were either potential or proven metastases.

At least three prior investigations have addressed the use of cervical and supraclavicular US in patients with lung cancer (1012). In one study, six (12%) of 51 patients with non–small cell lung cancer had metastatic nonpalpable supraclavicular lymph nodes, as determined at US-guided fine-needle biopsy (10). Another group of investigators reported a US study of neck and supraclavicular nodes, which included 25 patients who had lung cancer with palpable lymph nodes and 12 patients with no palpable nodes (11). In a third study, clinical palpation of the supraclavicular area was compared with US in 81 patients (12).

There is also a report of the successful use of US and neck CT to assess for metastatic supraclavicular and cervical adenopathy in patients with esophageal cancer (21). These investigators identified 11 (85%) of 13 patients with metastatic supraclavicular lymph nodes at CT by using a short-axis size criterion for significance of greater than or equal to 0.5 cm (21). This combination of procedures may have applications to other tumors besides those of the lung and esophagus, which may metastasize to supraclavicular lymph nodes, including breast, prostate, gynecologic, stomach, and pancreatic malignancies. The combination of chest CT and US may also be of value in sarcoidosis, where supraclavicular adenopathy is common (7,8,22).

US-guided fine-needle biopsy of supraclavicular lymph nodes is a simple and safe procedure that can usually be performed by a single operator. These nodes are nearly always superficial (most are less than 3 cm from the skin) at US. The procedure can be performed with the patient sitting up if he or she is unable to lie supine.

In our series of US-guided supraclavicular biopsies there were no complications. Although complications are likely to be uncommon with US-guided supraclavicular needle biopsies, there have been some infrequent complications with surgical biopsies that could apply to US-guided biopsies. These complications include bleeding; infection; pneumothorax; lymphatic duct injury; air embolism; and impairment of phrenic nerve, recurrent laryngeal nerve, and sympathetic chain (Horner syndrome) function either by means of injury or infiltration of local anesthesia (57,17,19). Impairment of phrenic or recurrent laryngeal nerve function could be of particular importance in a patient with underlying abnormal pulmonary function (5).

The complications identified in the 28 patients who underwent percutaneous transthoracic needle biopsy included a 29% pneumothorax rate, with 14% of the 28 patients receiving a chest tube. For these reasons alone, when it is feasible, US-guided supraclavicular needle biopsy is an attractive alternative to transthoracic needle biopsy.

Limitations of our study include the fact that we were at a tertiary care center and there could have been unintentional and other unidentified selection biases toward patients with advanced disease or an unusual case mix. Approximately 20%–25% of patients presenting with lung cancer have small cell lung cancer (2). We excluded patients with known small cell lung cancer from our study, and only four (7%) of 55 eligible patients had this diagnosis established after enrollment.

Of our 51 study patients with non–small cell lung cancer, 31% were considered surgical candidates and 24% underwent lobectomy or pneumonectomy for cure. The percentage of surgical candidates and the percentage of patients undergoing surgery for cure in our study are in the range of previously noted statistics for non–small cell lung cancer patients at presentation (2325). The suggested percentages of patients who present with non–small cell lung cancer who are candidates for surgery vary, ranging from about 15% to 40% (2325). One estimate of the percentage of patients who are able to undergo a curative surgical procedure at presentation is 20% (25). This suggests that patients in our study with non–small cell lung cancer were a representative sample of this group at presentation. Findings from our county tumor registry data for the year preceding our study also suggest that our case mix of patients was a fairly representative sample. When similar selection criteria were applied to our tumor registry data, we found that 12% (60 of 485) of patients had a small cell cancer and 31% (133 of 425 patients) with a non–small cell lung cancer underwent lobectomy or pneumonectomy.

We determined that a physician had examined but not palpated supraclavicular masses in our patients. A potential limitation is that we did not suggest a standardized approach to the physical examination. We are aware that physicians with various levels of experience and varying expertise had performed the physical examinations, as is often the case in medical practice. We know of at least two successful palpation-guided supraclavicular lymph node biopsies performed during our study in patients with lung cancer. The available databases did not allow for a complete search for the total number of contemporaneous palpation-guided supraclavicular node biopsies.

Other limitations were that the CT examinations were performed both at our hospital and at various other facilities with a variety of techniques, and the findings were summarized by a single observer. Some CT studies began at the lung apices, and in others, the supraclavicular area detail was obscured by streak artifacts because of variable technical quality. This study was not designed to be a formal multiple-observer evaluation of CT sensitivity and specificity for supraclavicular lymph nodes or to determine optimal scanning techniques. We anticipate that with optimization of CT scanning techniques, future studies will likely reproduce and improve our results.

We concluded that the majority of patients in our study with malignant supraclavicular biopsy results had lung cancer on the basis of typical intrathoracic CT findings (two had diagnostic bronchoscopies before enrollment). While this can be seen as a limitation, we chose not to have patients undergo an additional invasive procedure to correlate intrathoracic disease cell types with malignant supraclavicular biopsy results. The lack of an independent pathologic standard to confirm the cytologically benign and indeterminate supraclavicular needle aspiration samples was an additional limitation of our study.

It is likely that positron emission tomography, or PET, with 2-[fluorine-18]fluoro-2-deoxy-D-glucose will become more routinely used for staging of non–small cell lung cancer because of its value in depicting unsuspected metastases (26,27). CT and US will continue to be of value, because biopsy-proven supraclavicular disease obviates some PET scans.

In conclusion, we found that 31% of patients in our study had supraclavicular metastases. Our results and a review of the literature support the use of chest CT and US-guided fine-needle biopsy of nonpalpable supraclavicular lymph nodes in many patients presenting with lung cancer, even if the prevalence is only 12% (10) or 19.1% (the lower limit of our 95% CI). Our experience has been that beginning chest CT examinations at least 2 cm above the lung apices facilitates recognition of supraclavicular lymph nodes. A careful review of the supraclavicular area at chest CT will usually reveal any nonpalpable adenopathy, which can then be sampled with US-guided needle biopsy.

US can sometimes depict supraclavicular adenopathy that is not evident at CT. Metastatic supraclavicular adenopathy was found in 46% of patients with mediastinal adenopathy at CT and in 48% with suspected extrapulmonary nonnodal metastases. Therefore, supraclavicular US and a possible biopsy are worthwhile in patients without obvious supraclavicular adenopathy at CT who have mediastinal adenopathy and in those with suspected extrapulmonary nonnodal metastases (eg, symptomatic brain metastases) when there are no known lesions elsewhere that are easily accessible for biopsy.

US-guided needle biopsy of enlarged supraclavicular lymph nodes is a simple and safe alternative to other more invasive procedures; it can sometimes simultaneously establish a tissue diagnosis and lung cancer nonresectability (at least stage IIIB disease) and thus aid in appropriate therapeutic patient triage.

 

     ACKNOWLEDGMENTS
 
We thank Richard F. Raubertas, PhD, for his assistance with preparation of the statistical analysis. We are grateful for the efforts of our skilled US and CT staff. We also thank Jeanette Griebel, Iona Mackey, and Margaret Kowaluk of the radiology department, along with Marjorie Worden and the other office staff of the thoracic surgery section for secretarial, clerical, and/or technical assistance with the manuscript’s preparation.

 

     REFERENCES

Top
ABSTRACT
INTRODUCTION
MATERIALS AND METHODS
RESULTS
DISCUSSION
REFERENCES
 

  1. Greenlee RT, Murray T, Bolden S, Wingo PA. Cancer statistics, 2000. CA Cancer J Clin 2000; 50:7-33.

  2. American College of Radiology. ACR appropriateness criteria 2000: staging of bronchogenic carcinoma, non-small cell lung carcinoma. Radiology 2000; 215(suppl):611-619.

  3. Pretreatment evaluation of non-small-cell lung cancer: the American Thoracic Society and the European Respiratory Society. Am J Respir Crit Care Med 1997; 156:320-332.

  4. Mountain CF. Revisions in the international system for staging lung cancer. Chest 1997; 111:1710-1717.

  5. Brantigan JW, Brantigan CO, Brantigan OC. Biopsy of nonpalpable scalene lymph nodes in carcinoma of the lung. Am Rev Resp Dis 1973; 107:962-974.

  6. Pualwan FA, Sherman CD, Jr, Emerson GL, DeWeese JA, Schwartz SI, Walton BE. Scalene node biopsy: implications in abdominal and thoracic disease. Cancer 1958; 11:4-11.

  7. Rochlin DB, Enterline HT. Prescalene lymph node biopsies. Am J Surg 1958; 96:372-378.

  8. Miller WE, Taylor AM. Biopsy of scalene and supraclavicular lymph nodes: value in diagnosis. Cleve Clin Q 1965; 32:205-209.

  9. Goldberg RP, Austin RM. Computed tomography of axillary and supraclavicular adenopathy. Clin Radiol 1985; 36:593-596.

  10. Chang DB, Yang PC, Yu CJ, Kuo SH, Lee YC, Luh KT. Ultrasonography and ultrasonographically guided fine-needle aspiration biopsy of impalpable cervical lymph nodes in patients with non-small cell lung cancer. Cancer 1992; 70:1111-1114.

  11. Sugama Y, Kitamura S. Ultrasonographic evaluation of neck and supraclavicular lymph nodes metastasized from lung cancer. Intern Med 1992; 31:160-164.

  12. Monso E, Montserrat JM, Abad J, Texidó A, Roig J, Morera J. Usefulness of supraclavicular ultrasonography in the staging of lung cancer. Lung 1992; 170:243-244.

  13. Mountain CF, Dresler CM. Regional lymph node classification for lung cancer staging. Chest 1997; 111:1718-1723.

  14. Som PM, Curtin HD, Mancuso AA. Imaging-based nodal classification for evaluation of neck metastatic adenopathy. AJR Am J Roentgenol 2000; 174:837-844.

  15. Casella G. Refining binomial confidence intervals. Can J Stat 1986; 14:113-129.

  16. Rohwedder JJ, Handley JA, Kerr D. Rapid diagnosis of lung cancer from palpable metastases by needle thrust. Chest 1990; 98:1393-1396.

  17. Lee JD, Ginsberg RJ. Lung cancer staging: the value of ipsilateral scalene lymph node biopsy performed at mediastinoscopy. Ann Thorac Surg 1996; 62:338-341.

  18. Ikard RW. The Nashville experience with scalene node biopsy: a procedure of limited application. J Tenn Med Assoc 1985; 78:73-77.

  19. Bernstein MP, Ferrara JJ, Brown L. Effectiveness of scalene node biopsy for staging lung cancer in the absence of palpable adenopathy. J Surg Oncol 1985; 29:46-49.

  20. Schatzlein MH, McAuliffe S, Orringer MB, Kirsh MM. Scalene node biopsy in pulmonary carcinoma: when is it indicated?. Ann Thorac Surg 1981; 31:322-324.

  21. Van Overhagen H, Laméris JS, Berger MY, et al. Supraclavicular lymph node metastases in carcinoma of the esophagus and gastroesophageal junction: assessment with CT, US and US-guided fine-needle aspiration biopsy. Radiology 1991; 179:155-158.

  22. Lohela P, Tikkakoski T, Strengell L, Mikkola S, Koskinen S, Suramo I. Ultrasound-guided fine-needle aspiration cytology of non-palpable supraclavicular lymph nodes in sarcoidosis. Acta Radiol 1996; 37:896-899.

  23. Singhal S, Kaiser LR. Multimodality therapy for non-small cell lung cancer. In: Shields TW, LoCicero J, Ponn RB, eds. General thoracic surgery. 5th ed. Philadelphia, Pa: Lippincott Williams & Wilkins, 2000; 1415-1442.

  24. Evans WK. Adjuvant chemotherapy: results and perspectives. Lung Cancer 1995; 12(suppl 1):S35-S45.

  25. Spiro SG. Bronchial tumours. In: Brewis RAL, Corrin B, Geddes DM, Gibson GJ, eds. Respiratory medicine. 2nd ed. London, England: Saunders, 1995; 924-961.

  26. Lowe VJ, Naunheim KS. Positron emission tomography in lung cancer. Ann Thorac Surg 1998; 65:1821-1829.

  27. Pieterman RM, van Putten JWG, Meuzelaar JJ, et al. Preoperative staging of non-small cell lung cancer with positron-emission tomography. N Engl J Med 2000; 343:254-261.
作者: Patrick J. Fultz MD Richard H. Feins MD John G 2007-5-12
医学百科App—中西医基础知识学习工具
  • 相关内容
  • 近期更新
  • 热文榜
  • 医学百科App—健康测试工具