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Ann Thorac Surg 2004;77:1763-1768
© 2004 The Society of Thoracic Surgeons
a Divisions of Gastroenterology and Hepatology, Medical University of South Carolina, University of South Carolina, Charleston, South Carolina, USA
b Thoracic Surgery, Medical University of South Carolina, University of South Carolina, Charleston, South Carolina, USA
c Pulmonary Medicine and Critical Care, Medical University of South Carolina, University of South Carolina, Charleston, South Carolina, USA
d Department of Radiology, Medical University of South Carolina, University of South Carolina, Charleston, South Carolina, USA
e Department of Pathology and Laboratory Medicine, Medical University of South Carolina, University of South Carolina, Charleston, South Carolina, USA
Accepted for publication October 2, 2003.
* Address reprint requests to Dr Wallace, Director of Endoscopic Research, Mayo Clinic, Jacksonville, 4500 San Pablo Rd, Jacksonville, FL 32224, USA
e-mail: wallace.michael{at}mayo.edu
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Abstract |
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METHODS: Patients with NSCLC and CT scan showing no enlarged mediastinal lymph nodes (> 1 cm for all nodes except > 1.2 cm for subcarinal) in the mediastinum underwent EUS. Fine needle aspiration was performed on at least one lymph node, if present, in the upper mediastinum, aortopulmonary window, subcarinal, and periesophagus regions. Each specimen was evaluated with on-site cytopathology and confirmed with complete cytopathologic examination.
RESULTS: Sixty-nine patients without enlarged mediastinal lymph nodes were evaluated. Endoscopic ultrasound detected malignant mediastinal lymph nodes in 14 of 69 patients as well as other advanced (American Joint Committee on Cancer [AJCC] stage III/IV) in 3 others (1 left adrenal, and 2 with mediastinal invasion of tumor) for a total of 17 of 69 (25%, 95% confidence interval: 16% to 34%) patients. Eleven additional patients were found to have advanced disease by bronchoscopy (2), mediastinoscopy (2), and thoracotomy with mediastinal lymph node dissection (7). The sensitivity of EUS for advanced mediastinal disease was 61% (49% to 75%), and the specificity was 98% (95% to 100%).
CONCLUSIONS: Endoscopic ultrasound guided fine needle aspiration can detect advanced mediastinal disease and avoid unnecessary surgical exploration in almost one of four patients who have no evidence of mediastinal disease on CT scan. In addition to previously reported results in patients with enlarged lymph nodes on CT, these data suggest that all potentially operable patients with nonmetastatic NSCLC may benefit from EUS staging.
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Introduction |
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Computed tomography (CT) is the principal initial method of staging the mediastinum in most centers. It depends upon lymph node size for detection of abnormality, with more than 1 cm in short axis diameter being the most common criterion of lymph node enlargement. However, small lymph nodes are known to harbor metastatic foci and enlarged nodes may be benign, especially when an inflammatory component accompanies central tumors. Therefore, the accuracy of CT for mediastinal disease is low. In a recent meta-analysis of 20 studies and 3,829 patients by Toloza and colleagues [3], sensitivity was 0.57 and specificity 0.82. The negative predictive value of CT scans in the same meta-analysis was 82% (range, 63% to 85%). Thus, approximately 18% (range, 15% to 37%) of patients with a negative CT will have disease found if they undergo completed mediastinal staging (by surgery).
In order to decrease the finding of unexpected N2 disease at surgery, more aggressive mediastinal staging is often performed. Mediastinoscopy remains the gold standard for evaluation of nodal disease. It has a sensitivity of 90% to 95% [4]. However, only certain mediastinal lymph node stations are accessible (levels 2, 4, and anterior level 7). For sampling of levels 5 and 6, thoracoscopy, anterior mediastinotomy (Chamberlain procedure), or extended mediastinoscopy can be performed. The inferior mediastinum is easily evaluated by thoracoscopy. However, all these more aggressive staging procedures require general anesthesia, surgical incision, and are associated with higher costs [5, 6]. It was anticipated that positron emission tomography (PET) would increase the accuracy of mediastinal staging in NSCLC, and indeed, meta-analysis has confirmed its superiority [3]. However, more recent reports have tempered enthusiasm for using PET as the sole tool for evaluating the mediastinum [7].
We, and others [8–11], have previously reported that an outpatient procedure, endoscopic ultrasonography with fine-needle aspiration (EUS-FNA) is a highly accurate and safe method for lymph node sampling of patients with enlarged mediastinal lymph nodes on CT. However, very little information exists on the routine use of EUS-FNA in CT-negative scans. The specific aim of this study was to determine the prevalence and predictors of malignant mediastinal lymph nodes as detected by EUS-FNA in patients with NSCLC and CT scans showing no mediastinal lymph node enlargement.
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Material and methods |
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Noninvasive imaging
Computer tomographic examinations were performed in all patients and TNM staging, including the identification of distant metastases, was prospectively reported by a single thoracic CT radiologist, including those CT exams performed off site. On-site CT examinations were performed with a Picker PQ6000, Marconi MX8000, or Marconi MX8000D helical scanner using a single breath-hold technique (Phillips Medical Systems, Andover, MA). The use of intravenous contrast was at the discretion of the radiologist responsible for CT that day. Therefore, intravenous contrast was not utilized in all cases. Off-site CT scans were evaluated by the same radiologist for quality of the examination and included if they were of similar quality to onsite CT studies. If the quality of an off-site CT was inadequate, an on-site CT was performed. Lymph nodes were considered enlarged if the short axis diameter was greater than or equal to 1 cm in all mediastinal stations (levels 2, 3, 4, 5, 6, 8, 9) or greater than or equal to 1.2 cm in the subcarina (level 7).
Positron emission tomography (PET) was not routinely performed as part of the staging protocol; however, it was applied in selected cases at the discretion of the treating physician. Positron emission tomography was generally used when the CT scan identified suspicious but less than 1 cm mediastinal lymph nodes (typically a borderline 8 to 9 mm in a location other than subcarina) or the patient was considered high risk for invasive staging based on comorbid disease. In each case, sites of PET activity were confirmed by invasive staging (EUS-FNA or surgical biopsy).
EUS-FNA staging
After informed consent, transesophageal EUS was performed on an outpatient basis under conscious sedation as described previously [9]. Briefly, EUS was performed with radial instruments (Olympus, GF UM 30, 130, 160, Olympus Co. Melville, NY) to locate lymph nodes, followed by EUS-FNA with a linear-array echoendoscope (Olympus GF UC30P, UCT30), or with linear EUS-FNA only. The left adrenal gland was also routinely inspected from a position within the mid body of the stomach. If a mass was identified in the left adrenal (M1), this site was sampled with FNA first. In cases where the primary tumor was located medially, mediastinal invasion (T4) was considered definite when tumor could be seen within a mediastinal organ (esophagus, aorta, heart, vena cava). Mediastinal invasion of the tumor was considered possible when there was loss of the normal hyperechoic border between the tumor and the mediastinal pleura.
Lymph nodes were characterized according to features suggestive of malignancy (size > 1 cm, round shape, sharp margin, diffusely hypoechoic). The location of the lymph node (ATS levels) and side (ipsilateral-contralateral) were also characterized and classified as either N2 or N3. Lymph nodes with at least one feature suggestive of malignancy were sampled according to the following scheme. Contralateral lymph nodes were sampled first, and immediately stained and read by an onsite pathologist. If no malignant cells were seen, any suspicious midline (subcarinal) or ipsilateral lymph nodes were then sampled. All aspirates were stained immediately using a Diffquik stain (Baxter Healthcare Corp., Miami, FL) for immediate interpretation. Aspirates were obtained until a preliminary cytologic diagnosis of malignancy was given or until the cytologist felt that an adequate quantity of representative tissue had been obtained (usually 4 to 5 aspirates per lesion). The definitive cytologic diagnosis was given only after complete staining and interpretation were performed in the pathology department later. Lymph nodes were considered malignant only if the cytology or surgically resected sample showed malignant cells. Lymph nodes were considered benign if both the cytology and all surgically resected lymph nodes from that level were negative for malignancy.
Surgery and other invasive staging methods
Patients with lesions near the carina underwent bronchoscopy. Otherwise, patients without confirmed distant metastases, mediastinal lymph node metastases, or definite mediastinal invasion of tumor on EUS-FNA underwent surgical exploration. Mediastinoscopy was performed in selected cases where a suspicious lymph node on CT or PET was present in the pretracheal (levels 2, 4) or anterior subcarina (level 7) but not confirmed by EUS-FNA. Left anterior mediastinotomy (Chamberlain procedure) or left thoracoscopy was performed in cases of suspicious lymph nodes in the aortopulmonary window. In the absence of suspicious lesions, or with a negative mediastinoscopy (thoracoscopy), open thoracotomy with mediastinal lymph node resection was performed.
Statistical analysis
Demographic and proportional data were tabulated using Microsoft Access and Excel (Microsoft Co., Redmond, WA). Univariate analyses were performed using SPSS version 11.5 (SPSS Inc., Chicago, IL). The 
2, or Fischer's exact test where appropriate, were used to compare proportional data. The type I error was set at 0.05 for all analyses. Confidence intervals were calculated to 95% using standard formulas [12]. The sample size of the study was based on the number needed to obtain prevalence estimates with 95% confidence intervals with ±10% precision. We estimated, based on preliminary observations, that EUS-FNA would identify approximately 15% of CT-negative patients with mediastinal metastases [13]. The sample size necessary for this precision was approximately 50 patients.
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Results |
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Overall, 28 of 69 patients had advanced clinical disease (AJCC stage III or IV) (N2 to 3 [23], T4 [3], M1 [2]) and EUS-FNA identified 17 of 28 (sensitivity 61%, 95% CI 49% to 75%). Overall, 14 lymph nodes were identified by EUS, 2 by mediastinoscopy, and 7 by thoracotomy. The sensitivity of EUS-FNA for mediastinal lymph nodes was also 61% (14 of 23). Endoscopic ultrasonography correctly identified 40 of 41 patients without advanced stage disease (specificity 98%, 95% CI: 95% to 100%). Of the nine patients in whom EUS failed to detect mediastinal lymph node metastases, 5 had metastases to the aortopulmonary window or subcarinal lymph nodes, and all 5 had undergone EUS-FNA of lymph nodes in the respective regions. Final pathology revealed multiple benign, as well as at least one malignant, lymph node present in each region. Four patients had metastases to level 2 or 4 (upper or lower pretracheal) lymph nodes that were not seen or sampled with EUS-FNA.
Left upper lobe tumors were more likely than other locations to be associated with EUS-FNA detected mediastinal lymph node metastases (p = 0.02). Other factors, such as performance of CT onsite or offsite, T-stage as determined by CT, or tumor histology were not associated with EUS-FNA detected mediastinal lymph node metastases (Table 2).
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Comment |
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Surgical resection of NSCLC offers the best chance for cure in patients with tumor confined to the lung and lymph nodes confined to the ipsilateral lung and hilum. Metastases to mediastinal lymph nodes, distant sites, or tumor invasion into the mediastinum, confer a worse prognosis, and typically treatment is chemoradiotherapy. Although surgery is performed in selected cases of ipsilateral, isolated mediastinal lymph node metastases [14], it is unknown if this is more effective than radiochemotherapy alone.
The treatment implications for identifying small, malignant lymph nodes are unclear. Bulky mediastinal lymphadenopathy (> 2- to 3-cm nodes) is an independent predictor of poor outcome [15]. It is possible that patients with limited N2 lymph nodes, such as those identified in this study, have even better prognosis than 1 to 2 cm lymph nodes. In this group, surgical therapy may be a reasonable alternative to radiochemotherapy, although trials to compare these therapies have been limited by insufficient power [16, 17].
Identification of mediastinal lymph node metastases is thus critical to the management of NSCLC. Computer tomographic scans, and more recently PET, have been the most frequently utilized noninvasive methods to evaluate the mediastinum. However, both have limited accuracy. Computed tomographic scan staging is based on the size of the lymph node to determine the presence of malignancy. As noted, its sensitivity and specificity are low [3]. Positron emission tomography scanning relies on increased metabolic activity in the lymph node to determine malignancy. False negative PET scans are particularly common in lymph nodes with small metastatic foci, and false positives can occur in inflamed, but otherwise nonmalignant lymph nodes. In a large meta-analysis, the sensitivity of PET for mediastinal lymph node metastases is reported to be 84% (78% to 89%), with a specificity of 89% (83% to 93%) [3]. Pathologic confirmation is recommended in the setting of enlarged or PET positive mediastinal lymph nodes [18]. In the setting of a CT scan with no mediastinal nodal enlargement, further invasive mediastinal staging is controversial and may depend upon such factors as tumor size and location, histology, and surgeon philosophy.
In patients without evidence of enlarged mediastinal lymph nodes on CT scan, surgical exploration and resection can be considered the standard of care [19]. Unfortunately, the limited accuracy of noninvasive staging results in occult malignant mediastinal lymph nodes detected at the time of surgery. If metastases are found before lung resection, the procedure can be aborted. However, malignant lymph nodes may be detected only after open thoracotomy, resection of the primary tumor, and mediastinal lymph node dissection. Improved methods of preoperative detection would reduce the rate of aborted or unnecessary surgical explorations.
Endoscopic ultrasound guided fine-needle aspiration has been extensively evaluated as a minimally invasive method of mediastinal lymph node sampling in lung cancer [8–11]. The EUS-FNA is able to routinely access posterior mediastinal lymph nodes (levels 5, 7, 8, 9), as well as the left adrenal gland. The principal advantage of EUS-FNA over noninvasive methods is the ability to obtain pathologic confirmation of malignant disease. Compared to minimally invasive surgical methods such as mediastinoscopy or thoracoscopy, EUS requires only conscious sedation, can be routinely performed on an outpatient basis, and has been shown to be more cost effective [5, 6].
A disadvantage of FNA based approaches is the potential for false positive diagnoses. Although pathology (particularly histology) is routinely considered the "gold standard" for diagnosing malignancy, false positives can occur. In a recent study of EUS-FNA versus histology, the rate of false positive lymph node aspirates was 0.7% [20]. Our group has recently combined EUS-FNA specimens with reverse transcription-polymerase chain reaction (RT-PCR) of a cancer specific gene panel. This "molecular profiling" of lymph nodes may allow more sensitive detection of metastases, even in lymph nodes with no pathologic evidence of malignancy [21].
Mediastinoscopy with or without thoracoscopy can also be considered a principal method of mediastinal lymph node sampling. Advantages of this approach include the ability to obtain whole lymph nodes, which may increase detection of small foci of metastatic cancer deposits, compared to cytologic sampling. Indeed, 5 of 69 patients in out study had negative cytologic sampling of mediastinal lymph nodes in regions subsequently found to be malignant when the entire lymph node was resected. Mediastinoscopy and thoracoscopy also have access to lymph nodes which are not routinely accessible to EUS-FNA (pretracheal levels 2 and 4, level 6). In our study, 4 of 69 patients had lymph node metastases to sites that were not seen by EUS-FNA. Fundamentally, these methods of mediastinal access are complementary, with EUS-FNA having better access to the posterior and inferior lymph nodes, and mediastinoscopy (thoracoscopy) having better access to the anterior and superior lymph nodes. We believe a rational strategy is to begin mediastinal lymph node sampling with the less invasive and less costly method (EUS-FNA) and proceed to invasive surgical procedures when EUS-FNA is negative.
The prevalence of mediastinal lymph node metastases in our series is higher than in other surgical series, evaluating patients with negative mediastinal CT which report metastases found at the time of surgery in 15% to 20% of CT-negative patients [22]. One possibility is that we included patients with borderline lymph node enlargement. Patients were frequently referred with CT scans interpreted from outside facilities as showing "shoddy" lymph node enlargement. However, our use of standardized size measurements and a rigorous definition of enlargement found that many of these were not more than 1 cm (or > 1.2 cm for subcarina). Exclusion of these cases from other studies, or inclusion in our study, would increase the relative prevalence of malignant mediastinal lymph nodes in our study. Another possibility is that lymph nodes were more intensively sampled in our study, resulting in stage migration.
A limitation of our study is the lack of routine PET scanning. Although PET has become increasingly available and approved for lung cancer staging, it is still not routinely performed in practice. Recent guidelines for staging of NSCLC recommend PET staging, but found the evidence to support this only moderate [18]. Furthermore, the limitations in accuracy discussed above make it unlikely that PET, even in combination with CT, will replace the need for tissue sampling. A recent triple blinded trial of all three modalities suggests that EUS-FNA is still more accurate than CT and PET combined [23].
Like PET, EUS expertise is not universally available, however, many academic medical centers are able to provide this service. Recent efforts by the American Society for Gastrointestinal Endoscopy (ASGE) to offer training programs, multiple university-based training programs, and electronic training materials (video CD, DVD, simulators) have and will continue to improve availability.
Endoscopic ultrasound, even in expert hands, is not perfect. The sensitivity in our study for EUS was only 61%. In other studies, including our own, which evaluated patients with enlarged lymph nodes [9], the sensitivity of EUS for mediastinal lymph node metastases is much higher. We believe this difference is due to the selection, in this study, of patients with small lymph nodes. Small lymph nodes are more difficult to identify with any imaging modality (including EUS), likely contain a small number of malignant cells, and may be more difficult to target for FNA. Nonetheless, EUS-FNA identified nearly one in four patients with advanced disease whose CT failed to detect such disease. An alternative approach would be to perform invasive surgical staging in all patients, which would likely increase sensitivity but would be more invasive and costly.
In order to improve the sensitivity of EUS, we performed a detailed analysis of false negative EUS-FNA cases to determine the cause. Approximately half (5 of 9) were due to EUS-FNA sampling the correct region (eg, subcarina), but missing the malignant lymph node, either due to sampling error within a given lymph node or sampling a nonmalignant lymph node among a cluster of malignant and nonmalignant lymph nodes. This could be potentially improved by more extensive sampling of more lymph nodes. The remaining 4 of 9 cases were missed due to the inability of EUS to "see" lymph nodes in the pretracheal region. This could potentially be improved by combining EUS with bronchoscopy, bronchoscopic ultrasound, or mediastinoscopy.
This preliminary study suggests that EUS-FNA is capable of detecting advanced disease (mediastinal lymph node metastases, adrenal metastases, mediastinal invasion of tumor) in approximately one in four patients whose CT scan suggests early stage disease. Further study is required to confirm these findings and to compare EUS directly with minimally invasive surgical staging, transbronchial biopsy, and emerging technologies such as bronchoscopic ultrasound. Further study is also needed to compare therapies (surgery alone, chemoradiotherapy alone, or combinations) in patients with limited stage IIIa disease. However, these findings combined with previously reported results [9], suggest that EUS-FNA may be considered in the preoperative staging of all patients both with and without mediastinal lymph node enlargement on CT scan.
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