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Ultrasonography |
1 From the Division of Gastroenterology and Hepatology, Mayo Clinic, 200 First St SW, Eisenberg 8A, Rochester, MN 55905 (M.J.W., E.V.S.); and St Vincent Hospitals, Indianapolis, Ind (M.J.W., L.M.W.). Received March 9, 2000; revision requested April 5; final revision received August 4; accepted September 12. Address correspondence to M.J.W. (e-mail: wiersema.maurits@mayo.edu).
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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MATERIALS AND METHODS: Eighty-six consecutive patients with mediastinal lymphadenopathy who did not have a primary gastrointestinal neoplasm were examined. In 29 patients, endoscopic US–guided FNAB of mediastinal lymphadenopathy was performed as a component of staging non–small cell lung cancer (NSCLC); in the remaining 57 patients, it was performed to obtain a primary diagnosis. Final diagnosis was based on clinical follow-up, cytologic, and/or surgical results.
RESULTS: In 82 patients in whom a final diagnosis was available, the sensitivity, specificity, accuracy, negative predictive value, and positive predictive value of endoscopic US–guided FNAB in distinguishing benign from malignant mediastinal lymph nodes were 96%, 100%, 98%, 94%, and 100%, respectively. In those patients who underwent staging of NSCLC, endoscopic US–guided FNAB had superior mediastinal lymph node staging accuracy compared with endoscopic US alone (79%) and CT alone (79%) (P = .01). The results of endoscopic US–guided FNAB prompted a change to nonsurgical management in 66 (80%) of 82 patients who underwent the procedure. One minor complication, postprocedural fever that resolved with oral antibiotics, occurred (1%; 95% CI: 0%, 6%).
CONCLUSION: Endoscopic US–guided FNAB is accurate and safe for biopsy of mediastinal lymph nodes to stage NSCLC, establish a primary diagnosis, or examine patients with prior inconclusive biopsy results.
Index terms: Biopsies, technology, 60.126 • Lymphatic system, neoplasms, 60.3214, 60.342, 60.343 • Mediastinum, interventional procedures, 60.126 • Thorax, CT, 60.12112, 60.12115 • Thorax, neoplasms, 60.3214, 60.342, 60.343 • Thorax, US, 60.12981, 60.12984, 60.12985
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Percutaneous biopsy methods can be limited by the surrounding vascular structures and by the size of the targeted lesion (12,13). Traversal of the lung, which increases the frequency of complications, including pneumothorax, may occur (12,13). Collectively, the diagnostic sensitivity of flexible bronchoscopic FNAB in evaluating mediastinal lymphadenopathy in patients with NSCLC ranges from 25% to 81%; that of CT-guided FNAB ranges from 88% to 96% (8,9,11–20). In patients in whom these procedures are unsuccessful or who are not candidates for them, surgical biopsy by means of mediastinoscopy, mediastinotomy, thoracoscopy, or minimal or standard thoracotomy may be performed. These techniques are accurate but are more costly and are associated with greater morbidity (21). In addition, less invasive surgical approaches may not be applicable in patients with posterior mediastinal lymphadenopathy (17,22).
During the past several years, several case series in which endoscopic US–guided FNAB was used to evaluate mediastinal lymphadenopathy have been described. Since the initial description of endoscopic US–guided FNAB of mediastinal lymph nodes, this technique has been shown to be promising for facilitating a primary tissue diagnosis and assisting in the staging of patients with NSCLC (21, 23–33). The objectives of this study were to evaluate the safety and accuracy of endoscopic US–guided FNAB in a large cohort of patients with mediastinal lymphadenopathy in whom other nonsurgical biopsy procedures were not possible, less direct, or unsuccessful.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Patients were not considered for endoscopic US–guided FNAB when an unresectable tumor had been previously documented, a primary gastrointestinal tumor was present, uncorrectable coagulopathy or thrombocytopenia was present, or treatment would not be influenced by the endoscopic US–guided FNAB results. Institutional review board approval and informed consent from each patient were obtained. A final diagnosis of the evaluated mediastinal lymph node(s) was available in 82 of the 86 patients. The four excluded patients had benign endoscopic US–guided FNAB cytologic results but insufficient follow-up to ascertain a final diagnosis.
A compound reference standard was used for comparison purposes. Specifically, in the 35 patients with benign lymphadenopathy, this determination was based on (a) surgical-pathologic confirmation (mediastinoscopy and thoracotomy in seven patients each) or (b) results of clinical follow-up (21 patients) of at least 12 months demonstrating a lack of clinical or radiologic disease progression (median follow-up, 620 days; range, 371–2,039 days). In the 47 patients with malignant lymphadenopathy, this determination was based on (a) malignant cytologic results at endoscopic US–guided FNAB, with a subsequent clinical course consistent with malignant disease (44 patients), (b) surgical-pathologic confirmation (mediastinoscopy and thoracotomy in one patient each), or (c) autopsy findings (one patient).
Thoracic CT with intravenous contrast material was performed by using a transverse technique in 25 patients and by using a spiral technique in 57 patients. The scans were interpreted by one or more senior attending radiologists with recognized expertise in thoracic radiology. Mediastinal lymphadenopathy was classified according to the American Thoracic Society mediastinal staging system (34,35). In the 82 patients with sufficient follow-up data to ascertain a final diagnosis, the imaging abnormality that resulted in the request for endoscopic US–guided FNAB was (a) CT evidence of suspicious periesophageal mediastinal lymphadenopathy in 66 patients, (b) a peripheral lung or central lung lesion without mediastinal lymphadenopathy at CT in 10 patients, (c) an extrinsic compression of the esophagus at endoscopy, with or without CT abnormalities, in five patients, and (d) pericardial effusion of suspected but not proved malignant origin with no mediastinal lymphadenopathy at CT in one patient. In 22 of the 29 patients who underwent further staging of NSCLC, CT depicted suspicious mediastinal lymphadenopathy.
Eleven patients without mediastinal lymphadenopathy at CT underwent endoscopic US–guided FNAB for the following indications: (a) as a component of preoperative staging of known or suspected NSCLC, performed under an institutional review board–approved protocol, in seven patients; (b) to further evaluate a central lung lesion in three patients; and (c) to investigate a pericardial effusion of suspected malignant origin in one patient.
Procedures
All endoscopic US examinations were performed, with the patient under conscious sedation, by using a linear scanning echoendoscope (FG-32UA or FG-36UX; Pentax Precision Instruments, Orangeburg, NY) and in some cases by using a radial scanning echoendoscope (GF-UM20 or GF-UM3; Olympus America, Melville, NY) as well. Antibiotics were not given unless indicated for subacute bacterial endocarditis prophylaxis. In those patients who underwent staging of NSCLC, the most distant lymphadenopathy (eg, contralateral or N3) was selected for endoscopic US–guided FNAB initially. Although not all patients were identified as having suspicious mediastinal lymphadenopathy at CT, in all 82 study patients, mediastinal lymphadenopathy was identified at endoscopic US, and they therefore underwent biopsy (Figs 1, 2).
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Biopsy of all visualized lymph nodes was not performed in each patient unless only benign material was identified at the adequacy assessment. The median examination duration was 45 minutes (range, 30–60 minutes), and the procedure was performed on an outpatient basis unless the patient was already hospitalized for other reasons. Patients were contacted within 48 hours of the procedure to discuss the pathologic results and assess for complications, including chest pain, fever, shortness of breath, or any other symptoms that were not present before the examination.
After endoscopic US–guided FNAB, the patients who were considered to be eligible for surgical resection or in whom a tissue diagnosis had not been procured by using endoscopic US–guided FNAB underwent a surgical procedure. In those individuals with known, suspected, or ultimately discovered NSCLC, mediastinoscopy and/or thoracotomy was performed to allow mediastinal lymph node dissection and with resection when appropriate. In all other patients who underwent surgical biopsy, mediastinoscopy or thoracotomy was performed to obtain a tissue diagnosis. During mediastinal lymph node dissection, each node was mapped according to the American Thoracic Society classification. Histopathologic findings were then reported according to the location of the lymph nodes, and this permitted correlation with endoscopic US, endoscopic US–guided FNAB, and CT results.
Statistical Analyses
The sensitivity, specificity, accuracy, negative predictive value, and positive predictive value of both endoscopic US alone and CT in patients with NSCLC were determined by comparing the results of these examinations with the results of surgical-pathologic and cytologic analyses. In determining the sensitivity of endoscopic US–guided FNAB, the results in patients with malignant results at surgical-pathologic or cytologic analysis were included in the definition of the reference standard. In determining the specificity of endoscopic US–guided FNAB, patients with benign surgical-pathologic or extended clinical follow-up findings that demonstrated a benign course were included. Patients with inconclusive endoscopic US–guided FNAB cytologic results (eg, atypical or suspicious) were excluded from analysis; however, an inconclusive test rate was computed. Exact binomial 95% CIs for proportions were computed. Comparison of the continuous parameters was performed by using the two-tailed Student t test, with a P value of less than .05 considered to indicate a significant difference. For categorical parameters, comparison was performed by using the 
2 or Fisher exact test, with a P value of less than .05 considered to indicate a significant difference.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Four patients received an incorrect diagnosis at endoscopic US–guided FNAB. One patient each with surgically proved Hodgkin lymphoma and non-Hodgkin lymphoma had false-negative cytologic results. Two patients with benign disease had inconclusive cytologic results (inconclusive test rate, 2% [two of 82 patients; 95% CI: 0%, 9%). One patient with a history of thyroid carcinoma and mediastinal lymphadenopathy had atypia at endoscopic US–guided FNAB. A second patient with previously treated NSCLC had suspicious cytologic findings at endoscopic US–guided FNAB. Both patients underwent surgical biopsy with benign findings.
Twenty-nine patients with NSCLC and no prior therapy underwent endoscopic US–guided FNAB of 40 lymph nodes—nine benign and 31 malignant—for staging purposes. All seven patients with N0 disease at endoscopic US–guided FNAB underwent surgery, at which mediastinal lymph node dissection findings confirmed these results. None of the 22 patients with malignancy at endoscopic US–guided FNAB underwent surgery; however, autopsy subsequently performed in one of these patients 1 month after endoscopic US–guided FNAB confirmed lymph node metastases. The lymph node stage in these 29 patients was N0 in seven patients, N2 in 16, and N3 in six. The benign lymph nodes, as measured at endoscopic US, were smaller than the malignant nodes (mean width, 9 mm; range, 4–17 mm versus 24 mm; range, 10–60 mm [P < .01] and mean length, 15 mm; range, 9–30 mm versus 33 mm; range, 10–80 mm [P < .01]).
The echo features of the lymph nodes (ie, shape, echotexture, and border) were not significantly different between the benign and malignant groups; however, the number of patients with benign disease may have been too small to allow adequate assessment of this parameter. The operating characteristics of endoscopic US–guided FNAB, endoscopic US alone, and CT were compared (Table 4). Endoscopic US–guided FNAB enabled correct classification of all patients and had superior mediastinal lymph node staging accuracy (100%) compared with endoscopic US alone (79%) and CT (79%) in this group of patients with NSCLC (P = .01). In six patients, endoscopic US alone and CT led to incorrect staging of lymph node involvement (three false-positive and three false-negative findings for each test, respectively).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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Once a decision to obtain a tissue sample from a mediastinal lymph node has been reached, the technique used will depend on the clinical circumstances as well as the available local expertise. The results of seven studies (9,15–20) involving flexible bronchoscopy–guided FNAB of mediastinal lymph nodes in 257 patients with NSCLC demonstrated a sensitivity of 25%–81%, a specificity of 92%–100%, and an overall diagnostic accuracy of 34%–90%. Although this technique is safe, the shortcomings include the inability to depict the lymph node on which biopsy is being performed and to access the aortopulmonic and posterior lymph nodes. For institutions that have operators with technical expertise in bronchoscopic FNAB, this approach is the preferred method for patients who have radiographic evidence of enlarged mediastinal lymph nodes that are adjacent to the airways, because assessment for endobronchial lesions can be performed during the same procedure. Patients with mediastinal lymph nodes that are not immediately adjacent to the airways may be candidates for endoscopic US–guided FNAB if the lymphadenopathy is accessible through the esophagus.
CT-guided biopsy of mediastinal lymphadenopathy in NSCLC has been reported to have a sensitivity of 88%–96% (12–14). This technique is limited in that lymph nodes must be larger than 1.5–2.0 cm and there is associated morbidity: 22%–34% of patients develop pneumothorax (12–14). In addition, access to the region of the lymphadenopathy may be difficult owing to intervening vascular structures.
Collectively, the sensitivity, specificity, accuracy, and safety of endoscopic US–guided FNAB of mediastinal lymphadenopathy compares favorably with those of other available methods. In this series, the lymph nodes in all 29 patients with NSCLC were correctly staged with endoscopic US–guided FNAB, and the overall accuracy for all patients who underwent endoscopic US–guided FNAB was 98%. This is similar to the previously reported endoscopic US–guided FNAB accuracy of 83%–100% in six studies (21,29,30,32, 33,36) comprising 174 patients with mediastinal lymphadenopathy. Gress et al (21) observed an accuracy of 96% for endoscopic US–guided FNAB in the mediastinal lymph node staging of NSCLC; this is similar to the 100% accuracy observed in the current series. The single error in the series by Gress et al (21) occurred in a patient with a 2-mm cancer focus in an 8-mm lymph node.
The several advantages of endoscopic US–guided FNAB include (a) real-time targeting of the lymph node on which biopsy is being performed; (b) the absence of endoluminal tumor, which occasionally can lead to false-positive results with bronchoscopic FNAB; (c) the use of small-gauge needles, which reduces procedural risks; (d) the high diagnostic yield, which in this series was observed also in the subgroup of patients who underwent prior inconclusive biopsy; and (e) the ability to access posterior and aortopulmonic lymph nodes, which typically otherwise requires surgical sampling. In this series, performing real-time targeting of the biopsy site was a distinct advantage when sampling lymph nodes that were small, in close proximity to major vascular structures, necrotic, or irregularly replaced with tumor.
Several limitations of our study should be noted. Anterior lymph nodes, including those in the right paratracheal region and pretracheal regions, were not accessible at endoscopic US–guided FNAB owing to interposed structures (ie, trachea) and the limited depth of penetration with endoscopic US. Consequently, because of incomplete visualization of the mediastinum, endoscopic US did not enable complete information for NSCLC staging. In our study, we examined a select group of patients, most of whom had abnormal mediastinal lymph nodes in regions that were accessible at endoscopic US–guided FNAB. Nonetheless, in 11 patients who had a peripheral or central lung lesion, esophageal compression, and/or a pericardial effusion but no evidence of mediastinal lymphadenopathy at CT, we were able at endoscopic US to identify lymph nodes in the periesophageal space that at biopsy provided information that influenced patient treatment. These selected cases highlight the difficulty one may encounter when CT alone is used to detect mediastinal abnormalities.
All patients with NSCLC who were not identified at CT as having suspicious or enlarged lymph nodes were ultimately deemed to have mediastinal lymphadenopathy at endoscopic US and subsequently underwent FNAB. The high prevalence of mediastinal lymph nodes at endoscopic US, even in the absence of a thoracic abnormality, has been previously reported and is perhaps related in part to endemic histoplasmosis in some geographic regions (37). This complicates the staging of NSCLC and may in part explain the three false-positive CT examinations. However, there were also three false-negative CT examinations in this series of patients with NSCLC, and this suggests that further work is needed to clarify whether endoscopic US–guided FNAB can enable the diagnosis of malignant mediastinal lymphadenopathy that is not identified or suspected at CT. The identification of malignant mediastinal lymph nodes in patients who lack roentgenographic evidence of mediastinal disease is a difficult problem, and further experience is needed to clarify the importance of this finding.
The ability to diagnose lymphoma with endoscopic US–guided FNAB is limited (71% [five of seven patients] sensitivity in this series). Two false-negative results occurred in seven patients. Establishing a diagnosis of lymphoma, particularly Hodgkin lymphoma, is problematic with cytologic analysis alone (38). In this study, the presence of an attendant cytopathologist was helpful in ensuring that an adequate specimen was obtained. Although this is our standard practice, cost considerations may preclude the widespread use of this level of support. In our series, the use of flow cytometry did not improve our diagnostic yield substantially; however, the series was too small to ascertain this effect.
In summary, endoscopic US–guided FNAB is an accurate and safe method of evaluating lower paratracheal, subcarinal, aortopulmonic, and posterior mediastinal lymphadenopathies. Endoscopic US–guided FNAB is more accurate than endoscopic US alone or CT alone in staging mediastinal lymph nodes in patients with NSCLC. Studies with a direct comparison of the currently available biopsy methods and newer imaging techniques such as positron emission tomography are needed.
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Author contributions: Guarantor of integrity of entire study, M.J.W.; study concepts and design, M.J.W., E.V.S., L.M.W.; literature research, M.J.W., E.V.S.; clinical studies, M.J.W., L.M.W.; data acquisition, M.J.W., E.V.S., L.M.W.; data analysis/interpretation, M.J.W., E.V.S., L.M.W.; statistical analysis, M.J.W., E.V.S.; manuscript preparation, M.J.W., E.V.S., L.M.W.; manuscript definition of intellectual content, M.J.W., E.V.S., L.M.W.; manuscript editing, M.J.W., E.V.S., L.M.W.; manuscript revision/review, M.J.W., E.V.S., L.M.W.; manuscript final version approval, M.J.W., E.V.S., L.M.W.
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REFERENCES |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODS RESULTSDISCUSSIONREFERENCES |
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