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Right arrow Lung - cancer

Ann Thorac Surg 2005;79:263-268
© 2005 The Society of Thoracic Surgeons

Original article: General thoracic

Endoscopic Ultrasound-Guided Fine Needle Aspiration of Mediastinal Lymph Node in Patients With Suspected Lung Cancer After Positron Emission Tomography and Computed Tomography Scans

Mohamad A. Eloubeidi, MD, MHSa,d,*, Robert J. Cerfolio, MDb,d, Victor K. Chen, MDa, Renee Desmond, PhDd, Sujath Syed, MDa, Buddhiwardhan Ojha, MDc

a Department of Medicine, Division of Gastroenterology and Hepatology, The University of Alabama at Birmingham, Birmingham, Alabama, USA
b Department of Cardiothoracic Surgery, The University of Alabama at Birmingham, Birmingham, Alabama, USA
c Division of Nuclear Medicine, The University of Alabama at Birmingham, Birmingham, Alabama, USA
d Cancer Comprehensive Center, The University of Alabama at Birmingham, Birmingham, Alabama, USA

Accepted for publication June 27, 2004.

* Address reprint requests to Dr Eloubeidi, Division of Gastroenterology and Hepatology, The University of Alabama at Birmingham, 1530 3rd Ave S, ZRB 636, Birmingham, AL35294-0007 (E-mail: meloubeidi{at}uabmc.edu).


   Abstract
Top
 Abstract
Introduction
 Material and Methods
 Results
 Comment
 References
 
BACKGROUND: The treatment of patients with non-small cell lung cancer (NSCLC) depends on the stage. Positron emission and computed tomography (CT) scans can identify suspicious lymph nodes that require biopsy. We prospectively evaluated the yield and accuracy of endoscopic ultrasound-guided fine needle aspiration (EUS-FNA) in sampling mediastinal lymph nodes and compared its accuracy to that of 18F-fluorodeoxyglucose positron emission tomography (FDG-PET) and CT in staging NSCLC.

METHODS: A consecutive series of patients with suspicious nodes on PET or CT scan in the posterior mediastinal lymph node stations (#5, 7, 8, or 9) were prospectively evaluated by EUS-FNA. The reference standard included thoracotomy with complete lymphadenectomy in patients with lung cancer or if EUS-FNA was benign, repeat clinical imaging, or long-term follow-up.

RESULTS: There were 104 patients (63 men) with 125 lesions (117 lymph nodes, 8 left adrenal glands) who underwent EUS-FNA. The sensitivity, specificity, positive predictive value, negative predictive value, and accuracy of EUS-FNA were 92.5%, 100%, 100%, 94%, and 97%, respectively. EUS-FNA was more accurate and had a higher positive predictive value than the PET or CT (p < 0.001) scan in confirming cancer in the posterior mediastinal lymph nodes. EUS-FNA documented metastatic cancer to the left adrenal in all 4 patients with advanced disease. No deaths resulted from EUS-FNA. One patient experienced self-limited stridor.

CONCLUSIONS: EUS-FNA is a safe, accurate, and minimally invasive technique that improves the staging of patients with NSCLC. It is more accurate and has a higher predictive value than either the PET scan or CT scan for posterior mediastinal lymph nodes.


   Introduction
Top
 Abstract
 Introduction
Material and Methods
 Results
 Comment
 References
 
Lung cancer is the most common cause of cancer-related death in the United States [1]. Unfortunately, metastatic cancer is found in 28% to 38% of non-small cell lung cancer (NSCLC) at the time of diagnosis [2–4]. Preoperative chemotherapy or radiotherapy (or both) before pulmonary resection may lead to improved survival in patients with NSCLC in N2 (ipsilateral) or N3 (contralateral) mediastinal lymph nodes [5–8]. The metabolic imaging with 18-fluorodeoxyglucose position emission tomography (FDG-PET) and integrated PET-computed tomography (CT) is increasingly being used to stage patients with NSCLC [9–11]. Although FDG-PET improves the diagnostic accuracy of staging NSCLC compared with CT scan, false-positive results are common [9]. Tissue confirmation of suspected malignant lymphadenopathy is required before surgical resection [9, 11–13].

Endoscopic ultrasound uses the esophagus as an acoustic medium to image the posterior mediastinum and adjacent lymph nodes. With the advent of curvilinear echoendoscopes that allow tracking of the needle course, the transesophageal sampling of mediastinal lymph nodes is possible [14–19]. Currently, no published reports from the United States have evaluated the role of endoscopic ultrasound fine-needle aspiration (EUS-FNA) in confirming the nature of suspicious mediastinal lymph nodes detected by FDG-PET in patients with suspected or proven NSCLC. Therefore, we prospectively evaluated the yield and accuracy of EUS-FNA in sampling enlarged posterior mediastinal lymph nodes and compared its accuracy to that of FDG-PET and CT in staging NSCLC.


   Material and Methods
Top
 Abstract
 Introduction
 Material and Methods
Results
 Comment
 References
 
Between August, 2000 and February, 2003, one general thoracic surgeon (RJC) referred 104 patients with proven lung cancer (n = 63), suspected NSCLC (n = 30), or mediastinal lymph node enlargement in patients with prior cancer (n = 11). These patients had undergone CT or FDG-PET scanning that imaged suspicious posterior mediastinal lymph nodes (#5, 7, 8, or 9 lymph nodes station) according to the international system of lymph node staging and the revised Tumor, Nodes, Metastases (TNM) staging system. [8, 20] All patients had CT scans, but since FDG-PET had recently been introduced, only 74 patients had FDG-PET scans.

If either test was positive, patients were referred for EUS-FNA. FDG-PET was considered positive for one of these lymph nodes if it revealed hypermetabolic activity (standardized uptake value ≥ 2.5) (Fig 1). CT scans were considered positive if a lymph node was 1.0 cm or more in the short axis. The FDG-PET and CT scans were both reviewed by a nuclear medicine physician (BO) and a general thoracic surgeon (RJC).



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  		Fig 1. An 18F-fluorodeoxyglucose positron emission tomography scan illustrates a well-defined focal, intensely hypermetabolic area in the subcarina (level 7) (black arrow) in a patient with lung cancer. Endoscopic ultrasound-guided fine needle aspiration confirmed malignant involvement.

 
Endoscopic ultrasound was performed under conscious sedation by a single endosonographer (M.A.E.) as previously described [21]. The endosonographer was aware of the presence of suspicious lymph nodes but was blinded to the radiographic results. A radial echoendoscope (GF-UM130, Olympus America, Melville, NY) was first used to evaluate the presence or absence of lymphadenopathy. The examination started by a full evaluation of the left adrenal gland by imaging it from the fundus of the stomach. The echoendoscope was then gradually withdrawn to evaluate the inferior pulmonary ligament nodal station (#9), the periesophageal areas (#8), the subcarinal space (#7), the aortopulmonary window (#5), and the anterior pretracheal lymph nodes (#2 and 4). Once a lymph node was identified, the radial echoendoscope was removed and a curvilinear echoendoscope (Olympus UC-30P or UCT 140) was then inserted and EUS-FNA of the target lesion(s) (Fig 2) was performed as previously described [16].



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  		Fig 2. An echoendoscope placed in the mid esophagus allows imaging of a 19 x 11-mm lymph node in the subcarina. The circle at the 12 o'clock position in the image is the ultrasound transducer. Endoscopic ultrasound-guided fine needle-aspiration confirmed malignant involvement. (PA = pulmonary artery; LA = left atrium.) (Olympus UC-30 P scanning at 5 MHz, Olympus America, Melville, NY.)

 
All EUS-FNAs were preformed with 22-gauge adjustable-length Echotip needles (Wilson-Cook Inc, Winston-Salem, NC). Cytologic diagnosis of the aspirated lesion was classified into four categories: 1) benign or reactive, 2) positive for malignancy, 3) atypical or suspicious for malignancy, or 4) nondiagnostic. The endosonographic criteria for malignant involvement of the lymph nodes were documented in all nodes before cytologic evaluation as previously described [22]. The nodes were recorded as: 1) 1-cm in size or larger, 2) round shape, 3) homogeneous hypoechoic pattern, or 4) sharp and distinct borders.

A compound reference standard was used for the classification of the final diagnosis of the target lesion. In patients with benign lymphadenopathy, the determination was based on 1) surgical and pathologic confirmation by thoracotomy or 2) results of extended clinical follow-up of at least 6 months that demonstrated the lack of clinical or radiologic disease progression. Patients with known or suspected lung cancer and benign mediastinal adenopathy underwent thoracotomy with complete thoracic lymphadenectomy. During mediastinal lymph node dissection, all nodes from each station were completely removed. Each node was numbered according to the revised TNM staging system [8, 20]. In patients with malignant lymphadenopathy, the determination of the final status of the lesion was based on malignant cytologic results at EUS-FNA, with a subsequent clinical course consistent with malignant disease or surgical exploration.

Immediate complications were assessed by the endosonographer, and a nurse contacted the patient within 1 week, and 30 days of the procedure to assess complications. Specific questions asked were chest pain, fever, shortness of breath, or any symptoms perceived to be related to the procedure.

Informed consent was obtained from patients before the procedure. This study was approved by the Institutional Review Board of the University of Alabama at Birmingham.

Statistical Analysis
Categorical variables were reported as proportions. Continuous variables were reported as means and standard deviations or median and interquartile range (IQR) if data were not normally distributed. The prevalence of malignancy was calculated by using each test independently. Using the reference standard results as the gold standard, we calculated the sensitivity, specificity, positive and negative predictive values, accuracy, and the likelihood ratio positive of CT, FDG-PET, EUS (based on the lymph node echo features before FNA), and for EUS-FNA. The sensitivity, specificity, and negative predictive value of CT and FDG-PET were not calculated, as all patients included in this investigation were positive by one scan or the other. The exact binomial confidence intervals were computed for each estimate. The binomial approximation test was used to compare positive predicted value and accuracy. The analysis was conducted with SAS Version 8.02 (SAS Institute, Inc, Cary, NC) and an {alpha} level of 0.05 was deemed statistically significant.


   Results
Top
 Abstract
 Introduction
 Material and Methods
 Results
Comment
 References
 
One hundred four patients with mediastinal lymph nodes (N2 or N3) that were suspicious by CT scan or FDG-PET at levels #5, 7, 8, or 9 underwent EUS-FNA. The demographics, baseline characteristics, previous staging procedures, and the primary final diagnosis of these 104 patients are shown in Tables 1 and 2.


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  		Table 1. Demographic, Baseline Characteristics, and Location of Target Lesions in Patients Who Underwent Endoscopic Ultrasound-Guided Fine Needle Aspiration (n = 104)
 
Sixty-seven patients (64%) with suspected malignant lymphadenopathy had benign disease by EUS-FNA. Of this latter group, 41 patients (61%) underwent thoracotomy, pulmonary resection, and complete thoracic lymphadenectomy that confirmed benign lymphadenopathy in all but 3 patients. The remaining 26 patients underwent at least 6 months of clinical follow-up documenting no clinical or radiologic progression of their disease. The median follow-up for patients with benign disease was 310 days (IQR was 111 to 546 days).

In the patients with malignant lymphadenopathy, the determination of the final status of the lymph nodes was based on malignant cytologic results at EUS-FNA with a subsequent clinical course consistent with malignant disease (N = 37, 36%). In patients whose EUS-FNA identified malignant involvement, 31% had prior mediastinoscopy that proved benign disease in the anterior mediastinum. In a conservative analysis, 57% of the patients (37 malignant and 22 benign) avoided surgery to determine their lymph node status. When we evaluated the subset of patients with proven lung cancer, 30 of 63 patients (48%) had cancer diagnosed in lymph nodes, highlighting the utility of EUS-FNA in this subgroup. The final management of patients based on EUS-FNA results is illustrated in Figure 3.



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  		Fig 3. Management of patients on the basis of endoscopic ultrasound-guided fine needle aspiration (EUS-FNA) results. (Chemo = chemotherapy; CT = computed tomography; PET = positron emission tomography; XRT = radiation therapy.)

 
Table 3 shows the classification of individual patient test results compared with the reference standard. Table 4 depicts the operating characteristics of FDG-PET, CT scan, EUS alone, and EUS-FNA. We did not calculate the sensitivity, specificity, and negative predictive value for CT or FDG-PET because this study selected patients that had a positive CT or FDG-PET scan. EUS-FNA was more accurate than both FDG-PET and CT scan (p < 0.001) in confirming posterior mediastinal lymph node status. EUS-FNA had a higher positive predictive value than either test (p < 0.001). In addition, EUS-FNA was more accurate (p < 0.001) then EUS features alone. The likelihood ratio for a positive result was higher for EUS-FNA than CT, FDG-PET, and EUS alone. In patients with left adrenal gland enlargement, EUS-FNA documented metastatic disease to the left adrenal in 4 of 8 patients (50%). It was correct in all patients as corroborated by their subsequent clinical course.


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  		Table 3. Comparison of CT, PET, EUS and EUS-FNA to the Reference Standard
 

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  		Table 4. Operating Characteristics of CT, PET, EUS and EUS-FNA in Detecting Malignancy in Suspicious Mediastinal Lymph Nodes
 
One patient (0.96%) suffered from self-limited stridor during the procedure. At 1-week follow-up, 6 patients reported sore throat, 1 patient reported nausea and vomiting, and one reported cough. There were no esophageal perforations, mediastinitis, or deaths noted at 30-day follow-up.


   Comment
Top
 Abstract
 Introduction
 Material and Methods
 Results
 Comment
References
 
This investigation shows that EUS-FNA is the procedure of choice to document the status of abnormal posterior mediastinal lymph nodes (#5, 7, 8 or 9) detected by CT or PET. In this study, EUS-FNA provided tissue confirmation with 97% accuracy and avoided invasive surgical interventions in at least 57% of the patients. Moreover, in patients with proven lung cancer, 48% had cancer diagnosed in lymph nodes, highlighting the utility of EUS-FNA in this subgroup. The chest CT scan relies solely on the size of the node, which has been shown to be unreliable. A recent review that included 3,438 patients with lung cancer [13] illustrated that 44% of patients with "positive disease" by CT were falsely positive and 17% of patients with "negative disease" by CT had metastatic cancer to their mediastinal lymph nodes.

Similarly, studies that used FDG-PET on 1,045 patients with lung cancer showed a pooled sensitivity of 84%, specificity of 89%, positive predictive value of 79%, and a negative predictive value of 93%. These results suggest that 21% of patients with "positive disease" by PET are falsely positive and 7% of patients with "negative disease" by PET have malignant mediastinal lymph nodes [13]. The positive predictive value of FDG-PET was lower in our study, perhaps because of a higher prevalence of granulomatous diseases in the southeastern region of the United States [9]. We have previously found [9] that FDG-PET was most commonly falsely negative in the subcarinal (#7) and the aortopulmonary window (#5) lymph nodes stations. These stations are easily accessible by EUS-FNA.

Current guidelines [12, 23] suggest that patients with abnormal lymphadenopathy with suspected or proven NSCLC should undergo tissue sampling before undergoing surgical interventions. Currently, several invasive staging modalities provide tissue sampling of suspicious mediastinal lymph nodes in patients with NSCLC [24]. These include mediastinoscopy, anterior mediastinotomy, video-assisted thoracic surgery (VATS), transthoracic needle aspiration (TTNA), transbronchial needle aspiration (TBNA), and EUS-FNA. A comparison cannot be made between these techniques since each modality has the potential to better assess different lymph node stations. For example, mediastinoscopy has excellent access to stations #2R, #4R, #4L, #2L, and the proximal #7 subcarinal stations, but it cannot access the main or lower aspect of the subcarinal node (#7). Standard mediastinoscopy cannot perform a biopsy of the #5 aortopulmonary lymph nodes. EUS-FNA can, however, easily access the #7, #8 and #9 stations and can also get to the #5 station in many patients. In addition, EUS-FNA has the potential of excluding or documenting M1 or metastatic stage IV disease in locations such as the left adrenal gland [25]. Therefore, EUS-FNA offers highly accurate tissue diagnosis without the need for an incision or general anesthesia. It also has minimal risk in experienced hands.

Surgical options are performed under general anesthesia and have associated morbidity and rare mortality. TTNA can result in pneumothorax and bleeding [24]. TBNA and EUS-FNA are usually performed on an outpatient basis and have minimal morbidity. A recent study [26] compared EUS-FNA with TBNA in the evaluation of patients with suspected or confirmed lung cancer. The diagnosis of malignant mediastinal lymphadenopathy was superior for EUS-FNA compared with TBNA (92% vs 73%, p = 0.01).

EUS-FNA was the most economical approach in patients with NSCLC with mediastinal adenopathy on CT compared with TBNA or mediastinoscopy. This study and others [26, 27] suggested that when performed in patients with NSCLC and abnormal lymphadenopathy, EUS-FNA can reduce resource use. In addition, TBNA is underutilized despite the fact that bronchoscopy is more widely available than EUS-FNA [28].

A limitation to our study is that all 104 patients had either an abnormal FDG-PET or CT scan at the time of referral for EUS-FNA. In addition, the referring surgeon believed that EUS-FNA was the best staging modality to determine the nature of these lymph nodes. EUS was chosen to assess the posterior mediastinum nodes (#5, 7, 8, or 9) but not the anterior ones. We believe our study illustrates that EUS-FNA is a complementary tool that supplements other staging modalities. Moreover, this study reflects the "effectiveness" of EUS-FNA in real clinical practice. We did not evaluate patients whose CT scans and FDG-PET scans were negative. However, a recent study reported that EUS-FNA detects malignant mediastinal lymphadenopathy in 42% of patients where CT scans were falsely negative [18].

A second limitation is that we relied on a compound gold standard that used results obtained by EUS-FNA, surgical resection, and extended clinical follow up. To date, no false-positive EUS-FNA results from mediastinal lymph nodes have been reported in the literature. Furthermore, we felt that it was unethical to subject patients with malignant cytology by EUS-FNA to further invasive testing in order to verify a true-positive result. Of note, our methodology is similar to other investigations in the field [16, 18, 19].

In summary, EUS-FNA is a minimally invasive, safe, and accurate method that provides tissue from suspicious posterior mediastinal lymph nodes (#5, 7, 8, or 9) that have been targeted by CT or PET scan. EUS-FNA has a higher positive predictive value than CT or FDG-PET scan in determining posterior lymph node status. EUS-FNA complements other staging techniques and can obviate the need for more invasive surgical intervention in patients with NSCLC.


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  		Table 2. Primary Diagnosis of Patients Who Underwent Endoscopic Ultrasound-Guided Fine Needle Aspiration
 

   References
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 Introduction
 Material and Methods
 Results
 Comment
 References
 
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S. M. Janes and S. G. Spiro
Esophageal Endoscopic Ultrasound/Endobronchial Ultrasound-guided Fine Needle Aspiration: A New Dawn for the Respiratory Physician?
Am. J. Respir. Crit. Care Med., February 15, 2007; 175(4): 297 - 299.
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 Am. J. Respir. Crit. Care Med.Home page
P. Singh, B. Camazine, Y. Jadhav, R. Gupta, P. Mukhopadhyay, A. Khan, R. Reddy, Q. Zheng, D. D. Smith, R. Khode, et al.
Endoscopic Ultrasound As a First Test for Diagnosis and Staging of Lung Cancer: A Prospective Study
Am. J. Respir. Crit. Care Med., February 15, 2007; 175(4): 345 - 354.
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C. G. Micames, D. C. McCrory, D. A. Pavey, P. S. Jowell, and F. G. Gress
Endoscopic Ultrasound-Guided Fine-Needle Aspiration for Non-small Cell Lung Cancer Staging: A Systematic Review and Metaanalysis
Chest, February 1, 2007; 131(2): 539 - 548.
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 J. Thorac. Cardiovasc. Surg.Home page
R. J. Cerfolio
Reply to the Editor
J. Thorac. Cardiovasc. Surg., January 1, 2007; 133(1): 276 - 277.
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 Eur Respir JHome page
F. J. F. Herth, K. F. Rabe, S. Gasparini, and J. T. Annema
Transbronchial and transoesophageal (ultrasound-guided) needle aspirations for the analysis of mediastinal lesions
Eur. Respir. J., December 1, 2006; 28(6): 1264 - 1275.
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 ChestHome page
R. J. Cerfolio, A. S. Bryant, and M. A. Eloubeidi
Routine Mediastinoscopy and Esophageal Ultrasound Fine-Needle Aspiration in Patients With Non-small Cell Lung Cancer Who Are Clinically N2 Negative: A Prospective Study
Chest, December 1, 2006; 130(6): 1791 - 1795.
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R. J. Cerfolio, A. S. Bryant, E. Scott, M. Sharma, F. Robert, S. A. Spencer, and R. I. Garver
Women With Pathologic Stage I, II, and III Non-small Cell Lung Cancer Have Better Survival Than Men
Chest, December 1, 2006; 130(6): 1796 - 1802.
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R. J. Cerfolio and A. S. Bryant
Survival and Outcomes of Pulmonary Resection for Non-Small Cell Lung Cancer in the Elderly: A Nested Case-Control Study
Ann. Thorac. Surg., August 1, 2006; 82(2): 424 - 430.
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 J. Thorac. Cardiovasc. Surg.Home page
R. J. Cerfolio, A. S. Bryant, and B. Ojha
Restaging patients with N2 (stage IIIa) non-small cell lung cancer after neoadjuvant chemoradiotherapy: A prospective study
J. Thorac. Cardiovasc. Surg., June 1, 2006; 131(6): 1229 - 1235.
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 Ann. Thorac. Surg.Home page
R. J. Cerfolio, A. S. Bryant, B. Ojha, and M. Eloubeidi
Improving the Inaccuracies of Clinical Staging of Patients with NSCLC: A Prospective Trial
Ann. Thorac. Surg., October 1, 2005; 80(4): 1207 - 1214.
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 Ann. Thorac. Surg.Home page
M. A. Eloubeidi, A. Tamhane, V. K. Chen, and R. J. Cerfolio
Endoscopic Ultrasound-Guided Fine-Needle Aspiration in Patients With Non-Small Cell Lung Cancer and Prior Negative Mediastinoscopy
Ann. Thorac. Surg., October 1, 2005; 80(4): 1231 - 1239.
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K. G. Tournoy, M. M. Praet, G. Van Maele, and J. P. Van Meerbeeck
Esophageal Endoscopic Ultrasound With Fine-Needle Aspiration With an On-site Cytopathologist: High Accuracy for the Diagnosis of Mediastinal Lymphadenopathy
Chest, October 1, 2005; 128(4): 3004 - 3009.
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