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Ann Thorac Surg 2002;73:916-920
© 2002 The Society of Thoracic Surgeons

Original article: general thoracic

Clinical impact of endoscopic ultrasound-guided fine needle aspiration of celiac axis lymph nodes (M1a disease) in esophageal cancer

Kiran S. Parmar, MDa, Joseph B. Zwischenberger, MDb, Angela L. Reeves, CGRNa, Irving Waxman, MD*a

a Section of Endoscopy, University of Texas Medical Branch at Galveston, Galveston, Texas, USA
b Department of Surgery, University of Texas Medical Branch at Galveston, Galveston, Texas, USA

Accepted for publication November 15, 2001.

* Address reprint requests to Dr Waxman, University of Chicago, Section of Gastroenterology, 5758 S. Maryland Ave, MC 9028, Chicago, IL 60637, USA
e-mail: iwaxman{at}medicine.bsd.uchicago.edu


   Abstract
Top
 Abstract
Introduction
 Material and methods
 Results
 Comment
 References
 
Background. The purpose of this study was to determine how endoscopic ultrasound (EUS)-guided fine needle aspiration (FNA) with a histology confirmed biopsy protocol impacted on staging and managing esophageal carcinoma in terms of resectability and neoadjuvant therapy (chemotherapy and radiation therapy).

Methods. The records of 40 consecutive patients diagnosed with esophageal cancer referred for EUS staging were reviewed. Computed tomography (CT) scan then EUS imaging and EUS-guided FNA staging, including involvement of celiac node (M1a stage), surgical pathology, and subsequent treatment were correlated. Through-the-scope balloons were used for dilatation when needed to examine the celiac nodes.

Results. All 40 patients followed the protocol and were successfully imaged by EUS. Sixteen of the 40 required esophageal dilatation using the through-the-scope balloon. No complications were observed from esophageal dilatation for EUS. Twenty-three (58%) met the criteria for EUS-guided FNA biopsy from a total of 40 EUS imaging procedures. Twenty (87%) of the 23 EUS-guided FNA were directed toward the celiac nodes; 18 (90%) of the 20 were positive for malignancy and were treated by chemoradiation therapy and 2 (10%) FNA were negative for malignancy and were treated by surgical resection. The CT scan was able to detect only 6 (30%) of 20 cases of suspicious celiac lymph nodes, of which 5 (83%) were positive for malignancy by FNA.

Conclusions. EUS-guided FNA of celiac nodes (20 patients) directed management in all patients biopsied. EUS-guided FNA is superior to CT scan for diagnosing M1a disease. Protocol-directed EUS-guided FNA is a pivotal study when used in conjunction with stage-oriented treatment protocols for esophageal carcinoma.


   Introduction
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 Abstract
 Introduction
Material and methods
 Results
 Comment
 References
 
Once the diagnosis of esophageal carcinoma has been histologically established from esophagoscopy and biopsy, staging of the tumor is the next critical step in determining the risk versus benefit of available therapeutic options, which include chemotherapy, radiation, surgery alone or chemotherapy plus radiation and surgery. Outcome assessments have failed to demonstrate superiority of any of the available therapeutic options. Detailed staging therefore is imperative as future therapeutic trials are conducted.

Computed tomography (CT) scans are widely used for clinical staging of esophageal cancer owing to ready availability. The accuracy of CT scan in determining tumor invasion is 54% to 63% and for lymph node involvement, 55% to 57% [1, 2]. CT therefore lacks sufficient accuracy in locoregional staging to direct management algorithms. Positron emission tomography (PET) scanning appears superior to CT for detecting distal metastasis; however, PET scan is nonspecific for detection of locoregional disease and celiac node involvement [3, 4].

Endoscopic ultrasonography (EUS) is the latest addition to the armamentarium of diagnostic tools for staging of esophageal carcinoma. The overall staging accuracy of EUS imaging alone is reported as 79% for T and N staging combined [5] (Fig 3). When tumor volume by EUS imaging alone is used as a marker for predicting prognosis, tumors with volume less than 50 mm3 had a 100% 5-year survival rate [6]. In a comparison of EUS imaging versus CT scan, the sensitivity and specificity of EUS for celiac lymph nodes has been defined at 72% and 97%, respectively, and that of CT scan 8% and 100% [7]. With the development of EUS-guided fine needle aspiration (FNA), tissue-directed staging is now possible (Fig 4). As the sensitivity and specificity is increased, EUS-guided FNA has resulted in upstaging of tumors in as many as 80% of cases with distal lymph node involvement (M1 disease) [8]. The purpose of our study was to determine the impact of EUS-guided FNA compared with EUS imaging alone and CT scan on our algorithm-directed management.



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  		Fig 3. Radial ultrasonographic image of a T3 lesion (thick arrow) with locoregional lymph nodes, N1 (thin arrows).

 


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  		Fig 4. Curvilinear endoscopic ultrasonography image of a celiac axis (CEL AX) lymph node (LN) undergoing fine needle aspiration.

 

   Material and methods
Top
 Abstract
 Introduction
 Material and methods
Results
 Comment
 References
 
Institutional Review Board approval was obtained for a retrospective chart review of 40 consecutive patients with esophageal cancer who were referred for endoscopic ultrasound between April 1998 and October 2000. The staging protocol as outlined was followed (Fig 1). The average age of the patients was 58 years (range 38 to 83). There were 13 women and 27 men. The CT scans of all patients were reviewed with particular attention to celiac axis lymph nodes before each procedure with an attending radiologist. Nodes greater than 1 cm were considered as metastatic on CT imaging. Informed consent was obtained from all patients for the EUS procedure. The patients took nothing by mouth before the examination. Meperidine, droperidol, and midazolam were used as sedatives and all examinations were performed in the left lateral position.



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  		Fig 1. Endoscopic ultrasonography (EUS) fine needle aspiration (FNA) biopsy protocol. (CT = computed tomography; LN = lymph node.)

 
Equipment used to perform the examinations included a 7.5 to 12 MHz radial echoendoscope (GF-UM 30; Olympus America Inc, Melville, NY), curvilinear array echoendoscope ([CLA-E] FG-36UX; Pentax Precision Instruments, Orangeburg, NY), and a 21-gauge Echotip needle (Wilson Cook, Winston-Salem, NC), Through-the-scope (TTS) balloon dilators (Microvasive, Winston-Salem, NC). All the examinations were interpreted by the same experienced endosonographer (IW). A diagnostic forward viewing scope was passed first. If the lesion could not be transversed then TTS balloon dilators were used to dilate the lumen to allow passage of scope. The range of the dilators used was 8 mm to 18 mm.

Initially the radial echoendoscope was used to stage the lesion by imaging alone. Staging was performed using the TNM classification. All nodal stations (right upper, left upper, left lower and right lower paratracheal, aortopulmonary, right and left tracheobronchial, subcarinal, paraesophageal, and celiac) were examined with particular attention given to the celiac region in all patients. Any suspicious lymph nodes (having at least one of the following criteria: hypoechoic, greater than 1 cm, round to oval with well-defined margins) were identified and their location was recorded. Repeat examination with a CLA-E was performed. Suspicious lymph nodes that if proven positive would change stage were identified again and biopsied. The biopsy was obtained by puncturing the lymph node with a 21-gauge needle passed through the channel of the echoendoscope under ultrasound guidance. This technique has been described in greater detail earlier [9]. The sample was then examined in the room by an attending cytopathologist. If an adequate sample was obtained, the procedure was stopped and a preliminary diagnosis rendered. After the procedure the patient was observed until recovery from anesthesia. After EUS staging and EUS-guided FNA, the CT scan findings, including involvement of celiac node (as per staging protocol), surgical histopathologic (when performed), and management of these patients was reviewed (Fig 1).

Analysis
The sensitivity, specificity, accuracy, and negative and positive predictive values were calculated for EUS alone, EUS-guided FNA, and CT scan on the basis of cytology or surgical pathology and then compared. Then the results of EUS-guided FNA were compared with management decisions in terms of surgery versus adjuvant palliative treatment.


   Results
Top
 Abstract
 Introduction
 Material and methods
 Results
Comment
 References
 
We were able to evaluate celiac lymph node status by EUS imaging alone in all 40 patients (Fig 2). Sixteen (40%) patients required dilation with a TTS balloon in order to evaluate the celiac region. The dilations were performed using 8 mm to 18 mm balloons to provide access across the stricture for the echoendoscopes. No complications were experienced with the dilations and all lesions were imaged. Of the 40 esophageal cancers, 20 of the tumors were adenocarcinomas and 20 were squamous in origin. Twelve were located in the midesophagus with celiac nodes visualized in 4 of 12 and 18 were located in the distal esophagus with celiac nodes visualized in 16 of 18. Thirty-five (88%) patients were found to have nodes that fit the criteria for malignancy by EUS imaging alone and 5 patients did not (12%). These included celiac as well as locoregional lymph nodes (Fig 3).



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  		Fig 2. Flow diagram illustrating results and patient outcome according to our management algorithm for esophageal cancer. (Ca = cancer; Chemo/Rad = chemoradiation therapy; EUS = endoscopic ultrasonography; FNA = fine needle aspiration; LN = lymph node; + = positive; - = negative.)

 
Twenty-three of 40 patients underwent EUS-guided FNA (Fig 4). In 12 cases biopsies were not obtained from the locoregional lymph nodes as they would not change the stage of the disease. By EUS imaging alone 20 (50%) patients of the 40 had celiac nodes that were suggestive of malignancy, the rest were locoregional. Biopsies were obtained from 3 locoregional nodes, because if positive they would have an impact on tumor staging, 1 positive and 2 negative by FNA. Eighteen (90%) of the 20 patients with celiac nodes had cytology positive for malignancy (M1a) and the other 2 (10%) were negative for malignancy by FNA (stage I). Both of these patients underwent esophagectomy and were found to be negative for celiac node metastases on surgical histopathology. The 18 (100%) patients who had metastatic celiac lymphadenopathy were sent for combined palliative chemotherapy (5-fluorouracil and cisplatin) and concurrent radiation therapy (Fig 2).

CT scan was only able to detect a total of 6 (30%) cases of 20 with M1a disease. Five of the 6 (83%) were positive for metastatic disease. The CT scan sensitivity, specificity, and accuracy were 30%, 67%, and 35%, respectively. The sensitivity, specificity, and accuracy of EUS alone were 100%, 50%, and 90%, respectively. EUS-guided FNA sensitivity, specificity, and accuracy was 100% by cytology (Table 1). There were no procedural complications either from dilation or EUS-guided FNA reported.


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  		Table 1. Comparison of Computed Tomography (CT), Endoscopic Ultrasonography (EUS), and EUS Fine Needle Aspiration (FNA) for M1a Staging

 

   Comment
Top
 Abstract
 Introduction
 Material and methods
 Results
 Comment
References
 
Management of esophageal carcinoma requires accurate staging at the time of diagnosis to direct the treatment modality. Surgical resection is a potentially curative treatment available for locoregional esophageal cancer; however, it offers no clinically important survival advantage in patients with M1a or M1b disease [10]. The perioperative mortality ranges from 1.2% to 4.6% depending on surgeon experience [11, 12]. Thus staging provides us with not only the treatment modality to be used but can also help in anticipating the risk versus benefit of disease management. The predictors of long-term survival in this disease are T stage (depth of tumor), N stage (nodal involvement), and M stage (metastasis). Penetration of the tumor through the esophageal wall with invasion of adjacent major structures (stage T4) renders the patient inoperable. Patients with locoregional lymph node involvement have only a 31% 5-year survival [5]. Involvement of the celiac lymph nodes in esophageal carcinoma is considered to be metastatic disease (M1a disease). In patients with positive celiac nodes the median survival was only 3 months compared with 30 months in the absence of celiac lymph nodes, when surgery was used as the only treatment modality [13]. Van Dam and colleagues [14] reported 55 patients who underwent EUS before up-front chemoradiation therapy with a complete response rate of 60% in T2 patients, 33% in T3 patients, and 63% in T4 patients. The complete response rate was 38% for N0 disease versus 43% for N1, leading to the implication that staging did not affect response rates. Their study, however, did not include patients with metastatic disease, had no long-term follow-up data on survival, and staging was done by imaging rather than histology.

Until recently, surgical exploration with lymph node sampling has been the only means for definitively staging esophageal carcinoma. Advances in image technology have greatly changed the preoperative evaluation. Lymph node involvement may be assessed by CT scan, PET scan, EUS, or thoracoscopy/laproscopy. CT scan uses size and distortion of anatomy to determine if there is infiltration of the lymph nodes by tumor cells. A lymph node greater than 1 cm is considered malignant by CT scan with an accuracy rate of 50% [15]. Malignant celiac nodes (M1a) are more difficult to image due to location [16]. In our study, the CT scan accuracy rate was 35% with a sensitivity and specificity of 30% and 67% using a size threshold of 1 cm for positivity.

PET scans use a physiologic mechanism rather than size to yield information by utilizing 2-[18 fluorine]-fluro-2-deoxy-D-glucose (FDG), a glucose analogue that has an increased uptake in malignant tissue compared with normal tissue. PET scan appears to be an excellent modality for detecting distant metastasis with a reported accuracy of 91% and recurrent disease with a reported accuracy of 87% [17, 18]. In terms of tumor staging, PET scan is limited due to an intrinsic spatial resolution of about 5 mm and its locoregional nodal involvement accuracy, which varies from 24% to 90%. Overall, PET scanning’s main drawback is the lack of anatomic detail to assess local invasion for T staging and resectability [4].

The combination of video-assisted thoracoscopy and laparoscopy has been shown to double the number of positive lymph nodes identified by conventional noninvasive techniques like EUS, CT, and PET scans [19]. However, this staging combination is significantly more invasive and requires general anesthesia.

EUS has recently gained support as an accurate imaging modality available for T staging and the diagnosis of malignant locoregional lymph nodes in esophageal carcinoma. The local staging accuracy of as high as 92% and lymph node staging of 86% appears better than the CT scan, magnetic resonance imaging (MRI), and open staging performed at the time of operation [20]. The limitations of EUS include overstaging (especially in T1 and T2 lesions because of fibrotic or inflammatory changes surrounding the tumor), understaging (because of microscopic invasion below the resolution of the scanning device especially in T3 lesions), and the presence of strictures, which may prevent the passage of echoendoscope [21]. In our experience, these high-grade malignant strictures can be overcome by dilation with TTS balloons. We were able to dilate all strictures safely without complication and assess celiac lymph node status.

EUS imaging diagnosis of malignant lymph nodes is determined by the following criteria: size greater than 1 cm, hypoechoic, distinct margins, and round shape. Bhutani and associates [22] reported 35 lymph nodes in 25 patients with lung, esophageal, and pancreatic cancer. When all the above EUS imaging criteria were seen in the same lymph node, the diagnostic accuracy of EUS alone for predicting malignant invasion was 80%; however, only 25% of the visible lymph nodes met all four criteria [22]. In our study, when EUS-guided FNA was performed with disregard to imaging characteristics, the staging accuracy increased from 90% to 100% as compared with EUS alone. We were able to define malignant versus benign lymph nodes with 100% accuracy with EUS-guided FNA. Two cases were down staged by EUS-guided FNA from EUS imaging, as was proven on histopathology of surgical specimen. Our results were similar to a study by Giovannini and colleagues [8], who also had a 100% accuracy with EUS-guided FNA but that study included all lymph nodes (cervical, mediastinal, and celiac).

Options for esophageal cancer treatment include combined palliative chemotherapy and radiotherapy, surgery alone, and surgery with neoadjuvant chemoradiation, all of which are still under evaluation. Precise staging is required for patient selection for trials looking at chemoradiation versus surgery. At our institution we use the following algorithm: patients with M1a disease and good performance status receive neoadjuvant chemoradiation and those with poor performance status receive palliative chemoradiation. Those with stage II/III disease may receive neoadjuvant chemoradiation with intent to reduce the size of the tumor before surgery or go to surgery. Patients with stage I go directly to surgery (Fig 5). In our study, all patients had EUS and 20 (50%) patients underwent EUS-guided FNA of suspicious celiac nodes. Eighteen patients with positive celiac lymph nodes were treated with palliative chemoradiation. Both patients who were negative for celiac node malignancy by EUS-guided FNA were found to have no malignancy in the celiac lymph nodes at surgery. Therefore management was influenced in all patients who underwent EUS-guided FNA.



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  		Fig 5. Suggested management algorithm based on cytology proven nodal status. (CHEMO/RAD = chemoradiation therapy; CT = computed tomography; EUS = endoscopic ultrasonography; FNA = fine needle aspiration; PET = positron emission tomography.)

 
In summary, EUS-guided FNA of celiac nodes has an invaluable role in esophageal cancer management when used in conjunction with stage-oriented treatment protocols and should be performed in all patients with suspicious celiac axis nodes.


   References
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 Abstract
 Introduction
 Material and methods
 Results
 Comment
 References
 

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