Ann Thorac Surg 2007;83:2000-2002
© 2007 The Society of Thoracic Surgeons
Original Articles: General Thoracic
Endoscopic Ultrasound Compared With Laparoscopy for Staging Esophageal Cancer
Neeraj Kaushik, MDa,
Asif Khalid, MDa,
Debra Brody, RNa,
James Luketich, MDb,
Kevin McGrath, MDa,*
a Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania
b Division of Thoracic and Foregut Surgery, University of Pittsburgh Medical Center, Pittsburgh, Pennsylvania
Accepted for publication February 9, 2007.
* Address correspondence to Dr McGrath, UPMC Presbyterian, Mezzanine Level, C Wing, 200 Lothrop St, Pittsburgh, PA 15213 (Email: mcgrathk{at}dom.pitt.edu).
 |
Abstract
|
|---|
Background: Endoscopic ultrasonography (EUS) is an accurate modality for locoregional staging of esophageal cancer. Given an increasing prevalence of distal esophageal adenocarcinoma, some centers employ laparoscopic staging (LS) in addition to noninvasive staging methods. We sought to compare EUS and LS for nodal staging in patients with esophageal cancer.
Methods: All newly diagnosed, EUS-staged esophageal cancer cases during an 18-month period were reviewed. Patients who underwent both EUS and LS comprised the study cohort; EUS records, operative notes, and pathology reports were reviewed. Inability to pass the radial echoendoscope through the malignant stricture despite dilation was considered an incomplete EUS examination.
Results: Forty-seven patients were identified who underwent both modalities for staging; of these, 70% had complete EUS evaluation. For nodal staging, EUS–fine-needle aspiration was 90% accurate as compared with LS. Overall, staging accuracy of EUS compared with LS was 72%. Accuracy was 76% for patients with complete EUS staging compared with 64% for patients with incomplete EUS examinations. Staging differences were mostly reflected in distant metastases detected at LS (17%).
Conclusions: Endoscopic ultrasonography is nearly as accurate as LS in nodal staging for esophageal cancer. The value of LS is accurate abdominal nodal staging and detection of occult distant mestastases. Laparoscopic staging should, therefore, be incorporated into staging algorithms for neoadjuvant protocols. In the absence of preoperative therapy, LS should be performed at the time of planned esophagectomy. In those without occult metastases, curative resection may be attempted.
|
Introduction
|
|---|
Treatment and prognosis of esophageal cancer is dependent upon cancer stage at the time of diagnosis. A substantial majority of patients are not candidates for surgical resection owing to advanced stage at presentation [1]. Accurate locoregional staging of esophageal cancer is therefore of paramount importance as it directs appropriate treatment. Nonsurgical modalities currently used to stage esophageal cancer include helical computed tomography (CT), positron emission tomography (PET), and endoscopic ultrasound (EUS). While CT is the most widely available and least expensive of these modalities, it is not as sensitive or accurate in diagnosing inoperable T4 disease or metastatic celiac lymph nodes compared with EUS [2]. The diagnostic value of locoregional staging using PET is similarly limited owing to its low accuracy in determining local peritumoral spread and lymph node metastasis compared with EUS, although it is superior to CT in detecting distant metastasis [3]. Endoscopic ultrasonography and endoscopic ultrasound-guided fine-needle aspiration (EUS-FNA) are highly accurate and sensitive both for determining T stage and detecting locoregional and celiac lymph node metastasis [4, 5].
Combined thoracoscopic/laparoscopic staging (TS/LS) staging of esophageal cancer has been shown to be feasible, but requires hospitalization [6]. Invasive surgical staging is considered more accurate than noninvasive staging; however, PET plus EUS-FNA has been recommended as the preferred staging algorithm based on cost effectiveness and quality-adjusted life-years [7]. Some centers, including ours, employ laparoscopic staging (LS) in addition to noninvasive modalities, as LS alone can generally be performed as an outpatient procedure. As there is no study comparing EUS and LS, we sought to compare the accuracy of these two modalities in nodal staging of esophageal cancer.
|
Patients and Methods
|
|---|
A retrospective review was performed for all patients who underwent EUS staging of newly diagnosed esophageal cancer during an 18-month period. This initial patient list was then cross-referenced to identify those who also underwent LS. Patients undergoing both staging modalities without intervening neoadjuvant therapy comprised the study cohort. Endoscopic ultrasonography records, operative notes, and pathology reports of the study patients were reviewed, and accuracy of the two staging modalities was compared. The Institutional Review Board of our medical center approved this study and waived the need for patient consent.
All EUS examinations were performed by one of two experienced endosonographers (A.K., K.M.). Patients underwent standard esophagogastroduodenoscopy (EG 2730; Pentax Medical, Montvale, New Jersey) immediately before EUS. Patients with nontraversable malignant stenosis underwent Savary-type dilation (up to 15 mm) to allow passage of the echoendoscope. Endoscopic ultrasonography staging was performed using the radial echoendoscope (Olympus GF-UM 130; Olympus America, Center Valley, Pennsylvania) and the curvilinear array echoendoscope (FG-36 UA; Pentax Medical). Endoscopic ultrasonography-FNA of suspected metastasis was performed using a 22G or 25G FNA needle (EchoTip; Wilson-Cook Medical, Winston-Salem, North Carolina) unless intervening tumor precluded needle passage. Incomplete EUS examination was defined as failure to traverse the malignant stenosis with the radial echoendoscope despite dilation, as this precluded assessment for perigastric or celiac lymph node metastasis.
Laparoscopic staging was performed in the usual manner by an experienced surgical team. The peritoneal cavity, liver surface, and stomach were thoroughly explored, and the lesser sac was entered to examine lymph nodes along the lesser curvature of the stomach. The celiac trunk was identified, and biopsies obtained from suspicious lesser curve, gastrohepatic, and celiac lymph nodes. Any other suspicious metastatic focus was also biopsied at the time of LS.
|
Results
|
|---|
Forty-seven patients underwent both EUS and LS before receiving treatment during the study period; they comprise the study cohort. The mean interval between EUS staging and LS was 6 days (range, 1 to 32). Table 1
shows the details of the study group demographics and tumor characteristics.
Table 2
shows the accuracy of EUS staging compared with LS. Thirty-three of 47 patients (70%) had a complete EUS examination. In this cohort, EUS staging accuracy was 76% as compared with LS. Four patients (12%) were understaged by EUS; 3 were staged as having T3N1Mx disease using the American Joint Committee on Cancer staging classification [8], and the remaining patient had T3N1M1a disease. At LS, 1 patient had an omental metastasis, 1 had a metastatic peritoneal tumor implant along with tumor implant near the caudate lobe of the liver, 1 patient had right and left hepatic lobe metastasis, and 1 patient had a metastasis in the lateral segment of the left hepatic lobe. Four patients (12%) were overstaged by EUS; 3 were suspected to have M1a disease based on suspicious appearing celiac lymph nodes not amenable to FNA owing to intervening tumor; 1 was staged as T3N1 because of suspicious perigastric lymph nodes. Biopsies of these celiac and perigastric lymph nodes at LS were negative for metastasis in all 4 patients.
Eleven of 33 patients (33%) with complete EUS staging underwent FNA of suspicious lymph nodes. A total of 14 lymph nodes were sampled by EUS-FNA, 9 of which were celiac lymph nodes. All sampled nodes were cytologically proven malignant.
Endoscopic ultrasonography staging was incomplete in 14 of 47 patients (30%), defined as an inability to traverse the malignant stenosis with the radial echoendoscope despite dilation. Endoscopic ultrasonography staging accuracy dropped to 64% in this subgroup. Five of 14 patients (36%) were understaged by EUS compared with LS. Two of those patients had peritoneal metastases, 1 had a right adrenal metastasis, 1 had a liver metastasis, and 1 had malignant perigastric lymphadenopathy. The overall staging accuracy of EUS was 72% as compared with LS. Nodal staging accuracy of EUS was 90%; LS changed the nodal stage in 5 of 47 patients. Laparoscopic staging detected distant metastases in 17% of patients. There were no complications related to EUS staging or LS.
|
Comment
|
|---|
The importance of esophageal cancer staging is to prognosticate, direct treatment, and avoid unnecessary surgery in patients who would not benefit from such therapy. The ideal staging algorithm for esophageal cancer, currently unknown, would be widely available, cost effective, and accurate. A universally accepted staging algorithm is still lacking, as practices are influenced by local expertise and hospital resources.
Endoscopic ultrasonography is an accurate modality for locoregional staging of esophageal cancer; with the addition of EUS-FNA, accuracy for nodal staging is further increased and is significantly better than CT or EUS alone [4, 5, 9]. Our results support the high accuracy of EUS-FNA for nodal staging, being 90% accurate as compared with LS. Four patients (9%) in our study were overstaged by EUS. These 4 patients were suspected to have N1 or M1a disease based on malignant appearing perigastric or celiac lymph nodes that were not amenable to EUS-FNA because of intervening tumor; these nodes were benign when sampled at LS. As it is known that EUS-FNA is more accurate for nodal staging compared with EUS alone [4], one must be cautious assigning an N1 stage based on morphologic appearance. This issue will continue to be problematic as certain peritumorous lymph nodes cannot be sampled by EUS. In our series, there was no change in the management of the 4 patients overstaged by EUS; they received neoadjuvant therapy (based on T3 disease) and were ultimately resected. At our institution, the finding of N1 or M1a disease does not preclude resection; we acknowledge that these findings, particularly M1a disease, portends a worse prognosis. Laparoscopic staging changed nodal staging in a total of 11% of patients: 4 patients, as previously mentioned, were overstaged by EUS. One patient staged Nx by an incomplete EUS examination was upstaged to N1 status by LS. Specifically regarding patients staged as N0 by EUS, none were upstaged to N1 by LS.
Overall, EUS staging accuracy was only 72% as compared with LS. This finding is reflected in the unexpected high incidence (17%) of distant metastatic disease detected at LS and highlights the added benefit of LS. In centers like ours, where the vast majority of esophageal malignancy is distal adenocarcinoma, that is of paramount importance given the higher yield of finding metastatic disease in the abdomen. Of our entire cohort, 9 patients (19%) were understaged by EUS; 8 of these had distant metastatic disease (M1) discovered at LS. Sites of distant metastases included peritoneum (3), left hepatic lobe (2), right hepatic lobe (1), omentum (1), and right adrenal gland (1). Of these sites, only the left hepatic lobe can be reliably evaluated by EUS if the malignant stricture can be traversed.
The major limitation of this study is the retrospective nature. Surgeons performing LS were not blinded to EUS staging results. Additionally, as the majority of patients received neoadjuvant therapy, neither staging modality could be compared with final surgical pathology. Ultimately, only 6 of 47 patients (13%) underwent resection without neoadjuvant therapy; therefore, no statistical comparisons could be made regarding accuracy of EUS or LS with final surgical pathology.
The benefits of EUS include its low cost, ability to provide accurate T staging, and ability to assess and sample mediastinal lymph nodes when staging esophageal cancer. The limitations of EUS include its inability to sample peritumoruous lymph nodes when there is intervening tumor, and its inability to traverse the malignant stricture with the echoendoscope to assess for lymphadenopathy and T4 disease. This latter point is reflected in the higher staging accuracy (76%) for complete EUS examinations compared with the accuracy (64%) of incomplete examinations in our study. Benefits of LS include high N staging accuracy for abdominal lymph nodes, and the ability to detect distant metastases in the abdomen. Limitations of LS include an inability to assess for mediastinal lymphadenopathy, inability to provide reliable T staging, and higher cost when performed as an independent procedure. We view EUS and LS as complementary staging modalities.
In our study, we compared EUS and LS for staging esophageal cancer. Based on our results, we submit that initial staging of newly diagnosed esophageal cancer include CT or PET imaging along with EUS. Endoscopic ultrasonography-FNA of all suspicious lymph nodes and occult metastases should be pursued to increase the staging accuracy. Laparoscopic staging, as a procedure independent of planned or possible esophagectomy, should be incorporated into staging algorithms for neoadjuvant research study protocols to increase staging accuracy. In clinical programs that support neoadjuvant therapy, it is unclear whether patients with cytologically proven N1 disease by EUS-FNA should undergo independent LS. An argument can be made to administer preoperative therapy, then perform LS at the time of planned esophagectomy, when patients without evidence of distant metastases can proceed to an attempt at curative resection. Laparoscopic staging should be performed in all patients with incomplete EUS examinations to assess the abdomen for nodal or distant metastatic disease. In practices that do not utilize neoadjuvant therapy, LS should be performed at the time of planned esophagectomy, as that would be most cost effective. The accuracy of EUS compared with LS for staging esophageal cancer, particularly distal adenocarcinoma, deserves further study in a prospective, randomized, and blinded fashion.
|
References
|
|---|
- Lightdale CJ, American College of Gastroenterology Esophageal cancer Am J Gastroenterol 1999;94:20-29.[Medline]
- Romagnuolo J, Scott J, Hawes RH, et al. Helical CT versus EUS with fine needle aspiration for celiac nodal assessment in patients with esophageal cancer Gastrointest Endosc 2002;55:648-654.[Medline]
- Rasanen JV, Sihvo EI, Knuuti MJ, et al. Prospective analysis of accuracy of positron emission tomography, computed tomography, and endoscopic ultrasonography in staging of adenocarcinoma of the esophagus and the esophagogastric junction Ann Surg Oncol 2003;10:954-960.[Medline]
- Vazquez-Sequeiros E, Wiersema MJ, Clain JE, et al. Impact of lymph node staging on therapy of esophageal carcinoma Gastroenterology 2003;125:1626-1635.[Medline]
- Eloubeidi MA, Wallace MB, Reed CE, et al. The utility of EUS and EUS-guided fine needle aspiration in detecting celiac lymph node metastasis in patients with esophageal cancer: a single-center experience Gastrointest Endosc 2001;54:714-719.[Medline]
- Krasna MJ, Reed CE, Nedzwiecki D, et al. CALGB 9380: a prospective trial of the feasibility of thoracoscopy/laparoscopy in staging esophageal cancer Ann Thorac Surg 2001;71:1073-1079.[Abstract/Free Full Text]
- Wallace MB, Nietert PJ, Earle C, et al. An analysis of multiple staging management strategies for carcinoma of the esophagus: computed tomography, endoscopic ultrasound, positron emission tomography, and thoracoscopy/laparoscopy Ann Thorac Surg 2002;74:1026-1032.[Abstract/Free Full Text]
- Fleming ID, Cooper JS, Henson DE. AJCC cancer staging manual. 5th ed.. Philadelphia, Pennsylvania: Lipincott-Raven; 1997. pp. 65-69.
- Vazquez-Sequeiros E, Norton ID, Clain JE, et al. Impact of EUS-guided fine-needle aspiration on lymph node staging in patients with esophageal carcinoma Gastrointest Endosc 2001;53:751-757.[Medline]
This article has been cited by other articles:
|
|
|
|
 
A. Pennathur and J. D. Luketich
Resection for Esophageal Cancer: Strategies for Optimal Management
Ann. Thorac. Surg.,
February 1, 2008;
85(2):
S751 - S756.
[Abstract]
[Full Text]
[PDF]
|
|
|
Top
Abstract
Introduction
