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10.1245/ASO.2003.12.002
Annals of Surgical Oncology 10:954-960 (2003)
© 2003 Society of Surgical Oncology
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ORIGINAL ARTICLES

Prospective Analysis of Accuracy of Positron Emission Tomography, Computed Tomography, and Endoscopic Ultrasonography in Staging of Adenocarcinoma of the Esophagus and the Esophagogastric Junction

Jari V. Räsänen, MD, Eero I. T. Sihvo, MD, M. Juhani Knuuti, MD, PhD, Heikki R. I. Minn, MD, PhD, Markku E. S. Luostarinen, MD, PhD, Pekka Laippala, PhD, Tapio Viljanen, MSc and Jarmo A. Salo, MD, PhD

From the Division of General Thoracic and Esophageal Surgery (JVR, EITS, JAS), Department of Cardiothoracic Surgery, Helsinki University Central Hospital, Helsinki, Finland; Department of Oncology and Radiotherapy (MJK, HRIM, TV), Turku PET Center, University of Turku, Turku, Finland; Department of Surgery (MESL), Paijat-Hame Central Hospital, Lahti, Finland; and School of Public Health (PL), University of Tampere and Research Unit, Tampere University Hospital, Tampere, Finland.

Correspondence: Address correspondence and reprint requests to: Jarmo A. Salo, MD, PhD, Division of General Thoracic and Esophageal Surgery, Department of Cardiothoracic Surgery, Helsinki University Central Hospital, PO Box 340, Haartmaninkatu 4, FIN-00029 HUS, Helsinki, Finland; Fax: 358-9-471-74479; E-mail: jarmo.salo{at}hus.fi


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Exact preoperative staging of esophageal cancer is essential for accurate prognosis and selection of appropriate treatment modalities.

Methods: Forty-two patients with adenocarcinoma of the esophagus or the esophagogastric junction suitable for radical esophageal resection were staged with positron emission tomography (PET), spiral computed tomography (CT), and endoscopic ultrasonography (EUS).

Results: Diagnostic sensitivity for the primary tumor was 83% for PET and 67% for CT; for local peritumoral lymph node metastasis, it was 37% for PET and 89% for EUS; and for distant metastasis, it was 47% for PET and 33% for CT. Diagnostic specificity for local lymph node metastasis was 100% with PET and 54% with EUS, and for distant metastasis, it was 89% for PET and 96% for CT. Accuracy for locoregional lymph node metastasis was 63% for PET, 66% for CT, and 75% for EUS, and for distant metastasis, it was 74% with PET and 74% with CT. Of the 10 patients who were considered inoperable during surgery, PET identified 7 and CT 4. The false-negative diagnoses of stage IV disease in PET were peritoneal carcinomatosis in two patients, abdominal para-aortic cancer growth in one, metastatic lymph nodes by the celiac artery in four, and metastases in the pancreas in one. PET showed false-positive lymph nodes at the jugulum in three patients.

Conclusions: The diagnostic value of PET in the staging of adenocarcinoma of the esophagus and the esophagogastric junction is limited because of low accuracy in staging of paratumoral and distant lymph nodes. PET does, however, seem to detect organ metastases better than CT.

Key Words: Adenocarcinoma • Esophagus • Esophagogastric junction • Positron emission tomography • Staging


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The incidence of adenocarcinoma of the esophagus and the esophagogastric junction has increased markedly.1–3 Survival rates are closely related to the stage of the disease at the beginning of treatment and the completeness of surgical R0 resection.4–7 Accurate pretreatment staging is crucial for the optimal choice of treatment. Multimodal therapy may improve outcome even in more advanced cases.8–10 However, limited resection has been suggested as the optimal treatment for early adenocarcinoma.11

Conventional staging methods, such as computed tomography (CT) and endoscopic ultrasonography (EUS), are useful but not ideal; they provide information only about structural characteristics.12–17 EUS with fine-needle aspiration is promising but is still undergoing investigation.18 The role of laparoscopic and thoracoscopic staging remains controversial.19–21

Positron emission tomography (PET) is based on the accumulation of a fluorinated glucose analog (18F-fluorodeoxy-D-glucose; FDG) in malignant cells.22 This can be observed by a positron camera. Thus, PET provides the opportunity to detect altered tissue metabolism in malignant tumors.23 Several authors have postulated the usefulness of PET in staging patients with esophageal cancer.24–30 Previous studies have either had a mixture of epidermoid cancer patients and adenocarcinoma patients or have been retrospective. The number of patients in many studies has been small, and lymph node dissection has been incomplete. In our prospective study, the purpose was to stage adenocarcinoma of the esophagus and the esophagogastric junction by PET, EUS, and CT and to compare results with histopathology of the specimens obtained by radical two-field lymphadenectomy.


   PATIENTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Between December 1998 and July 2002, in this prospective analysis, 42 operable patients with histologically proven adenocarcinoma of the esophagus or the esophagogastric junction were studied before radical esophagectomy and 2-field lymphadenectomy at the Division of General Thoracic and Esophageal Surgery in the Department of Cardiothoracic Surgery of Helsinki University Central Hospital. Exclusion criteria were inoperability for medical reasons or for unresectable tumor in conventional staging. In addition to staging with endoscopy, CT, and EUS, all included patients underwent PET. Frozen sections taken during surgery showed 10 of these patients to have an unexpected metastatic disease (stage M1b).31 After diagnostic sampling, they received palliative treatment. All patients gave informed consent, and the study protocol was approved by the Ethics Committee of Helsinki University Central Hospital.

PET Imaging
The radiochemical synthesis of FDG was a modification of the method reported by Hamacher et al.32 All PET studies were performed after a minimum fast of 6 hours. A median dose of 370 MBq of FDG was injected into the vein of the forearm, and after a 50-minute uptake period, patients were positioned supine on a scanner couch. PET acquisition commenced with a GE Advance scanner (GE Medical Systems, Milwaukee, WI), which has an axial field of view of 15 cm and a spatial resolution of 6 mm. The emission scan was obtained in four to five bed positions (5 minutes per position), starting from the level of the maxilla and moving down to the mid abdomen. The first 19 patients were imaged without transmission correction for photon attenuation. At the beginning of November 2000, the imaging protocol was fulfilled, and postemission transmission scans after 3 minutes in the same bed positions were acquired. All images were corrected for decay, dead time, and photon attenuation and reconstructed in a 128 x 128 matrix, with an ordered subsets expected maximum likelihood reconstruction algorithm and four iterations. For patients without transmission-corrected scans, standard Hanning-filtered backprojection with a .3 cutoff level was applied for image reconstruction.

Transaxial, coronal, and sagittal views were visually evaluated on a high-resolution display monitor (SUN workstation; Sun Microsystems, Inc., Mountain View, CA). Corresponding diagnostic CT scans of the chest and abdomen, as well as radiology reports, were always available, but no direct co-registration of PET and CT images was performed. All focally increased FDG uptake not associated with a known physiological accumulation of tracer was scored on a three-grade scale as definitively positive, potentially positive, and unlikely positive for cancer. After co-reading of CT and/or transmission scans, the anatomical localization of the focus was included in the evaluation.

Surgery
Right thoracotomy and laparotomy were always performed in curative operations. Our conventional two-field lymphadenectomy consisted of en-bloc esophagectomy with removal of adjacent lymphatic and areolar tissue between the tracheal bifurcation and the superior border of the pancreas. The block of tissue removed included, along with the bronchial, subcarinal, paraesophageal, parahiatal, celiac, left gastric, and splenic artery lymph nodes, the rim of the diaphragmatic muscle around the hiatus, the thoracic duct, both right and left mediastinal pleura, and the lesser curvature of the stomach, with a 10-cm distal resection margin. The dissection was bounded anteriorly by the main bronchi and pericardium and posteriorly by the vertebral column and aorta. Two-field esophagectomy could be performed on 32 patients. Nine patients were judged inoperable at surgery because of unexpected organ metastases and one because of a widespread para-aortic lymph node growth into the aorta and other retroperitoneal organs. This patient also had positive left supraclavicular lymph nodes. The total number of dissected lymph nodes was 1041 for radical operations, and the average number of dissected lymph nodes per patient was 33 (range, 12–51). A biopsy of cervical lymph nodes was undertaken if the preoperative imaging showed cervical metastases. In most palliative cases, a careful sampling was performed both intra-abdominally and intrathoracically. Every distant metastasis was identified histologically either by biopsy samples taken during an exploratory operation (10 lesions) or from resected specimens obtained in radical surgery (5 lesions). Five patients who were operated on and had an M1a stage disease received their diagnosis when the final pathology reports became available. False-positive findings were verified either histologically during exploratory surgery (cervicotomy in two patients and laparotomy in one patient) or by a 4-year follow-up (one patient).

Data Analysis
The histopathology of specimens was the gold standard to which the results of imaging modalities were compared. Tumor-node-metastasis classification was used according to the latest edition of the International Union Against Cancer.31 The agreement between histopathologic staging and EUS, CT, and PET was studied by using {kappa} statistics with 95% confidence intervals (95% CI). Fleiss33 suggested that {kappa} values <.4 reflect poor agreement; from .4 to .7, satisfactory agreement; and >.7, strong agreement. Sensitivity, specificity, and accuracy were also calculated by using standard definitions and compared by the McNemar test.34 Significance was set at P < .05. The accuracy of diagnosis of distant metastases was studied for the whole study group, whereas diagnostic correctness of staging of regional lymph nodes was performed only after the radical operation. Pathologic and clinical T staging were compared only in cases in which the primary tumor was removed.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Primary Tumor
The primary tumor was detected in 35 of 42 patients by using PET (sensitivity, 83%). A false-negative finding was, however, identified in seven patients, five of whom had small pT1 lesions (four tumors of <7 mm in diameter and one of 30 mm in diameter) and two of whom had T2 lesions (20 and 30 mm in diameter) without positive lymph nodes. CT, by contrast, identified the primary tumor in 28 patients (sensitivity, 67%). A T4 tumor found in CT was actually pT3. EUS could detect all tumors. Passage of the endoscope was not possible because of malignant obstruction in 6 of 32 radically operated patients (19%). Nevertheless, the endoscopist could estimate the T stage of the tumor in every case. All tumors for which the passage was obstructed were pT3, except for one, which was pT2. The results of EUS regarding T staging are shown in Table 1. The accuracy of EUS for assessing the depth of tumor infiltration in the patients undergoing esophageal resection was 20 (63%) of 32. EUS overstaged the T stage in 10 (31%) and understaged it in 2 (6%) of 32 patients. Among those six patients for whom EUS was incomplete, four (67%) were correctly staged and two (33%) were overstaged.


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  		TABLE 1. Preoperative diagnosis of tumor (T) stage with endoscopic ultrasonography (EUS) compared with histopathologic findings in patients undergoing esophageal resection
 
Locoregional Lymph Node Metastases
At surgery, metastatic locoregional nodes were found in 19 patients. Diagnostic sensitivity, specificity, and accuracy of PET, EUS, and CT for detecting locoregional nodal metastases are presented in Table 2.


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  		TABLE 2. Results of positron emission tomography (PET), computed tomography (CT), and endoscopic ultrasonography (EUS) in identifying locoregional nodal metastases among patients undergoing two-field lymphadenectomy
 
The accuracy did not differ significantly among EUS ({kappa} = .455; 95% CI, .145–.766), CT ({kappa} = .358; 95% CI, .093–.622), and PET ({kappa} = .322; 95% CI, .099–.545). Although the sensitivity of EUS was significantly higher than that of either CT or PET (P < .05), its specificity was poorer (P < .05). Combining the use of these techniques did not improve results. The high specificity of CT and PET was at least partly due to their low sensitivity. Among the six patients who had obstructing tumors, EUS correctly predicted five with N1 disease and also recognized one without positive locoregional nodal disease.

Metastatic Disease
Fifteen (36%) of the 42 patients had metastatic lesions (6 distant lymph node metastases and 9 organ metastases). Nine patients were considered inoperable during operation because of organ metastases and one because of widespread para-aortic lymphatic growth and metastatic left supraclavicular lymph nodes. Of these patients, PET could identify seven and CT four. The difference was not statistically significant. By combined use of CT and PET, 8 of the 10 could be detected. In three patients, widespread peritoneal carcinomatosis could not be detected by any of the imaging modalities, although PET showed one of these patients to have metastasis in a rib, suggesting stage IV disease (Table 3). Among those who were resected, final pathology reports showed four patients to have celiac and one to have para-aortic distant lymph node metastases. EUS gave additional information about distant metastasis in one patient who had celiac metastasis, which was seen only on EUS. However, two patients had celiac metastases that could not be verified by EUS, PET, or CT. PET showed false supraclavicular metastasis on the left side in three patients, and CT showed a wrong positive finding in the spleen in one patient. The sensitivity, specificity, and accuracy of PET and CT for distant metastases are listed in Table 4. The accuracy did not differ significantly between CT ({kappa} = .342; 95% CI, .068–.0616) and PET ({kappa} = .384; 95% CI, .094–.674). There were also no significant differences in sensitivity or specificity.


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  		TABLE 3. Findings of computed tomography (CT), positron emission tomography (PET), and endoscopic ultrasonography (EUS) for patients with inoperable disease
 

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  		TABLE 4. Detection of distant metastases by positron emission tomography (PET) and computed tomography (CT) in 42 patients with adenocarcinoma of the esophagus or the esophagogastric junction
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
We have in our institute followed generally accepted guidelines in the treatment of adenocarcinoma of the esophagus and esophagogastric junction. Obviously, however, these guidelines are under continual revision as new treatment alternatives become available. More precise staging is therefore needed. Preoperative staging is important only if it facilitates selection between different treatment options. Exact T staging is crucial when less radical approaches, such as endoscopic mucosa resection35 or limited resection for early adenocarcinoma,11 are considered. Lymph node involvement is a decisive factor in whether to give neoadjuvant treatment. Equally important is to exclude patients who have advanced disease from undergoing unnecessary surgical treatment. In our prospective series, a homogeneously staged patient group was selected. The additional staging was performed with PET, and only those who were potentially operable were included. We wanted to have a reliable gold standard when estimating the invasion depth of tumor and therefore considered only those tumors that were resected. Thus, we did not stage tumors that had invaded adjacent structures. Our results are, however, valuable when estimating the usefulness of PET as an extra investigation.

Although a change of the image reconstruction method midway through the trial was applied in PET, a similar change has previously been shown not to affect the rate of tumor detection.36 We therefore analyzed all PET findings together. The main results of this study are, first, that PET could neither identify very small primary tumors nor detect small-sized metastatic lesions, such as intra-abdominal carcinomatosis, and, second, that its sensitivity for detecting lymph node metastases was inferior to that of EUS. The primary indication for PET is not to diagnose tumors. Nevertheless, the overall ability of PET to detect malignant tissue of esophageal origin is relevant. If PET cannot detect very small primary tumors, it is unlikely to be able to identify small-volume metastatic lesions either. Other authors have confirmed the low sensitivity of PET in detecting esophageal tumors of small volume (Tis or T1).24,37 In our study, two pT2 tumors were not even visible in PET. Although PET’s spatial resolution is 6 mm, some tumors of up to 30 mm in diameter went undetected. Obviously, spatial resolution is not the only restriction in the accuracy of PET. Therefore, PET in its current form has limitations in detecting small-volume adenocarcinoma tissue of esophageal origin.

EUS is the only effective method for detecting invasion depth of a tumor, although overstaging is common.15 This is, however, clinically more acceptable than understaging. In this study, the accuracy of EUS in T staging was no more than 63%, which was in concordance with Flamen et al.,37 who had similar study settings. Our results were certainly different from the 80% accuracy in T stage achieved by Richards et al.13 Fortunately, understaging happened in only two patients. Perhaps the low accuracy can be explained by our selection bias, because we included only patients who were potential candidates for radical surgery and because only resected tumors were included in the final analysis. All of our cases were therefore T1 to T3, which are more difficult to distinguish from one another than clear T4 cases.

The ability of PET to detect metastatic locoregional lymph nodes (N1 disease) in our study was less than Flanagan et al.24 or Kole et al.25 have reported. Our results were, however, very similar to those reported by Flamen et al.37 on the accuracy of PET in identifying metastatic local lymph nodes. The explanation for this is that the extensive two-field lymphadenectomy performed in this study and that of Flamen et al.37 produced more lymphatic tissue for histopathologic analysis and therefore provided a more reliable reference for imaging studies. Many reports13,17,38 have advocated EUS for the prediction of T and N stages, but Salminen et al.15 found limitations in the accuracy of EUS for this purpose. In their study, both understaging (3%) and overstaging (25%) of the N state occurred with EUS. Our results support theirs. Although EUS reached a fairly high sensitivity (89%), the accuracy was not significantly better than in PET or in CT (75%, 66%, and 63%, respectively). These results are in agreement with Luketich et al.,39 who found an accuracy of 65% in EUS by using thoracoscopically and laparoscopically obtained histological specimens as references. We did not exclude patients with incomplete passage of the endoscope from either T stage or N stage analysis because Vickers and Alderson38 showed that tumors that cause luminal obstruction are almost always T3 or T4 and often have concurrent lymph node metastases. This can be confirmed even with limited EUS of the mediastinum. This conclusion was also justified in our patients.

Promising reports of the ability of PET to detect stage IV disease in esophageal cancer have been published by several authors.24,25,28,37 Our finding showed that the overall accuracy of PET to detect stage IV disease was not any better than the ability of CT. This was mostly because of the lack of sensitivity in finding distant lymph node metastases and false-positive judgment of cervical lymph nodes. Three of our patients had a false-positive finding that was identified by our nuclear medicine physician to very likely be a lymph node metastasis in the supraclavicular nodes. Findings of distant lymph node metastases, even in PET, must always be verified by histology or cytology because of the high rate of false-positive findings. Confirmation was achieved in our study by exploratory laparotomies, thoracotomies, or cervicotomies. In fact, the number of exploratory laparotomies and thoracotomies was quite high because PET, as a new method, was not considered trustworthy by our patients. Remarkably, PET was better able to predict inoperability than CT (PET, 7 of 10 vs. CT, 4 of 10). Kole et al.25 stated in their work that the accuracy of PET and CT to predict resectability was 88% and 65%, respectively. These findings are also in line with reports by Flamen et al.37 Luketich et al.,40 in their series of 91 patients, found PET to have an accuracy of 84% in identifying distant metastases. They observed that all metastatic sites missed by PET were <1 cm in diameter, which is in accord with our results of undetected peritoneal carcinosis in three patients with small lesions. CT is also known to have limitations in detecting small distant metastases, such as carcinomatosis.39 This proved to be the case in our study as well.

In conclusion, all of the staging methods used in this study have shortcomings. EUS has problems with accuracy in detecting the T and N stages. The development of new high-frequency probes and EUS with fine-needle biopsy may solve these problems in the future. CT is insufficiently sensitive in detecting distant metastatic lesions and locoregional nodal metastasis. PET can identify organ metastases fairly well, but its lack of overall accuracy in predicting M1 disease and an inability to identify locoregional metastases limits its reliability. However, the number of patients evaluated by PET has been quite small in studies performed to date, and a large multicenter study is needed before final conclusions can be drawn about its usefulness in staging esophageal adenocarcinoma.


   ACKNOWLEDGMENTS
 
The acknowledgments are available online at www.annalssurgicaloncology.org.

The authors thank Yvonne Sundström for skillful secretarial assistance.


   FOOTNOTES
 
Positron emission tomography is limited in staging adenocarcinoma of the esophagus and esophagogastric junction because of low accuracy in detecting paratumoral and distant lymph metastases.

Received for publication December 2, 2002. Accepted for publication May 2, 2003.


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TOP
 ABSTRACT
 INTRODUCTION
 PATIENTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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F. Banki, R. J. Mason, D. Oh, J. A. Hagen, S. R. DeMeester, J. C. Lipham, K. Tanaka, K. D. Danenberg, W. N. Yacoub, P. V. Danenberg, et al.
Plasma DNA as a Molecular Marker for Completeness of Resection and Recurrent Disease in Patients With Esophageal Cancer
Arch Surg, June 1, 2007; 142(6): 533 - 539.
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 Ann. Thorac. Surg.Home page
N. Rizk, R. J. Downey, T. Akhurst, M. Gonen, M. S. Bains, S. Larson, and V. Rusch
Preoperative (18)[F]-Fluorodeoxyglucose Positron Emission Tomography Standardized Uptake Values Predict Survival After Esophageal Adenocarcinoma Resection.
Ann. Thorac. Surg., March 1, 2006; 81(3): 1076 - 1081.
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 Am. J. Roentgenol.Home page
H. L. van Westreenen, J. T. M. Plukker, D. C. P. Cobben, C. J. M. Verhoogt, H. Groen, and P. L. Jager
Prognostic Value of the Standardized Uptake Value in Esophageal Cancer
Am. J. Roentgenol., August 1, 2005; 185(2): 436 - 440.
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 JCOHome page
M. Armanios, R. Xu, A. A. Forastiere, D. G. Haller, J. W. Kugler, and A. B. Benson III
Adjuvant Chemotherapy for Resected Adenocarcinoma of the Esophagus, Gastro-Esophageal Junction, and Cardia: Phase II Trial (E8296) of the Eastern Cooperative Oncology Group
J. Clin. Oncol., November 15, 2004; 22(22): 4495 - 4499.
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W. Kneist, M. Schreckenberger, P. Bartenstein, C. Menzel, K. Oberholzer, and T. Junginger
Prospective Evaluation of Positron Emission Tomography in the Preoperative Staging of Esophageal Carcinoma
Arch Surg, October 1, 2004; 139(10): 1043 - 1049.
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M. Torabi, S. L. Aquino, and M. G. Harisinghani
Current Concepts in Lymph Node Imaging
J. Nucl. Med., September 1, 2004; 45(9): 1509 - 1518.
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