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Ann Thorac Surg 2001;71:290-294
© 2001 The Society of Thoracic Surgeons

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Original article: general thoracic

Evaluation of lymph node metastases in squamous cell carcinoma of the esophagus with positron emission tomography

^a Department of Thoracic and Cardiovascular Surgery, Sungkyunkwan University School of Medicine, Samsung Medical Center, Seoul, South Korea
^b Department of Nuclear Medicine, Sungkyunkwan University School of Medicine, Samsung Medical Center, Seoul, South Korea
^c Department of Radiology, Sungkyunkwan University School of Medicine, Samsung Medical Center, Seoul, South Korea

Accepted for publication July 17, 2000.

Address reprint requests to Dr Shim, Department of Thoracic and Cardiovascular Surgery, Samsung Medical Center, 50 Ilwon Dong Kangnam Gu, Seoul, Korea
e-mail: ymshim{at}smc.samsung.co.kr

	Abstract

Top Abstract Introduction Material and methods Results Comment References

 
Background. Previous studies suggest positron emission tomography (PET) may improve staging accuracy of esophageal cancer compared with conventional methods, especially in detecting occult distant metastases. We evaluated the accuracy of PET in the detection of lymph node metastasis prospectively with pathologic findings.

Methods. Fifty-three patients with squamous cell carcinoma underwent whole-body PET scan and chest computed tomography (CT). The findings of PET and chest CT of 50 patients who underwent curative esophagectomy with radical lymph node dissection were compared with the pathologic findings.

Results. Among 53 primary esophageal tumors, PET detected 51 (96.2%) and CT detected 49 (92.5%) tumors correctly. Nodal metastases were present in 108 of 436 dissected lymph node groups. PET detected 56 metastatic node groups (51.9% sensitivity, 94.2% specificity, 83.7% accuracy), compared with CT, which detected 16 (14.8% sensitivity, 96.7% specificity, 76.6% accuracy; sensitivity: p < 0.005).

Conclusions. PET was more sensitive than CT in the detection of nodal metastases and may improve staging of squamous cell carcinoma of the esophagus.

	Introduction

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The accurate staging of esophageal cancer is essential to select appropriate treatments and to anticipate disease progression. Conventional imaging methods that rely on detection of the structural changes caused by tumors are inaccurate in determination of the extent of esophageal cancer, especially lymph node metastasis. Positron emission tomography (PET) is a fundamentally different imaging technology that identifies focal areas of increased metabolism associated with malignancies. PET was found to provide useful information about lung cancer, breast cancer, malignant melanoma, and some other malignancies [1–7]. Some literature has recently demonstrated that fluorodeoxyglucose (FDG) PET is more sensitive than computed tomography (CT) for detecting regional and distant metastases in esophageal cancer patients and unnecessary surgery could be avoided using PET [8–11]. However, there are only a limited number of studies demonstrating the role of PET in the staging of esophageal cancer, and previous works were done primarily in patients with adenocarcinoma of the esophagus. We decided to compare the accuracy of the FDG-PET with that of CT in the staging of squamous cell carcinoma of the esophagus prospectively, especially focusing on lymph node metastasis with surgical biopsy specimens.

	Material and methods

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Between February 1997 and December 1998, 53 consecutive patients (50 men and 3 women) with biopsy-proven squamous cell carcinoma of the esophagus participated in this prospective study at Samsung Medical Center, Seoul, Korea. The median age was 61 years (range 41 to 76). Preoperative diagnosis was confirmed by pathologic review of fresh endoscopic biopsy specimens. Ten patients had associated pulmonary tuberculosis and three cases were active. All patients underwent CT and PET scanning at our institution with written consent. Bone scan was done in all patients, but endoscopic ultrasonography (EUS) was taken selectively when local invasion of the esophageal tumor or regional lymph node metastasis was suspected.

Three of these patients had inoperable diseases and thus were not candidates for this series: 1 patient had esophageal cancer with direct tracheal invasion that was confirmed by bronchoscopy, and the other 2 had multiple liver metastases diagnosed by abdominal ultrasonography. They were treated by chemotherapy and radiation therapy.

Surgery was performed in 50 patients and there was no patient who had neoadjuvant therapy. Twenty-six patients had tumors in the mid thoracic esophagus, 16 had tumors in the lower thoracic esophagus, and the remaining 8 had tumors in the upper thoracic esophagus. Transthoracic esophagectomy with extensive lymph node dissection was performed in 47 patients, and 13 of them also underwent three-field lymph node dissection. The remaining 3 patients underwent transhiatal esophagectomy (Table 1).

Positron emission tomography scanning
PET imaging was obtained with the GE Advance PET scanner (General Electrical Medical Systems, Milwaukee, WI), which allows simultaneous collection of 35 transverse slices over a span of 15.2 cm. The reconstructed spatial resolution under clinical imaging conditions is approximately 4.25 mm FWHM (full width at half maximum). Patients fasted for at least 4 hours before scanning. Before emission scanning, transmission scans were obtained for 20 minutes on the primary tumor region. We administered 370 MBq of [F-18] FDG intravenously and dynamic emission scans were obtained for 56 minutes. Attenuation-corrected images at 46 to 56 minutes after injection of FDG were obtained. Whole body emission scans were obtained for the detection of metastases (5 minutes for each bed). For quantitative evaluation, the region of interest was defined over the areas with increased FDG uptake (tumor and lymph node metastases). Regional FDG uptake was expressed as the standardized uptake value (SUV) and tumor involvement was defined as peak SUV greater than or equal to 3.5. All PET images were evaluated qualitatively by the consensus of two experienced nuclear medicine physicians without prior knowledge of the findings on CT.

Staging
Staging was based on TNM classification (American Joint Committee on Cancer, 1992), and lymph node grouping was made by the mapping of lymph nodes in carcinoma of the esophagus suggested by H. Akiyama [12] (Table 2).

	Results

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Primary tumors
The sensitivity of PET and CT was 96.2%(51 of 53) and 92.5%(49 of 53) at the initial diagnosis of primary tumors. False negatives on PET scan were a 1-cm carcinoma in situ (CIS) and a T1 stage cancer. CT scan was also false negative for them and for two more T1 stage cancers. The peak SUV in the primary tumor ranged from 3.5 to 19.2, with a mean value of 11.9 ± 3.2. There was only two distant organ metastases detected by PET; multiple liver metastases were confirmed by ultrasonography.

Lymph node metastases
Among 50 patients who underwent esophagectomy, two-field lymph node dissection was performed in 34 patients and three-field lymph node dissection was performed in 13 patients in whom the tumor located in the upper thoracic esophagus. We dissected 436 lymph node groups in 50 patients and the average number of dissected lymph node group was 8.7. The total number of dissected lymph nodes was 2,561 and the average number of dissected lymph node per patient was 51.2. According to histopathologic findings, nodal metastases were present in 108 of 436 lymph node groups.

The diagnostic sensitivity, specificity and accuracy of PET and CT for detecting nodal metastases is shown in Table 3. The sensitivity of PET was significantly higher than that of CT in detecting nodal metastases (p < 0.05). We believe that the high specificity of CT was probably due to low sensitivity. PET detected 40 metastatic lymph node groups that were missed by CT in 25 patients (Fig 1). Eight of 10 patients with either active or inactive pulmonary tuberculosis had a false positive lymph node group on PET (Fig 2). Among 52 false negative lymph node groups on FDG-PET, 36 lymph node groups were located in the cervical area or upper abdomen where attenuation correction was not performed and 10 lymph node groups were located adjacent to the primary tumor, and the other 6 lymph node groups were in the thorax not adjacent to the tumor. The accuracy of PET and CT for NM staging was 76% (38 of 50) and 54% (27 of 50), respectively. Thirteen of 50 patients had distant metastatic lymph node groups on histopathologic findings (7, cervical lymph node groups; 6, celiac lymph node groups). Whereas PET detected distant lymph node metastases in 9 patients (4 cervical, 3 celiac, and 2 both lymph node groups), CT could detect metastatic lymph node groups in only 2 patients, which were all celiac nodes.

View larger version (115K): [in this window] [in a new window]   Fig 1. Computed tomograms of the upper and mid thorax and the upper abdomen in 3 patients show no significantly enlarged lymph nodes. However, corresponding transaxial fluorodeoxyglucose positron emission tomography images demonstrate abnormal increased activities in regional lymph nodes that were positive for tumor on histopathology. (Top) right paratracheal lymph node; (middle) subcarinal lymph node; (bottom) left gastric artery lymph node.

View larger version (71K): [in this window] [in a new window]   Fig 2. Fluorodeoxyglucose positron emission tomography (FDG PET) and computed tomograms of 61-year-old patient with upper esophageal cancer. FDG PET demonstrates abnormal increased activity in upper esophagus, bilateral hilar, and right intrapulmonic lymph nodes; however, those lymph nodes were confirmed negative for tumor by histopathology. In this patient, a computed tomogram shows stable pulmonary tuberculosis in the left upper lobe, suggesting that those might be lymph nodes reactive to tuberculosis.

	Comment

Top Abstract Introduction Material and methods Results Comment References

Since CT was introduced in 1974, it has been the imaging test of choice for the preoperative evaluation of gastrointestinal malignancies and has made a great contribution in fact. But the role of CT in the evaluation of esophageal cancer is still controversial, especially in the detection of nodal metastasis [16–18]. Because CT detection of lymph node metastasis is based on the size of the nodes, limited tumor involvement in normal-sized nodes cannot be detected. EUS represents a significant advance in the accurate evaluation of tumor invasion and local lymph node involvement, but difficulties in EUS can arise when the tumor results in an esophageal obstruction or stenosis beyond which the endoscope cannot pass. In addition, although EUS is determined by lymph node outline and internal echoic pattern, it mainly relies on the size of the nodes to determine metastasis; therefore it cannot distinguish nodal metastasis from reactive hyperplasia or inflammation of the lymph nodes [15]. Metabolic changes often precede the structural changes associated with any given disease processes [7, 19].

Recently, it has become possible to assess regional metabolism noninvasively with PET and metabolic tracers. FDG is a glucose analogue that is now widely used to evaluate regional glucose metabolism in a variety of cancers. Like glucose, FDG is transported into most tissues and cells and phosphorylated by intracellular hexokinase. Unlike glucose-6 phosphate, FDG-6 phosphate is a poor substrate for further metabolism, cannot diffuse back through the cell membrane, and is therefore metabolically trapped within the cell. FDG accumulates in local tissues at a rate proportional to the local rate of glucose metabolism. Flanagan and colleagues [8] have demonstrated that both squamous cell carcinoma and adenocarcinoma of the esophagus avidly accumulate FDG. By using [F-18] FDG, PET provides information about focal increased glucose metabolism associated with malignancies, and thus PET has the potential to show metastases in normal-size lymph nodes. The clinical application of PET can be categorized into three major compartments: first, distinction between benign and malignant tumor (diagnosis of malignant tumor); second, staging of malignant tumor; and third, monitoring of therapeutic response. FDG PET has been successfully applied to a variety of malignant human tumors, such as primary intracranial tumor, breast cancer, malignant melanoma, and lung cancer [1–7].

Flanagan and associates [8] have shown in a group of 29 patients with esophageal cancer who underwent curative surgery that the accuracy of PET and CT for detection of nodal metastasis was 76% and 45%, respectively. They also reported that they could avoid of unnecessary surgery in 5 of 36 patients screened. Luketich and colleagues [11] reported that PET could detect 51 sites of distant metastases missed by CT scanning in 70 metastases and PET was more accurate than CT in detecting distant metastases. In our series, PET detected 9 of 13 (69.2% sensitivity) distant nodal metastases compared with CT’s detection of only 2 distant nodal metastases (15.4% sensitivity), which result is compatible with other reports. However, the sensitivity, specificity, and accuracy of PET and CT for detection of group nodal metastasis were 51.9%, 94.2%, 83.7% and 14.8%, 96.7%, 76.6%, respectively.

The sensitivity of PET and CT in this study was somewhat lower than those of other studies. We believe that there are several reasons causing lower sensitivity. First, we performed transthoracic esophagectomy with extensive lymph node dissection instead of transhiatal esophagectomy or lymph node sampling in almost all of our patients (47 of 50, 94%). And we performed operations even in patients with suspected distant lymph node (cervical and celiac) metastases on PET and CT instead of laparoscopic lymph node biopsy or other nodal sampling. In patients with tumor involving upper thoracic esophagus, we did three-field lymph node dissection for complete resection of the esophageal cancer. Second, we calculated sensitivity for each lymph node groups, not for N stage. Third, we studied prospectively to prevent sensitivity from being overestimated. And fourth, the histopathologic type of all patients who participated in this study was squamous cell carcinoma only, compared with previous works that were done mainly in patients with adenocarcinoma of the esophagus.

Diverse results of FDG PET scan have been expected in patients with pulmonary tuberculosis, and increased accumulation of FDG in lymph nodes with pulmonary tuberculosis contributed to 8 false-positive results. The high incidence of associated pulmonary tuberculosis in this study was caused by the prevalence of pulmonary tuberculosis throughout Korea in the 1960s. One of our most important findings is the location of false-negative lymph nodes. Among 52 false-negative lymph node groups on FDG-PET, 36 lymph node groups were located either in the cervical area or upper abdomen where attenuation correction was not performed and 10 lymph node groups were located adjacent to primary tumor. We speculate that primary tumor itself might obscure the delineation of very near surrounding lymph nodes. When metastatic nodal disease is abutting the primary tumor, it can be difficult to distinguish activity in the nodes from the intense activity in the primary tumor. We believe that EUS or CT will be helpful to overcome those weak points of PET scan, and attenuation-corrected images including the neck, thorax and upper abdomen may enhance the sensitivity of nodal metastasis.

In summary, PET is more sensitive than CT scan in the determination of regional and distant lymph node involvement in the squamous cell carcinoma as well as adenocarcinoma of the esophagus. PET can play an important role in evaluating the pretreatment staging of esophageal cancer. When there is coexistence of pulmonary tuberculosis, there should be cautious interpretation of PET findings of lymph node. Further studies will be required to define the role of PET in evaluating tumor response to clinical treatment as well as in the staging of esophageal cancer.

	References

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This Article Abstract Full Text (PDF) Alert me when this article is cited Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in PubMed Alert me to new issues of the journal Add to Personal Folders Download to citation manager Author home page(s): Kwhanmien Kim Seung Joon Park Young Mog Shim Permission Requests Citing Articles Citing Articles via HighWire Citing Articles via Google Scholar Google Scholar Articles by Kim, K. Articles by Shim, Y. M. Search for Related Content PubMed PubMed Citation Articles by Kim, K. Articles by Shim, Y. M. Related Collections Esophagus - cancer