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Ann Thorac Surg 2006;81:1076-1081
© 2006 The Society of Thoracic Surgeons

Original article: General thoracic

Preoperative 18[F]-Fluorodeoxyglucose Positron Emission Tomography Standardized Uptake Values Predict Survival After Esophageal Adenocarcinoma Resection

Nabil Rizk, MD a , * , Robert J. Downey, MD a , Timothy Akhurst, MBBS, FRACP b , Mithat Gonen, PhD c , Manjit S. Bains, MD a , Steven Larson, MD b , Valerie Rusch, MD a

a Thoracic Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, New York, New York
b Division Nuclear Medicine Service, Department of Radiology, Memorial Sloan-Kettering Cancer Center, New York, New York
c Biostatistics Service, Department of Epidemiology and Biostatistics, Memorial Sloan-Kettering Cancer Center, New York, New York

Accepted for publication September 22, 2005.

* Address correspondence to Dr Rizk, Thoracic Service, Department of Surgery, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021. (Email: rizkn{at}mskcc.org).


General thoracic surgery: To participate in The Annals of Thoracic Surgery CME Program, please visit http://cme.ctsnetjournals.org

 

   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
BACKGROUND: Clinical staging modalities for esophageal cancer are inaccurate at determining prognosis, especially in early-stage patients. We performed a retrospective review of patients with esophageal adenocarcinoma imaged by positron emission tomography before surgical resection to determine whether 18[F]-fluorodeoxyglucose uptake predicted overall survival independently of clinical and pathologic stage.

METHODS: The study is a retrospective review of patients with adenocarcinoma of the esophagus treated by surgery. All patients were imaged with computed tomography and positron emission tomography imaging, and most patients had an endoscopic ultrasound. We compared positron emission tomography standardized uptake values (SUVmax) with clinical and pathologic stage and survival. Prognostic variables were assessed by log-rank test, and survival by the method of Kaplan and Meier.

RESULTS: From January 1996 through June 2004, 50 patients meeting study eligibility criteria were analyzed. Median follow-up for surviving patients was 27 months. The median SUVmax was 4.5. Stratification of patients by the median SUVmax predicted survival. The 3-year survival was 57% for patients with an SUVmax greater than 4.5 and 95% for patients with an SUVmax of 4.5 or less (p = 0.02). The survival advantage of the SUVmax 4.5 or less group was also seen in clinically early-stage patients (defined as no adenopathy on computed tomography and positron emission tomography, and by endoscopic ultrasound T1–2 N0), as well as in patients with pathologically early-stage disease (T–2 N0).

CONCLUSIONS: In surgically managed esophageal adenocarcinoma patients, SUVmax predicts overall survival. Moreover, SUVmax identifies patients who have a poor prognosis from a subset of patients that would otherwise be considered to have early-stage disease.

Current clinical staging of esophageal cancer relies on a combination of studies, including positron emission tomography (PET) scan, computed tomography (CT), and endoscopic ultrasound (EUS) [1–3]. Computed tomographic scan is the most commonly used staging study, and its purpose is to establish the presence of distant disease as well as the extent of local and regional involvement (adenopathy) [3]. Positron emission tomography imaging has been shown to be better at uncovering subtle distant disease [4–9], but it is also used as an adjunctive study in high-risk patients to confirm the presence of visible adenopathy [2]. The principal benefit of EUS is to determine the depth of tumor invasion, and it has been shown that tumors with transmural involvement (T3) have a poor prognosis [10]. Endoscopic ultrasound has proven to be less reliable at predicting lymph node involvement [11].

The common objective of all these studies is to identify patients with evidence of either distant disease (PET, CT), or locally or regionally advanced disease (full-thickness invasion, adenopathy). This latter group of patients has been shown to have poor survival after surgical resection alone, and therefore their treatment usually includes combined modality therapies. However, a principal failing of these clinical studies is their inability to stratify patients accurately, especially those who are considered to be low risk clinically who show some variability in outcome after surgery alone, with an estimated 5-year overall survival for T1–2 N0 tumors of about 70% and a 5-year disease-free survival of 75% [12, 13]. Our group, as well as others, has investigated whether the change in PET SUVmax (the highest measured standardized uptake value of the tumor) in response to therapy is a predictor of outcome [14–16]. To date there is little available information regarding whether PET SUVmax at the time of the initial diagnosis of esophageal cancer correlates with survival after resection, especially for patients who have adenocarcinoma. A previous study by Choi and colleagues [17] in a prospectively studied group of 69 patients with surgically resected squamous cell carcinoma of the esophagus indicated a correlation between pre-treatment PET SUVmax of the primary tumor with overall survival. This result, however, was not independently predictive of survival when the analysis also included pathologic and clinical stage. Similarly, a retrospective study of 25 patients with resected squamous cell carcinoma by Kato and associates [18] showed that in addition to the correlation between pretreatment PET SUVmax with survival, there was also a correlation between depth of invasion, involved lymph nodes, and SUV.

In this study, we retrospectively review our experience with esophageal adenocarcinoma patients imaged preoperatively by 18[F]-fluorodeoxyglucose (FDG)-PET scan to determine whether SUV defined stage and prognosis. In addition, we also evaluated the prognostic value of the PET SUVmax in patients who would otherwise be categorized as early stage by PET, CT, and EUS (no adenopathy on CT and PET, and by EUS T0–2 N0), as well as in patients who are considered to be pathologically early stage (T1–2 N0). We limited our study to patients with adenocarcinoma of the gastroesophageal junction and distal esophagus treated by surgery only to analyze a homogeneous patient cohort with relevance to disease patterns currently seen in the Western hemisphere.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
We reviewed the medical records of all patients identified in a database maintained by the Thoracic Surgery Service who have undergone an esophagogastrectomy for adenocarcinoma of the distal esophagus or gastroesophageal junction between January 1996 and July 2004. January 1996 was the date when an institutional electronic medical record system was initiated and therefore represents the date at which highly reliable information became available. Patients were eligible for inclusion in the study if they had histologically proven adenocarcinoma of the distal esophagus and gastroesophageal junction, pathologic T1–3 N0–1 M0–1a disease that was treated primarily by esophagectomy alone (without any preoperative therapy). All patients had a PET scan performed either at Memorial Sloan-Kettering Cancer Center or at another facility from which complete PET data could be obtained for reanalysis. All patients must have survived their perioperative course and had adequate follow-up for survival analysis. Patients did not undergo postoperative adjuvant therapy. Data collected included patient demographics, PET scan data including the primary tumor SUV as well as evidence of FDG-avid lymph nodes, CT scan evidence of adenopathy, EUS depth of invasion (T status) and nodal involvement (N status: of note, nodes were not routinely biopsied and a morphologic estimation of involvement was made by the endoscopist), pathologic findings, and survival. This review was performed after approval had been obtained from the Memorial Sloan-Kettering Cancer Center Institutional Review Board, and in accord with an assurance filed with and approved by the US Department of Health and Human Services.

Technique of 18[F]-Fluorodeoxyglucose Whole-Body Positron Emission Tomography
The PET scans were performed on dedicated, conventional full-ring, high-resolution positron emission tomographs, with either the GE Advance (GEMS, Milwaukee, WI) or the CTI Biograph (CTI, Knoxville, TN) scanner. Patients were injected with pyrogen-free 18[F]-FDG (10 to 15 mCi) having been previously instructed to fast for at least 6 hours before scanning. All images were reconstructed using postemission-transmission attenuation–corrected data sets. Region of interest analysis tools, shipped with the scanners, were used to calculate the maximal FDG concentration within the primary tumor mass. Standardized uptake values (SUVmax) were obtained by correcting for the injected dose and the patient's weight, again using the standard software tools provided with the scanners. For the purposes of this study, only 18[F]-FDG uptake in the primary site of disease was analyzed. All PET scans were re-reviewed by a single radiologist, and the PET reviewer was blinded to patient clinical data.

Clinical Staging
Clinical staging was based on CT scan, EUS, and PET scan reports as reported by the reading physicians and recorded in the patient's chart. These studies represented the clinical data available to the surgeon at the time of resection. Computed tomographic adenopathy was typically based on the presence of enlarged lymph nodes (>1 cm on the long axis) on a contrast-enhanced scan. 18[F]-Fluorodeoxyglucose-PET–avid lymph nodes were recorded as local-regional adenopathy, as determined by the reading radiologist (of note, the presence of lymph nodes was assessed independently of the SUVmax of the primary tumor). Patients without PET and CT evidence of local-regional adenopathy and with an EUS T0–2 N0 lesion (for the patients who had an EUS) were classified as having early clinical stage disease. Patients with evidence of CT or PET local-regional adenopathy, or in whom a T3 or N1 lesion was noted by EUS, were assigned as having advanced clinical stage disease.

Pathologic Staging
Patients were assigned a T, N, and overall TNM stage according to the American Joint Committee on Cancer staging system [19]. Patients with T1–2 N0 tumors were assigned as having early pathologic stage, and patients with a T3 or N1 tumor were assigned as having advanced pathologic stage. The tumor histology type was determined from postresection pathology reports.

Overall Outcome
The outcome evaluated was overall survival, which was calculated from the time of operation, and the date of death was confirmed from the Social Security Death Index. Follow-up was through September 2004, constituting our censoring date for survival.

Statistical Analysis
The SUVmax was used both as a continuous and as a categorical variable. It was dichotomized using the observed median. The associations between SUVmax as a continuous variable and clinical staging were assessed by the Wilcoxon test (Kruskal-Wallis test for clinical variables with more than two categories). The associations between SUVmax as a dichotomous variable and clinical staging were assessed by Fisher's exact test. The association between SUVmax and survival was assessed by Cox regression (continuous SUVmax) or log-rank test (dichotomous SUV and other categorical variables). To ensure that type 1 error is protected at the nominal 5% level, the reference distributions for the log-rank tests were obtained by 1,000 permutations.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
From January 1996 through June 2004, 488 patients underwent an esophagectomy for adenocarcinoma of the distal esophagus and gastroesophageal junction. Of these 488 patients, 50 (44 men, 6 women; median age, 69.0 years) met the inclusion criteria for this study. This relatively small number of patients available for review reflects the fact that most of our patients receive induction therapy for locally advanced disease and were therefore ineligible for this study. In addition, PET was either unavailable or not routinely used in the earlier years of this study. All patients underwent preoperative PET and CT scans, and 39 patients also had an EUS. The distribution of clinical stage is shown in Table 1. The median SUV was 4.5 (range, 1.8 to 19.1). Because the median SUV represents a value for which there is no statistical bias, it was used for all analyses. We used the median SUV as the cutoff between the high (n = 25) and low (n = 25) PET SUV groups.


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  		Table 1. Radiographic and Pathologic Characteristics of Patients a
 
Correlation of Positron Emission Tomography Standardized Uptake Values to Clinical Stage
The two SUVmax groups differed significantly in their distribution of clinical stage as determined by CT, PET, and EUS. Most of the low PET SUV patients (21 of 25) had early clinical stage disease, whereas only 11 of 25 high PET SUV patients had early-stage clinical disease (p = 0.007; Table 2).


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  		Table 2. Correlation of Standardized Uptake Value to Clinical Stage and Pathologic Stage a
 
Correlation of Standardized Uptake Values to Pathologic Staging
There was a strong association between the low SUV group and early stage of disease. The likelihood of either an involved N1 or M1a node being found was 8.0% (2 of 25) in the low PET SUV group, but was 48% (12 of 25) in the high PET SUV group (p = 0.001). Similarly, a low PET SUVmax predicted an earlier T status (p < 0.001), with 90.0% (24 of 25) being T1–2 compared with 60.0% (15 of 25) in the high PET SUVmax group. The consequent stage distribution differed significantly between the two PET SUVmax groups (p = 0.001; Table 2).

Long-Term Outcome in All Patients
The median follow-up was 26.1 months in the high SUV group and 16.0 months in the low SUV group (p = 0.15). The overall survival in the low SUV group was significantly better than in the high SUV group (p = 0.021; Fig 1).


Figure 1
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  		Fig 1. Overall survival of all patients according to the positron emission tomographic maximal standardized uptake values (SUV) of the primary tumor is shown.

 
Long-Term Outcome in Early Clinical Stage Patients
Thirty-two patients in this study had early clinical stage disease. Patients in the early clinical stage group had a significantly improved survival compared with those in the advanced clinical stage group (p = 0.058; Fig 2A). Of the patients in the early clinical stage group, 21 of 32 patients (66%) were in the low SUV group, and 11 of 32 (33%) patients were in the high SUV group. Within this subset of early clinical stage patients, patients in the low SUV group had a significantly better survival (p = 0.008; Fig 2B).


Figure 2
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  		Fig 2. (A) Overall survival of patients with early versus advanced clinical stage disease. (B) Overall survival of patients with early clinical stage disease subdivided according to the positron emission tomographic standardized uptake values (SUV; high versus low) of the primary tumor.

 
Long-Term Outcome in Early Pathologic Stage Patients
Thirty-two of the 50 patients in this study were considered to have early pathologic stage disease based on a pathologic T1–2 N0 lesion. This group of patients had a significantly better survival than the advanced pathologic group (p = 0.007; Fig 3A). Of the patients in the early pathologic stage group, 22 of 32 (69%) were in the low SUV group, and 10 of 32 (31%) were in the high SUV group. Within this subset of early pathologic stage patients, patients in the low SUV group had a significantly better survival (p = 0.023; Fig 3B).


Figure 3
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  		Fig 3. (A) Overall survival of patients with early versus advanced pathologic stage disease. (B) Overall survival of patients with early pathologic stage disease subdivided according to the positron emission tomographic standardized uptake values (SUV; high versus low) of the primary tumor.

 
In summary, PET SUVmax identifies a group of high-risk patients from a subset of patients who would otherwise be considered to have early-stage disease, either clinically or pathologically.


   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
Most studies of PET scanning in the staging of esophageal cancer have focused on the its benefits in detecting distant disease, its improved specificity in detecting involved lymph nodes when compared with CT scan, and its ability to determine response to preoperative therapy. However, the main limitation of PET scanning in esophageal cancer is its lack of sensitivity at detecting locoregional lymph node involvement. A review of the literature indicates that the sensitivity of PET in detecting locoregional nodal metastases in esophageal cancer ranges from 22% to 71% [7, 12, 20–28] (Table 3). The significance of this poor sensitivity is that early-stage disease is not reliably identified by PET scan. Computed tomographic scan has similarly been shown to have low sensitivity (Table 3). Although EUS can accurately diagnose tumor T stage, it also fails to diagnose lymph node involvement reliably, especially in earlier T stages [29].


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  		Table 3. Results of Published Series Examining Sensitivity and Specificity of Positron Emission Tomography and Computed Tomography for Detecting Regional Disease in Esophageal Cancer
 
Little information exists regarding the potential of PET to predict prognosis. Only two previous reports have examined the issue, and these small series focused on squamous cell carcinoma rather than adenocarcinoma [17, 18]. Our data show that a high PET SUVmax is associated with lymph node involvement, transmural tumor invasion, and a poor prognosis after resection. The risk of death is eightfold greater in patients in the high PET SUVmax group. Although not included in this study, and as potential speculation for the basis of the association of PET SUVmax with prognosis, the high PET SUVmax group tumors were also more likely to show histologic evidence of tumor aggressiveness, including poor tumor grade (p = 0.005), neural invasion (p = 0.001), and vascular invasion (p = 0.09). There are two important aspects to our study. Our patients all had adenocarcinoma with a homogeneous tumor location, and all underwent homogeneous treatment (surgery only). Our finding that PET SUVmax identifies patients who have a poor prognosis from within a group of patients that would otherwise be considered to have early-stage, curable disease, is unique.

The use of the median PET SUV cutoff to distinguish low-risk from high-risk groups is deliberately chosen in an attempt to avoid inadvertent bias. However, when considered as a continuous variable, PET SUV also predicts the presence of any lymph node metastases (p = 0.008), and also the overall number of lymph nodes involved (p = 0.09). When PET SUV is used as a continuous variable, the risk of death increases by 11% for each unit increase in SUV (p = 0.055). The fact that the overall number of positive lymph nodes is predicted by the SUV is an important observation because we and others have shown that the number of involved lymph nodes is prognostically significant [13]. Currently PET SUVmax is the only noninvasive study able to predict this information.

In conclusion, the PET SUVmax of the primary tumor in esophageal adenocarcinoma predicts clinical stage, pathologic stage, and overall survival. In addition, a high PET SUVmax identifies a subset of patients who have early-stage clinical and pathologic stage disease but who have a poor prognosis. Therefore, PET SUV can potentially be used at diagnosis to select patients for induction therapy or to stratify patients for entry into clinical trials testing novel multimodality treatment strategies for esophageal adenocarcinoma.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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