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Ann Thorac Surg 2008;86:1131-1138. doi:10.1016/j.athoracsur.2008.05.019
© 2008 The Society of Thoracic Surgeons
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Original Articles: General Thoracic

Assessment of Treatment Response and Recurrence in Esophageal Carcinoma Based on Tumor Length and Standardized Uptake Value on Positron Emission Tomography–Computed Tomography

Johannes B. Roedl, MD, PhDa,b,*, Mukesh G. Harisinghani, MDa,b, Rivka R. Colen, MDa,b, Alan J. Fischman, MDb, Michael A. Blake, MDa, Douglas J. Mathisen, MDc, Peter R. Mueller, MDa

a Division of Abdominal and Interventional Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
b Division of Nuclear Medicine, Department of Radiology, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts
c Department of Thoracic Surgery, Massachusetts General Hospital, Harvard Medical School, Boston, Massachusetts

Accepted for publication May 6, 2008.

* Address correspondence to Dr Roedl, Department of Radiology, Fruit St 55, Boston, MA 02114 (Email: johannes.roedl{at}gmail.com).


   Abstract
Top
 Abstract
Introduction
 Patients and Methods
 Results
 Comment
 References
 
Background: Previous studies demonstrated that a decrease of the standardized uptake value between pretreatment and posttreatment positron emission tomography (PET) scans can predict histopathologic treatment response in patients with esophageal cancer.

Methods: Forty-seven patients who underwent PET–computed tomography (CT) scans before (scan 1) and after (scan 2) neoadjuvant chemoradiotherapy and during the follow-up period after surgery (scan 3) were included in this study. It was evaluated whether decrease of metabolic tumor length between scan 1 and scan 2 can predict histopathologic response to treatment. Moreover, the value of PET-CT was compared with PET in the assessment of tumor recurrence based on a visual analysis of scan 3. Reference standards for treatment response and recurrence were histopathology results.

Results: The reduction of tumor length between before and after chemoradiotherapy scans (between scan 1 and scan 2) was a better predictor of histopathologic response and of time to recurrence than the decrease in standardized uptake value. The most accurate differentiation was achieved when using a cut-off value of 33% reduction of the initial tumor length. Using this threshold to define metabolic response, the sensitivity was 91% (19 of 21) and the specificity was 92% (24 of 26) for predicting histopathologic treatment response. Based on a visual analysis, PET-CT was more accurate than PET in the differentiation of tumor recurrence from posttreatment tissue changes. Integrated PET-CT achieved a sensitivity of 91% (48 of 53) and a specificity of 81% (30 of 37) in identifying sites of tumor recurrence, compared with 83% (44 of 53) and 65% (24 of 37) with PET.

Conclusions: Decrease of tumor length was shown to be a better predictor of treatment response and disease-free survival than decrease of standardized uptake value. Furthermore, PET-CT is more accurate in the evaluation of recurrence than PET.


   Introduction
Top
 Abstract
 Introduction
Patients and Methods
 Results
 Comment
 References
 
Esophageal cancer is rapidly increasing in incidence and is ranked seventh in the list of causes for cancer-related deaths in 2007 [1]. Response to chemoradiotherapy and tumor recurrence are one of the most important factors determining patient prognosis [2–4]. Regarding treatment response, several studies have suggested the usefulness of fluorodeoxyglucose (FDG) positron emission tomography (PET) in identifying responding and nonresponding tumors before surgery. Studies showed that a decrease of the metabolic activity of the tumor between pretreatment and posttreatment PET scans is associated with histopathologic treatment response [5–7]. Metabolic tumor activity (or FDG uptake) is measured as the standardized uptake value (SUV) of the tumor. However, other investigations found no significant association between the decrease of SUV and the histopathologic response to treatment [8–10].

In the first part of the present investigation, we assessed the value of metabolic tumor length in comparison to the SUV for the differentiation of responders from nonresponders. Our hypothesis of using metabolic tumor length as a criterion for response to treatment is based on results of previous studies that demonstrated with endoscopy that lesion length is both in Barrett's metaplasia [11, 12] and in esophageal carcinomas associated with progression and stage of the disease [13, 14]. We also evaluated the association between tumor length and recurrence-free survival after surgery. Besides response to chemoradiotherapy, tumor recurrence is one the most important prognostic factors. Most of the patients present with recurrent disease within 2 years after starting therapy [15]. The early identification of recurrent disease is important, because with additional therapy, increased survival, and in some patients, even cure can be achieved [16]. In the second part of the present study, we therefore evaluated the additional value of combined PET–computed tomography (CT) over PET in the assessment of tumor recurrence after surgery in patients with esophageal carcinoma.


   Patients and Methods
Top
 Abstract
 Introduction
 Patients and Methods
Results
 Comment
 References
 
Patients
Our Institutional Review Board waived the need for patient consent and approved the study, which conforms with the Health Insurance Portability and Accountability Act. Forty-seven consecutive patients with squamous cell carcinoma and adenocarcinoma of the esophagus who underwent neoadjuvant chemoradiotherapy followed by surgery were included in the study. The clinical stage of all patients before neoadjuvant therapy was stage II or stage III. Table 1 demonstrates that there was no significant difference in demographic and tumor characteristics between metabolic responders and nonresponders. Metabolic response was defined as a decrease of tumor length of at least 33% between pretreatment and posttreatment PET-CT scans. This optimal threshold of a 33% decrease in tumor length was derived from the results of the present study, and it is explained in the results section how this cut-off was determined. All patients underwent three PET-CT studies: The first scan was before neoadjuvant chemoradiotherapy (mean days prior: 10.2 ± 4.1), the second scan was after neoadjuvant chemoradiotherapy (mean days after: 14.4 ± 5.9) and before surgery, and the third scan was 18.4 ± 5.2 months after surgery. The third PET-CT scan was earlier if tumor recurrence was indicated by suggestive symptoms, equivocal or suspicious findings on clinical examination, radiologic studies, or endoscopy. Esophageal cancer is a CMS (Centers for Medicare and Medicaid Services)–approved indication for diagnosis, staging, and restaging with PET-CT imaging. All major payers cover PET-CT studies to diagnose, stage, and restage esophageal carcinoma.


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  		Table 1 Pretreatment Patient Characteristics of Metabolic Responders and Nonresponders
 
Confirmation of final diagnosis, grading and typing of all esophageal lesions was performed by histology. Initial pretreatment tumor stage was assessed by endoscopic ultrasonography (EUS) with fine-needle aspiration, PET-CT, CT, magnetic resonance imaging (MRI), bone scintigraphy, and image-guided biopsy. Tumor stage after neoadjuvant chemoradiotherapy was determined by postsurgical pathology. The reference standard for assessing treatment response was the postsurgical pathology result. Pathologists classified the surgical specimens as responders or nonresponders according to a histopathologic scoring system [18]. Treatment response was defined as less than 10% viable tumor cells in the postsurgical specimen of the primary tumor. All patients underwent neoadjuvant concurrent chemoradiotherapy with 50.4 Gray radiation together with cisplatin and 5-fluorouracil at weeks 1 and 5. Chemoradiotherapy was followed by a left thoracoabdominal esophagectomy for low-lying lesions, and an Ivor-Lewis esophagectomy with extensive lymphadenectomy for higher lesions.

After surgical resection, patients were followed up at 3-month intervals during the first year, and at 6-month intervals during the second year. The median follow-up time was 25.0 months, with a range of 10.0 to 39.0 months. The disease-free survival was calculated as the time from the initiation of neoadjuvant therapy to the date of recurrence. Suspicious sites of recurrence and tumor progression (suspected on PET-CT) were proved by biopsy. A tumor/recurrence-free status at the 18 month follow-up PET-CT scan was confirmed by EUS and follow-up. An electronic database of patient files was available to acquire clinical information of the study subjects retrospectively.

Imaging
Before imaging, patients were instructed to fast for at least 6 hours or overnight. Subjects received an intravenous injection of 15 mCi (555 MBq) of FDG. Data were acquired 60 minutes after injection using an integrated PET-CT system (Biograph 16; Siemens Medical Solutions, Erlangen, Germany). Low-dose CT for attenuation correction was performed first with the 16- slice multidetector CT component of the combined PET-CT. Immediately after CT, the PET emission scan was obtained with a high-resolution lutetium oxyorthosilicate–based PET scanner in a three-dimensional mode. The transverse field of view was identical to the CT scan. Subsequently, patients received a diagnostic contrast-enhanced CT with 100 mL of 300 mg iodine per milliliter injected along with 20 mL saline. The parameters were as follows: table feed, 15 mm/s; pitch, 1.5; tube voltage, 140 kV; and tube current, 170 mA. Images were reconstructed with a 2-mm or 2.5-mm slice thickness.

Tumor Length and SUV
Two readers, each with 4 years of experience in PET-CT imaging, performed all measurements independently. The mean value of the measurements of both readers was used for statistical analysis. Figures 1 and 2 Go exemplify the length and SUV measurements. Previous studies suggested that assessment of esophageal lesion length is more accurate with PET than with CT [19]. Therefore, lesion length was first determined on the PET component of the combined PET-CT. Tumor length on PET was measured by determining the number of slices with tumor uptake greater than SUV 2.5 and then by multiplying the slice number by the slice thickness. A SUV above 2.5 is commonly used to delineate malignancy in PET and PET-CT imaging. The horizontal lines in Figures 1C and 2C represent the slices with FDG uptake greater than SUV 2.5. Subsequently, the lesion length was determined with fused PET-CT by considering the anatomic information from the CT component additionally to the metabolic information from the PET component. The PET-CT length corrected the previously assessed PET length when one of the following strict CT criteria indicated different cranial or caudal endpoints of the lesion: enhancing wall thickening, enhancing focal wall irregularities, or obvious mass. For quantitative analysis of regional FDG uptake, SUVs were assessed. The mean SUV in a region of interest with a 1.5 cm diameter (SUV mean) was assessed (arrow in Figs 1D, 2D) according to previous studies [7, 20, 21]. The SUV measurement was performed in the slice with the maximum FDG uptake of the lesion (Figs 1D, 2D). We preferred the mean SUV over the maximum SUV, because the mean SUV is less susceptible to outliers: The maximum SUV represents only one single pixel (the maxium pixel within the entire primary tumor), whereas the mean SUV in a region of interest of 1.5 cm represents the average SUV of 10 pixels (corresponds to 1.5 cm).


Figure 1
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  		Fig 1. Measurements of tumor length and standardized uptake value (SUV), T3N1M0 esophageal carcinoma. Length: 56 mm in positron emission tomography (PET) alone measurements, 54 mm in PET–computed tomography (CT) measurements; SUV: 8.7. An example of esophageal carcinoma (the carcinoma lies between the arrows in A–C, and is pointed out by the long arrow in D). (A) Depicted are sagittal views of the PET component alone, sagittal views of fused PET-CT with different color maps illustrating fluorodeoxyglucose (FDG) uptake, including (B) an "earth" color map, (C) an "ocean" color map, and (D) axial views of the "ocean" color map. The different color maps are only shown for illustrative reasons and have no effect on measurements. Color maps show relative differences of FDG uptake within the tumor. The horizontal lines in (C) indicate slices with FDG uptake greater than SUV 2.5. Tumor length was calculated by multiplying the number of slices with FDG uptake of 2.5 or greater with the slice thickness of the PET-CT scan. Circle in (D) represents the region of interest for SUV measurements.

 

Figure 2
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  		Fig 2. Measurements of tumor length and standardized uptake value (SUV), T2N0M0 esophageal carcinoma. Length: 24 mm in both positron emission tomography (PET) alone and PET–computed tomography (CT) measurements; SUV: 4.2. An example of esophageal carcinoma (the carcinoma lies between the arrows in A–C, and is pointed out by the long arrow in D). (A) Depicted are sagittal views of the PET component alone, sagittal views of fused PET-CT with different color maps illustrating fluorodeoxyglucose (FDG) uptake including (B) an "earth" color map, (C) an "ocean" color map, and (D) axial views of the "ocean" color map. The different color maps are only shown for illustrative reasons and have no effect on measurements. Color maps show relative differences of FDG uptake within the tumor. The horizontal lines in (C) indicate slices with FDG uptake greater than SUV 2.5. Tumor length was calculated by multiplying the number of slices with FDG uptake of 2.5 or greater with the slice thickness of the PET-CT scan. Circle in (D) represents the region of interest for SUV measurements.

 
Diagnosing Recurrent Disease With PET Compared With PET-CT
First, a team of experienced nuclear medicine physicians evaluated tumor recurrence at the anastomosis site of the resected primary tumor based on a visual analysis on the PET component of the third PET-CT scan (during the follow-up period after surgery). Then, a combined team of nuclear medicine physicians and radiologists evaluated tumor recurrence on the fused PET-CT images of the third PET-CT scan. Additionally, the following characteristics were used to describe FDG uptake on fused PET-CT images: the extent of the FDG uptake (focal, segmental, or diffuse uptake) and the eccentricity of the uptake. An eccentric FDG uptake pattern was defined as asymmetric uptake with tendency to one side of the esophageal wall, whereas concentric pattern was defined as uptake symmetric along the esophageal wall around the esophageal lumen. It was hypothesized that benign uptake (due to radiation or reflux esophagitis) tends be diffuse and concentric, whereas malignant uptake (residual tumor or recurrence) is focal and eccentric.

Data Analysis
All statistical tests were two sided and performed at the 5% level of significance by using SPSS for Windows, version 15.0 (SPSS, Chicago, Illinois). Differences in patient characteristics, in lesion lengths, and SUVs were evaluated with t tests. Binary logistic regression analysis with a stepwise approach determined which of the evaluated PET-CT variables was the best predictor of histopathologic response. Receiver operator curves were determined to assess the area under curve and the optimal cut-off value for predicting histopathology responders and nonresponders. Kaplan-Meier curves and Cox regression tests were performed for disease-free survival analysis.


   Results
Top
 Abstract
 Introduction
 Patients and Methods
 Results
Comment
 References
 
Tumor Length and Histopathologic Response
Tumor length was measured on both PET-CT and PET. Tumor length was assessed in PET-CT scans before (scan 1) and after (scan 2) chemoradiotherapy and the decrease of tumor length between both studies was calculated. A receiver operator curve analysis showed that the relative decrease of tumor length and SUV between pretreatment and posttreatment variable was a better predictor of histopathologic treatment response than the absolute pretreatment or posttreatment values. The area under the curve and the optimal cut-off value for each variable was determined in a receiver operator curve analysis. Table 2 demonstrates that a decrease of the PET-CT and PET length was a better predictor of histopathologic response (sensitivity, 91%; specificity, 92%) than the decrease of the SUV (sensitivity, 86%; specificity, 61%). There was no significant difference (p = 0.11; t = –1.6) in tumor length measured on PET (with a SUV threshold of 2.5) and tumor length measured on combined PET-CT (under additional consideration of the CT information).


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  		Table 2 Decrease of Metabolic Variables (Tumor Length and SUV) in Histopathology Responders and Nonresponders
 
Comparison Between PET-CT and PET in Detecting Recurrent Sites
Tumor recurrence at the site of the primary tumor, recurrence in lymph nodes and in distant sites was evaluated on the third PET-CT scan (in the follow-up period after surgery). Twenty-seven of the 47 patients were found to have recurrent disease, whereas 20 patients were recurrence free. A total of 90 sites suspicious of tumor recurrence were evaluated, 53 of which were malignant and 37 of which were proved to be benign on biopsy. Table 3 shows that PET-CT had a higher sensitivity (91%) and specificity (81%) in characterizing recurrent sites than PET (sensitivity, 83%; specificity, 65%). Especially the specificity was higher in PET-CT compared with PET.


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  		Table 3 Accuracy of Positron Emission Tomography–Computed Tomography (PET-CT) Compared With PET in Detecting Recurrent Sites Based on a Visual Analysis
 
FDG Uptake of Recurrent Disease
The FDG uptake at the anastomosis site of the resected primary tumor was evaluated on the third PET-CT scan (follow-up scan after surgery). At the time of this follow-up scan, 12 patients were proven to have recurrence at the site of the primary tumor, whereas 16 patients had only posttreatment changes (eg, radiation esophagitis), but no signs of residual or recurrent primary tumor. A focal and eccentric FDG uptake pattern was seen in 11 of the 12 patients who had a recurrent primary tumor (sensitivity 92%), whereas only 3 of the 16 patients who had no recurrent primary tumor showed focal and eccentric uptake (specificity 81%). Therefore, a focal and eccentric FDG uptake pattern might be used to differentiate recurrent or residual primary tumor uptake from benign (reflux or radiation esophagitis) uptake in follow-up PET-CT studies.

Tumor Length Measurements: Correlation With Endoscopy and Interrater Reliability
In a Pearson correlation model, excellent correlation was shown between pretreatment tumor length measurements with endoscopy and with PET-CT (r = 0.909, p < 0.001), and PET (r = 0.904, p < 0.001; Pearson correlation). Moreover, the interobserver reliability between both readers was excellent. The R2 value, which was assessed in a linear regression analysis, was 0.987 for PET-CT length, 0.990 for PET length, and 0.989 for SUV.

Tumor Length as a Prognostic Factor
In a Cox regression analysis with inclusion of tumor length (PET-CT length, PET length) and SUV, the decrease of the PET-CT length between pretreatment, and posttreatment scans was the best predictor of disease-free survival. Metabolic responders (defined as a decrease of the PET-CT length by at least 33%; Table 2) had a mean time to recurrence of 33 months, whereas metabolic nonresponders (decrease of the PET-CT length by less than 33%; Table 2) had a time to recurrence of only 19 months ({chi}2 19.0, p < 0.001; log-rank test; Fig 3).


Figure 3
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  		Fig 3. Kaplan-Meier curve. Disease-free survival in metabolic responders (solid line) and nonresponders (dashed line). Metabolic response was defined as a decrease of the tumor length of at least 33% between pretreatment and posttreatment positron emission tomography–computed tomography scans. Time to event was defined as the time from initiation of neoadjuvant chemoradiotherapy to the date of tumor recurrence. (X = censored.)

 

   Comment
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
References
 
In the present investigation, we observed that tumor length assessed with PET-CT or PET is a better predictor of treatment response than SUV. In the evaluation of tumor recurrence after definite treatment, PET-CT was more accurate than PET in diagnosing recurrence and in detecting recurrent sites of esophageal carcinoma.

A number of studies have evaluated whether metabolic response, measured by 18-FDG PET uptake, is prognostic of the pathologic response to chemoradiotherapy [5–10]. Metabolic response was suggested when there was a certain relative decrease of the SUV between pretreatment, and posttreatment PET scans. Several of these studies concluded that FDG-PET was an effective modality for the noninvasive assessment of pathologic tumor response to neoadjuvant chemoradiotherapy [5–7]. However, other investigations showed no association between metabolic and histopathologic response [8–10]. The reason for these discrepancies between studies could be explained, at least in part, by various confounding factors that have an effect on SUV measurements, including accurate recording of FDG dose, duration of time between FDG injection and imaging, patient body weight and height, glucose levels, size of the region of interest, and others [22]. Therefore, it is desirable to look for alternative, less variable quantitative tumor measurements besides SUV for the assessment of treatment response. In esophageal carcinoma, tumor length is an independent prognostic factor [13, 14, 23]. Tumor length is associated with T stage, and lymphatic spread of disease [13, 14]. We demonstrated in the present study that tumor length can be determined both with PET-CT and with PET with high interrater reliability. Furthermore, there was a very good correlation between the PET and PET-CT length and the endoscopically assessed tumor length. In the present study, metabolic tumor length was a better predictor of treatment response and overall survival than the SUV.

One of the most important prognostic factors of esophageal carcinoma is local recurrence. It is important that tumor recurrence is detected early, because additional therapy can result in significantly prolonged survival and in some cases, even cure [15, 24]. Conventional imaging modalities such as CT, EUS, and MRI are the methods widely used for detection of recurrence. However, the diagnostic value of these morphologic imaging techniques is limited because chemoradiotherapy often results in esophageal wall thickening due to inflammation, edema, and fibrosis that cannot be distinguished from recurrent malignant tissue by CT, EUS, or MRI [25–27]. Use of 18F-FDG PET as a functional imaging technique overcomes some of these obstacles, as the metabolic information offered by PET might more reliably differentiate between malignant tumor and inflammatory reaction or edema [26]. Positron emission tomography showed promising results in detecting recurrent disease of esophageal cancer [27]. However, the specificity of PET is also limited, because 18F-FDG uptake is not restricted to tumor cells, but it is also seen in areas of postoperative tissue repair or inflammation, making it difficult to differentiate benign from malignant uptake. The rate of false positive findings might be further increased by physiologic 18F-FDG uptake in the smooth muscle cells and the mucosa of the alimentary tract, including the esophagus, the gastric tube, and at sites of anastomosis after surgery [28]. Some of the limitations of PET and CT might be overcome by the combination of both in integrated PET-CT. The fused metabolic-anatomic images with PET-CT can facilitate the differentiation between malignant and benign uptake by the exact localization of the FDG focus with the CT component of the combined PET-CT [29].

Table 3 shows that 41 of the 53 recurrent sites were lymph nodes or distant metastatic sites (bone, liver, lung). Positron emission tomography–CT is the modality of choice in detecting recurrence in distant lymph node and in distant organs (lung, liver, and bone). Our study demonstrated that PET-CT achieves also high accuracy in diagnosing locoregional recurrence. Although EUS with FNA cannot detect distant metastasis, it is the current goldstandard in detecting locoregional recurrence. Despite the relatively high costs, we believe that PET-CT should be performed between 12 and 24 months after surgery to screen for distant metastasis and to evaluate the locoregional region. The PET-CT studies are covered by all major insurance companies to diagnose, stage, and restage esophageal carcinoma. Endoscopic ultrasonography with FNA should be used in cases of locoregional FDG uptake on PET-CT (at the esophagogastric anastomosis) and in patients with upper gastrointestinal symptoms (dysphagia, odynophagia, and so forth) suggestive of local reccurence.

In conclusion, the present study demonstrates that the decrease of tumor length between the initial and posttreatment PET-CT scan more accurately predicts treatment response and disease-free survival than does the decrease of SUV. In the evaluation of tumor recurrence, PET-CT was more accurate than PET both in a patient- and in a lesion-based analysis; and PET-CT should be used routinely between 12 and 24 months after surgery to screen for recurrent sites.


   References
Top
 Abstract
 Introduction
 Patients and Methods
 Results
 Comment
 References
 

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Donald E. Low
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