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Prediction of Response to Preoperative Chemotherapy in Adenocarcinomas of the Esophagogastric Junction by Metabolic Imaging

From the Departments of Nuclear Medicine, Surgery, Pathology, Radiology, and Medical Statistics, Technische Universität München, München, Germany.

Address reprint requests to Wolfgang A. Weber, MD, Nuklearmedizinische Klinik, Klinikum Rechts der Isar, Ismaningerstraße 22, 81675 München, Germany; email: w.weber{at}lrz.tum.de

	ABSTRACT

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: Preoperative chemotherapy in patients with gastroesophageal cancer is hampered by the lack of reliable predictors of tumor response. This study evaluates whether positron emission tomography (PET) using fluorine-18 fluorodeoxyglucose (FDG) may predict response early in the course of therapy.

PATIENTS AND METHODS: Forty consecutive patients with locally advanced adenocarcinomas of the esophagogastric junction were studied by FDG-PET at baseline and 14 days after initiation of cisplatin-based polychemotherapy. Clinical response (reduction of tumor length and wall thickness by > 50%) was evaluated after 3 months of therapy using endoscopy and standard imaging techniques. Patients with potentially resectable tumors underwent surgery, and tumor regression was assessed histopathologically.

RESULTS: The reduction of tumor FDG uptake (mean ± 1 SD) after 14 days of therapy was significantly different between responding (-54% ± 17%) and nonresponding tumors (-15% ± 21%). Optimal differentiation was achieved by a cutoff value of 35% reduction of initial FDG uptake. Applying this cutoff value as a criterion for a metabolic response predicted clinical response with a sensitivity and specificity of 93% (14 of 15 patients) and 95% (21 of 22), respectively. Histopathologically complete or subtotal tumor regression was achieved in 53% (eight of 15) of the patients with a metabolic response but only in 5% (one of 22) of the patients without a metabolic response. Patients without a metabolic response were also characterized by significantly shorter time to progression/recurrence (P = .01) and shorter overall survival (P = .04).

CONCLUSION: PET imaging may differentiate responding and nonresponding tumors early in the course of therapy. By avoiding ineffective and potentially harmful treatment, this may markedly facilitate the use of preoperative therapy, especially in patients with potentially resectable tumors.

	INTRODUCTION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
PREOPERATIVE chemotherapy for locally advanced esophageal cancer has been investigated for more than 20 years, but its role in patient management remains controversial. Recently published, randomized, controlled trials have shown no improvement in survival by preoperative chemotherapy compared with surgery alone.^1,2 Nevertheless, there has been a consistent observation that survival was significantly prolonged in patients who respond to preoperative therapy, compared with surgical treatment alone.^1-3 However, in the majority of the patients, no objective response is achieved; these patients undergo several months of toxic therapy without a survival benefit. In fact prognosis for patients with nonresponding tumors seems to be even worse than for patients treated by surgery alone.^1,2 This is probably due to therapy-induced side effects; selection of chemotherapy-resistant, biologically more aggressive tumor cells⁴; and delay of surgical treatment.^1,2 Therefore, a diagnostic test that allows prediction of response is considered to be crucial for the future use of preoperative chemotherapy in patients with esophageal cancer.

In the present study we evaluated whether positron emission tomography (PET) with fluorine-18 fluorodeoxyglucose (FDG) may be used for this purpose. FDG is an established radiopharmaceutical for measuring exogenous glucose utilization in vivo. Large accumulation of FDG has been documented for the majority of malignant tumors, including esophageal and gastroesophageal cancer.^5-8 Our basic hypothesis was that responding tumors show a decrease of glucose utilization within a few days after initiation of therapy while glucose utilization remains unchanged in nonresponding tumors.

To test this hypothesis we prospectively studied patients with locally advanced adenocarcinoma of the esophagogastric junction (AEG) during preoperative chemotherapy. Changes in glucose utilization, measured by FDG-PET after 2 weeks of therapy were compared with clinical response after completion of therapy, assessed by conventional imaging modalities. Furthermore, metabolic measurements were correlated with histopathologic assessment of tumor regression in the resected specimens and patient survival.

	PATIENTS AND METHODS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
Patients
PET imaging was performed as part of two phase II studies evaluating preoperative chemotherapy in patients with adenocarcinomas of the esophagogastric junction.⁹ Eligibility requirements included the presence of biopsy-proven adenocarcinoma of the distal esophagus (AEG type I) or cardia (AEG type II)¹⁰ with or without metastases in local lymph nodes (tumor stage T3/T4, NX, and M0 in the tumor-node-metastasis classification¹¹). Staging procedures included endoscopy, endoscopic ultrasound, laparoscopy, computed tomography (CT) of the chest and abdomen, and contrast radiography of the upper gastrointestinal tract. Details of the applied techniques have been recently published.^12-14 Eligible patients had to be fit for cisplatin-containing chemotherapy and consecutive surgical resection.

Patients with an Eastern Cooperative Oncology Group score worse than 1, previous or secondary malignancy, life expectancy of less than 3 months, uncontrolled bleeding from the tumor, pregnancy, diabetes, or age less than 18 years were excluded. Patients were also ineligible if they had undergone previous chemotherapy, radiotherapy, or endoscopic laser therapy. The study protocol was approved by the institutional review board at the Technische Universität München.

Preoperative Chemotherapy
Preoperative therapy consisted of two cycles of combination chemotherapy, each of 36 days’ duration. On day 1, cisplatin at a dose of 50 mg/m² body-surface area (BSA) was given as an intravenous infusion over a period of 1 hour. Thereafter patients received leucovorin 500 mg/m² BSA over a period of 2 hours, followed by fluorouracil 2 g/m² BSA over a period of 24 hours. Treatment with cisplatin was repeated on days 15 and 29. Infusion of leucovorin and fluorouracil was repeated on days 8, 15, 22, 29, and 36. AEG I tumors were additionally treated with paclitaxel 80 mg/m² BSA over a period of 3 hours, 1 day before infusion of cisplatin.⁹ Surgical resection of the tumor was scheduled 3 to 4 weeks after completion of chemotherapy.

PET Imaging
A baseline FDG-PET was performed during initial staging before initiation of preoperative therapy. Patients were excluded from further analysis when there was insufficient contrast between tumor and surrounding normal tissues (ratio of FDG uptake relative to the mediastinum < 2.0). FDG-PET was repeated on day 14 of the first chemotherapy cycle. Patients fasted at least 8 hours before PET imaging to ensure standardized glucose metabolism. Static emission images of the tumor region of 20 minutes’ duration were acquired 40 minutes after intravenous injection of 250 to 370 MBq of FDG as previously described.¹⁵ After the emission scan, transmission measurements were performed for attenuation correction. Blood glucose levels were measured before each PET study (first PET scan, 109 ± 27 mg/dL; second PET scan, 106 ± 29 mg/dL). Attenuation-corrected emission data were reconstructed by filtered backprojection using a Hanning filter with a cutoff frequency of 0.4 cycles/pixel. Image data were normalized for injected dose of FDG and patients’ BSA resulting in parametric images representing regional standardized uptake values (SUV).¹⁶ The spatial resolution of the reconstructed images is 6 to 8 mm at full width half maximum. For quantitative evaluation, a circular region of interest (diameter 1.5 cm, corresponding to 10 pixels) was placed over the tumor in the slice with maximum FDG uptake in the baseline scan. In the second PET scan, the region of interest was placed at the same position as in the baseline study using the anatomic landmarks of the transmission image as a reference. To assess the reproducibility of the quantitative evaluation of FDG-PET studies, all PET scans were analyzed by two independent, blinded observers. For further analysis the mean value of the two measurements was used.

Clinical Response Evaluation
Before surgery, all staging procedures mentioned previously were repeated, and a response evaluation was performed by the interdisciplinary tumor board of the Technische Universität München, without knowledge of the results of the FDG-PET studies. Tumors were classified as responding or nonresponding using predefined criteria. Response was defined as at least 50% reduction in the size of the primary tumor, as measured by endoscopy and imaging studies. Specifically, the definition of response required that the maximal wall thickness and length had decreased by more than 50% in CT. In addition, the length of the tumor had to be reduced by more than 50%, shown in a barium swallow test. Furthermore, no or only minimal amounts of residual tumor tissue could be present in endoscopy. Only when all these criteria were met was the tumor classified as responding. When there was a minor reduction of tumor size or when new metastatic lesions were detected, the tumor was classified as nonresponding. Similar criteria for response have been used in previous studies and have been shown to be of prognostic relevance.^2,17,18

Surgical Therapy and Histopathologic Analysis
The surgical procedure was a transhiatal esophagectomy for patients with AEG I.¹⁹ In patients with AEG II tumors, a transhiatal extended gastrectomy and an extended D2-lymphadenectomy, including a left retroperitoneal lymphadenectomy, were performed.²⁰ For assessment of histopathologic tumor regression, the resected primary tumors were evaluated by a single pathologist according to a score established by Mandard et al.²¹ For the purposes of this study, all patients with no or only a few scattered residual tumor cells (regression score 1 and 2) were classified as responding. All other tumors (regression score 3 to 5) were classified as nonresponding.²¹

Patient Follow-Up
After surgical resection, patients were followed-up at 3-month intervals by CT of the chest and abdomen and endoscopy. In patients with curative (R0) resection, time to recurrence was calculated as the time from initiation of neoadjuvant therapy to detection of local recurrence or distant metastases. In patients with no resection or residual tumor after resection (R1 and R2 resection, respectively), time to tumor progression or metastases was determined.

Statistical Analysis
All quantitative data were expressed as mean ± 1 SD and differences between groups of patients were tested by the Mann-Whitney U test. For intraindividual comparisons before and after preoperative therapy, a Wilcoxon signed rank test was applied. Survival without disease progression was calculated from the first day of chemotherapy, and survival rates were estimated according to Kaplan-Meier.²² Statistical comparisons between different groups of patients were performed with a log-rank test. The diagnostic accuracy of FDG-PET to predict subsequent response was evaluated by receiver operating characteristic (ROC) analysis.²³ The optimum cutoff value for differentiation of responding and nonresponding tumors was defined by the point of the ROC curve with minimum distance from the 0% false-positive rate and the 100% true-positive rate. After ROC analysis, sensitivity, specificity, and positive and negative predictive values of FDG-PET were calculated using standard formulas. In addition, 95% confidence intervals (CI) for these parameters were calculated by use of the F distribution. Differences in proportions of patients were analyzed by Fisher’s exact test.²² All tests were two-sided and performed at the 5% level of significance.

	RESULTS

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
FDG-PET
Forty consecutive patients (three female, 37 male; age 55 ± 11 years) were studied by FDG-PET before preoperative therapy. Clinical stage was T3N0 in two, T3N+ in 35, and T4N+ in three patients. The cranio-caudal extension of the tumors was 6.0 ± 2.3 cm and the wall thickness was 2.1 ± 0.7 cm. Twenty-four patients had adenocarcinomas of the distal esophagus (AEG I), and 16 patients had adenocarcinomas of the cardia (AEG II).¹⁰ Individual patient data are provided in Table 1. After the first PET scan, three patients were excluded from analysis because of insufficient image contrast. In these patients the tumor size was similar to the well-visualized tumors (wall thickness, 1.5, 1.5, and 1.4 cm; cranio-caudal extension, 3.0, 5.0, and 8.8 cm). Furthermore, blood glucose levels were less than 120 mg/100 mL for all three patients. In the remaining 37 patients, mean FDG uptake was 17.9 ± 8.1 (median, 17.5) SUV. In the second PET scan, mean FDG uptake decreased to 11.6 ± 5.5 (median, 10.6) SUV (P < .0001). The decrease in FDG uptake was not significantly different for the two chemotherapy regimens (all patients, -31% ± 27%; AEG I, -35% ± 24%; AEG II, -24% ± 33%; P = .28). Measurements of tumor FDG uptake by the two observers were closely correlated (first scan: r² = .99, mean difference between the two observers: -0.03 ± 0.5 SUV; second scan: r² = .95; mean difference: 0.1 ± 0.8 SUV).

In five patients (14%), local tumor growth (n = 1) or newly developed distant metastases (n = 4) did not allow surgical resection. Complete tumor resection (R0) was achieved in 22 patients (59%; CI, 42% to 75%). Histopathologically, no viable tumor cells at the site of the primary tumor were found in three patients. Two of these patients had microscopic residual tumor in regional lymph nodes. Thus the posttherapeutic tumor stage was pT0pN0 in one patient and pT0pN1 in two (Table 1). In six additional patients, only a few scattered tumor cells were detected at the site of the primary tumor. Thus nine tumors were classified as histopathologically responding, and 28 were classified as nonresponding (histopathologic response rate, 24%; CI, 12% to 41%). In the three patients who were not assessable because of low FDG uptake, a clinical and histopathologic response was achieved in two, and no clinical or histopathologic response was achieved in one.

The decrease in FDG uptake during therapy was markedly higher for clinical responders than for nonresponders (responders: -54% ± 17%, median: -54%; nonresponders: -15% ± 21%, median: 15%; P < .001; Fig 1 and Fig 2A). In the ROC analysis, a reduction of FDG uptake by more than 35% was found to provide the highest accuracy for differentiation of clinically responding and nonresponding tumors (Fig 2B). By applying this cutoff value, 14 of the 15 responding and 21 of the 22 nonresponding tumors were correctly identified, providing a sensitivity and specificity of 93% (CI, 68% to 100%) and 95% (CI, 77% to 100%), respectively. Positive and negative predictive values for subsequent clinical response were 93% (CI, 68% to 100%) and 95% (CI, 77% to 100%), respectively. No significant difference was observed for AEG I or AEG II tumors for any of these parameters. Due to this high diagnostic accuracy, a reduction of FDG uptake by more than 35% was used as a criterion for a metabolic response in PET imaging.

View larger version (32K): [in this window] [in a new window]   Fig 1. FDG-PET studies in patients with clinically responding and nonresponding tumors. In the responding tumor, FDG uptake decreases to background level 14 days after initiation of chemotherapy (first row). In contrast, FDG uptake is almost unchanged for the nonresponding tumor (second row).

View larger version (18K): [in this window] [in a new window]   Fig 2. (A) Changes in FDG-uptake and clinical response (boxes, 25th and 75th percentiles; horizontal bars, median; horizontal cross bars, 10th and 90th percentiles). (B) ROC curves for prediction of response by PET imaging. , clinical response; •, histopathologic response. and • arrows indicate the diagnostic accuracy for a cutoff value of -35% and -45%, respectively.

Median follow-up time was 14 months (range, 4 to 53 months). Disease progression or recurrence after complete resection has been diagnosed in 20 of the 37 patients. In 14 of this subset of patients (70%), no metabolic response had been achieved after 14 days of therapy. Median time to progression or recurrence was 11 months (2-year survival rate, 29%). In patients with a metabolic response, median time to progression or recurrence was 16 months (2-year survival rate, 49%), whereas it was only 9 months for patients without a metabolic response (2-year survival rate, 9%; P = .01; Fig 3A).

View larger version (20K): [in this window] [in a new window]   Fig 3. Kaplan-Meier plots showing (A) survival without disease progression or recurrence and (B) overall survival. For both parameters there is a statistically significant difference between patients with and without a metabolic response (P = .01 and P = .04, respectively).

There were no significant differences between patients with AEG I and AEG II tumors with respect to overall survival (P = .51) and survival without progression or recurrence (P = .69). In patients with clinically responding tumors, overall survival was significantly higher than in patients with nonresponding tumors (median survival, > 53 months v 13 months; P = .01). Similar significant differences were found for survival without progression or recurrence (median survival for clinically responding tumors, > 53 months v 10 months for nonresponding tumors; P = .01). Histopathologic response was also associated with improved survival. None of the nine patients with histopathologically responding tumors died during the follow-up period. Median disease-free survival for this group of patients was more than 53 months, whereas it was only 10 months for patients with histopathologically nonresponding tumors (P = .01).

	DISCUSSION

TOP ABSTRACT INTRODUCTION PATIENTS AND METHODS RESULTS DISCUSSION REFERENCES

 
This prospective study demonstrates that metabolic measurements using FDG-PET allow early differentiation of responding and nonresponding tumors during preoperative chemotherapy of adenocarcinomas of the esophagogastric junction. Reduction of metabolic activity after 2 weeks of therapy was associated with a subsequent decrease of tumor size, an increased rate of curative resections, and histopathologic tumor regression. Furthermore, there was a significant correlation between reduction of metabolic activity and patient survival.

Several molecular markers, such as thymidylate synthase and p53, have been evaluated for prediction of response to preoperative therapy in gastric and esophageal cancer. This approach has the principal advantage over FDG-PET that chemotherapy may be obviated before a dose is administered.^24-27 However, we are unaware of any studies that prospectively demonstrated that one molecular marker or a combination of markers can be used to predict response with the clinically required accuracy. This may be related to several factors. Tumor specimens obtained from pretherapeutic biopsies allow only analysis of a small percentage of superficially growing tumor cells. These findings may not be representative for the entire tumor mass because of tumor heterogeneity. Furthermore, prediction of response on the basis of molecular markers assumes that the markers analyzed in the pretherapeutic specimens remain stable during therapy. However, the mechanisms defining chemosensitivity are not fully understood, and cytotoxic therapy may in fact induce considerable changes in the expression of drug resistance–related proteins.⁴

In contrast to histopathologic techniques, PET allows noninvasive quantitative assessment of the entire tumor mass. Furthermore, changes in biologic parameters during therapy can easily be determined by serial PET studies. The use of FDG for monitoring cytotoxic therapy is supported by experimental and patient data that show rapid reduction of metabolic activity during chemotherapy.^28-31 Previous studies from our laboratory evaluating the reproducibility of the FDG signal indicate that tumor glucose utilization is stable without therapeutic interventions over the time period of the study protocol. The interstudy variability of repeated FDG measurements repeated within 3 weeks is less than 20%.³² The reported decrease in SUV values in our study population is clearly beyond the range of interstudy variability of FDG uptake. Furthermore, the interobserver variability in measurements of therapy-induced changes of FDG uptake was low in the present study. Thus the observed reduction of FDG uptake 2 weeks after initiation of therapy is specific for a therapy-induced effect. For the clinical application of FDG-PET, it is important to note that no sophisticated protocol for data acquisition or analysis was required for prediction of tumor response. Thus monitoring of preoperative chemotherapy by FDG-PET may be performed wherever PET imaging is available.

Compared with histopathologic response, the negative predictive value of FDG-PET remained as high as for clinical response. However, in seven patients no major histopathologic response was achieved despite a reduction in FDG uptake by more than 35%. Thus the specificity of PET imaging for prediction of histopathologic response was only 75%. However, the cutoff value for a metabolic response was chosen to ensure that almost all patients with a significant reduction of the macroscopic tumor mass would be detected by PET imaging. Therefore, it is not surprising that several of the patients did not meet the strict criteria for histopathologic response (complete or subtotal tumor regression) after completion of therapy. Applying a more pronounced decrease of FDG uptake ( > 45%) as a threshold for definition of a metabolic response resulted in a specificity of 86% without a decrease in sensitivity (Fig 2 B). However, we consider the relatively low threshold of 35% as most appropriate because it ensures that all patients who may have a potential benefit from therapy receive further treatment.

Both clinical and histopathologic response evaluations have specific limitations. According to strict World Health Organization criteria, the primary tumors of carcinomas of the esophagus and gastric cardia are not bidimensionally measurable.³³ Therefore, clinical response monitoring is less standardized than for other tumor types, although its clinical and prognostic relevance has been documented in numerous studies.^1,2,17,18 Furthermore, clinical response monitoring cannot differentiate whether a residual mass after therapy consists of viable tumor or fibrous tissue.^34,35 Histopathologic evaluation of tumor regression is based on a scoring system that describes the ratio of viable tumor cells relative to fibrotic tissue.²¹ However, there are currently no generally accepted quantitative criteria for assessment of histopathologic response. In the present study we classified patients with no or minimal residual tumor cells as histopathologically responding. Although this definition is somewhat arbitrary, its use is supported by previous studies in esophageal cancer²¹ and other tumor types³⁶ showing that patients with complete or nearly complete tumor regression are most likely to benefit from preoperative therapy. The present study confirms the relevance of clinical and histopathologic response reported in previous studies^1-3,21 by showing significantly higher survival for patients with responding tumors.

Finally, the findings in FDG-PET did not only correlate well with subsequent response but were also of prognostic relevance. After a follow-up period of up to 53 months, 10 of the 22 patients without a metabolic response had died. In contrast, 12 of the 15 patients with a metabolic response were still alive. Similar significant differences were observed for survival without progression or recurrence. Of note, five patients without a metabolic response even showed disease progression during preoperative therapy.

Although the findings of our study are encouraging, the following limitations should be noted. The optimal cutoff value for prediction of response has been derived from the data of the present study. This post hoc definition may overestimate the diagnostic accuracy of FDG-PET. Furthermore, the CIs for prediction of histopathologic response are relatively wide due to the small number of patients with complete or subtotal tumor regression. Thus the optimal cutoff value for prediction of response has to be confirmed in a larger independent patient population. Three patients (7.5%) were excluded from the present study because contrast between tumor and normal tissue was insufficient for quantitative analysis. In all three cases blood glucose levels were not elevated, and tumor size was comparable to the well-visualized tumors. Thus there seems to be considerable variability in glucose utilization of untreated adenocarcinomas of the esophagogastric junction, and in a small percentage of patients FDG-PET may not be used for therapy monitoring. Furthermore, a baseline and a follow-up PET scan are obviously required to assess tumor response.

Currently there are considerable efforts to improve the efficacy of preoperative therapy by using new chemotherapeutic drugs or a combination of chemotherapy with radiotherapy. However, validation of these approaches in phase II and phase III studies is still required. Therefore, it is unlikely that more effective preoperative therapy will be available in the near future. In contrast, early identification of nonresponding tumors by FDG-PET may allow an optimization of established therapeutic regimes. Patients who do not show a metabolic response after a short period of chemotherapy may undergo salvage therapy consisting of immediate surgery for those with potentially resectable disease or definitive chemoradiotherapy for patients with unresectable tumors. Using this individualized therapy, the prognosis of patients with esophageal and gastroesophageal cancer may be improved by preoperative therapy with currently available chemotherapeutic drugs. The encouraging data of our study indicate that this hypothesis should be tested in randomized trials.

	ACKNOWLEDGMENTS

 
We gratefully acknowledge the effort of the cyclotron and radiochemistry staff. Furthermore, we appreciate the excellent technical support by the technologists at our institution and the editorial help of Leishia Tyndale-Hines, BSc, in the preparation of the manuscript.

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Submitted October 17, 2000; accepted March 19, 2001.

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