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Evaluation of Response to Neoadjuvant Chemotherapy for Esophageal Cancer: PET Response Criteria in Solid Tumors Versus Response Evaluation Criteria in Solid Tumors

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Evaluation of Response to Neoadjuvant Chemotherapy for Esophageal Cancer: PET Response Criteria in Solid Tumors Versus Response Evaluation Criteria in Solid Tumors Journal of Nuclear Medicine, published on May 11, 2012 as doi:10.2967/jnumed.111.098699 Evaluation of Response to Neoadjuvant Chemotherapy for Esophageal Cancer: PET Response Criteria in Solid Tumors Versus Response Evaluation Criteria in Solid Tumors Masahiro Yanagawa*1, Mitsuaki Tatsumi*1,2, Hiroshi Miyata3, Eiichi Morii4, Noriyuki Tomiyama1, Tadashi Watabe2, Kayako Isohashi2, Hiroki Kato2, Eku Shimosegawa2, Makoto Yamasaki3, Masaki Mori3, Yuichiro Doki3, and Jun Hatazawa2 1Department of Radiology, Osaka University Graduate School of Medicine, Suita-city, Osaka, Japan; 2Department of Nuclear Medicine and Tracer Kinetics, Osaka University Graduate School of Medicine, Suita-city, Osaka, Japan; 3Department of Gastroenterological Surgery, Osaka University Graduate School of Medicine, Suita-city, Osaka, Japan; and 4Department of Pathology, Osaka University Graduate School of Medicine, Suita-city, Osaka, Japan onstrate the correlation between therapeutic responses and Recently, PET response criteria in solid tumors (PERCIST) have prognosis in patients with esophageal cancer receiving neoadju- been proposed as a new standardized method to assess vant chemotherapy. However, PERCIST was found to be the chemotherapeutic response metabolically and quantitatively. strongest independent predictor of outcomes. Given the signifi- The aim of this study was to evaluate therapeutic response to cance of noninvasive radiologic imaging in formulating clinical neoadjuvant chemotherapy for locally advanced esophageal treatment strategies, PERCIST might be considered more suit- cancer, comparing PERCIST with the currently widely used able for evaluation of chemotherapeutic response to esophageal response evaluation criteria in solid tumors (RECIST). Methods: cancer than RECIST. Fifty-one patients with locally advanced esophageal cancer who Key Words: RECIST; PERCIST; 18F-FDG PET; esophageal cancer; received neoadjuvant chemotherapy (5-fluorouracil, adriamycin, response to therapy and cisplatin), followed by surgery were studied. Chemothera- J Nucl Med 2012; 53:1–9 18 peutic lesion responses were evaluated using F-FDG PET DOI: 10.2967/jnumed.111.098699 and CT according to the RECIST and PERCIST methods. The PET/CT scans were obtained before chemotherapy and about 2 wk after completion of chemotherapy. Associations were statis- tically analyzed between survival (overall and disease-free sur- vival) and clinicopathologic results (histology [well-, moderately, and poorly differentiated squamous cell carcinoma], lymphatic In today’s medicine, various treatment options for cancer invasion, venous invasion, clinical stage, pathologic stage, resec- are available. The selection of an effective treatment and the tion level, reduction rate of tumor diameter, reduction rate of tumor uptake, chemotherapeutic responses in RECIST and PER- appropriate evaluation of treatment response are important CIST, and pathologic response). Results: There was a significant both for better management of cancer patients with prolonged difference in response classification between RECIST and PER- survival and for preserving quality of life. Many approaches to CIST (Wilcoxon signed-rank test, P , 0.0001). Univariate analysis objectively assess treatment response, which began with the showed that lymphatic invasion, venous invasion, resection level, original report by Moertel in 1976 and the subsequent World pathologic stage, and PERCIST were significant factors associ- Health Organization criteria in 1979 and were followed by the ated with disease-free or overall survival in this study. Although Response Evaluation Criteria in Solid Tumors (RECIST) in multivariate analysis demonstrated that venous invasion (dis- ease-free survival: hazard ratio [HR] 5 4.519, P 5 0.002; overall 2000 and RECIST 1.1 in 2009 (1–4), have been developed. survival: HR 5 5.591, P 5 0.003) and resection level (disease-free RECIST is widely used as an anatomic tumor response metric survival: HR 5 11.078, P 5 0.001) were the significant predictors, but is known to have limitations in the cases with tumors that PERCIST was also significant in noninvasive therapy response have obscure margins or scar tissue after treatment. Especially assessment before surgery (disease-free survival: HR 5 4.060, in patients with esophageal cancer, the measurement of the P 5 0.025; overall survival: HR 5 8.953, P 5 0.034). Conclusion: longest diameter of lesions on CT and resultant evaluation of RECIST based on the anatomic size reduction rate did not dem- treatment response are difficult. Moreover, some caution is required when predicting outcomes with novel molecularly Received Sep. 27, 2011; revision accepted Jan. 20, 2012. targeted cancer treatments with RECIST, which is based on For correspondence or reprints contact: Masahiro Yanagawa, Department of the reduction rate of morphologic size (5–10). Such treat- Radiology, Osaka University Graduate School of Medicine, 2-2 Yamadaoka, Suita-city, Osaka, 565-0871, Japan. ments, which tend to be more cytostatic than cytocidal, offer E-mail: [email protected] a substantial improvement in outcome, even without major *Contributed equally to this work. Published online nnnn. shrinkage of tumors as evidenced by the partial response COPYRIGHT ª 2012 by the Society of Nuclear Medicine, Inc. (PR) or complete response (CR) in RECIST (11,12). THERAPY EVALUATION IN ESOPHAGEAL CANCER • Yanagawa et al. 1 jnm098699-pm n 5/11/12 Copyright 2012 by Society of Nuclear Medicine. PET with the glucose analog 18F-FDG has been widely and adriamycin (30 mg/m2) given intravenously over 2 h on day 1 used as a technique for evaluating metabolic activity in and 5-fluorouracil (700 mg/m2) administered by continuous in- tumors. 18F-FDG PET is believed to be more informative travenous infusion on days 1–7. This course was repeated every for the evaluation of treatment response after chemotherapy 28 d unless patients showed progressive disease after the first course: (13). Recently, Wahl et al. proposed the PET Response 2 courses were performed. All patients underwent surgery 3–5 wk after the completion of neoadjuvant chemotherapy. Surgery con- Criteria in Solid Tumors (PERCIST) as a new standardized sisted of en bloc esophagectomy, reconstruction with a gastric tube, method for the quantitative assessment of metabolic tumor and 2- or 3-field lymphadenectomy. response. This method was proposed after review of ap- proximately 3,000 potentially relevant references regarding PET/CT Protocol qualitative and quantitative approaches to tumor response PET/CT was performed with an integrated scanner (Gemini assessment with 18F-FDG PET (14). Although the concept GXL; Philips). Whole-body images, generally from the top of the behind the method is quite reasonable, PERCIST should be skull to mid thigh, were acquired about 60 min after intravenous properly evaluated with regard to advantages over RECIST injection of 18F-FDG at the dose of 3.7 MBq (0.10 mCi)/kg of in clinical cases. The aim of this study was to compare the weight. PET was performed using the following parameters: 3-di- PERCIST and RECIST methods for evaluation of therapeu- mensional emission scan, 2-min scan per bed position · 11 posi- tic response to neoadjuvant chemotherapy in patients with tions, ordered-subset expectation maximization reconstruction, and esophageal cancer. 4.0-mm slice thickness per interval. Acquisition parameters for CT were as follows: breath-hold during normal expiration from the level of apex of lungs to the lower pole of kidneys; no intravenous MATERIALS AND METHODS or oral contrast medium; 120 kVp and 50 effective mAs; 16 slices; Study Design 1.5-mm detector collimation; and 5.0-mm slice thickness, with Records of 64 patients with histologically confirmed squamous a 4.0-mm interval. Coronal and sagittal CT images were recon- cell carcinoma of the thoracic esophagus, who underwent neo- structed using axial thin-section CT images with 1.5-mm slice thick- adjuvant chemotherapy at the Department of Gastroenterological ness. The PET/CT scans were obtained before chemotherapy and Surgery, Osaka University Graduate School of Medicine, between about 2 wk after completion of neoadjuvant chemotherapy. June 2007 and March 2010, were reviewed. At baseline, all patients underwent esophageal fiberscopy, esophagography, and enhanced Image Analysis According to PERCIST CT from the neck to the abdomen for tumor staging according to the The software used for this study might have limitations in obtain- TNM classification (15). CT image acquisition began 50 s after in- ing the peak SUV (SUVpeak) as exactly specified in PERCIST 1.0 travenous injection of contrast medium (iodine content, 300 mg of (14). These limitations are due to a maximum standardized uptake iodine/mL) at a rate of 2 mL/s. All patients were newly diagnosed value (SUV 5 tumor activity concentration/injected dose/body and had no prior treatment. Our indication for neoadjuvant chemo- weight) that is not necessarily included in the volume of interest therapy was as follows: patients with any tumor depth (clinical T1– because of the noise effects from patients’ bodies. We used a mod- 4) and lymph node involvement, including regional lymph node (N1) ified method to obtain SUVpeak as follows. First, the entire tumor and distant lymph node (M1 lym) without distant organ metastases. was enclosed using a manual volume of interest to determine the Clinical T1–3N1 was regarded as an absolute indication, and either pixel with the maximum SUV in the tumor on PET. Second, the cT3N0 with
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