FDG PET using SUVmax for preoperative T-staging of esophageal squamous cell carcinoma with and without neoadjuvant chemoradiotherapy

BackgroundAccurate T-staging is pivotal for predicting prognosis and selecting appropriate therapies for esophageal squamous cell carcinoma (ESCC). The diagnostic performance of fluorodeoxyglucose (FDG) positron emission tomography/computed tomography (PET/CT) for its T-staging is uncertain. We investigated use of FDG PET/CT for preoperative T-staging of patients with ESCC.MethodsPatients with ESCC given preoperative FDG PET/CT scans, either with (CRT[+] group) or without (CRT[−] group) neoadjuvant chemoradiotherapy, were retrospectively reviewed. Maximal standardized uptake value (SUVmax) of the primary tumors on FDG PET/CT scans were measured, and histopathological results were used as the reference standard. The associations between pathological T-stage and potential factors of age, tumor location, tumor grade, tumor size, and tumor SUVmax were analyzed. The cut-off levels of SUVmax for predicting different T-stages and for residual viable tumors after neoadjuvant chemoradiotherapy were determined using receiver operating characteristic analyses.ResultsWe enrolled 103 patients (45 in the CRT[−] group; 58 in the CRT[+] group). SUVmax, an independent predictive factor, positively correlated with the pathological T-stage in both groups (CRT[−] group: ρ = 0.736, p < 0.001; and CRT[+] group: ρ = 0.792, p < 0.001). The overall accuracy of the PET/CT with thresholded SUVmax for predicting the pathological T-stage was 73.3% in the CRT[−] group (SUVmax of T0: 0–1.9, T1: 2.0–4.4, T2: 4.5–6.5, T3: 6.6–13.0, T4: >13.0) and 67.2% in the CRT[+] group (SUVmax of T0: 0–3.4, T1: 3.5–3.9, T2: 4.0–5.5, T3: 5.6–6.2, T4: > 6.2). For CRT[−] group, the accuracy using an SUVmax cut-off of 4.4 to differentiate early (T0-1) from locally advanced disease (T2-4) was 82.2% (95% CI, 71.1–93.4%). For CRT[+] group, the accuracy using an SUVmax cut-off of 3.4 to predict residual viable tumors (non-T0) after completion of chemoradiotherapy was 82.8% (95% CI, 73.0–92.5%).ConclusionsThe FDG avidity of a primary esophageal tumor significantly positively correlated with the pathological T-stage. PET/CT with thresholded SUVmax was useful for predicting T-stage and differentiating residual viable tumors.

[1]  Val Gebski,et al.  Survival benefits from neoadjuvant chemoradiotherapy or chemotherapy in oesophageal carcinoma: a meta-analysis. , 2007, The Lancet. Oncology.

[2]  R. Munden,et al.  Utility of PET, CT, and EUS to identify pathologic responders in esophageal cancer. , 2004, The Annals of thoracic surgery.

[3]  N. Tamaki,et al.  Diagnostic Accuracy of Lymph Node Metastasis Depends on Metabolic Activity of the Primary Lesion in Thoracic Squamous Esophageal Cancer , 2013, The Journal of Nuclear Medicine.

[4]  Kyung-Ja Cho,et al.  FDG-PET in the prediction of pathologic response after neoadjuvant chemoradiotherapy in locally advanced, resectable esophageal cancer. , 2005, International journal of radiation oncology, biology, physics.

[5]  J. Pruim,et al.  OF THE STAGING PERFORMANCE OF 18 F-FLUORODEOXYGLUCOSE POSITRON EMISSION TOMOGRAPHY IN ESOPHAGEAL CANCER , 2018 .

[6]  W. Zoller,et al.  Different accuracy of endosonographic tumor staging after neoadjuvant chemotherapy and chemoradiotherapy in esophageal cancer , 2016, Surgical Endoscopy.

[7]  M. Dempsey,et al.  PET–CT Evaluation of Solitary Pulmonary Nodules: Correlation with Maximum Standardized Uptake Value and Pathology , 2013, Lung.

[8]  C. Mathers,et al.  GLOBOCAN 2012 v1.0, Cancer Incidence and Mortality Worldwide: IARC CancerBase No. 11 [Internet]. Lyon, France: International Agency for Research on Cancer , 2013 .

[9]  J. Siewert,et al.  Are squamous and adenocarcinomas of the esophagus the same disease? , 2007, Seminars in radiation oncology.

[10]  Jian Zhang,et al.  Relationship between 18F-fluorodeoxyglucose uptake in primary lesions and clinicopathological characteristics of esophageal squamous cell carcinoma patients , 2012, Experimental and therapeutic medicine.

[11]  R. M. Kwee Prediction of tumor response to neoadjuvant therapy in patients with esophageal cancer with use of 18F FDG PET: a systematic review. , 2010, Radiology.

[12]  D. Sugarbaker,et al.  Phase III trial of trimodality therapy with cisplatin, fluorouracil, radiotherapy, and surgery compared with surgery alone for esophageal cancer: CALGB 9781. , 2008, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[13]  A. Hölscher,et al.  Histological type of esophageal cancer might affect response to neo-adjuvant radiochemotherapy and subsequent prognosis. , 2009, Annals of Oncology.

[14]  J. Birkmeyer,et al.  Specialty training and mortality after esophageal cancer resection. , 2005, The Annals of thoracic surgery.

[15]  J. Takita,et al.  The incremental effect of positron emission tomography on diagnostic accuracy in the initial staging of esophageal carcinoma , 2005, Cancer.

[16]  E W Steyerberg,et al.  Preoperative chemoradiotherapy for esophageal or junctional cancer. , 2012, The New England journal of medicine.

[17]  T. Turkington,et al.  A systematic review of the factors affecting accuracy of SUV measurements. , 2010, AJR. American journal of roentgenology.

[18]  C. Compton,et al.  AJCC Cancer Staging Manual , 2002, Springer New York.

[19]  W. Allum,et al.  Long-term results of a randomized trial of surgery with or without preoperative chemotherapy in esophageal cancer. , 2009, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[20]  J. Birkmeyer,et al.  Outcomes after transhiatal and transthoracic esophagectomy for cancer. , 2008, The Annals of thoracic surgery.

[21]  D Delbeke,et al.  Prospective investigation of positron emission tomography in lung nodules. , 1998, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[22]  A. Livingstone,et al.  The role of endoscopic ultrasound in assessing tumor response and staging after neoadjuvant chemotherapy for esophageal cancer , 2012, Surgical Endoscopy.

[23]  J. Hainsworth,et al.  Preoperative combined modality therapy with paclitaxel, carboplatin, prolonged infusion 5-fluorouracil, and radiation therapy in localized esophageal cancer: preliminary results of a Minnie Pearl Cancer Research Network phase II trial. , 1999, The cancer journal from Scientific American.

[24]  Hao Wang,et al.  Complete response to neoadjuvant chemoradiotherapy in esophageal carcinoma is associated with significantly improved survival. , 2005, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[25]  D. Domagk,et al.  Endoscopic Ultrasound in Staging Esophageal Cancer After Neoadjuvant Chemotherapy—Results of a Multicenter Cohort Analysis , 2013, Journal of Gastrointestinal Surgery.

[26]  H. Nava,et al.  Role of Repeat 18F-Fluorodeoxyglucose Positron Emission Tomography Examination in Predicting Pathologic Response Following Neoadjuvant Chemoradiotherapy for Esophageal Adenocarcinoma. , 2015, JAMA surgery.

[27]  Su Jin Lee,et al.  The prognostic value of total lesion glycolysis via 18F-fluorodeoxyglucose PET–CT in surgically treated esophageal squamous cell carcinoma , 2015, Annals of Nuclear Medicine.

[28]  L. Neumayer,et al.  Comparing outcomes after transthoracic and transhiatal esophagectomy: a 5-year prospective cohort of 17,395 patients. , 2007, Journal of the American College of Surgeons.

[29]  R. Cerfolio,et al.  Maximum standardized uptake values on positron emission tomography of esophageal cancer predicts stage, tumor biology, and survival. , 2006, The Annals of thoracic surgery.

[30]  M. Schwaiger,et al.  Metabolic imaging predicts response, survival, and recurrence in adenocarcinomas of the esophagogastric junction. , 2006, Journal of clinical oncology : official journal of the American Society of Clinical Oncology.

[31]  E. Blackstone,et al.  Is FDG-PET indicated for superficial esophageal cancer? , 2007, European journal of cardio-thoracic surgery : official journal of the European Association for Cardio-thoracic Surgery.

[32]  Soo Young Kim,et al.  Value of complete metabolic response by (18)F-fluorodeoxyglucose-positron emission tomography in oesophageal cancer for prediction of pathologic response and survival after preoperative chemoradiotherapy. , 2007, European journal of cancer.

[33]  E. Mohammadi,et al.  Barriers and facilitators related to the implementation of a physiological track and trigger system: A systematic review of the qualitative evidence , 2017, International journal for quality in health care : journal of the International Society for Quality in Health Care.

[34]  L. Kong,et al.  Oesophageal squamous cell carcinoma: relationship between fluorine-18 fludeoxyglucose positron emission tomography CT maximum standardised uptake value, metabolic tumour volume, and tumour, node and metastasis classification. , 2012, The British journal of radiology.

[35]  Hua Wu,et al.  Pre-treatment metabolic tumor volume and total lesion glycolysis are useful prognostic factors for esophageal squamous cell cancer patients. , 2014, Asian Pacific journal of cancer prevention : APJCP.

[36]  Kyoungjune Pak,et al.  Clinical Implication of PET/MR Imaging in Preoperative Esophageal Cancer Staging: Comparison with PET/CT, Endoscopic Ultrasonography, and CT , 2014, The Journal of Nuclear Medicine.

[37]  Ora Israel,et al.  The additional value of PET/CT over PET in FDG imaging of oesophageal cancer , 2005, European Journal of Nuclear Medicine and Molecular Imaging.

[38]  Yu-Chung Wu,et al.  Positron emission tomography-computed tomography in predicting locoregional invasion in esophageal squamous cell carcinoma. , 2009, The Annals of thoracic surgery.