Advertisement
Esophagus| Volume 172, ISSUE 2, P584-592, August 2022

Prognostic value of quantitative parameters for esophageal squamous cell carcinoma determined by preoperative FDG-PET after trimodal therapy

      Abstract

      Background

      Associations between tumor metabolic and volumetric parameters determined by preoperative 18F-fluorodeoxyglucose–positron emission tomography and survival in patients with esophageal squamous cell carcinoma who underwent trimodal therapy have not been fully investigated.

      Methods

      We evaluated relationships between reductions in maximal standardized uptake value, metabolic tumor volume, and total lesion glycolysis in primary tumors on 18F-fluorodeoxyglucose–positron emission tomography images between before and after neoadjuvant chemoradiotherapy and the survival of 120 patients with esophageal squamous cell carcinoma who underwent neoadjuvant chemoradiotherapy followed by surgery.

      Results

      The optimal cutoffs of Δ maximal standardized uptake value, Δ metabolic tumor volume, and Δ total lesion glycolysis were defined to statistically yield the largest differences in recurrence-free survival for good and poor positron emission tomography responders to neoadjuvant chemoradiotherapy (cutoffs: 70%, 85%, and 90%, respectively). These cutoff values significantly stratified overall survival (Δ maximal standardized uptake value, P = .004; Δ metabolic tumor volume, P = .001; Δ total lesion glycolysis, P < .0001). Univariate analysis showed that Δ maximal standardized uptake value (hazard ratio, 0.50; 95% confidence interval, 0.32–0.79; P = .003), Δ metabolic tumor volume (hazard ratio, 0.50; 95% confidence interval, 0.31–0.81; P = .004), and Δ total lesion glycolysis (hazard ratio, 0.37; 95% confidence interval, 0.23–0.61; P < .001) were statistically significant for recurrence-free survival. Furthermore, Δ metabolic tumor volume (hazard ratio, 0.45; 95% confidence interval, 0.27–0.76; P = .003) and Δ total lesion glycolysis (hazard ratio, 0.37; 95% confidence interval, 0.22–0.63; P < .001) were independent factors for recurrence-free survival in multivariate analyses that included preoperative and pathological factors.

      Conclusion

      Together with significant pathological prognostic factors, Δ metabolic tumor volume and Δ total lesion glycolysis were valuable for patients with esophageal squamous cell carcinoma who received trimodal therapy. Thus, preoperative 18F-fluorodeoxyglucose–positron emission tomography is a useful and noninvasive diagnostic tool that might facilitate tailoring optimal therapies for locally advanced esophageal squamous cell carcinoma.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribe:

      Subscribe to Surgery
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Institutional Access: Sign in to ScienceDirect

      References

        • Sjoquist K.M.
        • Burmeister B.H.
        • Smithers B.M.
        • et al.
        • Australasian Gastro-Intestinal Trials Group
        Survival after neoadjuvant chemotherapy or chemoradiotherapy for resectable oesophageal carcinoma: an updated meta-analysis.
        Lancet Oncol. 2011; 12: 681-692
        • van Hagen P.
        • Hulshof M.C.
        • van Lanschot J.J.
        • et al.
        CROSS Group: preoperative chemoradiotherapy for esophageal or junctional cancer.
        N Engl J Med. 2012; 366: 2074-2084
        • Tepper J.
        • Krasna M.J.
        • Niedzwiecki D.
        • et al.
        Phase III trial of trimodal therapy with cisplatin, fluorouracil, radiotherapy, and surgery compared with surgery alone for esophageal cancer: CALGB 9781.
        J Clin Oncol. 2008; 26: 1086-1092
        • Demarest C.T.
        • Chang A.C.
        The landmark series: multimodal therapy for esophageal cancer.
        Ann Surg Oncol. 2021; 28: 3375-3382
        • Hamai Y.
        • Hihara J.
        • Emi M.
        • et al.
        Results of neoadjuvant chemoradiotherapy with docetaxel and 5-fluorouracil followed by esophagectomy to treat locally advanced esophageal cancer.
        Ann Thorac Surg. 2015; 99: 1887-1893
        • Murakami Y.
        • Hamai Y.
        • Emi M.
        • et al.
        Long-term results of neoadjuvant chemoradiotherapy using cisplatin and 5-fluorouracil followed by esophagectomy for resectable, locally advanced esophageal squamous cell carcinoma.
        J Radiat Res. 2018; 59: 616-624
        • Schmidt T.
        • Lordick F.
        • Herrmann K.
        • Ott K.
        Value of functional imaging by PET in esophageal cancer.
        J Natl Compr Canc Netw. 2015; 13: 239-247
        • Gillies R.S.
        • Middleton M.R.
        • Maynard N.D.
        • Bradley K.M.
        • Gleeson F.V.
        Additional benefit of 18F-fluorodeoxyglucose integrated positron emission tomography/computed tomography in the staging of oesophageal cancer.
        Eur Radiol. 2011; 21: 274-280
        • Hamai Y.
        • Hihara J.
        • Emi M.
        • et al.
        Ability of fluorine-18 fluorodeoxyglucose positron emission tomography to predict outcomes of neoadjuvant chemoradiotherapy followed by surgical treatment for esophageal squamous cell carcinoma.
        Ann Thorac Surg. 2016; 102: 1132-1139
        • Cong L.
        • Wang S.
        • Gao T.
        • Hu L.
        The predictive value of 18F-FDG PET for pathological response of primary tumor in patients with esophageal cancer during or after neoadjuvant chemoradiotherapy: a meta-analysis.
        Jpn J Clin Oncol. 2016; 46: 1118-1126
        • Ohsawa M.
        • Hamai Y.
        • Emi M.
        • et al.
        Tumor response in esophageal squamous cell carcinoma treated with neoadjuvant chemotherapy followed by surgery.
        Anticancer Res. 2020; 40: 1153-1160
        • Hamai Y.
        • Emi M.
        • Ibuki Y.
        • et al.
        Predictions of pathological features and recurrence based on FDG-PET findings of esophageal squamous cell carcinoma after trimodal therapy.
        Ann Surg Oncol. 2020; 27: 4422-4430
        • Han S.
        • Kim Y.J.
        • Woo S.
        • Suh C.H.
        • Lee J.J.
        Prognostic value of volumetric parameters of pretreatment 18F-FDG PET/CT in esophageal cancer: a systematic review and meta-analysis.
        Clin Nucl Med. 2018; 43: 887-894
        • Sonoda A.
        • Yoshida N.
        • Shiraishi S.
        • et al.
        Total lesion glycolysis ratio in positron emission tomography/computed tomography images during neoadjuvant chemotherapy can predict pathological tumor regression grade and prognosis in patients with locally advanced squamous cell carcinoma of the esophagus.
        Ann Surg Oncol. 2021; 28: 167-174
        • Tustumi F.
        • Duarte P.S.
        • Albenda D.G.
        • et al.
        Prognostic value of 18F-fluorodeoxyglucose PET/computed tomography metabolic parameters measured in the primary tumor and suspicious lymph nodes before neoadjuvant therapy in patients with esophageal carcinoma.
        Nucl Med Commun. 2021; 42: 437-443
        • Makino T.
        • Yamasaki M.
        • Tanaka K.
        • et al.
        Metabolic tumor volume change predicts long-term survival and histological response to preoperative chemotherapy in locally advanced esophageal cancer.
        Ann Surg. 2019; 270: 1090-1095
      1. Brierley J.D. Gospodarowicz M.K. Wittekind C. TNM Classification of Malignant Tumors. 8th ed. Wiley-Blackwell, Oxford2017
        • Hamai Y.
        • Emi M.
        • Ibuki Y.
        • et al.
        Distribution of lymph node metastasis in esophageal squamous cell carcinoma after trimodal therapy.
        Ann Surg Oncol. 2021; 28: 1798-1807
        • Hamai Y.
        • Hihara J.
        • Emi M.
        • et al.
        Clinical significance of 18F-fluorodeoxyglucose-positron emission tomography-positive lymph nodes to outcomes of trimodal therapy for esophageal squamous cell carcinoma.
        Ann Surg Oncol. 2019; 26: 1869-1878
        • Therasse P.
        • Arbuck S.G.
        • Eisenhauer E.A.
        • et al.
        New guidelines to evaluate the response to treatment in solid tumors.
        J Natl Cancer Inst. 2000; 92: 205-216
        • Makino T.
        • Miyata H.
        • Yamasaki M.
        • et al.
        Utility of response evaluation to neo-adjuvant chemotherapy by (18)F-fluorodeoxyglucose-positron emission tomography in locally advanced esophageal squamous cell carcinoma.
        Surgery. 2010; 148: 908-918
        • Chen Y.H.
        • Lue K.H.
        • Chu S.C.
        • et al.
        Combining the radiomic features and traditional parameters of 18F-FDG PET with clinical profiles to improve prognostic stratification in patients with esophageal squamous cell carcinoma treated with neoadjuvant chemoradiotherapy and surgery.
        Ann Nucl Med. 2019; 33: 657-670
        • Port J.L.
        • Lee P.C.
        • Korst R.J.
        • et al.
        Positron emission tomographic scanning predicts survival after induction chemotherapy for esophageal carcinoma.
        Ann Thorac Surg. 2007; 84: 393-400
        • Miyata H.
        • Yamasaki M.
        • Takahashi T.
        • et al.
        Determinants of response to neoadjuvant chemotherapy for esophageal cancer using 18F-fluorodeoxiglucose positron emission tomography (18F-FDG-PET).
        Ann Surg Oncol. 2014; 21: 575-582
        • Zhu W.
        • Xing L.
        • Yue J.
        • et al.
        Prognostic significance of SUV on PET/CT in patients with localised oesophagogastric junction cancer receiving neoadjuvant chemotherapy/chemoradiation: a systematic review and meta-analysis.
        Br J Radiol. 2012; 85: e694-e701
        • Han S.
        • Kim Y.I.
        • Woo S.
        • Kim T.H.
        • Ryu J.S.
        Prognostic and predictive values of interim 18F-FDG PET during neoadjuvant chemoradiotherapy for esophageal cancer: a systematic review and meta-analysis.
        Ann Nucl Med. 2021; 35: 447-457
        • Tamandl D.
        • Gore R.M.
        • Fueger B.
        • et al.
        Change in volume parameters induced by neoadjuvant chemotherapy provide accurate prediction of overall survival after resection in patients with oesophageal cancer.
        Eur Radiol. 2016; 26: 311-321
        • Choi Y.
        • Choi J.Y.
        • Hong T.H.
        • et al.
        Trimodality therapy for locally advanced esophageal squamous cell carcinoma: the role of volume-based PET/CT in patient management and prognostication.
        Eur J Nucl Med Mol Imaging. 2022; 49: 751-762
        • van Rossum P.S.N.
        • Fried D.V.
        • Zhang L.
        • et al.
        The value of 18F-FDG PET before and after induction chemotherapy for the early prediction of a poor pathologic response to subsequent preoperative chemoradiotherapy in oesophageal adenocarcinoma.
        Eur J Nucl Med Mol Imaging. 2017; 44: 71-80
        • Li C.
        • Lin J.W.
        • Yeh H.L.
        • Chuang C.Y.
        • Chen C.C.
        Good prediction of treatment responses to neoadjuvant chemoradiotherapy for esophageal cancer based on preoperative inflammatory status and tumor glucose metabolism.
        Sci Rep. 2021; 11: 11626
        • Kato H.
        • Takita J.
        • Miyazaki T.
        • et al.
        Correlation of 18-F-fluorodeoxyglucose (FDG) accumulation with glucose transporter (Glut-1) expression in esophageal squamous cell carcinoma.
        Anticancer Res. 2003; 23: 3263-3272