Original Article
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World J Gastroenterol. Dec 28, 2013; 19(48): 9282-9293
Published online Dec 28, 2013. doi: 10.3748/wjg.v19.i48.9282
Refining pathological evaluation of neoadjuvant therapy for adenocarcinoma of the esophagus
Fergus Noble, Luke Nolan, Adrian C Bateman, James P Byrne, Jamie J Kelly, Ian S Bailey, Donna M Sharland, Charlotte N Rees, Timothy J Iveson, Tim J Underwood, Andrew R Bateman
Fergus Noble, Luke Nolan, Tim J Underwood, Andrew R Bateman, Cancer Sciences Unit, Faculty of Medicine, University of Southampton, Southampton SO16 6YD, United Kingdom
Adrian C Bateman, Department of Cellular Pathology, University Hospital Southampton NHS Foundation Trust, Southampton SO16 6YD, United Kingdom
Fergus Noble, James P Byrne, Jamie J Kelly, Ian S Bailey, Donna M Sharland, Tim J Underwood, Department of Surgery, University Hospital Southampton NHS Foundation Trust, Southampton SO16 6YD, United Kingdom
Charlotte N Rees, Timothy J Iveson, Andrew R Bateman, Cancer Care, University Hospital Southampton NHS Foundation Trust, Southampton SO16 6YD, United Kingdom
Author contributions: Noble F and Nolan L contributed equally to this study; Noble F collected the data and analysed it; Noble F, Nolan L, Underwood TJ and Bateman AR wrote the manuscript; Bateman AC scored the initial patients for pathological regression before this was adopted by the multidisciplinary team; Underwood TJ and Bateman AR had overall responsibility for the scientific content of the manuscript; all authors conceived jointly the idea for the manuscript and contributed to the analysis and reviewed and edited the text.
Supported by A clinical research training fellowship from Cancer Research UK to Noble F; A Medical Research Council (United Kingdom) clinician scientist fellowship to Underwood TJ
Correspondence to: Dr. Andrew R Bateman, Lecturer, Consultant, Clinical Oncologist, Cancer Sciences Unit, Faculty of Medicine, University of Southampton, Somers Cancer Research Building, MP824, Tremona Road, Southampton SO16 6YD, United Kingdom. a.r.bateman@soton.ac.uk
Telephone: +44-23-80796184-6670 Fax: +44-23-80795152
Received: April 26, 2013
Revised: July 12, 2013
Accepted: July 23, 2013
Published online: December 28, 2013
Processing time: 263 Days and 3 Hours
Abstract

AIM: To assess tumour regression grade (TRG) and lymph node downstaging to help define patients who benefit from neoadjuvant chemotherapy.

METHODS: Two hundred and eighteen consecutive patients with adenocarcinoma of the esophagus or gastro-esophageal junction treated with surgery alone or neoadjuvant chemotherapy and surgery between 2005 and 2011 at a single institution were reviewed. Triplet neoadjuvant chemotherapy consisting of platinum, fluoropyrimidine and anthracycline was considered for operable patients (World Health Organization performance status ≤ 2) with clinical stage T2-4 N0-1. Response to neoadjuvant chemotherapy (NAC) was assessed using TRG, as described by Mandard et al. In addition lymph node downstaging was also assessed. Lymph node downstaging was defined by cN1 at diagnosis: assessed radiologically (computed tomography, positron emission tomography, endoscopic ultrasonography), then pathologically recorded as N0 after surgery; ypN0 if NAC given prior to surgery, or pN0 if surgery alone. Patients were followed up for 5 years post surgery. Recurrence was defined radiologically, with or without pathological confirmation. An association was examined between t TRG and lymph node downstaging with disease free survival (DFS) and a comprehensive range of clinicopathological characteristics.

RESULTS: Two hundred and eighteen patients underwent esophageal resection during the study interval with a mean follow up of 3 years (median follow up: 2.552, 95%CI: 2.022-3.081). There was a 1.8% (n = 4) inpatient mortality rate. One hundred and thirty-six (62.4%) patients received NAC, with 74.3% (n = 101) of patients demonstrating some signs of pathological tumour regression (TRG 1-4) and 5.9% (n = 8) having a complete pathological response. Forty four point one percent (n = 60) had downstaging of their nodal disease (cN1 to ypN0), compared to only 15.9% (n = 13) that underwent surgery alone (pre-operatively overstaged: cN1 to pN0), (P < 0.0001). Response to NAC was associated with significantly increased DFS (mean DFS; TRG 1-2: 5.1 years, 95%CI: 4.6-5.6 vs TRG 3-5: 2.8 years, 95%CI: 2.2-3.3, P < 0.0001). Nodal down-staging conferred a significant DFS advantage for those patients with a poor primary tumour response to NAC (median DFS; TRG 3-5 and nodal down-staging: 5.533 years, 95%CI: 3.558-7.531 vs TRG 3-5 and no nodal down-staging: 1.114 years, 95%CI: 0.961-1.267, P < 0.0001).

CONCLUSION: Response to NAC in the primary tumour and in the lymph nodes are both independently associated with improved DFS.

Keywords: Esophageal cancer; Gastro-esophageal cancer; Neoadjuvant; Regression

Core tip: Predictive markers of benefit from neoadjuvant chemotherapy (NAC) in esophageal adenocarcinoma are urgently required to provide a “personalised medicine” approach: directing treatment to those most likely to benefit. Before prospective studies can be initiated, retrospective series need to be interrogated to identify likely candidate markers of a positive response. In defining a positive response attention needs to be given to both response in the primary tumour and in the lymph nodes, as a previously unidentified group of patients who appear to have a poor tumoural response to NAC (tumour regression grade 3-5) do benefit from combination therapy by nodal downstaging.