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Signet-Ring Cell Or Mucinous Histology After Preoperative Chemoradiation and Survival in Patients with Esophageal Or Esophagogastric Junction Adenocarcinoma

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Signet-Ring Cell Or Mucinous Histology After Preoperative Chemoradiation and Survival in Patients with Esophageal Or Esophagogastric Junction Adenocarcinoma Vol. 11, 2229–2236, March 15, 2005 Clinical Cancer Research 2229 Signet-Ring Cell or Mucinous Histology after Preoperative Chemoradiation and Survival in Patients with Esophageal or Esophagogastric Junction Adenocarcinoma Lucian R. Chirieac,1 Stephen G. Swisher,2 Conclusions: Our study showed that patients with Arlene M. Correa,2 Jaffer A. Ajani,3 esophageal or EGJ adenocarcinoma who have signet-ring cell or mucinous histology benefited substantially from Ritsuko R. Komaki,4 Asif Rashid,1 preoperative chemoradiation and esophagectomy. Stanley R. Hamilton,1 and Tsung-Teh Wu1 Departments of 1Pathology, 2Thoracic and Cardiovascular Surgery, 3Gastrointestinal Medical Oncology and 4Division of Radiation Oncology, INTRODUCTION University of Texas M.D. Anderson Cancer Center, Houston, Texas Adenocarcinoma of the esophagus and esophagogastric junction (EGJ) is aggressive and has a poor prognosis (1–6). Esophagectomy has been the main approach for localized ABSTRACT esophageal carcinoma, although multimodality strategies, in- Purpose: The survival of patients with local-regional cluding preoperative chemoradiation followed by esophagec- adenocarcinoma of the esophagus or esophagogastric junction tomy, are accepted modalities of treatment (7). When surgical (EGJ) treated with preoperative chemoradiation is much resection is the primary therapy, the best predictor of overall better in patients with pathologic complete response than survival is pathologic stage (8–12). The outcome of patients those with residual tumor. Some adenocarcinomas have mixed after preoperative chemoradiation is much better if no residual patterns, including signet-ring cell and mucinous histology, carcinoma (stage 0) is found in the resected specimen, but the clinical significance of these subtypes is unknown. representing a pathologic complete response (13–21). However, Experimental Design: We studied 412 consecutive pathologic complete response occurs in <30% of patients who patients with esophageal or EGJ adenocarcinoma treated undergo surgery following preoperative chemoradiation (13). with chemoradiation followed by esophagectomy (193 A subset of adenocarcinomas has mixed histologic patterns, patients) or surgery alone (219 patients). We evaluated including signet-ring cell and mucinous histology. Signet-ring signet-ring cell and mucinous histology in the resection and cell carcinoma is a unique subtype of mucin-producing pretherapy biopsy specimens and compared clinicopathologic adenocarcinoma characterized by abundant intracellular mucin features with overall survival. accumulation and a compressed nucleus displaced toward one Results: The fraction of signet-ring cell and mucinous extremity of the cell. Mucinous carcinoma has abundant histology was similar in evaluated specimens of patients extracellular mucin. These two histologic morphologies com- treated with preoperative chemoradiation or surgery alone monly occur together. In general, the prognosis of patients with (17% and 18%, respectively). The overall survival rate at 5 signet-ring cell carcinoma of any organ site is poor (22–25). years of patients treated with preoperative chemoradiation However, in patients treated with chemoradiation therapy was significantly better if residual signet-ring cell or followed by esophagectomy, it remains unclear whether these mucinous histology was present in the esophagectomy particular histologic patterns indicate worse overall survival. specimen (63% versus 28%; P = 0.02). All 13 patients with Furthermore, acellular mucin pools with no evidence of residual acellular mucin pools and no residual carcinoma are still alive carcinoma cell are identified in a subset of surgical resection after an average follow-up time of 36 months. By contrast, in specimens of patients with local-regional carcinoma of the patients treated with surgery alone, overall survival rate was esophagus and EGJ. No report currently exists about the significantly worse if signet-ring cell or mucinous histology presence of acellular mucin pools predicting overall survival was present (14% versus 30%; P = 0.05). In multivariate for patients who have no residual carcinoma cell in the resected analysis, overall survival was independently predicted by specimen after preoperative therapy. presence of signet-ring cell or mucinous histology (P = 0.04). We have observed that patients with acellular mucin pools with no evidence of residual carcinoma cell in resected specimens have long-term survival after esophagectomy. There- Received 9/10/04; revised 12/8/04; accepted 12/15/04. fore, we hypothesized that patients with local-regional adeno- The costs of publication of this article were defrayed in part by the carcinoma of the esophagus and EGJ with signet-ring cell or payment of page charges. This article must therefore be hereby marked mucinous histology represents a subset of patients who have the advertisement in accordance with 18 U.S.C. Section 1734 solely to highest benefit from preoperative neoadjuvant chemoradiation. indicate this fact. Note: L. R. Chirieac is presently at the Department of Pathology, We also postulated that presence of residual acellular mucin Brigham and Women’s Hospital and Harvard Medical School, Boston, pools in the resection specimen of patients treated with Massachusetts. preoperative neoadjuvant chemoradiation is associated with a Requests for reprints: Tsung-Teh Wu, Department of Pathology, better prognosis. We therefore studied the clinical significance of University of Texas M.D. Anderson Cancer Center, Unit 085, 1515 Holcombe Boulevard, Houston, TX 77030. Phone: 713-745-4977; Fax: signet-ring cell and mucinous histology in 412 patients with 713-792-4049; E-mail: [email protected]. adenocarcinoma of the esophagus and EGJ and related the D2005 American Association for Cancer Research. findings to survival. Downloaded from clincancerres.aacrjournals.org on September 28, 2021. © 2005 American Association for Cancer Research. 2230 Signet-Ring Cells or Mucin in Esophageal Carcinoma MATERIALS AND METHODS cervical approach) in 25 (13%) patients, and transhiatal Patient Characteristics. This study included 412 consec- esophagectomy (abdominal-cervical approach) in 53 (28%) utive patients at the University of Texas M.D. Anderson Cancer patients (26, 27). One (1%) patient underwent two-stage Center who had histologically confirmed adenocarcinoma of the esophagectomy (Table 1). esophagus or EGJ treated with chemoradiation followed by The second group was treated with surgery alone. Patients esophagectomy or surgery alone between 1985 and 2003 and had with clinical stage I and IVB were excluded to serve as a control their pathology specimens available for review (Table 1). The group to patients treated with chemoradiation followed by study was approved by the institutional review board. esophagectomy, leaving 219 patients for study. The mean age The first group of 193 patients was treated with chemo- was 62.5 years (range, 28-84 years). There were 194 men and radiation followed by esophagectomy. The mean age was 25 women. The majority of cancers (93%) were in the distal 59.7 years (range, 32-79 years). There were 180 men and esophagus or EGJ with 7% in the middle or upper esophagus. 13 women. The vast majority of cancers (98%) were in the distal The pretreatment clinical stage was II in 83% of patients, III esophagus or EGJ with only 2% in the middle or upper in 15%, and IVA with celiac lymph node involvement in 2%. esophagus. Patients with clinical stage I or IVB disease Assessment of Esophageal Adenocarcinoma Specimens. (systemic metastases) were not eligible for preoperative chemo- H&E-stained slides from each case were reviewed with no radiation. Pretreatment clinical stage was determined by barium knowledge of the previous diagnosis, staging, or outcome for swallow esophagogram, computed tomographic scan, endo- each case. Patients who were treated with chemoradiation scopic ultrasonography, and positron emission tomography. The followed by esophagectomy had both the post-therapy surgical pretreatment clinical stage was II in 54% of patients, III in specimen and the pre-chemoradiation biopsy specimen evaluated 39%, and IVA with celiac lymph node involvement in 6%. for comparison of the results in the two types of specimens with Three agents were used for preoperative chemotherapy: greatly different sampling. Patients who were treated with fluorouracil, cisplatin, and a taxane. All patients underwent surgery alone had surgical resection specimen evaluated. Speci- computed tomographic simulation for radiation therapy. Clinical mens remained encoded for the entire histopathologic evalua- target volume was defined as the gross tumor volume plus a 5-cm tion. In patients treated with chemoradiation followed by margin superior to the highest extension and inferior to the esophagectomy, residual carcinoma status was determined in lowest extension of the carcinoma with a 2-cm radial margin. each surgical specimen. These patients had either complete Planning target volume was defined as the clinical target volume pathologic response or residual carcinoma present in fibrotic plus a 5-mm margin. The total dose of radiation therapy was tissue or in acellular mucin pools at the primary site. If residual 45 Gy in 25 fractions or 50.4 Gy in 28 fractions prescribed to carcinoma was identified grossly, tumor was sampled for cover at least 95% of the planning target volume. Radiation histologic evaluation in an average of 15 slides (95% confidence therapy was given with megavoltage (>6
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