Clinicopathologic features of synchronous colorectal carcinoma: A distinct subset arising from multiple sessile serrated adenomas and associated with high levels of microsatellite instability and favorable prognosis

Am J Surg Pathol. 2013 Nov;37(11):1660-70. doi: 10.1097/PAS.0b013e31829623b8.

Abstract

Analysis of synchronous colorectal carcinomas can provide a unique model to examine the underlying molecular alterations in colorectal carcinoma, as synchronous tumors arise in a background of common genetic and environmental factors. We analyzed the clinicopathologic and molecular features of synchronous colorectal carcinomas compared with solitary carcinomas to correlate the histologic findings with molecular alterations and to identify the prognostic significance, if any, of synchronous colorectal carcinoma. Of the 4760 primary colorectal carcinomas resected for the years 2002 to 2012 at our institution, 58 patients (1.2%) harbored 2 invasive primary adenocarcinomas and comprise the synchronous colorectal carcinoma study group. A control group of consecutively resected solitary colorectal carcinomas from 109 patients was also analyzed. Compared with solitary colorectal carcinomas, synchronous colorectal carcinomas more frequently were identified in older patients (median age 70 vs. 60 y; P=0.001), involved the right colon (42/58, 72% vs. 47/109, 43%; P=0.0003), were more often microsatellite instability-high (MSI-H) (21/58, 36% vs. 13/109, 12%; P=0.0005), and were more frequently associated with precursor sessile serrated adenomas (SSAs) (13/58, 22% vs. 2/109, 2%; P=0.0001). A statistically significant difference in overall survival was identified between patients with synchronous and solitary colorectal carcinomas (5 y overall survival 92% vs. 56%, P=0.02). A unique subgroup of 13 synchronous colorectal carcinomas demonstrated tumors arising from SSAs (SSA-associated). All SSA-associated synchronous colorectal carcinomas were seen in patients above 65 years of age, and 12/13 (92%) occurred in women. Most patients (12/13, 92%) with SSA-associated synchronous colorectal carcinomas demonstrated involvement of the right colon, and tumors were frequently stage I or II (9/13, 69%) and low grade (11/13, 85%). In 12/13 (92%) SSA-associated synchronous colorectal carcinomas, both tumors exhibited loss of MLH1 and PMS2 immunohistochemical expression with concurrent BRAF V600E mutation. Nine of 13 (69%) patients with SSA-associated colorectal carcinoma harbored additional SSAs. Three of 13 (15%) patients with SSA-associated synchronous colorectal carcinoma met the World Health Organization criteria for serrated polyposis. Notably, no patient with SSA-associated synchronous colorectal carcinoma developed disease recurrence or died of disease at last follow-up. In conclusion, synchronous colorectal carcinomas are enriched with MSI-H tumors, particularly those arising from SSAs, which contributes to the overall improved survival for patients with synchronous tumors compared with patients with solitary tumors. We demonstrate that SSA-associated synchronous colorectal carcinomas have a striking predilection for elderly women, are associated with a favorable prognosis, and are MSI-H and BRAF V600E positive.

MeSH terms

  • Adaptor Proteins, Signal Transducing / analysis
  • Adenocarcinoma / chemistry
  • Adenocarcinoma / genetics
  • Adenocarcinoma / mortality
  • Adenocarcinoma / pathology*
  • Adenocarcinoma / surgery
  • Adenoma / chemistry
  • Adenoma / genetics
  • Adenoma / mortality
  • Adenoma / pathology*
  • Adenoma / surgery
  • Adenosine Triphosphatases / analysis
  • Adult
  • Age Factors
  • Aged
  • Aged, 80 and over
  • Biomarkers, Tumor / analysis
  • Chi-Square Distribution
  • Colorectal Neoplasms / chemistry
  • Colorectal Neoplasms / genetics
  • Colorectal Neoplasms / mortality
  • Colorectal Neoplasms / pathology*
  • Colorectal Neoplasms / surgery
  • DNA Repair Enzymes / analysis
  • DNA-Binding Proteins / analysis
  • Female
  • Genetic Predisposition to Disease
  • Humans
  • Kaplan-Meier Estimate
  • Male
  • Microsatellite Instability*
  • Middle Aged
  • Mismatch Repair Endonuclease PMS2
  • MutL Protein Homolog 1
  • Mutation
  • Neoplasm Grading
  • Neoplasms, Multiple Primary / chemistry
  • Neoplasms, Multiple Primary / genetics
  • Neoplasms, Multiple Primary / mortality
  • Neoplasms, Multiple Primary / pathology*
  • Neoplasms, Multiple Primary / surgery
  • Nuclear Proteins / analysis
  • Phenotype
  • Prognosis
  • Proto-Oncogene Proteins B-raf / genetics
  • Retrospective Studies
  • Risk Factors
  • Sex Factors

Substances

  • Adaptor Proteins, Signal Transducing
  • Biomarkers, Tumor
  • DNA-Binding Proteins
  • MLH1 protein, human
  • Nuclear Proteins
  • BRAF protein, human
  • Proto-Oncogene Proteins B-raf
  • Adenosine Triphosphatases
  • PMS2 protein, human
  • Mismatch Repair Endonuclease PMS2
  • MutL Protein Homolog 1
  • DNA Repair Enzymes