Retrospective Study
Copyright ©The Author(s) 2019. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastrointest Oncol. Apr 15, 2019; 11(4): 335-347
Published online Apr 15, 2019. doi: 10.4251/wjgo.v11.i4.335
Significance of HER2 protein expression and HER2 gene amplification in colorectal adenocarcinomas
Xin-Yu Wang, Zhi-Xue Zheng, Yu Sun, Yan-Hua Bai, Yun-Fei Shi, Li-Xin Zhou, Yun-Feng Yao, Ai-Wen Wu, Deng-Feng Cao
Xin-Yu Wang, Yu Sun, Yan-Hua Bai, Yun-Fei Shi, Li-Xin Zhou, Deng-Feng Cao, Key laboratory of Carcinogenesis and Translational Research (Ministry of Education), Department of Pathology, Peking University Cancer Hospital and Institute, Beijing 100142, China
Zhi-Xue Zheng, Yun-Feng Yao, Ai-Wen Wu, Key Laboratory of Carcinogenesis and Translational Research (Ministry of Education), Gastrointestinal Cancer Center, Peking University Cancer Hospital and Institute, Beijing 100142, China
Zhi-Xue Zheng, Department of General Surgery, Beijing Jishuitan Hospital, Beijing 100035, China
Deng-Feng Cao, Department of Pathology and Immunology, Washington University School of Medicine, Saint Louis, MO 63110, United States
Author contributions: Wang XY and Zheng ZX contributed equally to this work; all authors helped to perform the research; Wang XY manuscript writing, performing procedures and data analysis; Zheng ZX contribution to writing the manuscript, drafting conception and design; Wang XY and Zheng ZX contribution to writing the manuscript equally; Sun Y manuscript writing, drafting conception and design, performing experiments, and data analysis; Bai YH, Shi YF, Zhou LX, Yao YF and Wu AW contribution to writing the manuscript; Cao DF contribution to writing the manuscript drafting conception and design.
Supported by Special Scientific Research Key Project for Capital Health Development, China, No. 2018-2Z-1026.
Institutional review board statement: This study was reviewed and approved by the Ethics Committee of Beijing Cancer Hospital.
Informed consent statement: Patients were not required to give informed consent to the study because the analysis used anonymous clinical data that were obtained after each patient agreed to treatment by written consent.
Conflict-of-interest statement: All authors declare no conflicts-of-interest related to this article.
Data sharing statement: No additional data are available.
Open-Access: This article is an open-access article which was selected by an in-house editor and fully peer-reviewed by external reviewers. It is distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/
Corresponding author: Yu Sun, MD, PhD, Associate Professor, Key laboratory of Carcinogenesis and Translational Research (Ministry of Education), Department of Pathology, Peking University Cancer Hospital and Institute, 52 Fucheng Road, Haidian District, Beijing 100142, China. sunyu_bch@163.com
Telephone: +86-10-88196700 Fax: +86-10-88196700
Received: December 26, 2018
Peer-review started: December 26, 2018
First decision: January 11, 2019
Revised: February 13, 2019
Accepted: March 16, 2019
Article in press: March 16, 2019
Published online: April 15, 2019
Processing time: 111 Days and 5.8 Hours
Abstract
BACKGROUND

Human epidermal growth factor receptor 2 (HER2) is an oncogenic driver, and a well-established therapeutic target in breast and gastric cancers. While the role of HER2 as a prognostic biomarker in colorectal adenocarcinomas (CRCs) remains uncertain, its relevance as a therapeutic target has been established. We undertook the present study to evaluate the frequency of HER2 expression in CRC and to correlate it with various clinicopathological variables.

AIM

To correlate HER2 protein expression and HER2 gene amplification with clinicopathological features and survival in surgically resected CRC.

METHODS

About 1195 consecutive surgically resected CRCs were analyzed by immunohistochemical staining (IHC) to assess HER2 protein expression, and 141 selected tumors were further evaluated by fluorescence in situ hybridization (FISH) to assess HER2 gene amplification. Follow-up information was available for 1058 patients, and using this information we investigated the prevalence of HER2 protein overexpression and gene amplification in a large series of surgically resected CRCs, and evaluated the relationship between overexpression and clinicopathological parameters and prognosis.

RESULTS

HER2 IHC scores of 3+, 2+, 1+, and 0 were seen in 31 (2.6%), 105 (8.8%), 475 (39.7%), and 584 (48.9%) tumors, respectively. HER2 gene amplification was seen in 24/29 tumors with an IHC score of 3+ (82.8%; unreadable in 2/31), 12/102 tumors with an IHC score of 2+ (11.8%; unreadable in 2/104), and 0 tumors with IHC score of 1+ (0/10). HER2 gene amplification was seen in 36/1191 tumors (3.0%; unreadable in 4/1195). Among the tumors with HER2 IHC scores of 3+ and 2+, the mean percentage of tumor cells with positive IHC staining was 90% (median 100%, range 40%-100%) and 67% (median 75%, range 5%-95%), respectively (P < 0.05). Among tumors with IHC scores of 2+, those with HER2 gene amplification had a higher number of tumors cells with positive IHC staining (n = 12, mean 93%, median 95%, range 90%-95%) than those without (n = 90, mean 70%, median 50%, range 5%-95%) (P < 0.05). HER2 gene status was significantly associated with distant tumor metastasis and stage (P = 0.028 and 0.025). HER2 protein overexpression as measured by IHC or HER2 gene amplification as measured by FISH was not associated with overall survival (OS) or disease-specific survival for the overall group of 1058 patients. However, further stratification revealed that among patients with tubular adenocarcinomas who were 65 years old or younger (n = 601), those exhibiting HER2 gene amplification had a shorter OS than those without (mean: 47.9 mo vs 65.1 mo, P = 0.04). Among those patients with moderately to poorly differentiated tubular adenocarcinomas, those with positive HER2 tumor IHC scores (2+, 3+) had a shorter mean OS than those with negative HER2 IHC scores (0, 1+) (47.2 mo vs 64.8 mo, P = 0.033). Moreover, among patients with T2 to T4 stage tumors, those with positive HER2 IHC scores also had a shorter mean OS than those with negative HER2 IHC scores (47.1 mo vs 64.8 mo, P = 0.031).

CONCLUSION

HER2 protein levels are correlated with clinical outcomes, and positive HER2 expression as measured by IHC confers a worse prognosis in those patients 65 years old or younger with tubular adenocarcinomas.

Keywords: Human epidermal growth factor receptor 2; Immunohistochemical staining; Fluorescent in situ hybridization; Prognosis; Colorectal cancers

Core tip: The manuscript investigated the prevalence of human epidermal growth factor receptor 2 (HER2) protein overexpression and gene amplification in a large series of surgically resected colorectal adenocarcinomas (CRCs), and evaluated their relationship with clinicopathological parameters and prognosis. We found that HER2 overexpression [immunohistochemical staining (IHC) score 2+ and 3+] is seen in a small percentage of colorectal adenocarcinomas and HER2 gene amplification occurs in the vast majority of tumors with 3+ IHC score but in a much lower percentage of tumors with 2+ IHC score. In addition, although the prevalence of HER2 overexpression by IHC in CRCs is low, HER2 protein status is correlated with clinical outcomes and positive HER2 expression by IHC confers a worse prognosis in 65 years or younger patients with tubular adenocarcinomas.