Basic Study
Copyright ©The Author(s) 2017. Published by Baishideng Publishing Group Inc. All rights reserved.
World J Gastroenterol. Oct 21, 2017; 23(39): 7087-7097
Published online Oct 21, 2017. doi: 10.3748/wjg.v23.i39.7087
Detection of KRAS G12D in colorectal cancer stool by droplet digital PCR
Susana Olmedillas-López, Dennis César Lévano-Linares, Carmen Laura Aúz Alexandre, Luz Vega-Clemente, Edurne León Sánchez, Alejandro Villagrasa, Jaime Ruíz-Tovar, Mariano García-Arranz, Damián García-Olmo
Susana Olmedillas-López, Luz Vega-Clemente, Alejandro Villagrasa, Mariano García-Arranz, Damián García-Olmo, Foundation Health Research Institute-Fundación Jiménez Díaz University Hospital, Madrid 28040, Spain
Dennis César Lévano-Linares, Mariano García-Arranz, Damián García-Olmo, Department of Surgery, School of Medicine, Universidad Autónoma de Madrid, Madrid 28029, Spain
Dennis César Lévano-Linares, Jaime Ruíz-Tovar, Department of Surgery, Rey Juan Carlos University Hospital, Madrid 28933, Spain
Carmen Laura Aúz Alexandre, Department of Pathology, Fundación Jiménez Díaz University Hospital, Madrid 28040, Spain
Edurne León Sánchez, Department of Biomedicine and Biotechnology, Universidad de Alcalá, Madrid 28805, Spain
Damián García-Olmo, Department of Surgery, Fundación Jiménez Díaz University Hospital, Madrid 28040, Spain
Author contributions: Olmedillas-López S and Lévano-Linares DC contributed equally to this work; Olmedillas-López S, Lévano-Linares DC, García-Arranz M and García-Olmo D conceived and designed the experiments; Olmedillas-López S, Aúz Alexandre CL, Vega-Clemente L, León Sánchez E and Villagrasa A performed the experiments; Olmedillas-López S, Lévano-Linares DC, Ruíz-Tovar J, García-Arranz M and García-Olmo D analyzed the data; Olmedillas-López S and Lévano-Linares DC wrote the paper.
Supported by “Fondo de Investigaciones Sanitarias (FIS)-FEDER”, Ministry of Health, Spain, No. PI13/01924 to García-Olmo D; and RETIC Program of ISCIII-FEDER, No. RD12/0019/0035 to Olmedillas-López S.
Institutional review board statement: This study was reviewed and approved by the Institutional Ethics Committee for Clinical Research of the Fundación Jiménez Díaz University Hospital (FJD) (PIC 63/2016_FJD).
Conflict-of-interest statement: The authors have no conflict of interest to declare.
Data sharing statement: Individual participant consent was not obtained for data sharing but the presented data are anonymized and there is no possibility of identification. 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/
Correspondence to: Susana Olmedillas-López, PhD, Postdoc Researcher, Foundation Health Research Institute-Fundación Jiménez Díaz University Hospital, Avda. Reyes Católicos 2, Madrid 28040, Spain. susana.olmedillas@fjd.es
Telephone: +34-91-5504800-2781 Fax: +34-91-5505353
Received: June 28, 2017
Peer-review started: June 28, 2017
First decision: August 15, 2017
Revised: September 15, 2017
Accepted: September 26, 2017
Article in press: September 26, 2017
Published online: October 21, 2017
Processing time: 115 Days and 21.2 Hours
ARTICLE HIGHLIGHTS
Research background

Clinical management of colorectal cancer (CRC) requires analysis of molecular biomarkers, such as KRAS or NRAS mutations, which are associated with the emergence of resistance to therapy with biological agents. Tumor genotyping is usually performed using DNA from tissue biopsies, and, in recent years, from blood as well. However, at early disease stages, levels of mutated copies in circulating cell-free DNA may be, in some cases, too low for detection. Thus, extremely sensitive and non-invasive alternative methods are still needed to improve detection and achieve accurate quantification of these biomarkers.

Research motivation

Stool is an alternative and non-invasive source of genetic material for tumor genotyping in CRC. To date, several strategies based on analysis of molecular markers in fecal samples have been proposed, though their application in clinical practice remains limited due to their elevated cost and reduced sensitivity at early stages of disease.

Research objectives

The aim of this study was to assess the potential of droplet digital PCR (ddPCR) to detect the KRAS G12D mutation in stool-derived DNA from CRC patients as a proof-of-concept for the applicability of this technology as a non-invasive method of studying clinically relevant DNA biomarkers in stool.

Research methods

KRAS mutations were determined by pyrosequencing in DNA obtained from formalin-fixed paraffin-embedded (FFPE) tumor tissues. Then, KRAS G12D mutation was analyzed by ddPCR in FFPE tumors and stool-derived DNA in samples obtained from patients carrying this point mutation.

Research results

The KRAS G12D mutation was detected by ddPCR in FFPE tumor-derived DNA and in stool-derived DNA in 80% of all fecal samples from CRC patients with this mutation.

Research conclusions

This is the first study to describe the detection of the KRAS G12D mutation in stool-derived DNA from CRC patients using a commercially available ddPCR platform, including in individuals with early stages of the disease. dPCR served as a reliable tool for detecting this clinically relevant mutation in stool-derived DNA from CRC patients. Several stool-based strategies involving digital PCR have been investigated to analyze relevant mutations for CRC management. However, none of these approaches has been further developed and subjected to clinical validation for stool DNA screening to date.

The advantages of ddPCR technology, together with instrumentation and protocols easily adoptable by any lab, support a potential translation of this approach to clinical scenarios. Our results show that KRAS G12D detection in stool-derived DNA from CRC patients by ddPCR is feasible and suggests this technology might be useful for the analysis of other molecular markers in stool. The authors hypothesized that ddPCR could be a reliable and sensitive method of analyzing KRAS mutations in stool-derived DNA, providing reproducible and accurate results.

This study proposed a new strategy based on detecting KRAS mutations in stool-derived DNA using a commercially available ddPCR platform. ddPCR is an emulsion-based amplification technology with fluorescently labelled probes. KRAS G12D mutation detection in stool-derived DNA by ddPCR is a fast, simple, and affordable approach which could be adapted to detect other clinically relevant molecular biomarkers for CRC management. This technique is more feasible for implementation into routine clinical practice than other previously described stool-based strategies.

ddPCR provided sensitive, accurate, and reproducible results for detection of the KRAS G12D mutation in stool-derived DNA from CRC patients, especially at early stages of the disease. In light of our results, it could be proposed that biomarker analysis by ddPCR in stool samples may complement current CRC screening methods; stool-derived nucleic acid testing by ddPCR offers an alternative to tissue genotyping and blood-based biomarker quantification, is a less invasive tool than the former and is likely more time-sensitive than the latter, especially at early stages, as tumor DNA will reasonably reach the fecal content more quickly than the bloodstream, at least during the initial phases of cancer development.

Research perspectives

KRAS mutations are analyzable by ddPCR in stool-derived DNA from CRC patients, including early-stage patients. This observation merits further studies aimed at evaluating and improving the efficiency of this approach prior to its clinical application. These results pave the way for ddPCR analysis of other molecular biomarkers of CRC in stool. Further studies involving larger cohorts of patients and samples collected at different time points throughout the progression of the disease should be performed in order to confirm the prognostic value and economic viability of this tool before implementation in clinical practice. A multiplex assay simultaneously covering all KRAS mutations relevant for anti-EGFR-therapy decision-making would maximize the benefits and optimize the cost-effectiveness of this approach. This strategy should be further investigated as a complementary screening test for early detection of CRC.