Published online Dec 14, 2024. doi: 10.3748/wjg.v30.i46.4950
Revised: October 14, 2024
Accepted: November 1, 2024
Published online: December 14, 2024
Processing time: 121 Days and 21 Hours
The feasibility of population screening for colorectal cancer has been demon
Core Tip: Despite the significant benefits of colorectal cancer (CRC) screening, current approaches need improvement. Here, we focus on molecular genetic techniques that may be useful in CRC screening. Their improvement and implementation are promising, on the one hand, due to their non-invasive nature, which enhances patient adherence to screening, and on the other hand, due to the personalization of screening programs based on an assessment of the individual risk of developing CRC.
- Citation: Emelyanova MA, Ikonnikova AY. Utilization of molecular genetic approaches for colorectal cancer screening. World J Gastroenterol 2024; 30(46): 4950-4957
- URL: https://www.wjgnet.com/1007-9327/full/v30/i46/4950.htm
- DOI: https://dx.doi.org/10.3748/wjg.v30.i46.4950
Although colorectal cancer (CRC) mortality has significantly decreased in recent decades due to screening and early detection, CRC remains the third leading cause of cancer-related death in the Western world[1,2]. Medical societies strongly recommend CRC screening in healthy adults aged 45 to 75; however, the adoption of this screening is below 50% in most countries[3-5]. In the editorial by Metaxas et al[6] the authors emphasized that improving adherence rates requires implementing awareness strategies and shifting from conventional endoscopy to non-invasive techniques as first-line screening. Currently, the most common screening strategies can be divided into two categories: stool tests and structural examinations. The former includes fecal occult blood tests, specifically guaiac-based fecal occult blood test, fecal immunochemical tests (FIT), and multi-target stool DNA test, while the latter encompasses colonoscopy and sigmoidoscopy[7]. The various CRC screening tests differ in terms of accuracy, risk of complications, cultural acceptance, and cost. However, adherence to these tests remains moderate due to the necessity for stool manipulation or the invasive nature of the procedure. In an observational survey, patients expressed a strong preference for non-invasive testing, with 83% indicating a preference for a blood-based test over a stool-based test[8]. Consequently, the development of non-invasive, more accessible and convenient screening tests and the selection of patients for more thorough cancer screening represent unmet clinical needs.
Although FIT is available worldwide, its sensitivity is relatively low, especially for early-stage CRC (73% for stage I and 79%-82% for stages II-IV) and advanced precancerous lesions (advanced adenomas or sessile serrated polyps, 24%)[9,10]. This limitation has led to the development of other stool-based tests that utilize specific molecular biomarkers, including genetic mutations, abnormally methylated DNA loci, and microRNAs, to improve the detection of CRC and precancerous lesions[11].
Epigenetic alterations play a crucial role in the development of CRC. Frequent aberrant DNA methylation is known to occur in certain genes during the early stages of CRC development. Several DNA methylation biomarkers have demonstrated high accuracy and reproducibility in detecting CRC[12]. For instance, BMP3 and NDRG4 are candidate tumor suppressor genes whose expression is often reduced or absent in CRC due to promoter methylation[13,14]. Activating mutations in the KRAS, which encodes a small GTPase, are also common in the early stages of CRC development[15]. So, the first multi-target stool DNA test, Cologuard (Exact Sciences Corporation, Marlborough, MA, United States), combines an immunochemical assay for human hemoglobin with the analysis of KRAS mutations, methylation of the NDRG4 and BMP3, and β-actin (a reference gene that reflects the amount of human DNA in stool). The multi-target stool DNA test exhibited a sensitivity of 92% for detecting CRC and 42% for detecting advanced precancerous lesions. The specificities for the multi-target stool DNA test and FIT were 89.8% and 96.4% respectively for participants with negative colonoscopy results. The multi-target stool DNA test detected significantly more CRCs in asymptomatic patients at average cancer risk than FIT, although it produced more false positives[10]. The multi-target stool DNA test was approved by the United States Food and Drug Administration (FDA) in 2014 as an option for stool-based CRC screening[16]. Critical limitations of this test include a much higher cost compared with FIT and a much lower sensitivity for detecting advanced adenomas compared with colonoscopy[17,18].
The CpG sites in the syndecan-2 gene (SDC2) are aberrantly methylated in the tumor tissues of most CRC patients. The integral membrane protein SDC2 is involved in cell proliferation, migration, and cell-matrix interactions[19]. Positive methylation of the SDC2 gene was detected in 100% of primary tumors, 90.6% of adenomatous polyps, 94.1% of hyperplastic polyps, and 0% of normal tissues[20]. Therefore, the stool DNA-based test EarlyTect®-C (Genomictree Inc., Daejeon, Korea) was developed to detect methylation of SDC2 using quantitative methylation-specific real-time polymerase chain reaction (PCR). The sensitivity of this test ranged from 83% to 86% for detecting stage I CRC and was 91% for detecting stage II CRC. The overall sensitivity was 90% for detecting CRC and 33% for detecting small polyps, with a specificity of 91%[20,21]. In 2018, it was approved by the Ministry of Food and Drug Safety of Korea for the early detection of CRC.
RNA markers can also be utilized for CRC screening. The multi-target stool-based RNA-FIT assay, ColoSense (Geneoscopy, Inc., St. Louis, MO, United States), is designed for the qualitative detection of colorectal neoplasia-associated RNA markers and of occult hemoglobin in human stool. The FDA approved ColoSense in 2024[22]. This decision was supported by data from the phase 3 CRC-PREVENT trial (NCT04739722), in which ColoSense demonstrated a sensitivity of 94% for detecting CRC and identified 100% of stage I CRC. Additionally, ColoSense detected advanced adenomas with 45.9% sensitivity and showed a specificity of 87.9% for no lesions on colonoscopy[23].
Despite the development of new stool-based tests, FIT remains the most widely used non-invasive CRC screening method due to its low cost[24,25]. Unfortunately, this test has only moderate sensitivity for detecting early stages of CRC and precancerous lesions. The development and introduction of new tests that combine FIT with the analysis of other genetic and epigenetic markers, such as somatic mutations, methylation, or RNA markers, can increase the sensitivity of the tests, but it may also significantly raise testing costs. The use of new stool-based tests does not fully solve the issue of inadequate population adherence to screening, as the need for stool manipulation remains. Thus, the development of blood-based tests for CRC screening appears more promising.
In recent years, liquid biopsy, which involves the use of circulating tumor molecules isolated from blood, has gained popularity in routine clinical practice. While it was initially intended for analyzing driver mutations in tumors, more studies are now exploring its potential for residual disease monitoring or cancer screening[26]. The sensitivity of liquid biopsy-based assays for detecting circulating tumor DNA (ctDNA) in blood is critical for their utilization in cancer screening. Somatic mutations specific to tumors can be detected by genotyping ctDNA, but the analysis may be limited due to the small amount of DNA shed by early-stage CRC or precancerous lesions. Several strategies, including the analysis of CRC-specific DNA methylation markers, fragmentomics, or proteomics, are being employed to improve the sensitivity of liquid biopsy-based assays for CRC screening[27].
Similar to stool-based tests, there are blood-based tests that evaluate aberrant methylation in ctDNA. The most sensitive single biomarkers for polyps and stage I/II CRC include MYO1-G, SEPT9, SDC2, and JAM3[28]. For example, the Epi proColon (Epigenomics AG, Berlin, Germany) and ColoVantage (Quest Diagnostics, Secaucus, NJ, United States) tests aim to detect methylation at the promoter region of the SEPT9[29,30]. These tests were developed based on the observation that detecting aberrant methylation of the SEPT9 reflects the presence of CRC[31]. SEPT9 is a filament-forming cytoskeletal GTPase involved in many important cellular functions, including cytokinesis, vesicle trafficking, polarization, deoxyribonucleic acid repair, membrane remodeling, cell migration, and apoptosis[32]. The Epi proColon 2.0 test had a sensitivity and specificity of 74.8% and 87.4% respectively for CRC detection. Positive SEPT9 methylation was detected in 66.7% of stage I, 82.6% of stage II, 84.1% of stage III, and 100% of stage IV CRCs. The sensitivity of SEPT9 for advanced adenomas was 27.4%. The Epi proColon 2.0 test was approved by the FDA in 2016 for CRC screening in individuals who have declined first-line screening tests[33]. However, some studies have shown its inconsistent sensitivity for detecting CRC and advanced adenomas, making its use in screening controversial[31,34].
The analysis of circulating cell-free DNA (cfDNA) from non-tumor cells, in addition to ctDNA, and the study of changes that early-stage cancer can cause in the blood provide additional avenues for cancer detection. Interactions between cancer cells and other cells, including fibroblasts, platelets, and immune cells, particularly in the tumor microenvironment, may be reflected in changes in the expression of genes that regulate interactions with tumor cells[35] and in changes in apoptosis patterns of immune cells[36]. Such changes in cell populations can be detected through cfDNA analysis, as cfDNA fragmentation and methylation patterns can recapitulate expected cellular epigenetic states[37-41]. This multi-omics approach to CRC screening has been implemented by Freenome Holdings Inc. (South San Francisco, CA, United States). They used machine learning to discover signatures in cfDNA that potentially reflect both tumor and non-tumor contributions. The authors reported a mean sensitivity of 85% and a specificity of 85% in a CRC cohort heavily weighted toward early-stage cancers (80% stage I/II)[35]. This test achieved 41% sensitivity and 90% specificity for colorectal advanced adenomas[42]. This method is currently being evaluated in the PREEMPT CRC trial (NCT04369053)[43].
Another blood-based test for CRC screening is the LUNAR-2 test (Guardant Health, Palo Alto, CA, United States). It is a multimodal single-sample next-generation sequencing test that incorporates ctDNA assessment of somatic mutations, tumor-derived methylation, and fragmentomic patterns, aimed at maximizing sensitivity for early-stage CRC detection. The sensitivity of the LUNAR-2 test was 88% for stages I and II and 93% for stage III, with a specificity of 94% in a case-control study of 434 South Korea patients with CRC[44]. This test is currently being evaluated in the ECLIPSE trial (NCT04136002)[45]. A refined version of the LUNAR-2 test, which includes integrated proteomic analysis besides genomic and epigenomic analysis, was tested by Bessa et al[27]. In this analysis, several protein markers with differential expression levels between cancer and normal tissues were selected for plasma-based evaluation. The results of the levels of these protein markers were integrated with the genomic and epigenomic classifiers. In the primary analysis, the sensitivity of CRC detection was 84% for stage I, 94% for stage II, and 96% for stage III with a specificity of 90%. The sensitivity for detecting advanced precancerous lesions was 23%[27].
Although blood-based tests are not yet superior to stool-based tests in terms of sensitivity and specificity, they address the convenience and accessibility limitations that prevent people from participating in current screening strategies. We believe that blood-based tests represent the most promising direction for developing tools to improve CRC screening.
The main challenges of molecular genetic screening tests include insufficient effectiveness, particularly in detecting precancerous lesions, as well as high costs and the need for laboratory equipment and highly qualified personnel. Compared with FIT, the most widely used minimally invasive test, other aforementioned stool-based tests (Multi-target Stool DNA Test, EarlyTect®-C, ColoSense) and blood-based tests (Freenome Blood Test, LUNAR-2 test) exhibit higher sensitivity for CRC detection, but all have lower specificity than FIT. Although most of these tests also outperform FIT in terms of sensitivity for detecting precancerous lesions, it remains low and does not exceed 45.9%. Therefore, increasing sensitivity for detecting precancerous conditions is a key direction for the further development of minimally invasive diagnostic tests.
There are several promising strategies to enhance the efficacy of molecular genetic testing. One approach is to combine several markers, which can be of the same or different types. For instance, the multi-target stool DNA test, which combines FIT with the analysis of KRAS mutation, NDRG4 and BMP3 methylation, and the evaluation of human DNA amount in stool by quantitative analysis of β-actin, significantly outperforms FIT alone in diagnostic properties[10]. The combination of markers of the same type can also improve diagnostic test performance. For example, recent study of plasma methylation markers demonstrated that the GALNT9/UPF3A combination discriminated advanced neoplasia with 78.8% sensitivity and 100% specificity, outperforming FIT and blood tests for methylated SEPT9[46]. A multilocus blood-based assay, ColonAiQ (qPCR test, six CRC methylation markers, Singlera Genomics Inc., La Jolla, CA, United States), also showed superior performance compared with these tests[47]. Multi-omics approaches, which have been actively developed in recent decades, hold great potential to improve the accuracy of CRC screening tests[48], but they remain considerably expensive for routine use and require clinical validation before implementation.
Another way to improve the efficiency of diagnostic tests is through the discovery of new powerful markers. Success in developing new minimally invasive approaches is directly related to basic research in carcinogenesis[49]. Understanding the mechanisms underlying tumor initiation and progression, molecular changes that occur in tumors and their microenvironments, and how tumors and precancerous lesions differ from normal tissues is essential for the further development of molecular genetic tests for CRC diagnostics. To this end, bioinformatics-based approaches have proven to be the most powerful and productive, as they can identify new biomarkers that advance our understanding of cancer mechanisms and can be used for diagnosis and treatment. In some cases, deep bioinformatics analysis using databases such as The Cancer Genome Atlas can identify relevant genetic biomarkers of CRC and their combinations. For example, in the study by Li et al[50], marker selection was performed based on bioinformatics and machine learning using The Cancer Genome Atlas database, followed by validation on a clinical cohort. As a result, a real-time multiplex PCR-based test for assessing hypermethylation of SEPT9, AXL4, and SDC2 were developed, showing 82.7% sensitivity for detecting CRC with 90.1% specificity and achieving 55% specificity for precancerous lesions, outperforming many other tests[50]. Bioinformatics approaches have been successfully used to identify markers in a wide range of oncology studies[51-53], including for early detection of CRC[54]. With the emergence of convenient bioinformatics tools for cancer genetic analysis, such as GEPIA[55], UALCAN[56], and GSCALite[57], this area is becoming more accessible to a broader range of researchers. As bioinformatics analysis methods improve and evolve, they are expected to impact the development of diagnostic tests for CRC.
Another significant barrier to the implementation of molecular genetic tests in clinical practice is their high cost and the need for laboratory equipment and highly qualified personnel. Currently, molecular genetic approaches are primarily implemented in large clinical centers with the necessary technical infrastructure. However, over time, these approaches are likely to become more accessible to smaller healthcare organizations. Even now, the different approaches underlying various tests can vary significantly in price. For example, PCR-based tests are already available for widespread use[20,21,47,50]. Laboratories can be equipped in stages, and with an established structure for inexpensive tests, it will be easier in the future to transition to more powerful multi-omics accurate tests, which, if trends continue, will become more cost-effective, sensitive, and more widespread over time.
Besides the aforementioned molecular genetic approaches that are used directly in the analysis of clinical specimens in CRC screening, there are other genetic approaches aimed at identifying individuals who may benefit from more frequent and thorough screening. First and foremost, these include individuals with a family history of CRC. Approximately 5% of people who develop CRC have family cancer syndromes (Lynch syndrome, familial adenomatous polyposis, and other rarer syndromes)[58]. Ideally, patients with a family history of CRC should be tested to determine whether they are carriers of genetic alterations and, if so, should undergo regular colonoscopy screening. In practice, many patients are apprehensive about genetic testing or do not understand its necessity, highlighting the need to increase awareness among patients and their relatives.
Another promising approach for selecting patients for more thorough screening is the assessment of polygenic risk scores (PRS) for CRC. The primary goal of using PRS is to identify individuals at high risk of CRC who may benefit most from intensive screening interventions, while those at low risk may avoid unnecessary procedures, ultimately leading to more targeted prevention and early detection of CRC. PRS is a value calculated by summarizing the individual effects of many single nucleotide variants in the genome, each of which has a small effect, but whose multiplicative effect is significantly associated with disease risk. PRS models, where each single nucleotide variant is assigned a risk coefficient, were created using data from genome-wide association analyses conducted on large cohorts of patients and healthy individuals. For CRC, PRS models include from 12 to over a million genetic variants[59].
In a large study of a European population, individuals with high PRS had a significantly increased risk of CRC, with a hazard ratio of 2.54 (95% confidence interval: 2.20-2.95) for the top decile and an hazard ratio of 2.68 (95% confidence interval: 1.82-3.96) for the top percentile[60]. The authors obtained an area under the curve of 0.629 to 0.654 for predicting the incidence of CRC based on PRS. However, predictive models become much more informative when other risk factors, such as family history, lifestyle, and environmental factors are included, and the combined estimates are superior in accuracy to PRS and non-genetic factors considered separately[61,62]. At the same time, Briggs et al[63] question the rationale for using PRS, as their study found that PRS only modestly improved risk prediction compared with clinical factors alone, while collecting the latter does not incur financial costs, unlike expensive genetic testing. Thus, the benefits of introducing genetic testing must be critically assessed in terms of both clinical utility and economic feasibility, thus requiring further prospective studies.
Identifying groups of individuals at high risk of CRC appears useful for individualizing screening and prevention programs. According to Zhang et al[64], screening significantly reduced morbidity and mortality from CRC in medium and high-risk groups based on PRS and non-genetic factors (approximately 60% of the study population), while it did not improve these indicators in the low-risk group. Hu et al[65] found that PRS-based prediction was more accurate for patients with early-onset CRC, whereas models using only clinical risk factors were more appropriate for patients with late-onset disease. Thus, PRS may be informative in identifying patients who would benefit from earlier screening. A notable example is the model developed by Jeon et al[66] that combines PRS and non-genetic factors to estimate the 10-year absolute risk of CRC and determine an individual recommended age for starting screening, differing by more than 10 years for individuals at low and high risk. Of course, this approach requires further prospective studies to assess its ability to improve early detection of CRC and its possible impact on population compliance with screening. Knowledge of risk levels can also motivate patients to address modifiable risk factors, particularly those related to lifestyle. For instance, excess weight and PRS have been associated with an increased risk of CRC in a multiplicative manner[67]. Thus, the overall risk can be reduced by adjusting modifiable factors. Patients with a high PRS have also been shown to benefit more from adherence to a healthy lifestyle[61].
Molecular genetic approaches hold great promise for improving existing screening strategies. Although not all of them currently possess sufficient diagnostic characteristics, new data on the mechanisms of carcinogenesis are emerging, forming the basis for developing modern diagnostic methods. This direction will undoubtedly continue to evolve. We are confident that the integration of molecular genetic approaches with traditional screening methods will significantly enhance the rate of early detection of CRC and make participation in screening programs more convenient for patients.
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