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Introduction
In the 21st century, colorectal cancer (CRC) emerged as a global public health concern due to its rising incidence, closely linked to factors like increased life expectancy and risky lifestyles such as sedentary behavior, alcohol consumption, smoking, and high red meat intake1. About 95% of CRC cases stem from adenomatous polyps, prevalent in roughly 40% of individuals aged over 50, with a 5-18-year transformation period into malignancy, offering a window for secondary prevention programs1,2. However, in Latin America, particularly low- and middle-income countries (LMICs), CRC screening initiatives are scarce3. According to The Global Cancer Observatory (GLOBOCAN), CRC was the leading cause of cancer death in Mexico in 2022; yet, the country lacks an effective screening program4. As a result of the high burden of CRC in Mexico, some valuable CRC screening initiatives have been implemented by tertiary hospitals (National Cancer Institute and Instituto Nacional de Ciencias Médicas y Nutrición Salvador Zubirán)5 and national researchers in the last decade6,7. This review outlines prevalent CRC early detection tests and the current screening landscape in Mexico, alongside challenges and potential solutions applicable to similar contexts worldwide.
Materials and methods
The objective of this narrative review is to evaluate CRC screening strategies in LMICs and discuss the importance of implementing a nationwide screening program in Mexico. A search was conducted in different literature databases and official websites of international health research organizations. Regarding national and international CRC epidemiology, we extracted the latest data provided by the International Agency for Research on Cancer. Using the interactive platform provided by the Global Cancer Observatory, we compared incidence, age-standardized incidence rate, deaths, and age-standardized mortality rate regarding CRC across the six World Health Organization (WHO) regions. To assess the current recommendations concerning CRC screening for average-risk adults, we explored three updated guidelines published in the United States (American Cancer Society in 2018, US Preventive Task Force in 2021, and National Comprehensive Cancer Network in 2022). To evaluate the experiences of LMICs regarding CRC screening programs, we conducted a search between April and June 2023 in MEDLINE, Latin American and Caribbean Health Sciences Literature and Google Scholar. We conducted our search and selection of articles to be included according to the international Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines. We used the keywords "CRC screening", "low- and middle-income countries", "fecal occult blood test", "fecal immunochemical test (FIT)", and "results". We included original observational studies, written in English or Spanish, of CRC screening programs implemented in any LMIC (as defined by the World Bank in 2022) that assessed for, at least the participation rate, positivity rate, and sensitivity of the screening method used. We excluded studies that were written in any other language and those with full texts unavailable.
Results
CRC epidemiology worldwide
CRC is the third most common cancer worldwide, with nearly 2 million new cases annually, causing 935,000 deaths in 2020 (second leading cause of cancer-related deaths). Both incidence and mortality rates are significantly higher in men4,8. While the risk rises after age 50, there is been an uptick in incidence among younger individuals in the 21st century9,10. The "Westernization of lifestyle," particularly Western diets, has driven these trends11. The global burden of CRC is projected to increase by 60% by 2030 due to the transition from low-to-medium HDI nations (Table 1)2.
Tabla 1 Epidemiology of colorectal cancer by WHO regions
| WHO Region | New cases | Age-standardized incidence rate* | Deaths | Age-standardized mortality rate* | ||||||||
|---|---|---|---|---|---|---|---|---|---|---|---|---|
| Men | Women | Total | Men | Women | World | Men | Women | Total | Men | Women | World | |
| Western Pacific (WPRO) | 464 483 | 353 577 | 818 060 | 30.6 | 20.5 | 25.3 | 223 433 | 172 615 | 396 048 | 14.3 | 9.0 | 11.5 |
| Europe (EURO) | 300 443 | 254 126 | 554 569 | 36.0 | 23.3 | 28.8 | 141 801 | 121 513 | 263 314 | 15.6 | 9.3 | 12.0 |
| Americas (PAHO) | 162 356 | 153 162 | 315 518 | 23.3 | 18.5 | 20.7 | 69 081 | 64 341 | 133 422 | 9.4 | 7.0 | 8.1 |
| South-East Asia (SEARO) | 83 942 | 57 986 | 141 928 | 8.5 | 5.5 | 7.0 | 47 876 | 32 208 | 80 084 | 4.9 | 3.1 | 4.0 |
| Eastern Mediterranean (EMRO) | 28 269 | 22 134 | 50 403 | 10.2 | 7.9 | 9.0 | 15 702 | 12 273 | 27 975 | 5.8 | 4.5 | 5.1 |
| Africa (AFRO) | 26 243 | 24 453 | 50 696 | 9.5 | 7.5 | 8.4 | 17 634 | 16 498 | 34 132 | 6.7 | 5.2 | 5.8 |
Source: Compiled by the authors based on data from the Global Cancer Observatory, 2020.
*per 100,000 population.
CRC epidemiology in Mexico
In Mexico, CRC ranks third in cancer incidence and first in cancer mortality. According to the International Agency for Research on Cancer (IARC), in 2022, Mexico ranked second and third among Latin American and Caribbean countries in CRC incidence and mortality, respectively, with over 16,000 new cases and 8,200 deaths. Men aged 50 and older have the highest incidence (50.7/100,000) and mortality (27.0/100,000)1,4. In addition, there is been an increase in CRC cases among those under 5012. Various individual and environmental factors contribute to this rise. From 1998 to 2018, the age-adjusted mortality rate rose from 3.6 to 5.5/100,000, especially in men13. Sociocultural differences across regions impact disease burden, with higher mortality rates observed in urban areas, particularly in northern Mexico13, where behaviors such as processed meat consumption14, excessive alcohol use15, and obesity prevail16, all contributing to CRC risk17.
Screening tests for CRC
CRC screening utilizes various tests, each with distinct pros and cons, categorized as fecal blood detection, endoscopic examination, and radiographic visualization18. Only guaiac-based fecal occult blood test (gFOBT) and sigmoidoscopy have proven to reduce CRC incidence and mortality in clinical trials19. Among fecal blood tests, gFOBT and FIT are commonly used, with FIT offering higher sensitivity and consistency. FIT's advantages include requiring only one stool sample, no dietary restrictions, and higher patient participation rates20-25. Colonoscopy, though invasive, is the gold standard due to its sensitivity, but it's costly and requires preparation and sedation. Computed tomography colonography, minimally invasive, provides similar detection rates to colonoscopy but may uncover extracolonic findings with uncertain benefits (Table 2)26,27.
Table 2 Characteristics of the tests currently used for colorectal cancer screening
| Screening tests | Recommended interval17-19 | Sensibility (%)24 | Specificity (%)24 | CRC deaths averteda,18 | Strengths | Limitations |
|---|---|---|---|---|---|---|
| Fecal blood detection | ||||||
| High-sensitivity gFOBT | Annual | 61.5-79.4 | 92.5 | 23 | At-home test Relatively low cost Available within the National Health System No bowel preparation or sedation required | Diet and medication restrictions Multiple samples required False-positive rate higher than other tests (FIT) |
| FITb | Annual | 62.3-83.3 | 96.4 | 25 | At-home test No diet and medication restrictions Single stool sample No bowel preparation or sedation required | Not widely available within the National Health System Health personnel are unaware of the utility of the test |
| Mt-sDNA | Every 1-3 years | 84.0-97.0 | 89.8 | 24-27 | At-home test No bowel preparation or sedation required | Insufficient evidence of performance False-positive rate higher than other tests (FIT) More expensive than other stool-based tests |
| Endoscopic examination | ||||||
| Colonoscopy | Every 10 years | 93.1-99.5 | 86 | 27 | Gold standard Combined screening and treatment procedure | Bowel preparation and sedation required Specialized personnel required Risk of perforation and hemorrhage Most expensive test |
| Flexible sigmoidoscopyc | Every 5 years | 93.1-99.5 | 87 | 23 | No sedation or hospitalization needed | Examination of the proximal colon is excluded Uncomfortable and painful |
| Radiographic visualization | ||||||
| Computed tomography colonography | Every 5 years | 75.6-92.4 | 88 | 26 | Extracolonic findings (it is unclear if this represents a benefit for patients) | Radiation exposure Bowel preparation required |
aPer 1000 people screened
bCut-off point at 100 ng/mL
cTaking the depth of insertion as reference (distal colon); CRC: colorectal cancer; gFOBT: guaiac-based fecal occult blood test; FIT: fecal immunochemical test; MT-sDNA: multitarget stool DNA.
Mexican health system
The Mexican health system is characterized by fragmentation between public and private sectors, including multiple social security institutions and programs catering to the uninsured28. This fragmentation compromises service quality and continuity of care for non-communicable diseases like cancer. Persistent differences among health institutions in prevention, diagnosis, and treatment processes contribute to inequities in early detection and survival rates for cancer patients.
In recent years, significant reforms have reshaped the Mexican health system. Notably, the dissolution of Seguro Popular and the establishment of INSABI in 2020 aimed to provide free health services and medication to the uninsured29,30. However, these responsibilities have now shifted to IMSS-BIENESTAR31.
The introduction of the MAS-BIENESTAR model, rooted in Primary Health Care principles, marks another significant development. Among its five intervention axes, the emphasis on disease prevention stands out, focusing on specific protection and early detection. While the model acknowledges the importance of early cancer screening, its current focus is primarily on cervical, breast, and prostate cancer32, potentially overlooking other cancer types.
CRC screening in Mexico
The Specific Action Program for Cancer Prevention and Control 2021-2024 aims to boost nationwide early cancer detection. However, its focus primarily on cervical, breast, and childhood cancer sidelines CRC33. While validated CRC screening tests are recognized, proposed actions prioritize other cancers. Institutional support, notably the National Cancer Institute's free CRC screening program since 2017, has been pivotal. This program offers FIT screening to individuals aged 45-76 years, with participation rates reaching 91.0% and colonoscopy completion rates among positive tests at 77.7%5,6. However, opportunistic CRC screening prevails in Mexico, with patients actively seeking available tests. The Mexican clinical practice guideline for CRC screening, last updated in 2009, recommends fecal occult blood testing (gFOBT or FIT) for low-risk individuals34. However, national comparative studies between these tests are lacking. Studies have indicated FIT's efficacy, with positive predictive values, especially with a cut-off point of 100 ng/mL, showing higher accuracy7,35.
CRC screening in regions with similar contexts to Mexico
In LMIC, implementing population-based CRC screening programs faces challenges, but recent evidence suggests feasibility and cost-effectiveness. Nearly all European Union member states have CRC screening programs, with Bulgaria and Romania being exceptions. Pilot studies in these nations using FIT showed varying participation rates and CRC detection rates36-38. Other LMICs in Europe, like Serbia, have seen success with organized CRC screening programs, boasting high participation rates and FIT's positive predictive value39.
In Southeast Asia, low participation rates in screening programs hinder efforts to reduce CRC mortality40. Malaysia and Thailand lack formal national strategies but have conducted local pilot screening programs using FIT, reporting moderate to high participation rates, especially among women and rural residents, with CRC detection rates up to 0.3%41-43.
A study in Thailand assessed the cost-effectiveness of CRC screening tests, finding that annual FIT screening could prevent a significant percentage of CRC cases compared to colonoscopy, which is significantly more expensive44. In Sub-Saharan Africa, evidence on population-level CRC screening is limited, but a study in Nigeria showed high FIT participation rates, particularly among older individuals and those with higher socioeconomic status45,46. In Latin America, Chile has a well-established national program for early CRC detection, but its high-income status presents challenges for replication across the region's diverse socioeconomic contexts (Table 3).
Tabla 3 Experiences of other low-and middle-income countries with colorectal cancer screening programs
| Authors | Location and study period | Target population | Screening test | Participation rate (%) | Positivity rate (%) | Follow-up with colonoscopy after a positive result (%) | CRC cases per 1000 people screened |
|---|---|---|---|---|---|---|---|
| Bărbulescu et al.36 | Romania Oct 2019- Sep 2022 | Patients over 18 years registered with the practice in charge of the screening | gFOBT FIT | 52.8 | 15.8 | 50.0 | 0.0 |
| Tsvetanova Dimova et al.38 | Bulgaria 2013 | Average-risk asymptomatic individuals, aged ≥ 45 years | FIT | 78.8 | 8.5 | 75.0 | 6 |
| Banković-Lazarević et al.39 | Serbia 2013-2014 | Individuals aged between 50 and 74 years | FIT | 62.5 | 5.9 | 42.1 | 2.1 |
| Abu Hassan et al.41 | Kedah, Malaysia 2013 | Asymptomatic participants aged ≥ 50 years, not on anticoagulant therapy | FIT | 94.7 | 9.6 | 68.1 | 1.3 |
| Khuhaprema et al.42 | Lampang, Thailand Apr 2011-Nov 2012 | Individuals aged 50 to 65 years, with no personal history of colorectal cancer | FIT | 62.9 | 1.1 | 71.8 | 0.3 |
| Abdullah et al.43 | Selangor, Kuala LumpurMalaysia Jul 2017-Jan 2019 | Participants of The Malaysian Cohort study recruited between 2006 and 2012 | FIT | 79.6 | 13.1 | 52.7 | 3.0 |
| Alatise et al.45 | Osun, Kwara, Lagos, Nigeria Jan-Apr 2021 | Average-risk asymptomatic individuals, aged 45-75 years | FIT | 90.5 | 20.5 | 66.0 | 1.4 |
CRC: colorectal cancer; gFOBT: guaiac-based fecal occult blood test; FIT: fecal immunochemical test.
Discussion
The implementation of population-based CRC screening programs remains a pending issue in most Latin American countries, including Mexico. While the burden of CRC has historically been higher in high-income countries, they have reduced CRC mortality in recent years through several early detection strategies9. Both financial and human resources are determining factors for the creation and development of cancer prevention programs. Unfortunately, such resources are usually limited in LMIC.
Despite being one of the most commonly diagnosed cancers every year, there are no official figures on health-care costs associated with CRC in Mexico. This lack of knowledge hampers the estimation of potential savings that the system could achieve if a national program for CRC early detection were implemented. Based on reports from other countries, CRC screening is cost-effective regardless of the test used47.
The presence of multiple risk factors for CRC among a significant percentage of the Mexican population warrants a transition from opportunistic screening to an organized approach. According to the IARC, organized screening programs should have six key characteristics: an explicit policy with specified age ranges, methods, and intervals; a defined target population; a team responsible for implementation; a health team for decisions and care; a quality-assurance infrastructure; and a method for identifying cancer occurrence in the target population48.
In addition, although clinical practice guidelines serve as valuable tools for health-care providers' decision-making, their usefulness diminishes when not regularly updated. Recent evidence has shown the effectiveness of population-based FIT in reducing CRC mortality; thus, it is appropriate to recommend it with greater emphasis, even prioritizing it over gFOBT. On the other hand, it is necessary to incorporate tools that facilitate the prediction of CRC in asymptomatic populations through risk stratification. In Asia, for example, the Asia-Pacific Colorectal Screening (APCS) score effectively identifies Asian populations at high risk for advanced colorectal neoplasia49. Local studies are required to test the validity of similar scores in the Mexican population.
Health education is another core element that should be integrated into any prevention strategy. Mexican studies have indicated a significant proportion of the population rejecting stool blood tests (specifically FIT) due to disinterest, low-risk perception, and fear, among other factors50. Similar findings have been reported in other LMICs, highlighting the inadequate training of primary health personnel on topics related to CRC51.
Conclusions
Given the prevalent epidemiological and sociocultural context in Mexico, it is imperative to consider the development and implementation of a national CRC screening program. Specifically, evidence from high-income countries indicates that the widespread use of tests such as FIT contributes to reducing CRC mortality. Moreover, experiences in other LMICs, along with cost-effectiveness analyses, suggest that the development of such strategies is feasible and can be adequately accepted by the population. However, the reconstruction of the country's health system raises more questions than answers and health priorities seem to be not entirely clear. It is crucial to redirect attention toward diseases with increasing morbidity and mortality rates, which also impose a considerable economic burden on the health system. Unlike other types of cancer, CRC presents a unique opportunity for early detection and subsequent treatment. Considering these factors, genuine political commitment from health authorities could be the missing piece to improve the current status of CRC in Mexico.
