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International Perspective on the Burden of Colorectal Cancer and Public Health Effects

2019; Elsevier BV; Volume: 158; Issue: 2 Linguagem: Inglês

10.1053/j.gastro.2019.10.007

1528-0012

Linda Rabeneck, Han‐Mo Chiu, Carlo Senore,

Genetic factors in colorectal cancer

Han-Mo ChiuView Large Image Figure ViewerDownload Hi-res image Download (PPT)Carlo SenoreView Large Image Figure ViewerDownload Hi-res image Download (PPT) Colorectal cancer (CRC) is a global public health issue. In 2018, the International Agency for Research on Cancer (IARC) estimated that there were 1.8 million new cases and 881,000 deaths worldwide.1Bray F. Ferlay J. Soerjomataram I. et al.Global Cancer Statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA Cancer J Clin. 2018; 68: 394-424Crossref PubMed Scopus (59528) Google Scholar This global burden of disease varies across and within countries. In 2018, the countries with the highest colon cancer incidence rates were in Europe, Australia/New Zealand, North America, and East Asia. The geographic pattern of rectal cancer incidence rates was similar. Incidence rates for colon and rectal cancer were low in Africa and southern Asia.1Bray F. Ferlay J. Soerjomataram I. et al.Global Cancer Statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA Cancer J Clin. 2018; 68: 394-424Crossref PubMed Scopus (59528) Google Scholar Countries with the highest incidence rates tend to have lower case fatality rates than those with the lowest incidence rates.1Bray F. Ferlay J. Soerjomataram I. et al.Global Cancer Statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA Cancer J Clin. 2018; 68: 394-424Crossref PubMed Scopus (59528) Google Scholar In addition to geographic patterns, CRC incidence and CRC mortality are associated with socioeconomic status (SES). Within developed countries, CRC mortality is higher among those with low SES.2Manser C.N. Bauerfeind P. Impact of socioeconomic status on incidence, mortality, and survival of colorectal cancer patients: a systematic review.Gastrointest Endosc. 2014; 80: 42-60.e9Abstract Full Text Full Text PDF PubMed Scopus (64) Google Scholar CRC incidence rises in parallel with economic transition. The Human Development Index (HDI) is a composite index of life expectancy, education, and per capita income indicators that is used by the World Bank to rank countries into 4 categories. As countries progress from low to high HDI, CRC incidence rises (Figure 1). HDI does not capture the heterogeneity of disease burden that is seen within and across countries. For example, Figure 2C shows that although Japan and the United States are both in the very high HDI category, the patterns of CRC incidence and mortality differ (Figure 2A and B). These differences in CRC incidence are at least in part related to differences in the prevalence of risk factors (eg, diet), whether (and how long) screening programs have been in place, and the extent of program uptake. This rising burden of disease reflects the progressive "Westernization" of lifestyle, including increased red and processed meat consumption, sedentary living, and obesity. Three patterns in temporal trends in CRC incidence and mortality have been described.3Arnold M. Sierra M.S. Laversanne M. et al.Global patterns and trends in colorectal cancer incidence and mortality.Gut. 2017; 66: 683-691Crossref PubMed Scopus (3186) Google Scholar Rapidly transitioning countries, where economic growth was associated with a shift toward the adoption of unhealthy lifestyle habits, paralleled by an increase in the prevalence of overweight and obesity, have shown an increase in CRC incidence and in CRC mortality (eg, Baltic countries). A decline in CRC mortality, likely related to best practices in cancer diagnosis and treatment, accompanied by an increase in CRC incidence, and likely related to the recent introduction of screening and/or persisting unfavorable lifestyle patterns, was observed in some countries (eg, Canada and the United Kingdom). Decreases in CRC incidence and CRC mortality observed in other countries (eg, the United States and Japan) likely reflect the introduction of screening and changes in risk factor prevalence, together with best practices in cancer diagnosis and treatment. Most of the increase in CRC burden in the next 25 years is expected in less developed countries because of economic transition and the adoption of Western lifestyle patterns. Primary prevention, which focuses on interventions to change Westernized lifestyle behaviors, will be important to address the anticipated rise in CRC burden. A combined approach that encompasses primary prevention and CRC screening is needed. CRC screening is a major public health intervention that varies across jurisdictions. Determinants, facilitators, and barriers to participation occur at the policy, organization, provider, and patient levels.4International Agency for Research on CancerColorectal cancer screening. IARC handbooks of cancer prevention. 17. WHO Press, Geneva, Switzerland2019Google Scholar The health policy in a country is a key determinant of the approach to CRC screening. In countries that adopt a public health policy, cancer screening is publicly funded by a single-payer universal access insurance system. In these settings (eg, Canada, The Netherlands, United Kingdom, Australia, New Zealand, Italy, and Taiwan), cancer screening is delivered in an organized, population-based approach. Organized cancer screening, as defined by the IARC, includes (1) an explicit policy with specified age categories and methods and intervals for screening, (2) a defined target population, (3) a management team responsible for implementation, (4) a health care team for decisions and care, (5) a quality assurance structure, and (6) a method for identifying cancer occurrence in the population.5International Agency for Research on CancerCervix cancer screening. IARC handbooks of cancer prevention. 10. WHO Press, Geneva, Switzerland2005Google Scholar In contrast, opportunistic screening is done outside of an organized screening program, often delivered through fee-for-service reimbursement of physicians. Compared with opportunistic screening, organized screening focuses much greater attention on the quality of each step in the screening process, including follow-up of participants, and reports publicly on cancer screening program performance. Thus, a key advantage of organized screening is that it provides greater protection against the harms of screening, including overscreening, poor-quality and complications of screening, and poor follow-up of those with positive test results. Organized, population-based screening is clearly a major public health intervention that requires substantial public support and a funding commitment from government. In 1968, Wilson and Jungner6Wilson J.M.G. Jungner G. Principles and practice of screening for disease. World Health Organization, Geneva, Switzerland1968Google Scholar set forth 10 principles of screening. Recently, Dobrow et al conducted a systematic review of subsequent work on population-based screening decisions to examine how these principles have evolved.7Dobrow M.J. Hagens V. Chafe R. et al.Consolidated principles for screening based on a systematic review and consensus process.CMAJ. 2018; 190: E422-E429Crossref PubMed Scopus (160) Google Scholar This review showed a shift in screening principles with an increasing focus on infrastructure requirements and resource or system capacity. The authors identified 12 principles, 3 focused on the disease (eg, epidemiology, natural history), 3 focused on the screening test (eg, test characteristics), and 6 focused on the program/system (eg, infrastructure, benefits and harms, economic evaluation). The adoption of this broader set of principles when the decision is made to move forward with an organized population-based cancer screening program requires careful consideration of the long-term sustainability of available screening options as well as the need to ensure equity of access. Organized, population-based screening programs involve considerable initial up-front investment of public funds, with benefits accruing much later. However, given the rising costs of systemic treatment, CRC screening programs may show favorable cost-effectiveness over a relative short time frame.8Goede S.L. Rabeneck L. van Ballegooijen M. et al.Harms, benefits and costs of fecal immunochemical testing versus guaiac fecal occult blood testing for colorectal cancer screening.PLoS One. 2017; 12e0172864Crossref PubMed Scopus (32) Google Scholar In making the case for organized screening to governments and stakeholders, formal, rigorous economic evaluation is crucial. To design, plan, pilot, and implement an organized population-based CRC screening program takes at least a decade,9Von Karsa L. Lignini T.A. Patnick J. et al.The dimensions of the CRC problem.Best Pract Res Clin Gastroenterol. 2010; 24: 381-396Crossref PubMed Scopus (137) Google Scholar and it is even longer before the impact of the program can be assessed. In many countries, there is insufficient capacity in terms of health human resources (endoscopists, pathologists, surgeons, oncologists) and access to high-quality treatment. In such situations, building capacity in health infrastructure and resources is a needed first step. The World Health Organization recommends strengthening diagnostic and treatment capacity and quality first. Coupled with this is raising public awareness of the need to seek medical attention and diagnostic work-up in the event of large-bowel symptoms.10Guide to cancer early diagnosis. World Health Organization, Geneva, Switzerland2017Google Scholar Taken together, these aspects—raising awareness of the importance of large-bowel symptoms and making high-quality colonoscopy and treatment readily available—make up an early detection program. In essence, it does not make sense to attempt to implement CRC screening when the necessary capacities for diagnosis and treatment are not available. In the past 20 years, there has been remarkable progress globally in CRC screening efforts.11Young G.P. Rabeneck L. Winawer S.J. The global paradigm shift in screening for colorectal cancer.Gastroenterology. 2019; 156: 843-851Abstract Full Text Full Text PDF PubMed Scopus (59) Google Scholar In the United States, at the health policy level, insurance status is the most important determinant of CRC screening, and mostly the approach is with opportunistic colonoscopy. The best US example of organized CRC screening is in the Kaiser Permanente Northern California (KPNC) integrated health system. In that system, which serves approximately 4 million members, before 2006, CRC screening was opportunistic, predominantly using sigmoidoscopy and guaiac fecal occult blood test (gFOBT). Starting in 2007, screening transitioned to mailed fecal immunochemical test (FIT) outreach to individuals who were not up to date. Opportunistic colonoscopy was an option throughout. Thus, KPNC transitioned from opportunistic to organized CRC screening with the launch of the FIT.12Levin T.R. Corley D.A. Jensen C.D. et al.Effects of organized colorectal cancer screening on cancer incidence and mortality in a large community-based population.Gastroenterol. 2018; 155: 1383-1391Abstract Full Text Full Text PDF PubMed Scopus (287) Google Scholar In 2008, Ontario, which has a population of 14.4 million, was the first Canadian province to launch an organized, population-based CRC screening program,13Rabeneck L. Tinmouth J.M. Paszat L.F. et al.Ontario's ColonCancerCheck: Results from Canada's first province-wide colorectal cancer screening program.Cancer Epidemiol Biomarkers Prev. 2014; 23: 508-515Crossref PubMed Scopus (42) Google Scholar based on gFOBT for those 50–74 years at average risk and colonoscopy for those at increased risk, defined by a family history of 1 or more first-degree relatives with the disease. The program replaced the gFOBT with FIT in 2019. Six of the other 9 Canadian provinces have launched organized CRC screening programs, using FIT (in 5 provinces) or Hemoccult II Sensa (in 1 province). Three provinces and all 3 territories have yet to implement organized CRC screening programs. Uruguay has the highest CRC incidence among Latin American countries (CRC incidence, 35.0/100,000). In 1996, Uruguay began a FIT pilot, and in 2017 the transition to an organized, population-based program began. Several FIT pilots are underway in Latin America, including those in Brazil, Chile, and Argentina. In 2003, the European Union (EU) Council called for the introduction of evidence-based screening, adopting a population-based approach.14European Council L 327/34Council recommendation of 2 December 2003 on cancer screening (2003/878/EC). Official Journal of the European Union, 2003: 34-38Google Scholar The EU quality assurance guidelines15Segnan N. Patnick J. Von Karsa L. European guidelines for quality assurance in colorectal cancer screening report on the implementation of the council recommendation on cancer screening (first report). Publications Office of the European Union, Luxembourg2010Google Scholar concluded that there was limited evidence of the effectiveness of screening colonoscopy, reasonable evidence (based on the 1 randomized controlled trial published at the time) of the effectiveness of sigmoidoscopy (FS), and good evidence to support the adoption of FIT, which was recommended as the fecal test of choice for population-based programs. The EU Code Against Cancer16Armaroli P. Villain P. Suonio E. et al.European code against cancer. 4th edition: cancer screening.Cancer Epidemiol. 2015; 39: S139-S152Crossref PubMed Scopus (65) Google Scholar recommended starting screening by inviting people between ages 50 and 60 years and to continue sending invitations up to those aged 70–75 years. The EU guidelines17Anttila A. Lönnberg S. Ponti A. et al.Towards better implementation of cancer screening in Europe through improved monitoring and evaluation and greater engagement of cancer registries.Eur J Cancer. 2015; 51: 241-251Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar also provided evidence-based recommendations on the quality assurance of screening programs, defining key quality indicators covering the entire process, from delivery of screening to treatment and surveillance, and setting performance standards. International cooperative projects involving both EU member states17Anttila A. Lönnberg S. Ponti A. et al.Towards better implementation of cancer screening in Europe through improved monitoring and evaluation and greater engagement of cancer registries.Eur J Cancer. 2015; 51: 241-251Abstract Full Text Full Text PDF PubMed Scopus (49) Google Scholar and non-EU countries18Giordano L. Bisanti L. Salamina G. et al.Euromed Cancer working group. The EUROMED CANCER network: state-of-art of cancer screening programmes in non-EU Mediterranean countries.Eur J Public Health. 2016; 26: 83-89Crossref PubMed Scopus (22) Google Scholar focused on quality assurance initiatives, supporting national and international comparisons and benchmarking. By 2018, population-based programs with active invitation at regular intervals of the entire target population, identified through screening registries, had been established, or piloted, in 22 of 28 EU member states and in 7 of 19 non-EU countries, with 3 EU member states having approved plans for introducing a population-based program in the near future. Colonoscopy capacity influences screening program design. The majority of population-based programs have adopted or are planning to adopt biennial FIT,19Ponti A. Anttila A. Ronco G. Senore C. Against cancer. Cancer screening in the European Union. European Commission, Brussels, Belgium2017https://ec.europa.eu/health/sites/health/files/major_chronic_diseases/docs/2017_cancerscreening_2ndreportimplementation_en.pdfhttp://www.epaac.eu/screening-and-early-diagnosisDate accessed: November 15, 2017Google Scholar and about half of them are targeting older age groups, starting at age 55 or 60 years and stopping at age 69 or 74 years. The choices of the age range and the FIT positivity threshold are determined by the need to match local colonoscopy resources.19Ponti A. Anttila A. Ronco G. Senore C. Against cancer. Cancer screening in the European Union. European Commission, Brussels, Belgium2017https://ec.europa.eu/health/sites/health/files/major_chronic_diseases/docs/2017_cancerscreening_2ndreportimplementation_en.pdfhttp://www.epaac.eu/screening-and-early-diagnosisDate accessed: November 15, 2017Google Scholar Only Poland has implemented colonoscopy screening, offered once in the lifetime, within an organized program, and the Luxembourg and Swiss programs are offering a choice of colonoscopy or FIT. FS screening, offered once in the lifetime, has been adopted in 1 region in Italy (Piedmont), with FIT being offered as an alternative test for those refusing FS. In England, the Bowel Cancer Screening Program was launched in 2006, based on gFOBT. After the full rollout of the FIT program for those aged 50 to 74 years, FS will be maintained as an alternative option in England. Participation rates across countries in Europe show wide variation, reflecting differences in cultural and organizational backgrounds.19Ponti A. Anttila A. Ronco G. Senore C. Against cancer. Cancer screening in the European Union. European Commission, Brussels, Belgium2017https://ec.europa.eu/health/sites/health/files/major_chronic_diseases/docs/2017_cancerscreening_2ndreportimplementation_en.pdfhttp://www.epaac.eu/screening-and-early-diagnosisDate accessed: November 15, 2017Google Scholar,20Senore C. Basu P. Anttila A. et al.Performance of colorectal cancer screening in the European Union member states: data from the second European screening report.Gut. 2019; 68: 1232-1244Crossref PubMed Scopus (95) Google Scholar The Asia–Pacific region contributes the largest numbers of incident CRC cases (957,896, 51.8%) and CRC deaths (461,422, 52.4%) in the world.1Bray F. Ferlay J. Soerjomataram I. et al.Global Cancer Statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries.CA Cancer J Clin. 2018; 68: 394-424Crossref PubMed Scopus (59528) Google Scholar Currently there are 6 countries in the region, Australia, Japan, Korea, New Zealand, Singapore, and Taiwan, with nationwide screening programs funded (total or partial) by governments. Most programs provide screening starting at age 50 years except for Japan, which starts at age 40 years. Only Australia and Taiwan have an upper age limit (74 years). Owing to constraints in colonoscopy capacity or human health resources, all 6 programs use FIT as the initial screening test, with diagnostic colonoscopy offered to those with a positive FIT result. Consensus recommendations on CRC screening have been developed for the Asia–Pacific region.21Sung J.J. Ng S.C. Chan F.K.L. et al.An updated Asia Pacific Consensus Recommendations on colorectal cancer screening.Gut. 2015; 64: 121-132Crossref PubMed Scopus (338) Google Scholar Some pilot programs are ongoing in regions such as Hong Kong (phase II of a territory-wide full program, offering screening for those aged 56 to 75 years from January 2019)22Government of Hong Kong Special Administrative RegionDH to extend colorectal cancer screening programme on January 1.https://www.info.gov.hk/gia/general/201812/21/P2018122100294.htmGoogle Scholar and some areas in Thailand.23Sarakarn P. Promthet S. Vatanasapt P. et al.Preliminary results: colorectal cancer screening using fecal immunochemical test (FIT) in a Thai population aged 45-74 years: a population-based randomized controlled trial.Asian Pac J Cancer Prev. 2017; 18: 2883-2889PubMed Google Scholar In multiethnic countries such as Malaysia, where the risk of CRC is quite distinct among Chinese (highest), Malay, and Indian (lowest), it is difficult to obtain a consensus on implementing a nationwide screening program. The Asia–Pacific risk score, which uses common population demographics (age, sex) and factors (smoking, family history) as predictors of increased risk, has been validated and is effective in selecting persons at increased risk of advanced neoplasia, thereby reducing colonoscopy demand, and is useful in regions where population screening programs are not in place.24Chiu H.M. Ching J.Y. Wu K.C. et al.A risk-scoring system combined with a fecal immunochemical test is effective in screening high-risk subjects for early colonoscopy to detect advanced colorectal neoplasms.Gastroenterology. 2016; 150: 617-625Abstract Full Text Full Text PDF PubMed Scopus (76) Google Scholar A recent study from KPNC reported an increase in the proportion of individuals who were up to date with CRC screening associated with implementing organized FIT screening in the context of preexisting opportunistic colonoscopy in persons at average risk.12Levin T.R. Corley D.A. Jensen C.D. et al.Effects of organized colorectal cancer screening on cancer incidence and mortality in a large community-based population.Gastroenterol. 2018; 155: 1383-1391Abstract Full Text Full Text PDF PubMed Scopus (287) Google Scholar The increased participation was accompanied by a 25.5% reduction in CRC incidence and 52.4% reduction in CRC mortality. In Europe, preliminary reports of CRC incidence and CRC mortality after the introduction of population-based programs show a beneficial impact of screening on CRC burden at the population level. For example, in the Veneto region of Italy, biennial FIT screening was associated with a reduction in CRC mortality based on a comparison between early and late screening areas.25Zorzi M. Fedeli U. Schievano E. et al.Impact on colorectal cancer mortality of screening programmes based on the faecal immunochemical test.Gut. 2015; 64: 784-790Crossref PubMed Scopus (221) Google Scholar In the Asia–Pacific region, insufficient public awareness of CRC and CRC screening, with resultant low FIT screening participation and follow-up diagnostic colonoscopy rates, which may affect the effectiveness of screening, are major challenges. Further efforts to deal with these problems are needed. Nevertheless, in Taiwan, the effectiveness of FIT screening in reducing CRC mortality has been reported. In the initial 5 years of this program, FIT screening was associated with a 10% reduction in CRC mortality when comparing those who did and did not participate in screening.26Chiu H.M. Li-Sheng Chen S. Ming-Fang Yen A. et al.Effectiveness of fecal immunochemical testing in reducing colorectal cancer mortality from the one million Taiwanese Screening Program.Cancer. 2015; 121: 3221-3229Crossref PubMed Scopus (192) Google Scholar One of the challenges in CRC screening globally has been the lack of a standardized approach to program evaluation that would facilitate international comparisons and the identification of performance gaps. In 2019, IARC launched CanScreen5,27International Agency for Research on CancerCanScreen5.https://canscreen5.iarc.fr/index.phpDate accessed: December 30, 2019Google Scholar which is intended to fill this gap. CanScreen5 provides a platform for data collection and comparative evaluation of screening performance indicators around the world, following the experience of the EU screening report.19Ponti A. Anttila A. Ronco G. Senore C. Against cancer. Cancer screening in the European Union. European Commission, Brussels, Belgium2017https://ec.europa.eu/health/sites/health/files/major_chronic_diseases/docs/2017_cancerscreening_2ndreportimplementation_en.pdfhttp://www.epaac.eu/screening-and-early-diagnosisDate accessed: November 15, 2017Google Scholar All countries/regions should seriously consider contributing their data to CanScreen5, so we will have a much better understanding of where we stand. CRC is a major global public health problem, and the expected increase in the burden of disease related to economic transition may be associated with widening disparities among and within countries. The trends in the exposure to unhealthy habits and in the availability of and access to health care resources observed across countries in different HDI categories, and within countries by SES, could result in a widening gap in CRC mortality rates. CRC screening may mitigate these trends if effective policies are established to ensure sustainability over time and equity of access. Raising participation in hard-to-reach populations is a challenging but is a key accountability for those who lead CRC screening programs. In the United States, most CRC screening is opportunistic, with colonoscopy the dominant screening method for those at average risk. In many other countries, organized, population-based screening is being implemented, with FIT as the dominant screening method. Early results indicate a reduction in CRC mortality associated with the implementation of organized CRC screening. However, variability in the performance of population-based screening programs underscores the need to improve participation and strengthen the quality of all steps in the screening process.