Abstract
It is often reported that participation in the German colorectal cancer (CRC) screening program is low. However, it must be considered that fecal occult blood testing (FOBT) and colonoscopy are offered in parallel and both are also used for diagnostic purposes. We aimed to quantify and characterize the uptake of these colorectal examinations in Germany. Using the claims database German Pharmacoepidemiological Research Database (~20% of the German population), we included persons aged 50 in 2011 in cohort 1 (cohort 2: age 55) and assessed whether they utilized FOBT or colonoscopy for screening or diagnostic purposes until age 59 (cohort 2: age 64). We have stratified the analyses, i.e. by gender and educational level. Among 185 949 50-year olds, 80% of women and 63% of men had ≥1 colorectal examination (i.e. FOBT or colonoscopy) until age 59; 25% of women and 31% of men had ≥1 colonoscopy (among those, 76 and 62% had a screening colonoscopy). In women with lower vs higher education, 79 vs 82% had any colorectal examination; in men, these proportions were 60 vs 67%. Among 156 258 55-year olds, 78% of women and 69% of men had ≥1 colorectal examination until age 64. Our study demonstrates a high utilization of colorectal examinations in Germany. It also illustrates the value of health claims data to monitor CRC screening in Germany due to their longitudinal character and because they include information on screening, on examinations done for diagnostic reasons as well as information suitable to characterize users and nonusers.
Keywords: colonoscopy, colorectal cancer, diagnostic, fecal occult blood test, Germany, screening, utilization
Introduction
In Germany, ~55 000 persons were diagnosed with colorectal cancer (CRC) and ~24 000 died from the disease in 2020 (Robert-Koch Institut und die Gesellschaft der epidemiologischen Krebsregister in Deutschland e.V., 2023). During the past two decades, CRC incidence has declined by more than 20% and CRC mortality by more than 30% (Cardoso et al., 2021). Germany has one of the longest-standing CRC screening offers in Europe; the guaiac-based fecal occult blood test (FOBT) was already reimbursable in the 70s (IARC, 2019). Since 2002, the guaiac-based FOBT has been offered annually from age 50 to 54 and biennially from age 55 onwards. In 2017, the guaiac-based FOBT was replaced by the immunochemical FOBT (fecal immunochemical test for hemoglobin). There is no standard FOBT in Germany; it has to be quantitative and the minimum sensitivity and specificity for the detection of advanced neoplasia is specified, but there are no instructions for sampling, that is, it is up to the manufacturer to specify this. In addition to FOBT, screening colonoscopy was introduced in 2002 for all persons aged 55 or older; specifically, two screening colonoscopies with an interval of 10 years are reimbursable (Haug, 2018); in 2019, the starting age for screening colonoscopy was lowered to 50 years for men (Gemeinsamer Bundesausschuss, 2023). Furthermore, elements of an organized CRC screening program were introduced in 2019 such as information letters which are sent to all persons aged 50, 55, 60, and 65 years (Gemeinsamer Bundesausschuss, 2023).
It is often reported that participation in the German CRC screening program is low (Brenner et al., 2010; Altenhofen, 2016; Kretschmann et al., 2019). However, it has to be considered that there are two parallel screening offers with different screening intervals. In addition, colonoscopy and FOBT are also used as examinations for other purposes such as symptom assessment, which can also exert a CRC-preventive effect. A comprehensive description of the utilization of colorectal examination, ideally accompanied by a characterization of those with and without such examinations, is important for interpreting trends in CRC incidence and mortality. Existing studies on the utilization of CRC screening in Germany, however, only covered parts of these aspects (Altenhofen et al., 2010; Stock and Brenner, 2010; Stock et al., 2011; Altenhofen, 2016; Starker et al., 2017; Guo et al., 2019; Kretschmann et al., 2019; Cardoso et al., 2020; Steffen et al., 2020; Grobe and Szecsenyi, 2021; Pardey et al., 2021; Prütz and Rommel, 2021; Tillmanns et al., 2022).
To fill this gap, we aimed to systematically assess the proportion of persons utilizing colorectal examination from age 50 onwards and characterize users and nonusers based on longitudinal data from a large German healthcare database.
Methods
Data source
This study was conducted using the German Pharmacoepidemiological Research Database (GePaRD) (Haug and Schink, 2021) which is based on claims data from four statutory health insurance providers in Germany and includes information on approximately 25 million persons who have been insured with one of the participating providers since 2004 or later. In addition to demographic data, GePaRD contains information on drug dispensations as well as outpatient (i.e. from general practitioners and specialists) and inpatient services and diagnoses. Per data year, there is information on approximately 20% of the general population and all geographical regions of Germany are represented.
In GePaRD, information on the use of colonoscopy and FOBT, including the date of the procedure, is available based on codes of the Operations and Procedure Coding System (OPS) and/or the German Uniform Assessment Standard (EBM). For colonoscopy, a distinction can be made between screening and diagnostic purposes as there are different reimbursement codes for these procedures. Also regarding FOBT, there is not only a screening code, but also a code for diagnostic FOBT, although it is not clear in which situations a diagnostic FOBT is actually used, as symptomatic patients should normally undergo a colonoscopy rather than an FOBT.
Study population and study design
Using a cohort design, we included persons aged 50 (starting age of CRC screening in Germany) in 2011 and followed them up until 2020, that is, until age 59 (cohort 1). Further inclusion criteria were a continuous 2-year pre-observation period (years 2009 and 2010), which was required to assess baseline characteristics and to identify prevalent CRCs, as well as a continuous 10-year follow-up period to assess the utilization of colorectal examinations. We excluded persons with prevalent CRC, and persons without valid information on sex or age as well as persons not residing in Germany. For comparison, we conducted a second cohort study including persons aged 55 in 2011 using the same follow-up and inclusion/exclusion criteria as described above (cohort 2). The second cohort was of interest given that screening colonoscopy was offered from age 55 onwards in 2011.
Assessment of the utilization of colorectal examinations
We classified persons into seven mutually exclusive groups based on claims codes for colorectal examinations (FOBT or colonoscopy) recorded during follow-up: (1) screening colonoscopy and screening FOBT; (2) screening colonoscopy, no screening FOBT; (3) screening FOBT, no screening colonoscopy. Persons from groups 1 to 3 may have also used diagnostic examinations. Persons without screening examinations, but diagnostic examinations were assigned to the following groups: (4) diagnostic colonoscopy and diagnostic FOBT, (5) diagnostic colonoscopy, no diagnostic FOBT; (6) diagnostic FOBT, no diagnostic colonoscopy. All persons who used none of these examinations were assigned to group 7. Of note, if the interest is to compare screening participation with other studies, the proportions of groups 1–3 may be summed up. It should also be noted that persons without a screening colonoscopy but a positive FOBT followed up by colonoscopy were in group 3 given that such colonoscopies were reimbursed based on the code for diagnostic colonoscopy during the time of the study.
Characterization of the study population
We characterized the study population regarding the educational level, which was estimated as previously described based on the highest school degree or occupation (Asendorf et al., 2022). Persons were either assigned to the category ‘higher education’ or the category ‘basic secondary degree/secondary degree or missing/unknown information’. The decision to assign people with missing or unknown information to the latter category was made based on insights from previous analyses showing that this group of persons is more similar to those with a basic secondary degree/secondary degree than to those with higher education. Furthermore, we characterized the study population regarding the utilization of other preventive services (e.g. other cancer screening, health check-up) using pre-baseline information. Morbidities were defined based on previously developed algorithms ensuring a high specificity in the definition of morbidities (Riedel et al., 2023).
Data analyses
We characterized included men and women with respect to the educational level, use of other preventive measures, and comorbidities. Then, we described men and women in cohort 1 and cohort 2 according to their 10-year utilization of colorectal examinations as described above. Furthermore, we compared men and women who used any colorectal examination (i.e. screening or diagnostic examinations) with those who used none of these examinations within 10 years according to educational level and the use of other preventive measures. Then, we described the proportion of comorbidities among men and women who used screening or diagnostic examinations compared to those who used none of these examinations within 10 years.
The analysis was carried out with the statistical software SAS 9.4 (SAS Institute, Inc., Cary, North Carolina, USA).
Results
Overall, we included 185 949 persons (55% female) in cohort 1 (i.e. aged 50 in 2011) and 156 258 persons (55% female) in cohort 2 (i.e. aged 55 in 2011) (Supplementary Figure 1, Supplemental digital content 1, http://links.lww.com/EJCP/A538). Supplementary Table 1a, Supplemental digital content 1, http://links.lww.com/EJCP/A538 characterizes included persons of both cohorts regarding educational level, the use of other preventive measures, and comorbidities.
Utilization of colorectal examinations
As shown in Fig. 1a, 80% of women and 63% of men had at least one colorectal examination between age 50 and 59 years (cohort 1). In women, 16% had both a screening colonoscopy and an FOBT (men: 10%), 3% had a screening colonoscopy only (men: 9%), 5% had a diagnostic colonoscopy (men: 10%), 54% had screening FOBT(s) only (men: 29%), and 1% had a diagnostic FOBT only (men: 3%). This means that in men, about half of those with a colorectal examination had at least one colonoscopy (31% out of 63%), while this proportion was lower in women (25% out of 80%). Supplementary Table 3, Supplemental digital content 1, http://links.lww.com/EJCP/A538 shows that among women without any colorectal examination between age 50 and 59 years, 9% already had a colorectal examination before age 50; in men, this proportion was 11%.
Fig. 1.
Proportion of men and women in cohort 1 (a) and cohort 2 (b) according to utilization of colorectal examinations within 10 years (groups are mutually exclusive).
Between age 55 and 64 (cohort 2), 78% of women and 69% of men had at least one colorectal examination (Fig. 1b). In women, the proportion with screening FOBT(s) only was 40%, that is, 14 percentage points lower compared to cohort 1, while the proportion with at least one colonoscopy was 36% (screening colonoscopy: 28%), that is, 11 percentage points higher compared to cohort 1. In men, the proportion with screening FOBT(s) only was rather similar to cohort 1 (27%); the proportion with at least one colonoscopy was 39% (screening colonoscopy: 30%), that is, 8 percentage points higher as compared to cohort 1. Among those without any colorectal examination between age 55 and 64 years, 37% of women and 22% of men already had a colorectal examination before age 55 (Supplementary Table 3, Supplemental digital content 1, http://links.lww.com/EJCP/A538). This means that until age 64, at least 86% of women and at least 76% of men had a colorectal examination.
To assess whether the exclusion criterion ‘continuous insurance from 2011 to 2020’ had an impact on our results, we compared the utilization of colorectal examinations with and without applying this exclusion criterion. The difference in the proportion of persons without any colorectal examination between both analyses was 4 percentage points in men and women of both cohorts (see Supplementary Table 2, Supplemental digital content 1, http://links.lww.com/EJCP/A538). The distribution of characteristics shown in Supplementary Table 1a, Supplemental digital content 1, http://links.lww.com/EJCP/A538 did not change when this exclusion criterion was not applied (Supplementary Table 1b, Supplemental digital content 1, http://links.lww.com/EJCP/A538).
Characteristics of persons with and without colorectal examinations
Figure 2 shows the proportion with any colorectal examination stratified by educational level. The difference in the proportion with any colorectal examination between women with lower vs higher education was 3–4 percentage points (cohort 1: 79 vs 82%; cohort 2: 76 vs 80%). In men, the difference was 6–7 percentage points (cohort 1: 60 vs 67%; cohort 2: 66 vs 72%).
Fig. 2.
Proportion of persons utilizing colorectal examinations within 10 years stratified by sex and educational level (cohort 1: a; cohort 2: b).
Figure 3 shows the proportion utilizing other preventive measures stratified by utilization of colorectal examinations. Across both cohorts and sexes, utilization of other preventive measures was higher in those with vs without colorectal examinations. In women, the difference was 35 percentage points in cohort 1 (90 vs 55%), and 28 percentage points in cohort 2 (94 vs 66%). In men, the difference was 24 percentage points in cohort 1 (64 vs 40%) and 27 percentage points in cohort 2 (70 vs 43%).
Fig. 3.
Proportion of women and men utilizing other preventive measures in cohort 1 (a) and cohort 2 (b) according to utilization of colorectal examinations within 10 years.
As shown in Fig. 4, the prevalence of severe comorbidities and treated hypertension was mostly rather similar in persons utilizing colorectal examinations for screening and in persons without colorectal examinations, while the prevalence tended to be higher in persons utilizing colorectal examinations for diagnostic reasons. For example, the prevalence of severe comorbidities was 7% in women of cohort 1 with no or colorectal screening examinations (men: 10–11%), while it was 12% in women with colorectal examinations done for diagnostic reasons (men: 17%). Detailed information on the prevalence of comorbidities is provided in Supplementary Table 4, Supplemental digital content 1, http://links.lww.com/EJCP/A538.
Fig. 4.
Prevalence of severe comorbidities and treated hypertension only (i.e. no severe comorbidity) in cohort 1 (a) and cohort 2 (b) according to utilization of colorectal examinations within 10 years, stratified by sex. Any severe comorbidities include the following: Crohn’s disease/ulcerative colitis, liver disease, coronary heart disease, congestive heart failure, myocardial infarction, stroke, COPD, hepatitis (B, C), renal insufficiency (terminal), diabetes with organ damage, treated HIV, dementia, and hemiplegia. COPD, chronic obstructive pulmonary disease.
Discussion
To the best of our knowledge, this is the most comprehensive and largest longitudinal study on the utilization of colonoscopy and FOBT in Germany. Our study shows that 78–80% of women had at least one of these examinations from age 50 to 59 and from age 55 to 64. In men, these proportions were also above 60%. More men than women already had a colonoscopy between age 50 and 59 (31 vs 25%). Utilization hardly differed according to educational level. By contrast, there was a strong correlation with utilization of other preventive measures: it was 24–35 percentage points higher among those with vs without colorectal examinations. The prevalence of comorbidities was quite similar in persons with and without CRC screening, suggesting that there is no strong selection for health status, as would be expected due to the so-called ‘healthy screenee bias’.
In view of our results, it is difficult to understand why participation in the German CRC screening program is typically presented as a major problem. Our study shows how important it is to look at the big picture, that is, considering both screening and diagnostic examinations together over a longer follow-up period. Although we did not investigate whether those who utilized FOBT did so regularly, our results show that this second pillar of the German colorectal screening program is important to reach a high coverage. From a public health perspective, it is in any case questionable whether compliance with the screening intervals recommended for FOBT in Germany is of high relevance. The test is offered annually from age 50 to 54 and biennially from age 55 onwards. For the immunochemical FOBT, introduced in 2017 to replace the guaiac-based FOBT, a cut-off lower than in any other European country is used (Gemeinsamer Bundesausschuss, 2020), which typically screen at an interval of 2 years. This means that the sensitivity of the test for precursor lesions and preclinical cancer is relatively high in Germany, questioning whether noncompliance with annual or biennial intervals is a major problem, as a lower cutoff could compensate for longer screening intervals (Haug et al., 2017).
Regarding cumulative uptake of screening colonoscopy, the most important study for comparison was conducted by Steffen et al. (2020) and analyzed outpatient health insurance data from all persons with a statutory health insurance in Germany; it included 326 337 men and 411 872 women aged 55 years in 2009. Reassuringly, the proportion they reported for screening colonoscopy use was similar to that observed in cohort 2 in our study, which shows that GePaRD (four statutory health insurance providers) is representative of all persons with a statutory health insurance in this regard. We assume that this also holds true for FOBT use and the use of diagnostic colonoscopy but due to differences in the methodology a direct comparison was not possible. For example, in the study by Steffen et al. only the proportion using ≥3 FOBTs between age 55 and 64 was reported and information on diagnostic colonoscopies conducted in the inpatient setting was not considered. As the study by Steffen et al. had another focus, there was no characterization regarding educational level and comorbidity to which we could compare our findings.
It is often a concern that preventive measures primarily reach those with a higher socioeconomic status, leading to health inequalities and higher utilization by people with a lower risk. Our results do not support that this concern is justified with respect to utilization of colonoscopy and FOBT in Germany. A report using claims data between 2012 and 2021 from a statutory health insurance provider in Germany whose insured persons tend to have a lower socioeconomic status overall than those considered in our analyses showed a similarly high utilization of colorectal examinations in persons aged 50–64 years (Schnee, 2008; Tillmanns et al., 2022). The proportions were even slightly higher but this is likely due to methodological differences, for example, billing codes for screening consultations were also considered as ‘utilization of CRC screening’ in that analysis. Furthermore, two large German health surveys found only minor differences in the utilization of CRC screening according to educational level (Starker and Saß, 2013; Prütz and Rommel, 2021) and also other studies from Germany did not find a relevant association between educational level and FOBT or colonoscopy use (Sieverding et al., 2010; Hermann et al., 2015; Hornschuch et al., 2022).
Our study showed interesting differences between men and women. The substantially higher utilization of FOBT among women in Germany has already been described previously and points to the long-standing tradition of gynecologists in Germany to dispense FOBT. In a prior study analyzing health claims data, 95% of FOBTs in women were dispensed in gynecological practices, while general practitioners played only a minor role. In men, by contrast, about half of FOBTs were dispensed by general practitioners (Stock et al., 2011). Also the study by Steffen et al. (2020) using data from 2018 showed that the vast majority (77%) of FOBTs in women aged 50–74 years were dispensed by gynecologists. Despite the higher overall utilization of colorectal examinations in women, more men than women already had a colonoscopy between age 50 and 59 (31 vs 25%). As men have a higher CRC risk compared to women, this pattern is in line with what would be aimed for with risk-adjusted screening, that is, screening those with a higher risk more intensively. However, following this reasoning, it would actually also be desirable for the overall uptake to be higher in men than in women.
Our study provides important insights regarding the potential for improving CRC screening and data collection for monitoring CRC screening in Germany. First, it should be noted that the utilization of colonoscopy and FOBT in Germany is quite high overall and there are no significant differences according to educational level, which is positive from a public health perspective. There have often been demands for the FOBT to be sent by mail to all eligible persons in Germany, as is the case in the Netherlands, for example, In view of our results, this should be viewed critically, as it is difficult to harmonize with current utilization of colorectal examinations and there is a risk of overuse if this were to be added to current offers. It might also decrease utilization of colonoscopy in favor of FOBT although colonoscopy is more effective in preventing CRC. The finding of an overall high uptake of colorectal examinations could be taken as an opportunity to focus more attention on ensuring the quality of colonoscopy, which is in need of improvement in Germany (Schwarz et al., 2023), rather than on uptake. Second, even though we observed a strong correlation between utilization of colorectal examinations and other preventive measures, the proportion using other preventive measures among nonusers of colorectal examinations was still high (women 50–59 years: 55%; men 50–59 years: 40%). This supports to further sensitize physicians who offer other preventive measures (e.g. the general health check-up) to the topic of CRC screening so that they also address it. This would be particularly important for men in order to counteract the current sex difference in the overall uptake of colorectal examinations, which does not do justice to the fact that CRC risk is higher in men than in women. Third, our study clearly demonstrates that an approach solely collecting data on colorectal screening examinations to monitor CRC screening in Germany falls far short of the mark. Non-consideration of colorectal examinations done for diagnostic reasons (i) provides a downwardly distorted picture of the overall utilization of colonoscopy and FOBT in Germany, (ii) particularly underestimates utilization in subgroups with comorbidities, and (iii) hinders the monitoring of colonoscopic follow-up of positive FOBTs, as such colonoscopies are currently usually coded as diagnostic and not as screening examinations. However, solely collecting data on colorectal screening examinations is precisely the approach that has been enshrined in law to date for program monitoring, that is, there is an urgent need to rethink this.
The particular strengths of our study in terms of sample size and comprehensiveness have already mentioned above. In addition, the existing studies are mostly quite old (Stock and Brenner, 2010; Stock et al., 2011; Guo et al., 2019) and some of them, unlike our study, could have be affected by recall nor nonresponder bias (Stock and Brenner, 2010; Guo et al., 2019). There are also limitations to be considered in the interpretation of our results. First, it has been said that the guaiac-based FOBT was partly paid for by the individuals themselves or provided by their physicians because it was so cheap. This would have led to underestimating the uptake of the FOBT based on claims data until 2017, that is, the year when the immunochemical FOBT was introduced. However, indirect evidence from a study we conducted on screen-detected CRC does not suggest that under-ascertainment of FOBT before 2017 was a major issue (Hornschuch et al., 2024). We therefore assume that the impact on our results is small and would further support our conclusion as it would mean that the true uptake is even higher. Second, our database contains no information on diagnostic colonoscopies performed in the hospital but billed as outpatient procedures. This would also underestimate actual utilization but from a clinical perspective, it seems plausible that most of these procedures, which are conducted in specific risk constellations, are preceded or followed by additional colonoscopies in the outpatient setting, that is, the patients would still have been classified as having had a colonoscopy. Thirdly, the focus was placed on a 10-year data period (2011–2020), which was a compromise between the screening interval for colonoscopy, data availability, and the goal of providing the most up-to-date information possible. As shown in the ‘Results’ section, exclusion of persons who could not be followed up during this period had no relevant impact on our results.
In summary, our study demonstrates a high utilization of colorectal examinations in Germany and illustrates the value of longitudinal health claims data in this context as it covers not only information on screening but also on examinations done for diagnostic reasons as well as information to characterize users and nonusers.
Acknowledgements
The authors would like to thank all statutory health insurance providers which provided data for this study, namely AOK Bremen/Bremerhaven, DAK-Gesundheit, Techniker Krankenkasse (TK), and hkk Krankenkasse. We also would like to thank Philipp Alexander Volkmar and Inga Schaffer for statistical programming of the datasets and analyses.
M.H., S.S., and U.H. conceptualized the study and developed the data analysis plan. M.H. and S.S. contributed to data analysis. M.H. drafted the first version of the manuscript. All authors contributed to interpretation of the results and critically revised the manuscript draft. All authors approved the final version of the manuscript. U.H. supervised the project.
As we are not the owners of the data we are not legally entitled to grant access to the data of the German Pharmacoepidemiological Research Database. In accordance with German data protection regulations, access to the data is granted only to BIPS employees on the BIPS premises and in the context of approved research projects. Third parties may only access the data in cooperation with BIPS and after signing an agreement for guest researchers at BIPS.
Conflicts of interest
There are no conflicts of interest.
Supplementary Material
Footnotes
Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's website (www.eurjcancerprev.com).
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