Heterogeneity in the Utilization of Fecal Occult Blood Testing and Colonoscopy among Migrants and Non-Migrants in Austria: Results of the Austrian Health Interview Survey

: Many European studies report lower participation in colorectal cancer screening among migrants than non-migrants. A major limitation of these studies is that usually, the heterogeneity of migrants cannot be accounted for. The aim of this investigation was to examine differences in the utilization of fecal occult blood testing and colonoscopy between non-migrants and the ﬁve largest migrant groups residing in Austria using data from the Austrian Health Interview Survey 2019. The two outcomes were compared between non-migrants and migrants using multivariable logistic regression adjusted for socioeconomic and health variables. Migrants from a Yugoslav successor state (OR = 0.61; 95%-CI: 0.44–0.83), Turkish (OR = 0.35; 95%-CI: 0.22–0.55), Hungarian (OR = 0.37; 95%-CI: 0.16–0.82) and German migrants (OR = 0.70; 95%-CI: 0.51–0.98) were less likely to have used a fecal occult blood test compared to non-migrants. Participation in colonoscopy was lower among Turkish migrants (OR = 0.42; 95%-CI: 0.27–0.67) and migrants from a Yugoslav successor state (OR = 0.56; 95%-CI: 0.42–0.75) than among non-migrants. The ﬁndings are consistent with studies from other countries and highlight barriers migrants face in accessing the health care system. To address these barriers, the heterogeneity of the population must be taken into account when developing educational materials in order to promote informed decisions about whether or not to participate in colorectal cancer screening.


Introduction
Colorectal cancer accounts for approximately 12.7% of all new cancer diagnoses and 12.4% of all cancer-related deaths in Europe [1]. Risk factors for colorectal cancer include personal lifestyle factors such as smoking, lack of exercise, high consumption of red meat and a low-fiber diet. In addition, a family history of the disease and advancing age contribute to an increased risk of colorectal cancer [2]. Colorectal cancer screening can significantly reduce colorectal cancer incidence and mortality [3][4][5]. Screening may comprise both invasive and non-invasive methods. In order to detect microscopic amounts of blood in the stool, non-invasive stool tests such as the guaiac fecal occult blood test (gFOBT) and the fecal immunochemical test (FIT) can be used. Colonoscopy, on the other hand, is an invasive screening method used to examine the colon for polyps and potentially malignant neoplasms, which can be treated accordingly once identified [6].
Despite its benefits, colorectal cancer screening can also be associated with disadvantages and is therefore not without controversy [7]. The advantages of colorectal cancer screening, such as early detection and removal of precancerous lesions and the associated By using data from a representative population-based survey, the aim of the present study was to examine disparities in the use of colorectal cancer screening among nonmigrants and the five largest groups of migrants residing in Austria (individuals with a nationality from a Yugoslav successor state, Turkey, Romania, Hungary and Germany [31]). By shedding light on potential heterogeneities, the findings can contribute to tailoring strategies of diversity-sensitive health care in order to ensure the provision of equal access to colorectal cancer screening for migrant communities.

Results
Of the 8267 respondents aged 50 and older, 222 (2.7%) were migrants from a Yugoslav successor state, 208 (2.5%) were German, 85 (1.0%) were Turkish, 40 (0.5%) were Romanian and 27 (0.3%) were Hungarian migrants. The population groups differed in their socioeconomic and health profile ( Table 1). On average, migrants were younger, were more likely to live in urbanized areas, rated their health status worse than non-migrants and were more likely to have chronic diseases. Turkish migrants, in particular, had a significantly lower level of education than non-migrants. All migrant groups showed a significantly lower utilization of fecal occult blood testing compared to non-migrants. While 80.8% of non-migrants had utilized a fecal occult blood test at least once prior to the survey, the proportion was lower among Turkish (60.9%), Hungarian (63.0%), Romanian (70.0%), migrants from a Yugoslav successor state (72.5%) and German migrants (75%). Regarding the participation in colonoscopy, the proportion of Turkish migrants (43.5%), Hungarian migrants (48.1%), migrants from a Yugoslav successor state (50.0%) and Romanian migrants (55.0%), who had a colonoscopy at least once in their lifetime, was significantly lower than among non-migrants (61.8%). German migrants (62.0%) and non-migrants (61.8%) reported a similar utilization of colonoscopy (Table 1).
For both outcomes, neither interaction effects between migration status and sex nor between migration status and age were identified.

Discussion
Different studies have shown that migrants use colorectal cancer screening less frequently than the native populations of the countries they reside in [16,17,29,30]. However, a limitation of many of these studies is that they do not take into account the heterogeneity of migrants. The present study used a nationwide population-based cross-sectional survey to investigate participation in colorectal cancer screening among non-migrants and the five largest migrant groups residing in Austria. The results of the study showed that all migrant groups, with the exception of Romanian migrants, participated less frequently in fecal occult blood testing than non-migrants. Regarding colonoscopy participation, the results showed that Turkish migrants and migrants from a Yugoslav successor state, in particular, had significantly lower utilization rates than non-migrants. These differences were not due to a different distribution of sociodemographic, regional or health factors among the population groups.
The findings are in line with a large number of studies from different countries showing a lower uptake of cancer screening among migrants [32][33][34][35][36][37][38][39]. Non-participation in cancer screening may result from barriers migrants experience in the health care system. Such barriers, for example, may be a low proficiency in the language of the country of residence. Similarly, poor health literacy [40,41], including limited knowledge about colorectal cancer and screening in general, may be barriers to participation [42,43]. They may contribute to migrants' inability to communicate their existing level of knowledge about cancer and cancer prevention, to ask questions and to express themselves openly to health care providers [44]. A general mistrust of the health care system, a poor patientprovider relationship, and unmet expectations about screening may also be associated with lower uptake of colorectal cancer screening [45,46]. Furthermore, non-participation in colorectal cancer screening may be attributed to cultural beliefs and values, such as the discomfort of Muslim women to be treated by a male health care provider, highlighting the need to make female health care providers available to female patients [47,48]. For some patients, religious beliefs also include considering the cure for illness to be in God's hands, thus forgoing cancer treatment and early detection [46,49]. In addition, cancer and cancer prevention may be taboo topics among some population groups and, therefore, not readily discussed within the family [44]. Open discussion of the process of performing a fecal occult blood test or colonoscopy may also contribute to shame and embarrassment among migrants and discourage participation [48].
To avoid the discomfort of colonoscopy, alternative methods used for the early detection of colorectal cancer are available. These include, for example, genetic stool tests that detect mutations in the stool of patients with colorectal cancer and, with lower frequency, patients with adenomas [7]. The assumption here is that tumor appearance and development are associated with somatic genetic alterations, which, however, are rarely found in general populations. A study from China has investigated the utility of copy number variation (CNV) as a potentially clinically useful biomarker for the detection of early colorectal cancer, achieving an acceptable sensitivity of 91.7% and specificity of 88.9% for early colorectal cancer detection. These results suggest that CNV in plasma may be a potential tumor biomarker with high sensitivity and specificity. However, some limitations of this study must be considered, including the limited number of samples [50]. In addition to genetic stool examinations, there are also virtual colonography procedures, which include CT and MR colonography. CT colonography involves performing an abdominal CT scan of the colon to investigate the presence of neoplasia based on images. Patients with colorectal lesions are referred for colonoscopy. CT colonography is controversial. Thus, the implementation and evaluation of the examination have not yet been standardized [7]. In addition, data suggest that although CT colonography can detect polyps >9 mm in size with high sensitivity, smaller polyps have a lower detection rate [51][52][53]. This limitation adds to radiation exposure, which is considered to be associated with an increased risk of malignancies. MR colonography is unlike CT colonography, free from radiation exposure; however, it has so far been insufficiently investigated. Due to the aforementioned disadvantages, virtual colonography procedures are currently only recommended in cases where colonoscopy is not possible [7].
Other reasons for lower participation in colorectal cancer screening could be that migrants perceive their risk of colorectal cancer as lower than the native population [36,54,55] and that they are more likely to be unaware of the symptoms [44]. Culturally sensitive information on colorectal cancer screening, which is tailored to the linguistic specificities of migrants and takes the heterogeneity of this population group into account, can promote informed decision-making [23].
By taking into account different countries of origin, the present study shows that the utilization of cancer screening is particularly low among Turkish migrants and migrants from a successor state of Yugoslavia. This could possibly be attributed to the fact that Turkish migrants and migrants from a successor state of Yugoslavia have a poorer command of the national language than Romanian and Hungarian migrants. Studies show that Turkish migrant women, in particular, often have low German language skills [56]. Studies from other countries also show that Turkish migrants, in particular, are less likely to attend cancer screening [57,58]. The lower participation of Turkish migrants and migrants from a successor state of Yugoslavia may also be related to lower acculturation, as research from the Netherlands has illustrated [59]. Studies from the US have shown that long residence in the country of immigration is associated with higher screening rates [43,60,61]. Since information on the duration of residence was not available in the data, this association, however, could not be further examined in our study and should be the subject of future research.
The strengths of the present study include the large sample size and data that are representative of the population of Austria. A major limitation, however, is that the data are not based on administrative or routine data but on self-reporting by the survey participants. Since the survey refers to previous screenings that may have occurred up to 10 or more years ago, recall bias may be present. While individuals who have recently undergone screening may be overrepresented in the present sample, potentially overestimating the use of screening, we do not consider this proportion to differ between the population groups studied. Furthermore, in the analysis of the present study, only respondents aged 50 years and older were included, as in Austria, colorectal cancer screening is only recommended for this age group. However, studies show that the number of people who develop colorectal cancer at a young age has increased in recent decades [62,63]. For this reason, the U.S. Multi-Society Task Force recommends that colorectal cancer screening begins at age 45 for individuals at average risk [64]. This is consistent with the recommendations of other U.S. professional societies such as the American Cancer Society (ACP) [65], the American College of Gastroenterology (ACG) [66] and others. However, it has to be considered that there are no clinical data on the impact of colorectal cancer screening in individuals younger than 50 years with respect to colorectal cancer incidence and mortality. In contrast, European guidelines still recommend that colorectal cancer screening starts at age 50 [67,68]. Another limitation is that the survey was conducted exclusively in German. Consequently, migrants with poor language skills could not participate in the survey and are, therefore, underrepresented in the study. As migrants with poor language proficiency are particularly vulnerable to experiencing barriers in the health care system [69], excluding this group by means of the study design may underestimate the true amount of differences in colorectal cancer screening utilization between migrants and non-migrants. It also must be given due consideration that information such as a family history of (colorectal) cancer, which could potentially increase the awareness of individuals towards the relevance of screening services, was not available. Likewise, we were only able to broadly distinguish between three educational groups, with no information available on health literacy or a health-related background, which could likely affect the decision to undergo screening.

Data
The study draws on data from the "Austrian Health Interview Survey 2019", which was conducted by Statistics Austria on behalf of the Federal Ministry of Social Affairs, Health, Care and Consumer Protection and the Federal Health Agency in 2018/2019 following the approach of the European Health Information Survey. It is a representative population-based cross-sectional survey providing data on 15,461 randomly selected individuals aged 15 years and older recruited on the basis of the Central Population Register and spatially stratified according to the 32 health care regions of the Austrian Structure Plan. Computer-assisted face-to-face and web-based interviews, amended by self-administered questionnaires completed by the respondents themselves, were used for data collection. Participation in the survey was voluntary, and the response rate was 50.5%. For the present study, only respondents ≥50 years of age were included since, from this age onwards, colorectal cancer screening is recommended in Austria [70]. The final sample studied consists of n = 8267 individuals.

Study Variables
Utilization of colorectal cancer screening was assessed by asking respondents when they last had a test for hidden blood in the stool ("within the last 12 months", "1 to less than 2 years ago", "2 to less than 3 years ago", "3 years ago or more", and "never") and when they last attended a colonoscopy ("within the last 12 months", "1 to less than 5 years ago", "5 to less than 10 years ago", "10 years ago or more" and "never"). We dichotomized each of these two outcome variables to distinguish between respondents who had had a fecal occult blood test or colonoscopy at least once in their lifetime and those who had never had one. The outcomes were compared between non-migrants and the five largest migrant groups living in Austria, i.e., individuals with a nationality from or born in a Yugoslav successor state, Turkey, Romania, Hungary and Germany. Respondents were considered migrants if they either had non-Austrian citizenship or were born outside of Austria [24]. Several covariates were taken into account. Aside from sex (male, female), we included age (five-year age groups), partnership status (living with a partner in the same household vs. not living with a partner in the same household), occupational status (employed, not employed), household income (quintiles) and the educational level (low, moderate, high). In addition, the region (province) of residence of the respondents, the degree of urbanization (high, moderate, low), the self-rated health status (1-very good to 5-very poor) and the presence of chronic diseases (yes, no) were also included to account for contextual and health differences between the population groups.

Analysis
For purposes of sample description, differences between the population groups were analyzed using chi-square tests with the significance level set to p < 0.05. Two multivariable logistic regression analyses were conducted to examine adjusted differences between the population groups in terms of the two outcomes of interest (fecal occult blood testing and colonoscopy). The results were reported as adjusted odds ratios (aOR) with 95% confidence intervals (95%-CI). Moderation effects by age and sex were studied by means of interaction terms included in each of the two regression models. All analyses were conducted using IBM SPSS Statistics version 26.

Conclusions
To the best of the authors' knowledge, this is the first study to investigate differences in the uptake of colorectal cancer screening between non-migrants and the five largest migrant groups in Austria. Although the findings show that many of the included migrant groups tend to have lower utilization of fecal occult blood testing and colonoscopy, disparities are particularly pronounced for Turkish migrants and migrants from a successor state of former Yugoslavia. This corresponds to findings from others fields of health care and is likely due to barriers migrants face in accessing the health care system.
Policies to remove such barriers are essential. They need to take into account the heterogeneity of migrants when developing educational materials in order to enable this population group to make an informed decision about whether or not to participate in colorectal cancer screening. In addition, health care providers need to be aware of the needs and expectations of this population group and, in case of language barriers, should be assisted by professional interpreters. Future research should particularly examine the barriers migrants experience with regard to making informed decisions about colorectal cancer screening utilization, their expectations and needs related to colorectal cancer screening, and develop strategies and interventions that promote informed decision-making with respect to participation among this population group.

Institutional Review Board Statement:
The study is based on a secondary analysis of data collected by Statistics Austria on behalf of the Federal Ministry of Social Affairs as part of an anonymous and voluntary national survey. Before participation, participants provided informed consent. In line with previous analyses of the same and similar data and following national guidelines and recommendations for secondary data analyses, no further ethical approval was required for the present study.
Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.

Conflicts of Interest:
The authors declare no conflict of interest.