Rates of ever receiving CRC testing for FDRs of CRC patients were relatively high in the current study, with approximately 70% of FDRs across each level of risk ever receiving CRC testing. The rate of FDRs ever receiving CRC testing was not found to be significantly higher among population groups at higher relative risk of CRC (i.e. persons at “moderately increased risk” and “potentially high risk”, compared with persons “at or slightly above average risk”). In an Australian context, rates of participation in CRC testing or testing undertaken in adherence to guidelines among FDRs of CRC have previously only been evaluated in two other studies [28, 31].
The current study highlighted low levels of CRC screening in accordance with guideline recommendations across varying levels of risk: “at or slightly above average risk” (25%); “moderately increased risk” (47%); and “potentially high risk” (49%). International comparisons of risk-appropriate screening in accordance with guideline recommendations are difficult to ascertain, given that healthcare authorities’ endorsement of screening modality and timing of repeat testing vary across countries [18, 33, 34]. Few studies have assessed CRC screening in accordance with guideline recommendations for persons with an affected FDR with CRC [28–30]. This study, to our knowledge, is the first Australian population-based examination of CRC screening participation among FDRs of CRC patients
Screening of first-degree relatives “at or slightly above average risk” in accordance with guidelines
The low rate of screening in accordance with guideline recommendation for FDRs “at or slightly above average risk” identified in this study is comparable to that of the general population in Australia [35, 36]. Two separate population-based evaluations among persons over 50 years of age have indicated that 33% of respondents at “average risk” had undertaken FOBT screening in the previous five years  and 18.4% in the previous two years . The most recent investigation of CRC screening participation among at-risk persons (i.e. those aged over 55 years) since the National Bowel Cancer Screening Program’s introduction in 2006 indicated that screening in accordance with guideline recommendation for persons “at or slightly above average risk” was 20 per cent . Although community-based studies in the United States (US) have generally established rates of FOBT screening in accordance with guideline recommendations among FDRs of CRC patients of between 9% and 42%, [37–40] the studies with the highest screening rates had recruited participants through advertisements [38, 39]. Such samples are unlikely to be representative of FDRs of CRC patients in general, and are likely to be biased as they include participants more likely to engage in screening,  thus reducing the findings’ relevance for indicating population-based estimates.
Screening of first-degree relatives at elevated risk (“moderately increased risk” and “potentially high risk”) in accordance with guidelines
Current study findings indicated that 47% of FDRs of CRC patients at “moderately increased risk” and 49% of persons at “potentially high risk” were screened in accordance with the Australian guideline recommendation (i.e. colonoscopy screening every five years). This is much higher than other Australian data on risk-appropriate CRC testing among FDRs, which had identified three FDRs among 225 were screened in accordance with Australian guidelines . The most recent study in Victoria among first and second-degree relatives selected from case and population control probands in the Melbourne metropolitan area identified that 6% (70/1236) of persons at “moderately increased risk” were screened in accordance with guideline-recommendation . For relatives of probands at “potentially high risk” 1% (3/389) were adherent to guideline- recommended screening .
For the most part, the rate of screening in accordance with guideline recommendations for FDRs of CRC patients at elevated levels of risk (i.e. “moderately increased risk” and “potentially high risk”) in the current study is similar to rates identified in the general population [24, 35]. The most recent Australian community-based study of CRC screening participation found that among persons over 55 years of age, 45% of those at “moderately increased risk” and “potentially high risk” were screened in accordance with guideline CRC screening recommendation (i.e. colonoscopy screening every five years) . Another population-based investigation among persons aged over 50 years at “above average risk” indicated that 30% had undertaken endoscopy (colonoscopy or sigmoidoscopy) in the previous five years . Data available from a US population-based National Health Interview Survey sample of persons 41-75 years of age with a FDR diagnosed with CRC indicated that 28% of FDRs had undertaken colonoscopy screening in the previous ten years . For this study, direct compliance with guideline screening recommendation was not ascertained. Another study recruiting siblings of CRC patients diagnosed younger than 56 years of age through four cancer centres in the US indicated that 57% of siblings older than 34 years were screened in accordance with guidelines . Study findings from another investigation of FDRs of CRC patients participating in a free FOBT screening program indicated that 22% of respondents were screened in accordance with guidelines . In Canada, the most recent evaluation of CRC screening among FDRs of CRC patients aged over 40 years selected through the Alberta Cancer Registry indicated that 60% were appropriately screened for CRC screening (i.e. FOBT within one year, barium enema or sigmoidoscopy within five years, or colonoscopy within 10 years) . In summary, the available evidence suggests that, worldwide, the screening rates of FDRs of CRC patients in accordance with guideline recommendations rarely exceed 50 percent, well short of rates likely to be necessary for reducing CRC incidence and mortality on a population basis.
Factors associated with colorectal cancer testing and adherence to colorectal cancer screening guidelines
The present study identified a number of socio-demographic and provider-level factors impacting upon CRC testing and screening in accordance with guideline recommendations. It is well-established that older age is a consistent predictor of CRC screening [23, 42, 43]. The current study identified that the odds of receiving CRC testing increased with increasing age of FDRs. This finding is consistent with previous literature among the FDR population [25, 41, 44]. For persons “at or slightly above average risk”, adherence to screening guidelines was significantly more likely to occur for male compared with female FDRs. This is contrary to other studies of FDRs that have, on the whole, largely indicated no association between gender and screening behaviour .
Previous literature has indicated that having medical insurance is significantly correlated with CRC screening adherence [36, 43, 45]. Consistent with this literature, the current study identified that the likelihood of ever receiving CRC testing was at significantly higher odds for FDRs with private health insurance. This suggests that the costs of medical consultation or screening itself represent significant barriers to CRC screening rates among persons without private health insurance.
The current study also found that siblings compared with children of the index case were at significantly increased likelihood of ever receiving CRC testing and receiving CRC screening in accordance with screening guideline recommendations for persons at “moderately increased risk” and “potentially high risk”. Previous literature has largely analysed either CRC screening among siblings only [29, 46] or FDRs combined and not separated into type of FDRs (i.e. parent, child or sibling) [37, 41, 47]. A previous Australian investigation found that being a sibling of a CRC patient, consistent with current study findings, was significantly associated with increased likelihood of previous participation in CRC testing . Further, a multi-centre nation-wide study in Spain identified a higher rate of adherence to colonoscopy screening for siblings and children, compared with parents, when offered screening by a gastroenterologist . Current data suggest that screening compliance may be lower among CRC patients’ children who are deemed eligible for screening in accordance with screening guidelines compared to their siblings. There is a pressing need to ensure equality in CRC screening uptake across at-risk FDRs e.g. children, siblings and parents.
This study also found that persons “at or slightly above average risk” with a higher level of education were at significantly increased odds of receiving screening in accordance with guideline recommendations. Previous findings related to CRC testing and educational attainment for persons with a family history of CRC are mixed, with some studies indicating a positive trend [29, 30, 48] and others indicating no association between CRC testing and level of education [28, 38, 47]. For persons at “moderately increased risk” and “potentially high risk”, screening according to guideline recommendations was significantly more likely to occur for FDRs who were married or partnered, compared with those not partnered. For the most part, marital status has been identified as a significant factor influencing screening participation in the general population [43, 49–51] and among FDRs of CRC patients, [21, 47] with increased screening compliance commonly found for married and partnered persons.
The role of geographical barriers to CRC screening was also evident in the current study, as screening in accordance with guideline recommendations for persons at “moderately increased risk” and “potentially high risk” was significantly more likely to occur for persons residing in metropolitan areas, compared with regional or remote areas. This finding is plausible, given the high concentration of colonoscopy services in major hospitals in large cities in Australia . Future attention to equality in access to CRC screening services for those at increased levels of risk (i.e. “moderately increased risk” and “potentially high risk”) is clearly required.
The FDRs of CRC patients in the current study who had ever been asked about their family history of CRC by a doctor were also at significantly higher odds of ever undertaking CRC testing and undertaking testing in accordance with guideline recommendations for persons at “moderately increased risk” and “potentially high risk”). This finding highlights the need for assessment and on-going monitoring of family history of CRC within both the primary and specialist healthcare settings. Although physicians have been found to follow appropriate guideline recommendations for CRC screening once increased risk has been identified, the family history information gathered is often insufficient for risk stratification purposes [53–55]. The wider incorporation of recently developed cancer risk assessment tools, showing both feasibility and effectiveness in the collection of family history information, automation of familial risk stratification and risk-appropriate screening advice, [56, 57] should be considered in the primary and secondary healthcare systems.
Despite the evidence that physician recommendation to screen has a powerful motivating effect on CRC screening uptake,  FDRs are most often not informed by physicians about the need for CRC screening . A significantly higher rate of colonoscopy screening can result among those siblings where the index cases were aware of their FDRs’ increased risk . Improvements in CRC screening among the higher-risk populations (i.e. persons at “moderately increased risk” and “potentially high risk”) rely on physicians’ active involvement in discussions with index cases and their FDRs surrounding their families’ increased risk and need for CRC screening.
Strengths and limitations of the study
In interpreting study findings, several limitations should be considered. The response rates among index cases and FDRs were low. Given that people interested in their health are more likely to participate in health research, it is likely that this has resulted in an over-estimate rather than an under-estimate of the true screening rates. It should be noted that the index case response rate achieved in the current study is comparable to the only other Australian-based investigation of CRC screening among FDRs that had adopted a Cancer Registry based recruitment method .
Personal history of adenomatous polyps was not investigated in this study, making it difficult to calculate precisely the proportion of persons “at or slightly above average risk” undertaking colonoscopy screening (i.e. in the previous five years) not in accordance with guideline recommendation. Nonetheless, the available data are suggestive of significant over-use of colonoscopy, given that a large proportion of persons “at or slightly above average risk” had received recent colonoscopy without any other CRC screening (i.e. FOBT or sigmoidoscopy) beforehand.
Family history and CRC screening behaviour were self-reported, rather than objectively assessed. Nonetheless, studies have indicated that self-reported family history of CRC is moderately accurate [60, 63]. The level of risk obtained for FDRs was allocated on the basis of index case self-reported information about family history, thus allowing only a potential estimate. It was not practical to obtain a full family history from each FDR of CRC patients for this study.