Obstacles to the uptake of breast, cervical, and colorectal cancer screenings: what remains to be achieved by French national programmes?

Cancer is one of the leading causes of disease and mortality [1]. Breast and colorectal cancer are among the most commonly diagnosed cancers worldwide [2]. Studies published in the mid-1990s have shown that prevention practices and cancer screening both play a key role in reducing cancer prevalence, morbidity, and mortality [3–5]. A recent report from the French National Cancer Institute [6] reaffirms this finding and highlights the central role that primary care physicians play in providing cancer screening. However, recent analyses of the inequalities in screening uptake in France as well as other northern countries are in general agreement, highlighting the persistent role of socioeconomics (e.g., income, educational level, private health insurance access) and family structure [7–11]. For instance, concerning breast and cervical cancer, poor, unmarried women with lower levels of education and less access to health care are less likely to be tested [11, 12]. Beck and Gautier [13] emphasise the positive impact of being older, living in a couple, having children, and more frequently consulting a general practitioner (GP) on colorectal cancer screening uptake. Kobayashi et al. highlight health literacy and Lo et al. highlight dislike of the test as barriers to colorectal cancer screening in England [14] (and Great Britain [15], respectively).

Policy mechanisms have been implemented based on these findings, and cancer screening remains one of the main thrusts of the French 2009–2013 Cancer Plan, with a stated priority of combating inequalities in access to and use of screening. There is no national programme for cervical screening (only experiments are ongoing), but national screening programmes targeting breast cancer and colorectal cancer have been established in France since 2004 and 2009, respectively. The national screening programme for breast cancer targets women between 50 and 74 years of age and consists of sending a voucher through the mail that allows each eligible woman to benefit from a free screening at a radiological centre participating in the programme. The national screening programme for colorectal cancer targets men and women between 50 and 74 years of age and consists of sending a faecal occult blood test (FOBT) (accompanied by directions on how to perform the test) through the mail, for a free laboratory analysis. In addition to these programs, incentives directed towards GPs have been implemented in France, targeting breast cancer screening since 2009 and cervical cancer screening since 2012. These incentives consist of financial bonuses to referral GPs who have screened 80% of their eligible patients. Yet, the impact of these schemes has not been evaluated thus far.

Numerous studies have examined the determinants of cancer screening uptake, but few studies have analysed how these determinants have changed over time, particularly in response to the recent implementation of mass screenings and/or national programmes. The results of preliminary studies indicate that in France, the impact of the social gradient seems to have decreased in 2010 (vs. 2005); however, the inequalities in access for the poorest individuals have persisted [16]. In a different context, De Maio et al.[17] show that the impact of income and educational level on cervical cancer screening use remained stable between 2005 and 2010 in Argentina, but in the case of breast cancer, the impact of education has decreased.

In the context of the strengthening of prevention policies through the implementation of national screening programs, financial incentives, and a third National Cancer Plan, one would expect the screening rates for breast and colorectal cancers to have increased and the inequalities related to socioeconomics and/or health care access to have decreased between 2006 and 2010. The objective of this paper is to model the determinants of the failure to participate in cervical, breast, and colorectal cancer screenings in France and to study the trends in these determinants over time, i.e., between 2006 and 2010. The goal is twofold: first, to contribute to the debate on the efficacy of policies implemented to reduce screening disparities and/or inequalities and, second, to identify potential remaining obstacles to screening to better target and tailor policies promoting screening use. Throughout the paper, the term "inequalities" refers to observed disparities in cancer screening uptake that are assumed to arise from access to care or systemic barriers. The term "differences" refers to the associations between other variables/determinants (e.g., socioeconomic status, risky behaviours) and cancer screening uptake, for which determining whether they are related to the choices of patients or the equity of the health care system is not possible.

This study aimed to examine the determinants of and trends in the failure to receive breast, cervical, and colorectal cancer screenings in France between 2006 and 2010, a period in which various incentive policies were implemented. We focused on three types of cancer that were either the focus of recent debate or the subject of mass screening policies that were implemented following national and international guidelines. However, the supply context and incentive policies related to these types of screening differ. A national programme for breast cancer screening has been in place since 2004 and highly publicised for many years. Mammography is generally prescribed by a GP or gynaecologist and performed in a radiology centre. A Pap smear is most often performed by a gynaecologist or GP before it is sent to a laboratory for analysis, but a national programme has not been established (only experiments are ongoing). This test has been the focus of a number of economic evaluations aiming to provide recommendations for the vaccine against human papillomavirus. A national programme for colorectal cancer screening that targets the entire population over the age of 50 years was recently implemented. Colorectal cancer screening is most often prescribed by a GP but may also be recommended by a gastroenterologist or anatomopathologist.

Our results show that the rates of cervical and breast cancer screening use in France decreased between 2006 and 2010. These results, which are consistent with those of other studies obtained in different contexts and countries [21], are particularly disappointing given the maintenance or reinforcement of certain incentive policies (Cancer Plan 2009–2013). In contrast, the rate of colorectal cancer screening uptake increased substantially between 2006 and 2010. This result can be explained by the introduction of a national cancer screening programme in 2009 that combined two actions: a voucher mailed to eligible individuals on the demand side and a lump sum payment to GPs on the supply side.

According to our results, young age, low socioeconomic status, and poor or fair self-rated health had the strongest negative impact on cervical screening uptake relative to breast and colorectal cancer screening uptake. This result could be explained by the absence of a national programme for cervical screening and, as a consequence, reduced media attention on cervical screening and/or by the costs associated with cervical screening (i.e., the screening is not free) [22]. Furthermore, the context of cervical screening differs from that of other types of cancer screening, as cervical screening is often provided directly by a gynaecologist during a consultation, which increases inequalities related to access to care. Women who lived in a couple were more likely to consult a gynaecologist for contraceptive treatment and thus were more likely to be screened. In addition, the higher screening uptake for women aged between 25 and 34 years was likely related to consultation for one or several pregnancies, which are associated with more frequent visits to specialists. By extension, the provision of cervical screening may be related to the proximity of a gynaecologist (i.e., living in a more urban area where the density of specialists is much higher). Indeed, having consulted a gynaecologist in the past 12 months constituted a very strong determinant of Pap smear and mammography uptake. We performed separate analyses including gynaecologist visits adjusted for all other covariates and found that this variable had a substantial impact on cervical screening uptake (OR = 7.8 [6.2-9.4]) and a less pronounced impact on mammography screening (OR = 3.5 [2.5-4.7]). These results confirm the need to strengthen efforts to reduce inequalities in access to specialists, especially for cancers that are not the subject of a national programme (e.g., cervical cancer).

Concerning breast cancer screening, socioeconomic characteristics had affected the likelihood of undergoing a mammogram, but the effect was less pronounced than that for cervical screening. A possible explanation for this result is that the combination of highly publicised information campaigns for breast cancer in France and the national screening programme indeed targeted a larger population, but economic inequalities have persisted: not having private complementary health insurance (whether free or not) decreased the probability of screening. In France, not having complementary health insurance and, to a greater extent, receiving free complementary health insurance are often associated with low to very low household income. Moreover, even though mammograms are free of charge in the context of organised cancer screening, lower overall access to the health system (e.g., physician care) may prevent individuals from receiving the test. Thus, even though a national programme was implemented in 2004, i.e., before the study period, inequalities in access to breast cancer screening persist and do not seem to have declined over time.

Regarding colorectal cancer screening, despite the introduction of a national programme in 2009, age-related screening disparities have persisted: individuals under 54 years of age were less likely to have been tested. The complementary health insurance variable had no effect on colorectal cancer screening uptake, in contrast to cervical and breast cancer screening uptake, over the study period. However, among males, inequalities related to having free complementary health insurance (the CMU-C) were significant in 2010. Moreover, individuals with less access to health care (GPs or specialists) were less likely to be tested. Thus, health authorities could intensify efforts to promote increased access to screening for the most disadvantaged populations. For this purpose, a national programme is one mechanism among many and should likely be complemented by targeted primary prevention policies aimed at reducing these inequalities.

Another interesting result of our paper concerns the impact of individual risk behaviours and the use or nonuse of other screening tests. The results for individuals who engaged in high-risk behaviours in terms of alcohol and tobacco consumption were consistent with our expectations and the results of previous studies [23, 24]. One possible rationale for their lower screening uptake could relate to economic trade-offs based on time preferences [25] and/or fear of disease. However, surprisingly, individuals reporting very healthy behaviours (never consuming alcohol, never smoking) also had lower levels of screening uptake. This result is interesting, as it suggests that more targeted primary prevention policies are needed for these individuals, for instance, by combating the notion that cancer only affects individuals with more risky lifestyles.

Our results demonstrate that persistent obstacles to screening, which are primarily related to socioeconomic characteristics, health care access, and risky behaviours, remain. However, we could not precisely determine if low screening uptake result from lower patient uptake (i.e., patient choice) or from less access to screening services (i.e., system-level barriers). Further studies should more specifically investigate the associations among attitudes/beliefs, individual barriers in access to care, and screening uptake.

Greater coordination between the different actors involved in cancer screening also seems necessary because, in the context of French national programmes—particularly the breast cancer screening programme—the GP or gynaecologist is not always aware of whether their patients have received a mammogram. Some studies argue that the GP’s role should be to coordinate the patient’s various screenings [34, 35]. Indeed, GPs are the most relevant actors in the prescription of colorectal cancer screening [36], and they play an important (advisory) role in breast cancer and cervical screenings [37].

^aFor a complete description of the authorisation: http://legimobile.fr/fr/cnil/del/aut/2010/2010-003/.

^bIn France, private complementary health insurance is generally purchased to cover reinsurable copayments that are not covered by public health insurance: for any given service, the reimbursement is computed as a percentage of regulated prices, and some providers are also allowed to charge additional fees. Below a certain income threshold, individuals can benefit from a form of free complementary health insurance called the CMU-C. Individuals benefiting from the CMU-C are generally more socially and economically disadvantaged.

^cWe did not include breast cancer and colorectal cancer screening as predictors of cervical cancer screening uptake because the age groups differed.

^dWe thank an anonymous referee for offering two other rationales for this stratification: first other factors affecting colorectal screening may differ by sex (e.g. health consumption, risky behaviours); second, this stratification is useful for examining whether breast cancer screening compliance predicts the likelihood of colorectal screening among women.

^e http://www.invs.sante.fr/Dossiers-thematiques/Maladies-chroniques-et-traumatismes/Cancers/Evaluation-des-programmes-de-depistage-des-cancers/Evaluation-du-programme-de-depistage-du-cancer-du-sein.

^f http://www.invs.sante.fr/Dossiers-thematiques/Maladies-chroniques-et-traumatismes/Cancers/Evaluation-des-programmes-de-depistage-des-cancers/Evaluation-du-programme-de-depistage-du-cancer-colorectal.

We attest that each author has provided 1) substantial contributions to the conception and design of the study, 2) a draft or revision of the article, and 3) final approval of the version of the article to be published. JS performed the statistical analyses and drafted the manuscript. CF participated in the methodology assessment, helped in interpreting the results and in drafting the manuscript. All authors read and approved the final manuscript. Each author has participated sufficiently in the work to take public responsibility for an appropriate portion of the content.