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Abstract

Objective

Uptake of cancer screening tends to be lower for colorectal cancer (CRC) than cervical or breast cancer. Dislike of the test itself has often been identified as a barrier to CRC screening with the Faecal Occult Blood (FOB) test, but there have been no head-to-head comparisons of the three tests.

Methods

Women aged 50–80 (n = 890) were recruited in spring 2012 as part of a population-based TNS Research International survey in Great Britain. Those in the eligible age range were asked if they had ever participated in breast, cervical or CRC screening. For each screening test, women who had never participated were asked for their ‘main reason’ using a checklist of barriers.

Results

Among eligible women, 67%, 83% and 90% reported ever having been screened for CRC, cervical and breast cancer respectively. More socioeconomically deprived women were less likely to report any screening, and single women were less likely to report CRC or breast screening than married women. Age was not associated with participation. Overall there were few differences between tests in the reported barriers, but dislike of the test was endorsed more often for CRC screening.

Conclusion

This was the first study to compare barriers to participation in organised screening programmes for CRC, breast and cervical cancer. Cancer screening tests share many barriers, but dislike of the test appears to be a stronger barrier to CRC screening. Women who are non-participants in more than one programme may have more global barriers to screening, such as cancer fatalism. The findings suggest that uptake of CRC screening could be improved by targeting the unpleasantness of stool sampling.

INTRODUCTION

Screening reduces cancer-related deaths for breast, cervical and colorectal cancer.¹ Most developed countries recommend screening at specified ages and time intervals for these cancers. Worldwide, uptake of colorectal cancer (CRC) screening tends to be lower than uptake of breast or cervical screening, even in countries such as the United Kingdom (UK) where organised programmes offer screening without cost to the individual using a call-recall system.^2–5

Improving uptake of CRC screening could be facilitated by a better understanding of the barriers to participation, and particularly barriers that might be unique to CRC screening. Predictors of colorectal, breast and cervical screening uptake have been extensively examined^6–9, and include demographic, psychological (including perceived barriers), and service factors. Studies have shown some differences in sociodemographic predictors of uptake between cancers^2,10–12, although findings have not been consistent across studies. Similarly, general health status has been differentially associated with uptake between cancers.¹³

However, few studies have compared specific barriers to screening across different cancer types. Previous studies conducted in the United States have compared provider-related and other barriers to screening for different cancers^14,15, but results are not easily generalisable to countries that have universal medical coverage. One UK-based qualitative study exploring barriers to cancer screening uptake among ethnic minority groups suggested many common barriers to screening, such as cancer fatalism, language barriers and unhelpful GPs’ attitudes.¹⁶ However, some cancers (e.g. cervical cancer) were perceived to be subject to stronger cultural taboos than others, due to their association with promiscuity. To our knowledge, no study has previously examined barriers to screening between different cancer types among a population-representative sample in the context of organised screening programmes.

Most population-based CRC screening programmes use the Faecal Occult Blood (FOB) test.^17,18 In the UK, guaiac-FOB tests are used, which require stool samples to be taken from three separate bowel motions. This test is self-completed at home, whereas mammography and cervical screening tests are carried out by health care professionals in medical settings. Although home-based tests avoid barriers such as scheduling an appointment, arranging transport, or taking time off work, they pose the additional challenge that the responsibility of initiating and completing the screening process lies with the individual. Procrastination could therefore play a greater role.² In the case of the FOB test, there is also a well-documented distaste for and embarrassment about stool sampling.^19–22 Dislike of the test itself is also reported for breast and cervical cancer screening^23–25, but may be more of a deterrent for a test carried out in the home setting, given the self-discipline needed to complete it, than when the test is done by health professionals in a medical setting.

Another possible factor relates to public awareness of the risk of CRC and, by implication, the benefits of CRC screening. Public awareness of a cancer has been consistently associated with higher uptake.^26–29 Data from the UK, however, show that the public are largely unaware that CRC is a common cancer.³⁰ It is therefore possible that low perceived risk for CRC could explain the lower screening uptake.^6,31

We therefore tested the hypothesis that dislike of the test, not getting round to doing it, and low perceived risk of CRC, would be cited as barriers by a larger proportion of women who had not been screened for CRC than women who had not been screened for breast or cervical cancer. No differences between CRC and other types of screening were hypothesised for other commonly cited barriers, such as cancer fatalism^16,32, lack of perceived benefits of screening^8,33,34, or a previous bad experience with screening.^35,36 We also carried out a sub-group analysis using women who were eligible for CRC as well as breast and/or cervical screening. In this group, we compared barriers to CRC screening endorsed by women who had participated in cervical/breast screening, but not CRC screening (CRC-specific non-participants), with those endorsed by women who were unscreened for CRC and at least one other cancer (generic non-participants), and with women who were screened for CRC but not breast and/or cervical cancer (CRC-specific participants).

METHODS

Data were collected as part of a population-based survey among middle- and older-aged adults, carried out by TNS Research International in March – April 2012, using home-based, computer-assisted personal interviewing (CAPI). The TNS omnibus survey defines sample points using 2001 Census small-area statistics and the Postcode Address File (stratified by Government Office Region and social grade) which are then selected using random location sampling. At each location, quotas are set for age, gender, children in the home and working status.

Participants

The total sample included 2024 men and women, aged 50–80, living in Great Britain. For the present analysis, only women eligible for at least one type of screening were included, resulting in a final sample of 890 women aged 50–77. The age range for each analysis was determined by the eligibility criteria for each screening programme in England, Scotland and Wales (see Table 1). Automatic invitations are sent to all eligible residents of Great Britain. Because of programme-specific variation in timing of first invitations, women might not be invited immediately when they enter the eligible age range. We therefore selected the sample to be three years and one year older than the lower age limit for breast and CRC screening, respectively, to ensure that all respondents should have received an invitation. Women up to three years above the upper age limit were included because the question was about ‘ever having been screened’.

Table 1

Eligible age range for screening in each programme

	Colorectal		Cervical		Breast
	Age range	N	Age range	N	Age range	N
England	60–69 (61–72)	374	25–64 (50–67)	569	50–70 (53–73)	623
Scotland	50–74 (51–77)	89	20–60 (50–63)	53	50–70 (53–73)	72
Wales	60–74 (61–77)	26	20–64 (50–67)	31	50–70 (53–73)	34

Total		489		653		729

(italics): range included in our analysis

Measures

Respondents were asked about uptake of CRC, breast and cervical cancer screening. For CRC screening, the question was: ‘The NHS bowel screening programme sends out home-based stool sample test kits. Have you ever taken part in the bowel screening programme using one of these kits’ (yes/ no/ not sure).⁽ⁱ⁾ For breast screening, the question was: ‘The NHS breast screening programme invites women to have regular mammograms (x-rays of their breasts). Have you ever been for breast screening, also called mammography’ (yes/ no/ not sure). For cervical screening the question was: ‘The NHS cervical screening programme invites women to have regular screening using the smear or Pap test.⁽ⁱⁱ⁾ Have you ever been for cervical screening?’ (yes/ no/ not sure).

Gender, age, marital status (single/ married/ divorced, separated or widowed), ethnicity (white/ non-white), education, housing tenure, and car ownership were recorded for each respondent. An index of individual-level socioeconomic deprivation was created by combining responses to questions on education (passed public examinations in school or college; yes = 0, no = 1), housing tenure (owning = 0, renting = 1), and car ownership (one or more cars = 0, no car = 1), based on a scale used in previous research.³⁷ This gave a scale of 0–3, with 3 being the most deprived. Due to relatively low number of deprived respondents, those with scores 2–3 were combined into one category.

For each screening programme, women who reported that they had never been screened (i.e. non-participants) were asked their ‘main reason’ using a checklist of commonly cited reasons for not participating in screening. The question wording was: ‘Please could you say which of these statements best describes the reason you haven't taken part in the bowel screening programme/ been for breast screening/ been for cervical screening’ (1 ‘I haven't been invited to take part’⁽ⁱⁱⁱ⁾; 2 ‘I haven't got round to it yet, but I do intend to take part’; 3 ‘I'd rather not know if I had [bowel/ breast/ cervical] cancer’^(iv); 4 ‘I don't like the idea of [doing the stool sample test/ having the mammography test/ having the smear test]’; 5 ‘I don't think [bowel/ breast/ cervical] screening works’; 6 ‘I don't think I'm at risk of [bowel/ breast/ cervical] cancer’; 7 ‘I've had a bad experience of cancer screening in the past’; 8 ‘Other, please specify’). ‘Other’ responses were coded by two independent coders (SHL and JWAL), with coding disagreements resolved through discussion. Medical conditions were the only frequently stated ‘other’ reason. The remaining ‘other’ responses varied, and some could not be clearly interpreted. Categories 9 ‘Medical reasons’, 10 ‘Miscellaneous’, and 11 ‘Unclear/ don't know/ blank’, were created after the coding process.

Data analysis

Demographic predictors of screening participation, and reasons for non-participation for each test were analyzed for women who were currently eligible or within three years of having been eligible for screening (see Table 1). Univariate logistic regression analysis was used to examine associations between CRC, breast and cervical screening participation. Multivariate logistic regression was used to examine demographic predictors of participation. To compare endorsement of barriers to participation in colorectal versus breast and cervical screening among non-participants, we calculated two-sample tests of proportions and associated confidence intervals by use of bias-corrected bootstrap with 10000 re-samplings. Among those eligible for CRC and at least one other type of screening, we also compared barriers between CRC-specific non-participants (i.e. women who had participated in breast and/or cervical screening but not CRC screening), generic non-participants (i.e. non-participants for CRC as well as breast and/or cervical screening) and CRC-specific participants (i.e. women who had taken part in CRC screening but not breast and/or cervical screening).

RESULTS

The sample consisted of 890 women with a mean age of 61 (SD = 7.28), predominantly from white ethnic backgrounds (96%). The majority (54%) were married, 37% were divorced, separated or widowed, and 9% were single. On our socioeconomic deprivation scale, 38% had no markers of deprivation, 30% had one, and 32% had two or three markers of deprivation. Due to the small number of non-white respondents eligible for screening (n = 8 for CRC; n = 19 for breast; n = 30 for cervical), we were unable to explore any differences between ethnic subgroups.

Screening participation

Among women currently or recently eligible, 67%, 83% and 90% indicated they had ever participated in colorectal, cervical and breast screening respectively. Participation in CRC screening was higher among women who had ever taken part in cervical (OR = 2.27, 95% CI: 1.24–4.14, p < .01) and breast (OR = 5.14, 95% CI: 2.57–10.30, p < .001) screening. Uptake rates by deprivation, marital status and age are presented in Table 2.

Table 2

Descriptive statistics and multivariate demographic predictors of colorectal, breast and cervical cancer screening uptake

	Colorectal (n = 478)ⁱ				Cervical (n = 640)ⁱ				Breast (n = 719)ⁱ
	N	Uptake %	Adjusted OR	95% CI	N	Uptake %	Adjusted OR	95% CI	N	Uptake %	Adjusted OR	95% CI
Age
50–59 years	28	53.6%	ref (1.00)		360	84.5%	ref (1.00)		222	86.9%	ref (1.00)
60–69 years	322	70.5%	1.94	0.87–4.35	280	80.5%	0.73	0.47–1.11	360	92.6%	1.77	1.00–3.12
70–77 years	128	60.5%	1.41	0.60–3.32	–	–			137	88.3%	1.26	0.64–2.49

Deprivation
0 markers of deprivation	166	75.3%	ref (1.00)		294	88.8%	ref (1.00)		287	94.1%	ref (1.00)
1 marker of deprivation	151	66.9%	0.68	0.41–1.12	166	82.5%	0.64	0.37–1.10	208	92.3%	0.71	0.35–1.46
2–3 markers of deprivation	161	55.8%	0.56*	0.34–0.94	180	74.3%	0.39***	0.23–0.66	224	82.3%	0.31***	0.16–0.58

Marital status
Married	240	74.1%	ref (1.00)		366	87.0%	ref (1.00)		371	92.2%	ref (1.00)
Divorced/separated/widowed	202	61.6%	0.68	0.44–1.05	205	79.2%	0.76	0.47–1.23	282	89.4%	1.02	0.57–1.81
Single	36	47.2%	0.36**	0.17–0.76	69	71.0%	0.43**	0.23–0.81	66	80.3%	0.52	0.24–1.11

Due to missing data on one of the predictor variables or the outcome variable, the sample sizes are slightly smaller than shown in Table 1.

* p < .05; ** p < 0.01; ***p < .001

Multivariate analysis showed that socioeconomic deprivation was the only significant independent predictor of uptake of all three types of screening, with lower uptake among more deprived respondents (results differed slightly between screening types, see Table 2). Single respondents were also less likely than those who were married to have participated in colorectal (p < .01) or breast screening (p < .05), with a similar trend for cervical screening. Age was not a significant predictor of uptake for any type of screening.

Reasons for non-participation

For each type of screening, respondents who indicated that they had never been screened were asked for their primary reason for non-participation. The number and proportion of non-participants endorsing each reason are presented in Table 3.

Table 3.

Reasons for non–participation in screening for each test

	Never had CRC screening (n = 160)			Never had cervical screening (n = 111)			Never had breast screening (n = 72)
Never attended because [choose one reason]…	N	%	95% CI	N	%	95% CI	N	%	95% CI
…I haven't been invited to take part	55	34.4%	28.1–42.5%	50	45.0%	36.9–55.0%	18	25.0%	16.7–36.1%
…I haven't got round to it but I do intend to take part	25	15.6%	10.6–22.5%	11	9.9%	4.5–15.3%	9	12.5%	6.9–22.2%
…I don't like the idea of the test	29	18.1%^a	11.9–23.8%	5	4.5%^a**	1.8–9.9%	12	16.7%	6.9–25.0%
…I'd rather not know if I had [bowel/breast/cervical] cancer	14	8.8%^a	5.0–14.4%	5	4.5%^a*	1.8–9.9%	9	12.5%	6.9–22.2%
…I don't think [bowel/breast/cervical] screening works	2	1.3%	0.6–1.9%	0	0.0%	−¹	4	5.6%	1.4–9.7%
…I don't think I'm at risk of [bowel/breast/cervical] cancer	6	3.8%^ab	0.6–6.3%	18	16.2%^a**	10.8–24.3%	9	12.5%^b*	6.9–22.2%
…I've had a bad experience of cancer screening in the past	2	1.3%	0.6–1.9%	0	0.0%	−¹	1	1.4%	1.4–5.6%²
…medical reasons	13	8.1%^b	5.0–13.1%	15	13.5%	9.0–21.6%	0	0.0%^b***	−¹
…miscellaneous reasons	2	1.3%	0.6–2.5%	1	0.9%	0.9–3.6%²	2	2.8%	1.4–4.2%
…unclear/ don't know/ blank	12	7.5%	3.1–11.3%	6	5.4%	0.9–9.0%	12	11.1%	4.2–18.1%

ⁱdifference colorectal versus cervical screening; ^b: difference colorectal versus breast screening

¹ confidence intervals could not be calculated due to zero positives

² the percentile bootstrap method was used to calculate the confidence interval due to the very small number of cases

* p < .05; ** p < 0.01; ***p < .001

The overall distribution of reasons for non-participation was similar across the three screening programmes, but a few significant differences emerged. Not liking the idea of the test was more likely to be cited among non-participants in CRC than cervical screening (p < .001). Not wanting to know if one had cancer was more likely to be cited for CRC than cervical screening (p < .05). Medical reasons were more likely to be reported for CRC than breast screening (p < .05). Contrary to expectations, not ‘getting round to doing the test’ was cited by a similar proportion of women across all three screening types. Also contrary to expectation, not feeling at risk was less likely to be endorsed for CRC than breast (p < .05) or cervical (p < .01) screening.

Reasons for non-participation among women eligible for multiple screening programmes

Among women eligible for CRC and at least one other type of screening, reasons for non-participation were compared between women who were unscreened for CRC only (CRC-specific non-participants) and those who were unscreened for CRC and at least one other cancer (generic non-participants). CRC-specific non-participants were also compared with women who had screened for CRC but not breast and/or cervical cancer (CRC-specific participants). Results are presented in Table 4.

Table 4.

Reasons for non-participation among CRC-specific non-participants, generic non-participants and CRC-specific participants

	CRC-specific non-participants (not screened for CRC, but screened for breast and/or cervical cancer) (n = 108)			Generic non-participants (not screened for CRC and not screened for breast and/or cervical cancer) (n = 45)			CRC-specific participants (screened for CRC, but not screened for breast and/or cervical cancer) (n = 39)
Never attended because [choose one reason]…	N	%	95% CI	N	%	95% CI	N	%	95% CI
…I haven't been invited to take part	37	34.3%	25.0–42.6%	12	26.7%	13.3–37.8%	12	30.8%	15.4–43.6%
…I haven't got round to it but I do intend to take part	19	17.6%	12.0–26.9%	6	13.3%	2.2–22.2%	0	0.0%^b***	−¹
…I don't like the idea of the test	25	23.1%^ab	16.7–32.4%	3	6.7%^a**	2.2–11.1%	3	7.7%^b**	2.6–12.8%
…I'd rather not know if I had [bowel/breast/cervical] cancer	5	4.6%^a	1.9–10.2%	9	20.0%^a*	6.7–31.1%	2	5.1%	2.6–7.7%
…I don't think [bowel/breast/cervical] screening works	1	0.9%	0.9–3.7%²	1	2.2%	2.2–8.9%²	0	0.0%	–¹
…I don't think I'm at risk of [bowel/breast/cervical] cancer	3	2.8%^b	0.9–5.6%	3	6.7%	2.2–11.1%	12	30.8%^b***	15.4–43.6%
…I've had a bad experience of cancer screening in the past	1	0.9%	0.9–3.7%²	1	2.2%	2.2–8.9%²	0	0.0%	–¹
…medical reasons	12	11.1%^a	4.6–16.7%	1	2.2%^a*	2.2–8.9%²	4	10.3%	2.6–17.9%
…miscellaneous reasons	1	0.9%	0.9–3.7%²	1	2.2%	2.2–8.9%²	0	0.0%	–¹
…unclear/ don't know/ blank	4	3.7%^a	0.9–6.5%	8	17.8%^a*	6.7–26.7%	6	15.4%	2.6–25.6%

^a:difference CRC-specific non-participants versus generic non-participants; ^b: difference CRC-specific non-participants versus CRC-specific participants

¹ confidence intervals could not be calculated due to zero positives

² the percentile bootstrap method was used to calculate the confidence interval due to the very small number of cases

* p < .05; ** p < 0.01; ***p < .001

CRC-specific non-participants were significantly more likely to cite not liking the idea of doing the test (p < .01) and medical reasons (p < .05) as the reason for not participating in CRC testing than generic non-participants. In contrast, generic non-participants were significantly more likely to endorse ‘I'd rather not know if I had cancer’ than CRC-specific non-participants (p < .01). Differences in endorsement of these barriers were not found between specific and generic non-participants for breast or cervical screening (data not shown).

When compared with the barriers to cervical and/or breast screening endorsed by CRC-specific participants, CRC-specific non-participants were more likely to endorse not having got round to it yet (p < .001) and not liking the idea of doing the test (p < .01), but less likely to endorse not being at risk of cancer (p < .001).

DISCUSSION

This study is the first to compare barriers between CRC and other cancer screening tests offered in national screening programmes in a population-based sample. Consistent with figures for screening uptake rates in Britain^2,4,5, a smaller proportion of age-eligible respondents had ever participated in CRC screening than breast or cervical screening. Also consistent with other data, uptake was lower for all three types of screening in more socioeconomically deprived groups^2,40 and lower among single than married respondents.⁴¹ We also found – as others have reported^10,42,43 – that CRC uptake was positively associated with uptake of other types of screening.

Overall, no strong pattern of barriers emerged to explain lower uptake in CRC than breast or cervical screening. This suggests that despite varying levels of uptake, many similar barriers are cited as deterrents across screening tests. This is consistent with previous studies on screening participation which have found many common barriers.^15,16,44 The most consistent difference that emerged was the role of dislike of the test. Not liking the idea of doing the test was endorsed more frequently by CRC than cervical non-participants. Similarly, among women who had taken part in breast or cervical screening but not CRC screening (CRC-specific non-participants), dislike was a more frequent barrier than among women who had not taken part in CRC screening as well as breast and/or cervical screening (generic non-participants). CRC-specific non-participants were also more likely to endorse dislike of the test than those who had screened for CRC but not breast and/or cervical cancer (CRC-specific participants). These results give some support to the hypothesis that distaste for stool sampling plays a role in the relatively low uptake of CRC screening. This finding should encourage efforts to increase the acceptability of home-based stool tests and is in line with research suggesting that simplifying the procedural requirement of FOB testing is positively associated with uptake.⁴⁵

Contrary to expectations, there was limited evidence that not getting round to doing the test was a greater barrier to CRC than breast or cervical screening. This barrier was more likely to be endorsed by CRC-specific non-participants than CRC-specific participants, but none of the other comparisons with this barrier showed significant differences. This suggests that despite the home-based nature of the test, procrastination may not be a major barrier unique to CRC screening. Future research should further examine the extent to which procrastination is a barrier for all types of screening or CRC screening specifically. Furthermore, the results did not suggest that low perceived risk was a CRC-specific barrier to screening, despite the fact that the UK public underestimates the prevalence of colorectal cancer³⁰ and previous findings that suggest perceived risk plays an important role in CRC screening.^6,46 Women who had not participated in CRC screening were less likely to cite not being at risk for that cancer as the reason for not doing the test than those who had not participated in breast or cervical screening.

We also found little evidence that non-participants were particularly sceptical about the effectiveness of CRC screening. Finally, CRC-specific non-participants were less likely to report not wanting to know if they had colorectal cancer than generic non-participants, suggesting that cancer fatalism is unlikely to be a driver of poor uptake of CRC screening specifically. Cancer fatalism may therefore be associated with more generalized negative attitudes to cancer screening, perhaps being a marker of a hard-to-reach group that does not engage with cancer screening across the board.

These results describe a novel approach to investigating barriers to screening. National data suggests that 91% of women in the UK have been screened for cervical cancer at some time in their lives, compared with 83% of our sample.⁴⁷ Although equivalent data are not available for breast or CRC, this suggests that ‘never screened’ women were well represented in our sample. Nevertheless, because of the small absolute numbers of non-participants in some analyses, our results should be treated with caution. It should also be noted that the conclusions drawn are based on an analysis of the main reason for not participating; other potential contributing factors have not been examined. Furthermore, consistent with ethnic minority figures of the older British population⁴⁸, our population-representative sample contained a very small proportion of non-white participants, so the results might not be generalisable to ethnic minority populations.

In conclusion, we found few barriers specific to CRC screening that could explain the lower uptake of FOB testing compared with breast and cervical screening in Great Britain. The exception was dislike of the test which appeared to be a CRC-specific deterrent, whereas cancer fatalism seemed to be a barrier associated with a more global non-participation in screening. Improving the acceptability of CRC screening could improve uptake, but more research into comparative barriers both within individuals and between tests could help to identify new strategies to promote uptake.

Footnotes

ACKNOWLEDGEMENTS

This work was supported by a Cancer Research UK programme grant to Jane Wardle (C1418/A14134). We are grateful to David Boniface for his statistical advice for the analyses presented in this paper.

(i)

In Great Britain, “bowel cancer” is the term commonly used to refer to colorectal cancer.

(ii)

“Smear” and “Pap” tests have been commonly used terms to refer to cervical screening tests for many years. Since 2008, liquid-based cytology (LBC) tests have replaced traditional Pap smears in the NHS cervical screening programme.

(iii)

Not having received an invitation could be due to one of the following reasons: issues in the mailing process (including inaccurate address details or mail delivery issues), other screening programme related issues (e.g. programmes delaying invitations due to local capacity issues), and user-related issues (including people not recognizing or remembering the invitation).

(iv)

Although cervical screening aims to detect pre-cancer rather than cancer, we included this option for cervical screening because previous studies have shown that incorrect beliefs about the purpose of screening are common among eligible British women.^38,39

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Comparing barriers to colorectal cancer screening with barriers to breast and cervical screening: a population-based survey of screening-age women in Great Britain

Abstract

Objective

Methods

Results

Conclusion

INTRODUCTION

METHODS

Participants

Measures

Data analysis

RESULTS

Screening participation

Reasons for non-participation

Reasons for non-participation among women eligible for multiple screening programmes

DISCUSSION

Footnotes

ACKNOWLEDGEMENTS

(i)

(ii)

(iii)

(iv)

References