The Effects of Colorectal Cancer Screening on Health Attitudes and Practices1

Vol. 12, 651–655, July 2003 Cancer Epidemiology, Biomarkers & Prevention 651

Short Communication The Effects of Colorectal Cancer Screening on Health Attitudes and Practices1

Anne Miles, Jane Wardle,2 Kirsten McCaffery, Again, the association between screening outcome and smoking Sara Williamson, and Wendy Atkin behavior only approached significance. Cancer Research UK Health Behavior Unit, Department of Epidemiology and Public Health, University College London, London WC1 6BT, United Materials and Methods Kingdom [A. M., J. W., K. M., S. W.], and Cancer Research UK Colorectal Cancer Unit, St. Mark’s Hospital, Harrow, United Kingdom [W. A.] In this study, we evaluated attitudes toward and practice of health behaviors before and after screening in a large sample of adults attending for CRC4 screening as part of the United The purpose of this study is to establish whether a negative Kingdom FS Trial. Participants were a population sample of screening result leads to complacency about health and poorer average-risk adults ages 55–64 years, identified from Family health practices. Participants were 3535 older adults, ages Health Services Authority registers for participating general 55–64 years, taking part in the United Kingdom Flexible Sig- practices (primary health care in the United Kingdom) in 14 moidoscopy Trial. They were sent postal questionnaires before centers across the United Kingdom. Local research ethics ap- and after screening attendance. Eating fruit and taking exercise proval was obtained for each of the participating centers. Those were both rated as more important after screening than before, eligible for inclusion in the trial were written to by their general whereas ratings for the importance of avoiding fatty foods and practitioner with an information leaflet on CRC and FS screen- attending cervical and breast cancer screening did not change. ing and were asked whether, if invited, they would accept the Fruit and vegetable intake increased, exercise increased, and offer of screening. The information leaflet described the aims of smoking rates decreased from before to after screening. FS screening as the detection and removal of premalignant Changes in diet, exercise, and smoking were not significantly polyps and did not refer to possible causes of CRC. The leaflet related to screening outcome. These findings provide reassur- was received before the prescreening questionnaire. Respon- ance that screening does not lead to a less healthy lifestyle in dents who replied saying they were interested in screening were the short term and could be used as a context in which to randomly allocated to screening or usual care. The design of the promote positive health behavior change. main FS trial has been described elsewhere (4). Screening outcomes were described as negative when ei- Introduction ther no pathological specimens were detected or when patho- Complacency about health, leading to deterioration in health logical analysis of specimens showed no significant pathology behaviors, has been hypothesized to represent an undesirable (65%); lower risk when the pathology detected was considered Ͻ consequence of negative screening results (1). However, sur- minor [e.g., 1–2 small adenomatous polyps ( 1 cm) with a Ͻ prisingly few studies have investigated the impact of screening tubular histology and mild to moderate dysplasia or 20 on health behaviors. The specter of adverse behavioral effects hyperplastic polyps; 30%]; and higher risk when 3 or more was raised in the Telemark Study when the results showed adenomas or 20 or more hyperplastic polyps were detected, or trends toward “improvement in smoking category”3 and greater significant pathology was found (e.g., adenomatous polyps Ͼ body mass index gains in the group who had a negative flexible that were either large ( 1 cm) or had tubulovillous or villous sigmoidoscopy screening result compared with those who had histology or severe dysplasia; 5%), and a colonoscopy polyps detected (2), although neither effect was statistically was recommended (see Ref. 5 for additional details). Those significant. Lower smoking cessation and smoking reduction eligible to receive the postscreening questionnaire were people rates were also observed in a small group of older adult smokers who had attended FS screening (and colonoscopic screening, if who had received a clear computed tomography scan for early- recommended) and who had received a nonmalignant screening stage lung cancer compared with those receiving an abnormal outcome. result (3), although both groups had higher than expected quit Health attitudes and behaviors were assessed by question- ϭ rates, and the results were interpreted as showing that screening naire in a randomly selected subset (n 5942) of the individ- participation was a catalyst to positive health behavior change. uals in the screening arm of the trial in trial centers in Oxford, Portsmouth, and Swansea. Questionnaires were sent before the screening appointment and 3 months after screening. The atti- tude items were based on the measures used in the European Received 3/21/03; revised 3/21/03; accepted 4/22/03. Health Survey (6) and were as follows: “in general, how im- The costs of publication of this article were defrayed in part by the payment of portant do you feel the following health measures are? to avoid page charges. This article must therefore be hereby marked advertisement in accordance with 18 U.S.C. Section 1734 solely to indicate this fact. fatty foods; to eat plenty of fruit; to take regular exercise; for 1 Support from Cancer Research UK, the Medical Research Council, and NHS women to have a cervical smear test at least every 5 years; for R&D funding are gratefully acknowledged. 2 To whom requests for reprints should be addressed, at Cancer Research UK Health Behavior Unit, Department of Epidemiology and Public Health, Univer- sity College London, London WC1 6BT, United Kingdom. Phone: ϩ44 (0) 20 7679 6627; Fax: ϩ44 (0) 207813 2848; E-mail: [email protected]. 4 The abbreviations used are: CRC, colorectal cancer; FS, Flexible Sigmoidos- 3 From smoking Ͼ10 cigarettes/day to Ͻ10 cigarettes/day. copy; CI, confidence interval.

women to have a breast screen (mammogram) at least every of the postscreening questionnaire in the higher risk outcome 3 years?” group. This resulted in an addition of 234 cases, putting the Health behaviors were assessed as follows: “about how overall response rate up marginally to 63% but did not alter the many servings of fruit do you eat (fresh, frozen or canned)”, pattern of results so will not be discussed further. “about how many servings of vegetables do you eat (including The effect of screening outcome on continuous variables salad but excluding potatoes),”“do you take regular exercise was assessed using repeated measures ANOVA, with time each week,” and “do you smoke cigarettes at all nowadays” (all (pre- versus postscreening) as the within-subjects variable and items from Ref. 6; Table 1). Response options for each question outcome group and gender as between-subjects variables. A are shown in the table footnote. significant group-by-time interaction was taken as evidence for Demographic details were also collected. differences in behavior change after screening. The effect of screening outcome on the binary variables was assessed using Results logistic regression with prescreening health behavior scores, gender and screening outcome as the predictors, and post- A total of 4644 of 5942 (78%) of prescreening questionnaires screening health behavior scores as the dependent variable. were returned. A total of 4329 (73%) of those invited, attended Change over time was assessed in the continuous variables by screening, of whom 3789 had completed the prescreening ques- examining the main effect of time within the ANOVAs and in tionnaire. Of the latter, 20 were not eligible for follow-up, either the binary variables with conditional logistic regression. because they were diagnosed with cancer (n ϭ 16), or they did ϭ Ͻ Eating fruit [F(13,440) 33.9, P 0.001] and taking not have a colonoscopy (n ϭ 4; Fig. 1). The response rate for ϭ Ͻ exercise [F(13,422) 53.3, P 0.001] were rated as more the postscreening questionnaire among attenders who had com- important after screening than before, but ratings for the im- pleted the prescreening questionnaire was high (93%; 3535 of portance of avoiding fatty foods and attending cervical and 3769), although slightly lower in the higher risk outcome group breast cancer screening did not change. There were no signif- ␹2 ϭ ϭ (85%) than the other groups (both 94%; 27.0, df 2, icant interactions with screening outcome group. P Ͻ 0.001). ϭ Fruit and vegetable intake increased [F(13,445) 41.4, Overall, 60% of those originally invited to participate in Ͻ ϭ Ͻ P 0.001; F(13,435) 17.5, P 0.001] exercise increased this study completed both questionnaires and attended screen- (odds ratio: 1.91; 95% CI: 1.62–2.25; P Ͻ 0.001), and smoking ing (3535 of 5942), and they are referred to here as completers. rates decreased (odds ratio: 0.67, 95% CI: 0.46–0.98, The limited demographic information on the full sample shows P ϭ 0.04) from before to after screening (Table 1). There was a higher percentage of men than women completed the study no evidence that change in health behavior related to screening (61 versus 58%), but there was no difference in age between outcome. Fruit intake and vegetable intake showed no time completers and noncompleters. Additional information was Ͻ by screening outcome interaction [F(23,445) 1, ns and available on those who had filled out the prescreening ques- Ͻ F(23,435) 1, ns, respectively]. Exercise status did not vary by tionnaire, showing that completers were less socioeconomically screening outcome, controlling for pre-screening exercise deprived (indexed by educational qualifications and car and (Wald ϭ 0.38, df ϭ 2, ns). The change in smoking status was home ownership), reported higher fruit and vegetable consump- more variable across outcome groups (Table 1). Among smok- tion, and were more likely to report taking regular exercise and ers at baseline, the percentages describing themselves as non- to describe themselves as nonsmokers than noncompleters. smokers at follow-up across the three outcome groups were Among completers, the majority were white (98%) and married 15.5% (clear outcome), 10.5% (lower risk outcome), and 16% (81%) and approximately half had some educational qualifica- (higher risk outcome; ␹2 ϭ 2.70; df ϭ 2; ns). tions (54%). The average number of daily servings of fruit Among nonsmokers at baseline, the percentages saying (1.47, SD: 1.05) and vegetables (1.54, SD: 0.99) were broadly they were smoking at follow-up were 1.1% (clear), 2% (lower comparable with the national average in the United Kingdom risk), and 2.6% (higher risk; ␹2 ϭ 4.82; df ϭ 2; P ϭ 0.09), i.e., (7), although well below the recommended five servings a day. the opposite direction to a complacency effect. The effect of Reported rates of doing regular exercise (66.6%) were higher, screening outcome approached significance as a predictor of and smoking rates (13.9%) were lower than population figures postscreening smoking controlling for prescreening smoking for this age group (8), suggesting a measure of health selection ϭ ϭ ϭ 5 and gender (Wald 5.59; df 2; P 0.06), but the into the trial. pattern of results shows this was towards lower quit rates in the This study addressed the issue of whether health behaviors lower risk outcome group compared with the other two and attitudes became less positive in the group who received a groups (P ϭ 0.106 for the quadratic contrast within logistic negative (clear) screening outcome compared with the other regression). two groups. No specific hypotheses were made about how the lower risk and higher risk positive groups might differ from one another in their health attitudes and behaviors. Results are Discussion reported here from participants for whom both pre- and post- The present findings can be interpreted as broadly reassuring. screening data were available. Three of five health attitudes changed in a positive direction, The analyses were also repeated for all those eligible for and all four health practices showed a modest improvement follow-up by carrying forward the prescreening score for cases after attendance at screening. Although the changes were small, with missing postscreening data (an intention-to-treat analysis). they do at least provide some evidence against the view that In this analysis, it was assumed that nonresponders had not screening leads to a less healthy lifestyle, at least in the short changed their behaviors and beliefs from baseline to give a term. Furthermore, there was no evidence of complacency in more conservative estimate of behavior change after screening the clear outcome group compared with those who had polyps and compensate for the slightly higher level of noncompletion detected. In the Telemark study, there was a trend toward improved smoking status among those with higher risk polyps (2), and 5 Internet address: http://www.doh.gov.uk/stats/trends1.htm. this finding was based on a comparison between participants

Table 1 Demographic characteristics, health attitudes and behaviors before and after screening in relation to screening outcome (completers only) Means or percentages with 95% CIs.

Screening outcome Negative Lower risk positive Higher risk positive (n ϭ 2311) (n ϭ 1051) (n ϭ 173) Age (yr) 60.7 (2.9) 60.7 (2.9) 61.0 (3.0) Marital status (%) Married/living as married 80.6 82.7 79.8 Other 18.4 16.5 19.7 Missing 1.0 0.8 0.5 Educational qualifications (%) With 53.0 47.7 46.2 Without 41.9 47.3 49.8 Missing 5.1 5.0 4.0 Ethnic group (%) White 97.4 97.5 99.4 Nonwhite 1.1 0.7 — Don’t wish to answer/missing 1.5 1.8 0.6 Health attitudesa Importance of avoiding fatty foods (1–5) Preb 3.66 [3.62–3.69] 3.58 [3.53–3.64] 3.57 [3.43–3.71] Post 3.74 [3.70–3.77] 3.69 [3.63–3.75] 3.53 [3.38–3.69] Change ϩ0.08 ϩ0.11 Ϫ0.04 Importance of eating fruit (1–5) Preb 3.97 [3.94–4.01] 3.90 [3.85–3.95] 3.86 [3.73–4.00] Post 4.11 [4.08–4.15] 4.09 [4.04–4.14] 3.96 [3.82–4.09] Changec ϩ0.14 ϩ0.19 ϩ0.10 Importance of taking regular exercise (1–5) Preb 3.84 [3.81–3.88] 3.76 [3.72–3.83] 3.67 [3.53–3.81] Post 4.02 [3.98–4.05] 3.94 [3.88–3.99] 3.89 [3.75–4.02] Changec ϩ0.18 ϩ0.18 ϩ0.22 Importance of women having a cervical smear at least every 5 years (1–5) Pre 4.64 [4.61–4.66] 4.65 [4.61–4.69] 4.72 [4.60–4.84] Post 4.64 [4.60–4.67] 4.64 [4.60–4.68] 4.69 [4.57–4.81] Change 0 Ϫ0.01 Ϫ0.03 Importance of women having a breast screen (mammogram) at least every 3 years (1–5) Pre 4.66 [4.63–4.69] 4.66 [4.62–4.70] 4.75 [4.63–4.86] Post 4.65 [4.62–4.68] 4.68 [4.63–4.72] 4.74 [4.62–4.86] Change Ϫ0.01 ϩ0.02 Ϫ0.01 Health behaviors Mean number of daily servings of fruitd Preb 1.55 [1.51–1.60] 1.36 [1.30–1.42] 1.18 [1.03–1.34] Post 1.69 [1.65–1.74] 1.50 [1.44–1.57] 1.33 [1.17–1.49] Changec ϩ0.14 ϩ0.14 ϩ0.15 Mean number of daily servings of vegetablesd Preb 1.61 [1.57–1.65] 1.43 [1.37–1.50] 1.44 [1.29–1.59] Post 1.74 [1.70–1.78] 1.56 [1.50–1.63] 1.52 [1.36–1.68] Changec ϩ0.13 ϩ0.13 ϩ0.08 Regular exercisee (% ‘’Yes’) Pre 67.9 [65.9–69.9] 64.4 [61.4–67.4] 67.8 [60.3–75.2] Post 73.5 [71.6–75.3] 71.3 [68.5–74.1] 75.0 [67.9–82.1] Change ϩ5.6 ϩ6.9 ϩ7.2 Percent change ϩ8.2 ϩ10.7 ϩ10.6 Smokinge (% ‘’Yes’) Preb 9.8 [8.37–11.2] 20.6 [18.5–22.7] 30.3 [25.1–35.5] Post 9.3 [7.90–10.7] 20.1 [18.1–22.2] 27.3 [22.1–32.4] Changec Ϫ0.5 Ϫ0.5 Ϫ3.0 Percent changef Ϫ5.0 Ϫ2.0 Ϫ10.0 a Response options: 1 ϭ not at all; 2 ϭ somewhat; 3 ϭ moderately; 4 ϭ very; 5 ϭ extremely. b Negative outcome group rate the importance of/the practice of health behaviors as significantly higher than those with polyps prescreening. c Change over time significant. d Response options: 1 ϭ less than one serving/week; 2 ϭ one serving/week; 3 ϭ 2–4 servings/week; 4 ϭ 5–6 servings/week; 5 ϭ one serving/day; 6 ϭ 2 servings/day; 7 ϭ 3 servings/day, 8 ϭ 4ϩ servings/day. These were recoded to represent number of servings/day. Responses 1 and 2 were both coded 0.14 servings/day, response 3 as 0.43, response 4 as 0.79, response 5 as 1, 6 as 2, response 7 as 3, and response 8 as 4 servings/day. e Response options response yes/no. f Computed by dividing “change” by “prescreening percent.”

Fig. 1. Flow chart showing randomisation and study attrittion.

with negative results and those with any polyp detected. How- health beliefs and behaviors in the population differ from ever, in the latter study, everyone with polyps was referred for changes shown by the screening participants as a whole. colonoscopy. In the present study, colonoscopy referrals were Generalization of these results to other populations is restricted to the higher risk group. This raises the possibility limited by the fact that it was carried out among 55–64-year-old that the experience of more extensive medical interventions, British adults who had consented to take part in a trial of a new rather than the detection of polyps per se, might be the factor screening program and that only 60% of those invited to take that influenced smoking reduction in the Telemark study. In part in the study completed it. Those completing the study this study there was no difference between the clear outcome reported better health behaviors than noncompleters. Although and higher risk outcome groups in the likelihood of smoking this is consistent with the findings of higher rates of health postscreening controlling for prescreening smoking status, but behaviors among those attending screening compared with non- the sample size among those referred for colonoscopy was attenders (9–11), less healthy groups may respond differently small, and larger scale studies may detect a significant differ- to screening outcomes and, in addition, may represent a sub- ence. In addition, the present study looked at quit rate rather group in whom any deterioration in health behaviors would be than reduction in number of cigarettes smoked and the former more detrimental to health. Noncompleters also had higher arguably provides a better indicator of positive health change. levels of socioeconomic deprivation, and it is possible that Although Hoff et al. (2) mention a significant change in quit responses to screening outcomes may differ in relation to un- rates in the abstract of their article, no statistic is reported in the derstanding of the meaning of the different screening outcomes. text. An additional limitation concerns the measures of health One limitation of this study and the other two discussed in attitudes and behaviors, which were self-report and single this article is the absence of an unscreened control group. Given items. This was a limitation imposed by the need to avoid a long the concern over health complacency after a clear screening and complex questionnaire, which would have compromised outcome and its potential effect on all-cause mortality raised by response rates, particularly among those with lower levels of the Telemark study (2), there is an urgent need for future education. However, the association between prescreening rat- research to establish whether any differential smoking cessation ings of health behaviors and subsequent findings at sigmoid- or reduction rates come from lower quitting or smoking reduc- oscopy screening provide evidence of their validity (12, 13). tion in lower risk groups (a complacency effect) or higher Overall, however, these results could be taken as reassur- quitting or smoking reduction in higher risk groups, which may ing in relation to hypothesized undesirable behavioral effects of represent the healthy screening catalyst effect. The use of an screening and encouraging in relation to using the screening unscreened control group would also show whether changes in context to promote cancer-preventive health behaviors (14).

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Anne Miles, Jane Wardle, Kirsten McCaffery, et al.

Cancer Epidemiol Biomarkers Prev 2003;12:651-655.

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