Factors that could influence women's participation in colorectal cancer ...

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Key words: Colorectal cancer, screening, women, adherence, Italy. Parole chiave: Cancro del Colon Retto, screening, donne, adesione, Italia. Abstract.
Ann Ig 2017; 29: 151-160 doi:10.7416/ai.2017.2142

Factors that could influence women’s participation in colorectal cancer screening: an Italian study G. Bocci1, G. Troiano1, G. Messina2, N. Nante2, S. Civitelli3 Key words: Colorectal cancer, screening, women, adherence, Italy Parole chiave: Cancro del Colon Retto, screening, donne, adesione, Italia

Abstract Background. Colorectal cancer (CRC) is the 2nd most common cancer in women worldwide. In Italy, only 50% of people invited to get the Fecal Occult Blood Test (FOBT) decided to do it. Women’s participation in breast and cervical screening is, instead, very high (>70%). The aim of our study was to investigate the beliefs, the feelings and the psychological factors that could influence the participation of women in CRC screening. Methods.We conducted a cross sectional study, in the Hospital of Siena, Central Italy, in 2011. We administered a questionnaire to 507 women of all ages, who attended mammography or clinical breast examination. The adherence to CRC screening was analyzed only in the group of 207 older women (age >50 years). We performed descriptive, bivariate and logistic regression analysis to identify whether an association was present between participant characteristics, willingness and adherence to screening. Results. Family history of colorectal cancer (OR 4.3; p= 80

137 (66.2) 53 (25.6) 15 (7.3) 2 (0.9)

Primary school Middle school High school Graduated

18 (8.7) 42 (20.3) 89 (43) 58 (28)

Married Unmarried Divorced Widowed

166 (80.2) 10 (4.8) 11 (5.3) 20 (9.7)

Educational Level

Marital status

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Table 2 - Number of women participating in thescreenings Age 50-59 60-69 70-79 >80 TOT

Pap test N (%) 126 (69.6) 42(23.2) 12 (6.6) 1 (0.6) 181/207 (87.4)

Mammography N (%) 129 (66.9) 49(25.4) 13(6.7) 2 (1.0) 193/207 (93.2)

193 women (93.2%) believed that colorectal cancer could be prevented, with no association between those who underwent some screening and those who did not. 98.5% of the women affirmed to be informed about health problems. The GPs resulted to be the primary source of information (162), followed by magazines (62) Internet (50), TV (57) and friends (24). Almost 2/3 of women (70.5%) knew that the screening program was offered by Region Tuscany; 71.9% of women who participated in he screening for colorectal cancer referred to know this possibility offered by the Region, while the percentage dropped to 58% among those who had never performed the screening. Knowledge of the three screenings is associated with the participation in that for CRC. However, only 48 women (23%) quoted exactly the three screenings offered by the Region. Respondents (86.5%) believed to be at greater risk of developing breast cancer than colorectal cancer. 71.5 % of women believed that cancer of the uterus is more common than the colorectal cancer. Among the risk factors for colorectal cancer, nutrition is indicated at the first place followed by familiarity. The majority of respondents believed that the most common age for developing colorectal cancer is over 50 years and the most important symptom is the presence of blood in the stools.65.7 % of women believed that colonoscopy is more “annoying” than a

FOBT N (%) 62 (62) 31(31.0) 6(6.0) 1(1.0) 100/207 (48.3)

Colonoscopy N (%) 52(56.5) 30(32.6) 10 (10.9) 0 (0) 92/207 (44.4)

mammogram and 42% of women believed that colonoscopy is more embarrassing than Pap test. Fear, embarrassment, anxiety, fear of cancer and preparation for the exam are the reasons that they gave to define “annoying” this kind of screening; among those who have done the screening, preparation is considered the most important reason.Colonoscopy caused anxiety in 158 participants. Most women believed that the colonoscopy would be less embarrassing if the endoscopist was a woman. Family history of colorectal cancer resulted associated with screening compliance (OR 2.72 p = 0.0087) and also with age (OR 1.04, p = 0.0338).The GPs’advice was significantly associated with adherence to colorectal cancer screening (OR: 4.6; p50 performed at least one Pap test in a lifetime, while only 48% a FOBT).The reasons for a lower response to FOBT (non-invasive and a source of less anxiety) are very different. FOBT takes longer time than a Pap test or a mammogram because it consists of two steps (pick up and delivery of the tube). The greater time is not the only reason; in fact, other studies (9) showed that the risk of CRC is largely underestimated by women. According to other studies (11, 17, 18), screening is considered by women as a useful tool to reduce the risk of CRC and the knowledge of the screening methods seems to positively influence the participation in prevention programs. This aspect should be better developed in Italy to improve the adherence rate. Weinberg (19), in a study conducted in the U.S. on women who were visited by a gynecologist stated that a correct knowledge about colorectal cancer, about the screening methods, are not accompanied by attitudes towards screening. One of the most common wrong answer is related to the incidence of CRC in their sex (20). Almost a quarter of women believed, in fact, that the cancer is not preventable.

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In our study, over 90% of women considered the CRC a preventable cancer, but the percentage of those who considered themselves at risk of becoming affected is around 20%, with a small gap between those who practiced the prevention and those who did not. A study by Kim (21) confirmed that the perception of risk influences attitudes towards screening for CRC, but also underlined that this perception acted differently on women of different ethnic groups, and attributed it to an unequal access to health information (20). The hypothesis that the misinformation plays a key role seems to be confirmed by the high proportion of women(more than 95%) referring to be informed about their health. Being aware of a positive family history of CRC is accompanied by a greater adherence to CRC screening, as confirmed by other authors (22) but, in its absence, women tend to underestimate the risk of becoming affected by CRC. Study participants knewthat the age is a risk factor for the development of CRC but only one woman in five believed that the CRCcould occur also in young people (before 40 years) and 1 out of 3 believed that, after the age of 70, the incidence decreases. This could be due to the knowledge that the screening campaigns are addressed to people between 50 and 70 years.When not aware of that, women can be brought to believe that the NHS has selected this age group because this is the only one affected by CRC. The excess of attention to the sexualreproductive health is the basis for the so-called “bikini syndrome”, that limits the focus on women’s health to the reproductive diseases. In fact socio-cultural and mediatic influences created an overestimation of the risk of getting a carcinoma of the uterus (a cancer relatively rare in our reality). Less than half of the women in our study believed that the CRC is frequent and is common in women, and over 70% of them placed cancers of the uterus to a secondary

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place for epidemiological importance in the female population, after breast cancer. Sach and Whynes (23) in a British study designed to assess views about cancer in both sexes, said that women were less likely to underestimate overall cancer incidence. Their conclusion was that it is important to understand the knowledge and perceptions of cancer by men and women, in order to allocate more efficiently the resources for an effective health promotion. One effect of bad publicity campaigns about cancer may be an overestimation of the risk of getting cancer. In fact, our interviews showed that almost all women indicated cancer as a leading cause of death in women over 55 and not, as it is true, cardiovascular diseases. Finally, more than 50% of them said they did not know any of the screening methods offered for CRC. An interesting phenomenon, observed by other studies (18, 24, 25), is that the main source of information about health are the GPs, who positively affected the adhesion to screening (26-28). However, the GPsare not inclined to encourage women to prevent the CRC which is often less recommended than screening for breast cancer in women of the eligible age (respectively 46.75% and 77.12%). Our data, however, appear to be optimistic when compared to that of the Passi study (10), according to which only 23% of the population accepting the screening was advised by a GP or by a healthcare professional. The same study underlined that FOBT was completed,as recommended, by 75% of those who received the invitation letter associated with the doctor’s advice, as opposed to the scant 4% of those who were not reached by any promotion. Stockwell also (29), who collected data in five health centers in the Boston area, concluded that the lack of a recommendation by the GPs is the main reason for which women did not participate in the screening for CRC. Other authors confirmed that an ineffective communication between GPs and patients is

Factors influencing participation in colorectal cancer screening

the major obstacle for the participation in screenings (30). Conversely, according to a study conducted in a population of Central Italy, women are informed primarily by friends and TV, and only a small percentage by the GPs. In fact, the media (magazines, TV and internet) are also widely consulted by our women, but it must be considered that over the past 9 years, the Ministry of Health did not promote any campaign for the prevention of the CRC. The data of the National Screening showed that the response of women to the invitation to FOBT screening was higher than that of men, even if limited to the age group between 55 and 69 years. In the case of FOBT positivity, colonoscopy is practiced more often by men, respectively 83.3% vs 81.6%. We have not investigated how many women, once got a positive FOBT response, have accepted a colonoscopy. Women reported a greater embarrassment to accept a colonoscopy compared to a Pap test. However, almost half of our sample considered the colonoscopy as “embarrassing” and that it can cause feelings such as fear / pain, anxiety and embarrassment. These negative feelings are more frequent in those who have never done it and it is quoted by other papers (28) as one of the motivations of the women who refused to practice it. Over 40% of our sample referred that they would feel less embarrassed if colonoscopy was performed by a person of their sex and this could be used to motivate women to take the exam. A study (30) showed that women who were offered the opportunity to choose the gender of the endoscopist are not more likely to undergo the examination then those who were not offered that option. Other studies (29) confirmed our data: 3048% of women, particularly those who work and have a woman GP, prefer a female endoscopist (31-34) and the possibility to choose the gender of the endoscopist promotes adherence to screening (35).

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In our study, unlike others, the adhesion to screening for CRC was not related to the marital status or to the education level (31, 36).

Conclusions Embarrassment, pain and the GP’s advice are the factors that correlated more strongly with adherence to CRC screening. This observation could be usefully applied to implement information campaigns about CRC for the population, especially for women, and to organize refresher courses for GPs, in order to improve the adherence rate to the screening program. It could also be interesting to evaluate the effectiveness in improving the adherence of the distribution of the kit for the collection of fecal occult blood before mammography or gynecological examination. Study limitations and strengths It should be noted that almost all of our participants had a high level of education and were married. The relatively young age of the participants and the location of the survey (a center dedicated to the prevention of cancer) could represent a limit in our study. Funding statements The authors declare that there is no conflict of interest. Acknowledgments I had full access to all the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis.

Riassunto I fattori che possono influenzare la partecipazione ai programmi di screening del carcinoma del colon retto: uno studio italiano Introduzione. Nel mondo il cancro del colon-retto (CRC) rappresenta la seconda neoplasia più comune nelle donne. La partecipazione delle donne allo screening per il carcinoma della mammella e della cervice uterina è alta

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mentre per quanto riguarda il CRC l’adesione al sangue occulto nelle feci risulta essere molto bassa (50% in Italia, inferiore però nelle donne). Lo scopo dello studio è quello di indagare le conoscenze, le opinioni e i fattori psicologici che possono influenzare la partecipazione delle donne allo screening per il CRC. Metodi. Abbiamo effettuato uno studio trasversale nell’Ospedale di Siena, Italia, nel 2011.distribuito Abbiamo somministrato un questionario a 507 donne, di tutte le età, in attesa di sottoporsi a mammografia e/o visita senologica. Per l’analisi dei risultati sono state considerate solo le donne con età uguale o superiore a 50 anni (n = 207). Per l’analisi abbiamo utilizzato un modello di analisi multivariata. Risultati. Una storia familiare di CRC è associata positivamente con l’adesione allo screening (colonscopia) (OR 4,3; p