Barriers to the Cervical Cancer Screening in the Northern Slovakia

A barrier to screening is a specic attitude, opinion or state that prevents the patient from seeking preventive care. The aim of this study was to identify and compare barriers to cervical cancer screening (CCS) in Northern Slovakia between women seeking and not seeking CCS. Data collection was performed in twenty gynaecological departments, each department sending data from ve healthy women and ve untreated women with cervical cancer. Women completed a validated and standardized questionnaire with 28 statements (the CPC-28 questionnaire: “Creencias, Papanicolaou, Cancer-28” questionaire – Beliefs about Papanicolaou and Cervical Cancer). A four-point Likert scale (item score from 1 to 4) was used to assess responses. A linear transformation was made to calculate the responses. Differences with a p value of < 0.05 were considered statistically signicant. From the 200 questionnaires, 135 (67.5%) participants were divided into the women seeking CCS (n = 97) and the women not seeking CCS (n = 38). The women not seeking CCS vs seeking CCS had higher barriers according to the CPC-28 domain one (median; interquartile range: 33.33; 28.70-40.74 vs 14.82; 7.41–29.63; p < 0.001). The risk of not seeking CCS was statistically signicant in non-working (OR; 95% CI: 2.458; 1.127–5.358; p < 0.024), non-childbearing women (OR; 95% CI: 3.302; 1.421–7.671; p < 0.006) and women without cervical cancer (OR; 95% CI: 4.709; 1.960-11.317; p < 0.001). 7.1.5 and Statistica 13. The data from the introductory part of the questionnaire (demography, gynaecological history, risk factors) were analysed by using descriptive statistics. Chi-square test, non-parametric tests (Mann–Whitney U test) and Odds ratio were used for statistical signicance rating. Differences with a p value of < 0.05 were considered statistically signicant. examinations and screening programmes. Our results were realized by a standardized and validated CPC-28 questionnaire. Comparing our results with those of other countries will help to understand the barriers to cervical cancer screening. When comparing our results with the results of studies in other countries it is important to understand the different socio-economic and cultural conditions, the demographic characteristics of women’s populations, the various methodologies applied and the target groups of women in the research. The limitation of our study is in the local evaluation of the women’s population. On the other hand, it is positive that the issues related to cervical cancer screening are studied and compared globally. The results of such studies may contribute to a better understanding of the reasons why people do not care about their health as they could.


Abstract
Background A barrier to screening is a speci c attitude, opinion or state that prevents the patient from seeking preventive care. The aim of this study was to identify and compare barriers to cervical cancer screening (CCS) in Northern Slovakia between women seeking and not seeking CCS.

Methods
Data collection was performed in twenty gynaecological departments, each department sending data from ve healthy women and ve untreated women with cervical cancer. Women completed a validated and standardized questionnaire with 28 statements (the CPC-28 questionnaire: "Creencias, Papanicolaou, Cancer-28" questionaire -Beliefs about Papanicolaou and Cervical Cancer). A four-point Likert scale (item score from 1 to 4) was used to assess responses. A linear transformation was made to calculate the responses. Differences with a p value of < 0.05 were considered statistically signi cant.

Conclusion
We identi ed barriers to cervical cancer screening in both of our groups but the results were more frequent and statistically signi cant in the women not seeking CCS.

Background
Slovakia is a country in Middle Europe belonging to a group of developed countries with well-organized healthcare systems that include free preventive gynaecological examinations with cervical cancer screening. On average, 650 new cervical cancer cases occur in Slovakia each year, especially among women of productive age [1]. According to available data from health insurance companies, only 46% of women participate in preventive gynaecological examinations. In comparison with other countries this is a very low percentage [2]. Therefore, it is necessary to understand and de ne the reasons why women do not attend preventive gynaecological check-ups. A barrier to screening is a speci c attitude, opinion or state that prevents the patient from seeking preventive care. In general, barriers are divided into two groups: barriers to screening caused by healthcare system disorganization and barriers from the patient's perspective. In Slovakia we have not found any studies aimed at the identi cation of barriers to cervical cancer prevention. In countries with much higher cervical cancer screening utilization (US, Sweden, Norway, Italy) many scienti c studies are aimed at a better understanding of the barriers among women who do not participate in the preventive programme [3]. Irregular or no participation in the screening examination is connected to the diagnosis of cervical intraepithelial lesions in advanced stages. Non-participation in the screening programme is considered to be one of the risk factors for further development of cervical cancer [4][5][6].
The aim of this study The aim of this study was to identify and compare barriers to cervical cancer screening (CCS) in Northern Slovakia between women seeking and not seeking CCS.

Questionnaire
A validated and standardized questionnaire was used as the instrument for data collection: the CPC-28 questionnaire ("Creencias, Papanicolaou, Cancer-28" questionnaire -Beliefs about Papanicolaou and Cervical Cancer). The source was an original questionnaire developed and validated in 2009 (Cronbach's α = 0.735) [7, Additional le 1]. We translated and validated the CPC-28 questionnaire into the Slovak language (Cronbach's α > 0.8 in all six domains) [8]. In the introductory part, the questions are aimed at demographic indicators, gynaecological history and the presence or absence of chronic diseases and other cervical cancer risk factors [5].
The CPC-28 questionnaire consists of 28 statements [7,8]. Women indicate one of the four alternatives provided to show whether they agree or disagree with the given sentence. The statements are divided into six domains (Domain 1: Barriers to have a Pap test; Domain 2: Cues to action to have a Pap test; Domain 3: Severity of cervical cancer; Domain 4: Need to have a Pap test; Domain 5: Susceptibility to cervical cancer; Domain 6: Bene t to have a Pap test); nine questions aimed at the barriers to cervical cancer screening in Domain 1 ( Table 1). Labelling of the statements in this article comes from the order in the original version of the questionnaire. In the case of agreement with the given sentence, a barrier is present. A four-point Likert scale was used to assess responses (1: Strongly agree, 2: Agree, 3: Disagree, 4: Strongly disagree). To each answer the corresponding item score was added. A linear transformation was made to calculate the responses for range 0-100 according to the formula adjusted to each domain. The higher the score on the scale from 0-100, the stronger is barrier. Table 1 The statements in CPC-28 a aimed at the identi cation of cervical cancer screening barriers -Domain 1 b   Cervical cancer screening barriers were investigated in Domain 1. The statistically signi cant differences between the women not seeking and seeking CCS were found in all items of Domain 1 (Table 4). The risk of not seeking CCS was statistically signi cant in the non-working, non-childbearing women and the women without cervical cancer. Education, smoking, hormonal contraception, and chronic diseases also increased the risks of not seeking CCS but were not statistically signi cant. This indicates the in uence of risk factors that limit seeking CCS (Table 5).

Discussion
Barriers to cervical cancer screening among the female population exist in both developing and developed countries. Numerous scienti c studies all over the world have been conducted to de ne the reasons for low participation of women in preventive gynaecological programmes. Current articles show that the women's reasons for non-attendance at screening are diverse [9][10][11][12][13]. The barriers to cervical cancer screening, according to the results of numerous studies, can be divided into ve main groups: informational; psychological; socio-economic; behavioural and cultural; and geographical. The boundaries between the groups of barriers are blurred and overlap each other. Reasons why women do not participate in screening are subjective and therefore di cult to clearly describe and de ne [14][15][16].
The CP-28 questionnaire focuses on barriers to seeking CCS. In all items of domain one, we found higher scores in the women not seeking CCS. The results were statistically signi cant. There was an interesting study in which the authors addressed the question of cervical cancer screening utilization among women living in England (London), who were originally from Slovakia, Poland and Romania. Women were informed about cervical cancer screening but they did not understand its importance for their health. They said they were positively motivated by invitation letters and reminders however but did not know how often the Pap test was performed and at what age it was necessary to undergo it for the rst time [17].
A study conducted in Germany and Norway found that married women, mothers and non-smokers underwent the Pap test more often than unmarried women.
In these countries, women receive a reminder every three years to undergo a screening. Women who underwent the screening had better knowledge about its frequency and screening attendance increased with age [18].
In our research, 38.7% of women did not have enough information about the age for a Pap test (item A4). 36.1% subjects in the women seeking CCS and 39.4% subjects in the women not seeking CCS did not have knowledge about the frequency of cervical cancer screening.
Long waiting times for the check-up (item A5) were considered to be a barrier for 21.1% of the women not seeking CCS, with a statistically signi cant difference in relation to the second group where this barrier was present in only 7.3% of women. Compared with studies from other countries, we have found more time-related barriers in Slovakia. In Poland, research was carried out at secondary schools and universities in Krakow that involved 400 women aged 17-26 years; overall, 11.2% of women perceived screening as time-consuming [19]. Authors from Estonia published the results of a study involving 1054 women where long waiting times were considered a barrier in 12.9% of women [20].
Inadequate behaviour of healthcare workers (item A3) was a statistically signi cant stronger barrier present in 2.6% of the women not seeking CCS vs 1.0% of women seeking CCS. Women in England described disappointment with the doctor's approach and felt better if they perceived empathy and a more sensitive attitude [21]. Compared to other countries, our research found far weaker barriers related to inadequate or inappropriate behaviour of medical staff and healthcare workers (doctors or nurses).
Fear of positive cervical cancer diagnosis (item A7) was seen as a barrier in 2.1% of the women seeking CCS vs 0.0% of the women not seeking CCS. Embarrassment at undergoing a gynaecological examination (item A9) was present in 5.2% of the women seeking CCS 2.6% of the women not seeking CCS.
In the Danish study, embarrassment (16.6%) and fear and anxiety (8.4%) decreased with age. An unpleasant experience from previous genital examinations increased with age. Pregnancy, breastfeeding or infertility treatment was a reason for not participating in screening. Interestingly, 0.7% of women do not participate in screening purely on principle, through their own convictions, without specifying further reasons. However, Denmark is one of several countries where experience has con rmed that invitations directly from a doctor lead to a slight increase in screening participation and willingness to undergo the Pap test [22].
In the women seeking CCS and the women not seeking CCS 7.2% and 13.1% of women, respectively, did not have enough time to undergo cervical cancer screening (item A2). Opening hours of healthcare or gynaecological centres were not compliant with women's time management (item A8) in 2.0% and 10.5% of the women seeking CCS and not seeking CCS, respectively. In Estonia, unsatisfactory opening hours (11.8%) were more often expressed as a barrier than in Slovakia [20].
Problems with getting an appointment for the preventive gynaecological screening (item A11) were expressed as a barrier in 5.1% and 13.1% of the women seeking CCS and not seeking CCS, respectively. In Denmark, 32.3% of the 9484 women participating in the study reported organizational barriers as the main reason for not participating in regular screening. Most often they had forgotten to keep an appointment. Other problems with appointments were seen in 9.8% of women [22]. In healthcare systems where it is necessary to make an appointment for an examination, appointment di culties can pose a signi cant barrier to cervical cancer screening.
The psychological barriers involved in the CPC-28 questionnaire include the fear of positive examination results and embarrassment. In Chile, 127 women diagnosed with cervical cancer were involved in the study. This group of women is much more sensitive to cervical cancer-related issues and barriers to cervical cancer screening were found in 38%: including embarrassment (50%), inadequate behaviour of healthcare workers and a negative experience from previous examinations preventing their return. Time-related problems, fear of diagnosis and lack of knowledge about the preventive effect of the Pap test were expressed as other barriers [23,24]. There is a lack of randomised controlled trials designed to speci cally address falling cervical screening uptake in amongst young women [25]. Educating women about barriers and training the health-care professionals can facilitate an effective dialogue between two groups [26,27].

Strengths and limitations
This research is the rst of its kind in Slovakia and can serve as a source for similar research in relation to other preventive examinations and screening programmes. Our results were realized by a standardized and validated CPC-28 questionnaire. Comparing our results with those of other countries will help to understand the barriers to cervical cancer screening. When comparing our results with the results of studies in other countries it is important to understand the different socio-economic and cultural conditions, the demographic characteristics of women's populations, the various methodologies applied and the target groups of women in the research. The limitation of our study is in the local evaluation of the women's population. On the other hand, it is positive that the issues related to cervical cancer screening are studied and compared globally. The results of such studies may contribute to a better understanding of the reasons why people do not care about their health as they could.

Figure 1
Study ow chart

Supplementary Files
This is a list of supplementary les associated with this preprint. Click to download. CPC28questionnaire.docx