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Research ArticleClinical Studies

Barriers to Organized Mammography Screening Programs in Hungary: A Questionnaire-based Study of 3,313 Women

MIHÁLY ÚJHELYI, DÁVID PUKANCSIK, PÉTER KELEMEN, ESZTER KOVÁCS, ISTVÁN KENESSEY, MIHÁLY BAK, MIKLÓS KÁSLER, TIBOR KOVÁCS and ZOLTÁN MÁTRAI
Anticancer Research March 2018, 38 (3) 1727-1734;
MIHÁLY ÚJHELYI
1Department of Breast and Sarcoma Surgery, National Institute of Oncology, Budapest, Hungary
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  • For correspondence: ujmisi@gmail.com
DÁVID PUKANCSIK
1Department of Breast and Sarcoma Surgery, National Institute of Oncology, Budapest, Hungary
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PÉTER KELEMEN
1Department of Breast and Sarcoma Surgery, National Institute of Oncology, Budapest, Hungary
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ESZTER KOVÁCS
2Department of Radiological Diagnostics, National Institute of Oncology, Budapest, Hungary
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ISTVÁN KENESSEY
3National Cancer Registry, National Institute of Oncology, Budapest, Hungary
4Second Department of Pathology, Semmelweis University, Budapest, Hungary
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MIHÁLY BAK
5Department of Cytopathology, National Institute of Oncology, Budapest, Hungary
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MIKLÓS KÁSLER
6National Institute of Oncology, Budapest, Hungary
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TIBOR KOVÁCS
7Breast Unit, Guy's Hospital, London, U.K.
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ZOLTÁN MÁTRAI
1Department of Breast and Sarcoma Surgery, National Institute of Oncology, Budapest, Hungary
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Abstract

Background/Aim: Despite well-organized Hungarian invitational mammography screening, participation rates have never reached 50%. This is similar to rates in Central Eastern Europe. In order to reduce breast cancer mortality, the participation rate should be at least 70%. This questionnaire-based study assessed the barriers associated with low adherence rates. Materials and Methods: Women 45-65 years of age were interviewed by questionnaire containing 15 structured questions focused on socioeconomic status and barriers to screening. Results: A total of 3,313 women completed the questionnaire. The main reasons for avoiding screening were work absenteeism (18.9%), fear of painful examination (18.39%), and poor understanding of mammography screening (14.94%). Conclusion: Education is required to increase awareness among women about the utility and availability of breast screening services. This report provides information on the appropriate level of intervention needed to increase screening participation in Hungary and other developing countries in Central Eastern Europe to reduce breast cancer-related mortality.

  • Breast neoplasms
  • mammography
  • mass screening
  • surveys and questionnaires

Breast cancer is one of the most prevalent malignancies and is the main cause of cancer death for women in the Western world (1). Most breast cancer deaths are caused by locally advanced or stage IV disease. Therefore, many countries have implemented organized mammography screening programs (OMSP) in order to detect breast cancer at an earlier stage and reduce breast cancer mortality (1-3). In January 2002, Hungary initiated a nationwide OMSP for women 45-65 years of age with a biannual screening interval (4). The efficacy of mammography screening in preventing breast cancer deaths has been shown in randomized controlled trials, with a reduction of mortality between 17% and 32% (5-9). However, some recent studies have questioned the efficacy of early-stage tumour detection in reducing mortality (10, 11). These authors believe that in advanced breast cancer effective adjuvant therapy may play a greater role in reducing breast cancer mortality than screening (12-14).

One of the most important roles of OMSP is to disclose breast tumours before they become palpable, during stage 0, thereby decreasing the percentage of advanced breast cancer cases and thus reducing breast cancer-related mortality (15-17).

The Hungarian National Cancer Registry recorded nearly 7,900 new cases of breast cancer in women, with more than 2,100 deaths in 2014. While not statistically significant, the incidence of breast cancer in Hungary has been increasing since the implementation of an OMSP, but the mortality has not changed measurably between 2002 and 2014 (18, 19) (Figure 1). According to the World Health Organization (WHO), the breast screening adherence rate should be at least 70% in order to reduce breast cancer mortality (20). Despite the fact that screening is invitational and free of charge, participation in the Hungarian OMSP has never reached 70%. The total screening and diagnostic coverage of mammography examinations was 53.46% from 2002 to 2003, 50.8% from 2004 to 2005, 49.7% from 2006 to 2007 and 50.1% from 2008 to 2009. Thus, participation in the Hungarian OMSP program did not change considerably between 2002 and 2009 (21-23).

The association between marital status, education level, socioeconomic characteristics, knowledge, and beliefs about breast cancer and mammography screening have not been properly analysed to date. There is an urgent public health need to explore the barriers to the OMSP (24). It is important to have a validated instrument to answer this question. The current study examined the factors associated with women's screening behaviour, beliefs, and barriers based on interviews of the target population via questionnaire to assess and report on the psychometric and demographic properties of the barriers leading to low adherence rates in the Hungarian OMSP. Our goal was to acquire information on the appropriate level of intervention necessary to increase screening participation.

Figure 1.
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Figure 1.

Breast cancer incidence and mortality per 100,000 women in Hungary between 2001 and 2014 (19).

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Table I.

Breast cancer screening programs in 2010 and last update: coverage by test, coverage by invitation, participation rate in Austria, Bulgaria, Latvia, Poland, the Czech Republic and Hungary (22, 26).

Neighbouring Central Eastern European countries such as Poland, the Czech Republic, Bulgaria, Austria and Latvia have similar economies and living standards, and also present low breast screening coverage rates comparable to those in Hungary (25, 26) (Table I).

Increased knowledge regarding the barriers to mammography screening may provide information to extend our knowledge of breast cancer screening and effective treatment in Hungary and above mentioned Central-Eastern European countries.

Materials and Methods

This study was performed in accordance with the Research Ethics Committee of the National Institute of Oncology which conforms to the provisions of the Declaration of Helsinki. The study was performed without additional financial support at the National Institute of Oncology in Budapest between 2015 and 2016. The study received non-financial administrative support from the Hungarian AVON Cosmetics Company and the Mellrákinfó advocacy group.

A cross-sectional survey was designed to examine women's screening behaviour, beliefs, and barriers to OMSP. The Hungarian breast screening target population of women 45-65 years of age were interviewed anonymously using web-based and printed questionnaires containing 15 structured questions. The questionnaire was designed to assess and report on the psychometric and demographic properties of barriers leading to low participation rates (Table II). The 15-item questionnaire was composed of four sections. The first five questions focused on education level, marital status, residence (capital, provincial town, or village) and county of residence. Three questions focused on mammography receptive behaviour, five questions directly addressed OMSP (receiving invitation letter, participation frequency in mammography screening, distance from screening centre), and two questions focused on barriers that prevented women from attending the screening program.

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Table II.

Questionnaire containing 15 structured questions given to women aged 45-65 years regarding their participation in national organized mammography screening programs in Hungary.

The sample population was reached via e-mail and Facebook campaign through web-based questionnaires by the Hungarian AVON Cosmetics Company. The questionnaire link was secured by Hypertext Transfer Protocol Secure system. The survey's web-based link was sent to the e-mail contact list and Facebook followers of the Hungarian AVON Cosmetics Company. Printed forms were sent by mail and distributed at local social functions by the Mellrákinfó advocacy group and Hungarian AVON Cosmetics Company. Hungarian AVON used its own contacts to reach the target population.

To ensure that the study sample was representative of the screening population, only surveys from women 45-65 years of age were accepted. Answering the survey questions was voluntary and anonymous. The data protection law was followed and respected. Questionnaires with unreadable or unclear answers were excluded from the analysis.

All answers were statistically analysed in the context of marital status, educational level, and type of residence using chi-square test; p-values of less then 0.05 were considered to be significant. Statistical analysis was performed using PAST 1.86 and Statistica 12.0 (StatSoft, Tulsa, OK, USA) (27).

Results

A total of 58,839 questionnaire links were sent via e-mail, 21,501 links were sent by Facebook campaign, 500 printed questionnaires were mailed, and 293 questionnaires were completed at social events. A total of 12,345 links were opened via e-mail and 5,739 links were opened via Facebook. Overall, 1,774 women 45-65 years of age completed the survey by e-mail, 1,262 on Facebook, 76 forms by mail and 201 at social events. The online response rate was 18.32% and 15.2% for mailed forms. A total of 3,313 women between 45 and 65 years of age completed the questionnaire.

The demographic characteristics of the respondents are summarized in Table III. The majority of responders were married, had completed secondary school or lived in provincial towns.

Descriptive statistical analysis of the answers for structured questions (Q6-Q14) of the questionnaire is shown in Table IV. The questions that focused on barriers to participating were also systematically analysed. A total of 1,042 women responded to the questions regarding their reasons for not undergoing breast screening. Briefly, the main barriers to participation in the OMSP were work absenteeism (18.9%), fear of painful examination (18.39%) and false beliefs regarding mammography screening (14.94%). Of survey respondents, 13.92% of those who did not attend the OMSP underwent opportunistic screenings; 11.11% answered that their designated screening centre (DSC) was too far from their home. Only 5.49% of those who did not participate in screening reported not having enough information on mammography screening and 4.85% answered that it was too expensive to get to the screening centre. Fear of breast cancer diagnosis prevented 3.58% of non-participants from attending the OMSP, and 2.04% did not participate for fear of mastectomy.

Based on patient marital status and place of residence, the responses were analysed to compare a number of criteria. (Table V) There was a significant association (p=0.029) between the responders' marital status and OMSP attendance, with married women attending breast screenings more frequently than single women. There was also a significant difference (p=0.038) between the place of residence and the frequency of mammography examination: women from the capital or from provincial towns more frequently underwent and were more compliant with screening than women who lived in villages. There was a significant association between the responders' residence and the distance from the DSC (p<0.0001): women living in the capital or provincial towns had better access to their DSC than those living in villages.

There was a significant association between the place of residence and the travel expenses incurred to reach the DSC (p=0.009) (Table VI). Compared to those living in the capital, women in rural populations reported financial difficulties in traveling to their DSC. Female residents of the capital were more likely to choose opportunistic screening compared to those living in rural areas (p=0.005). Barriers such as lack of information on mammography screening (p=0.001) and fear of breast loss (p=0.003) were also significantly associated with lower education level. Educated women were less likely to fear breast cancer and more likely to have sufficient information regarding mammography screening compared to interviewed women with lower levels of education. In the current study, married marital status appeared to be a protective factor against barriers such as feeling embarrassed about the examination (p=0.0002) and expenses incurred to reach the DSC (p<0.0001).

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Table III.

Responders' demographic characteristics (by response to questions 2, 3, and 5 of the questionnaire, Table II) (n=3,313).

Discussion

To improve breast cancer screening attendance among Hungarian women, it is imperative to have a valid instrument for exploring and understanding the factors associated with their screening behaviour. Our questionnaire has the appropriate psychometric properties to provide insights into tailor-made strategies designed to address the needs of the screening target population.

Our findings highlight that the main reasons for not attending the OMSP were work absenteeism, fear of pain associated with the examination, and false beliefs regarding mammography screenings. To reduce barriers such as work absenteeism, a paid day off might increase women's willingness to participate in the OMSP. It would be important for employers also to participate in helping their employees utilize preventative measures.

The results of our questionnaire study show that women with lower levels of education were less likely to have adequate information on breast screening, and were more likely to fear mastectomy compared to women with higher levels of education. There is a need for a multi-pronged strategy to inform and educate women about breast awareness and bring about a behavioural change. It may be beneficial to provide more information about breast cancer, breast cancer treatment, and the importance of mammography screening through health awareness education in primary school or through alternative information channels such as magazines, TV advertisements, online sites and brochures. Other authors with similar findings came to the same conclusion (28).

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Table IV.

Descriptive statistical analysis of the responses to structured questions (Q6-Q14) of the questionnaire (Table II).

Fear of pain in the examination was the second most common reason for avoiding mammography examinations. According to a previous study, discomfort was reduced when women were provided with written or verbal information, and when a breast cushion was used (29). Providing verbal or written information, as well as supporting women during the examination, is a simple and easily achievable intervention and can help to reduce pain during screening mammography. Use of alternative breast compression strategies or premedication with acetaminophen has not been reported to significantly reduce breast pain and discomfort (29).

It is important to note that half of responders in the current study chose opportunistic screening and that 13.92% of non-participants chose a location other than their DSC for their mammography examinations. This finding is consistent with reports that opportunistic screening only covers half of the screened target population in Hungary (21-23). The non-participants described other barriers such as long waiting times in clinics, unorganized DSCs, dissatisfaction with facility staff, difficulties in changing scheduled mammogram appointments, and a lack of concern about breast cancer. To increase screening attendance rates, these barriers should also be addressed. The environment and facility staff are important for women's satisfaction and their willingness to attend their next screening. Similar barriers and suggestions have been described in other studies (30-33). A patient navigator system could utilize prevention nurses to organize an effective screening program by offering education on breast awareness, screening invitation, and management of biennial mammogram appointments (34).

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Table V.

Significant associations between patient marital status, residence, and responses to the questionnaire (by response to questions 3, 5-8, and 13, Table II).

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Table VI.

Statistical analysis of significant barriers to undergoing mammography screening associated with socioeconomic status (answer to question 14: Why did you not undergo organized mammography screening?).

Only two-thirds of responders had received an Invitation Letter for Screening (ILS) in the previous 2 years, which is below the minimum 70% adherence rate required by the WHO to reduce breast cancer mortality (20). Further investigations are needed to determine the causes for the lack of receipt of ILS.

In our study, the fear of breast cancer and fear of mastectomy among non-participants emphasizes the barriers to participating in the OMSP. This finding is similar to a previous study where cancer anxiety and worry were associated with avoidance of breast cancer screening (35).

Married status appeared to be a protective factor against barriers, including embarrassment regarding the examination, financial challenges associated with travelling to the DSC and avoiding breast screening. Single women, mainly widows, were more likely to skip or were less likely to participate in the OMSP compared to married women. There is strong positive association between relationship and participation behaviour in mammography screening, which is also supported by other authors (36). Single women require special attention to inform them about the importance of breast screening, which could be addressed through well-organized patient navigation programs, as well as breast cancer support groups and self-help organizations.

In subjective response to the question “How far is the designated screening centre from your residence?”, one-quarter of women answered far, while fewer than 2% answered very far. Excessive distance to reach the DSC was the fifth most frequent barrier to breast screening. Statistical comparative analyses indicated that living in villages or in single households were associated with lower participation rates because of financial difficulties and problems in travelling long distances to the DSC. Others concluded similarly that women living in rural areas were less likely to participate in OMSPs compared with those living in urban areas (37). According to a previous interview-based survey, time required to travel to and distance from the DSC are important factors for women (38). Well-situated units with advanced promotion about public transportation and parking facilities may encourage greater uptake. Rural women require special attention because of their lower participation rates in mammography examination. Patient navigation, free public transport for the day of screening, specialized round-trip bus lines, or mobile breast screening units may help to overcome these barriers.

In conclusion, our findings highlight that the main reasons for women to avoid participation in OMSP included work absenteeism, fear of painful examination, lack of adequate information, and false beliefs about mammography screenings.

Acknowledgements

The Authors thank the Hungarian Avon Cosmetics Company and Mellrákinfó for providing non-financial administrative support for this study. We express special thanks to Professor Dr. Joseph Molnar from the University of Szeged, Faculty of Medicine for critical review of the article.

Footnotes

  • Conflicts of Interest

    The Authors received non-financial administrative support from the Hungarian Avon Cosmetics Company and Mellrákinfó advocacy group.

  • Financial Support

    The study was performed without additional financial support at the National Institute of Oncology in Budapest.

  • Received October 24, 2017.
  • Revision received November 9, 2017.
  • Accepted November 10, 2017.
  • Copyright© 2018, International Institute of Anticancer Research (Dr. George J. Delinasios), All rights reserved

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Anticancer Research: 38 (3)
Anticancer Research
Vol. 38, Issue 3
March 2018
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Barriers to Organized Mammography Screening Programs in Hungary: A Questionnaire-based Study of 3,313 Women
MIHÁLY ÚJHELYI, DÁVID PUKANCSIK, PÉTER KELEMEN, ESZTER KOVÁCS, ISTVÁN KENESSEY, MIHÁLY BAK, MIKLÓS KÁSLER, TIBOR KOVÁCS, ZOLTÁN MÁTRAI
Anticancer Research Mar 2018, 38 (3) 1727-1734;

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Barriers to Organized Mammography Screening Programs in Hungary: A Questionnaire-based Study of 3,313 Women
MIHÁLY ÚJHELYI, DÁVID PUKANCSIK, PÉTER KELEMEN, ESZTER KOVÁCS, ISTVÁN KENESSEY, MIHÁLY BAK, MIKLÓS KÁSLER, TIBOR KOVÁCS, ZOLTÁN MÁTRAI
Anticancer Research Mar 2018, 38 (3) 1727-1734;
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