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The Impact of Education About Cervical Cancer and Human Papillomavirus on Women's Healthy Lifestyle Behaviors and Beliefs

Using the PRECEDE Educational Model

Koç, Zeliha, PhD, RN; Özdeş, Emel Kurtoğlu, MD; Topatan, Serap, PhD, RN; Çinarli, Tuğba, MSc, RN; Şener, Asuman, MSc, RN; Danaci, Esra, MSc, RN; Palazoğlu, Cansu Atmaca, MSc, RN

doi: 10.1097/NCC.0000000000000570
ARTICLES
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Background Early detection of cervical cancer improves the chances of successful treatment.

Objective The aim of this study was to determine the effect of education about cervical cancer and human papillomavirus on the healthy lifestyle, behavior, and beliefs of Turkish women who were without cancer, using the PRECEDE education model.

Methods This qualitative and quantitative study was conducted as a prospective, randomized, 2-group (intervention and control) trial at a community training center in north Turkey. A total of 156 Turkish women who were without cancer participated in this study. The semistructured interview form, the SF-36 Health Status Questionnaire, the Health Belief Model Scale for Cervical Cancer and Pap Smear Test, and the Healthy Lifestyle Behavior Scale II were used.

Results The subdimension scores of the Health Belief Model Scale for Cervical Cancer and Pap Smear Test were found to be higher among women in the study group (cervical cancer seriousness, P = .001; health motivation, P = .001) as compared with the control group after the education program. The SF-36 Health Status Questionnaire domain scores for physical role limitations, mental role limitations, and general health perceptions increased in the study group after the intervention.

Conclusion The posteducation health motivation of women in the study group was improved, the women's perceptions of obstacles to Papanicolaou testing decreased, and through increased knowledge and awareness, the rate of Papanicolaou testing increased.

Implications for Practice Educational programs aimed at motivating women to increase their awareness of cervical cancer, preventing cervical cancer, and having Papanicolaou testing are necessary and beneficial in this sample.

Author Affiliations: Health Science Faculty, Department of Nursing (Dr Koç); Medicine Faculty, Department of Obstetric Gynecology (Mrs Özdeş); Health Science Faculty, Department of Midwifery (Dr Topatan); and Health Services Vocational School (Mrs Çinarli and Dr Şener), Ondokuz Mayis University, Samsun; Ahmet Erdoğan Health Services Vocational School, Bülent Ecevit University, Zonguldak (Mrs Danaci); and Health Services Vocational School, Gümüşhane University (Mrs Palazoğlu), Turkey.

This project, no. 214S560, was supported by TÜBİTAK.

The authors have no conflicts of interest to disclose.

Correspondence: Zeliha Koç, PhD, Samsun Health Science Faculty, Department of Nursing, Ondokuz Mayis University, University Campus, 55139 Samsun, Turkey (zelihaceren@hotmail.com).

Author Contributions: All the authors contributed to the study design, data analysis, and manuscript preparation.

Accepted for publication September 15, 2017.

Cervical cancer is a significant health problem in developing countries. According to the International Cancer Research Agency, cervical cancer is the second most frequent cancer among women between the ages of 15 and 44 years, and approximately 500 000 new cases are detected each year.1 In Turkey, cervical cancer is the third most common genital cancer, with an estimated incidence rate of 7.1 in 2011.2

Cervical cancer is a preventable disease; moreover, early cervical cancer is often treatable. In the past 30 years, the rate of cervical cancer has declined in most developed countries as a result of screening programs; however, it has increased or remained the same in most developing countries.1 There are various risk factors for cervical cancer, including human papillomavirus (HPV) infection, early age of the first sexual intercourse, multiple sexual partners, sexually transmitted infections, a family history of cancer, smoking, immune system suppression, malnutrition, number of children, and the use of oral contraceptives.3–5

Women may not consider cervical cancer to be a health risk. However, they are at risk if they are infected with HPV.6 Human papillomavirus is transmitted through genital contact, especially through vaginal or anal sex. The chance of getting HPV increases because of having multiple sexual partners. Certain types of HPV (HPV 6 and 11) cause genital warts, and some types may cause cervical cancer (HPV 16 and 18). Cancer development has not been observed in all HPV-infected women. However, the incidence of cervical cancer increases with smoking, HIV infection, a weakened immune system, and a lack of regular Papanicolaou testing.7

Reduced cancer-related mortality is closely associated with an early diagnosis via screening methods. The World Health Organization has reported that screening tests for breast, cervix, and colorectal cancer have significantly reduced disease-related mortality.1 In addition to encouraging healthy sexual practices and early diagnosis, most developed countries have training and screening programs, which have resulted in significant reductions in mortality and morbidity due to cervical cancer.8,9 However, this is not the case in Turkey, where the greatest risk factor for cervical cancer is inadequate awareness and knowledge among women about the importance of cervical cancer.10–13

Certain studies on cervical cancer and HPV have reported that women have low appreciation of the severity of this issue. They do not perceive themselves to be at risk of HPV infection,6,14–17 and they do not have regular Papanicolaou tests.18,19 Sociodemographic characteristics, a lack of awareness about Papanicolaou tests,10,12,20 and women's negative health-seeking behaviors and beliefs18,19 affect the potential benefits of early detection methods.

The American Cancer Association recommends that women older than 21 years have Papanicolaou tests or Papanicolaou tests plus HPV DNA tests and that, before the age of 21 years, women should start cervical cancer screening testing approximately 3 years after vaginal intercourse. It also recommends that cervical cancer screening be performed in women who have received the HPV vaccine.3 According to a large-scale health study conducted by the Turkish Statistical Institute in 2012, only 22.1% of Turkish women are having Papanicolaou tests.2 Thus, in Turkey, the testing rate is very low and has not reached target levels.10,12

The World Health Organization has reported that, in most developing countries, women's knowledge of cervical cancer is limited; most women have not heard about cervical cancer, and even if they have, they do not have any information about cervical cancer testing.1 Communities' knowledge levels and cultural beliefs may inhibit the participation of women in cervical cancer testing. Therefore, community knowledge levels and lifestyle behaviors related to this issue, as well as the beliefs of women in the target group, should be considered to organize an effective training strategy and enhance women's participation in cervical cancer testing.

Promoting healthy lifestyle behaviors and beliefs among women and the implementation of culture-specific training programs may encourage women to participate in testing21 and increase the number of requests for testing to healthcare institutions that provide cervical cancer testing services.22 Trainings are a significant part of cancer prevention strategies because they increase women's awareness of the signs and symptoms of cancer.1 The primary ways to prevent cervical cancer are through education, knowledge, respect, responsibility, honesty, and individuals and their communities taking joint responsibility.8 Studies have shown that collective education has a positive effect on individuals' attitudes and behaviors and also promotes the adoption of a healthy lifestyle that helps to reduce the risk of cervical cancer.23

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Conceptual Framework

Different health educational models have been used for health-related education. The PRECEDE-PROCEED model, developed by Green,24,25 is a health improvement model used for determining priorities and targets and analyzing conditions. The PRECEDE-PROCEED model consists of 8 phases, four for the PRECEDE part (social assessment; epidemiological, behavioral, and environmental assessment; educational and ecological assessment; and administrative and policy assessment) and four for the PROCEED part (implementation, process evaluation, impact evaluation, and outcome evaluation).24,25 Our analysis focused on the PRECEDE phases.

In the social assessment stage of the PRECEDE model, focus group interviews, discussions, and observations were performed; a questionnaire was developed; and major problems and requirements were defined. For the participants, quality of life, general well-being, physical and mental health disorders, current problems, and requirements were defined, and their demands and requirements were clarified to improve their quality of life. Moreover, the importance of cervical cancer and HPV testing for women was determined at this stage.

In the second stage of the PRECEDE model, which is the epidemiological, behavioral, and environmental assessment, health problems and behavioral and lifestyle factors regarding these problems were clarified. The genetic characteristics of the participants, such as family members having the history of cervical cancer, were considered to define groups at a high risk of cervical cancer. The health problems and risks of women were identified by examining studies regarding cervical cancer and HPV, as well as the findings from the interviews with the participants. Furthermore, the relationship between cervical cancer and environmental factors that the participants are exposed to, as well as their behaviors, was examined. Significant and modifiable behavioral and environmental factors and lifestyle changes related to cervical cancer were revealed. The environmental factors that may affect participants' access to early detection services for cervical cancer and the effects of media, family, and culture were defined.

In the third stage of the PRECEDE model, which is the educational and ecological assessment, the preparative, enhancing, and maturation factors that may support or prevent changes to lifestyle, behaviors, or environmental factors were determined. Of the preparative factors, the perceptions of participants about the risk of cervical cancer; their knowledge, attitudes, and beliefs about cervical cancer; and their self-efficacy were considered. Of the enhancing factors, the responses of community training center course mates, family members, or compeers; access to early detection services for cervical cancer; current resources; support obtained from healthcare professionals; and support obtained from the community and the media were considered. Of the maturation factors, being able to benefit from early cancer detection and screening and training centers, as well as factors facilitating health practices, such as training classes, books, and Web sites, was considered.

In the fourth stage of the PRECEDE model, which is the administrative and policy assessment, the factors that might affect the training program and the training program's sources were analyzed. The training that will be given is intended to improve the health and expectations of participants regarding cervical cancer. At this stage, place and time, staff, facilitators, responsibilities, necessary supports, and coordination were clarified. The aims regarding the cervical cancer training, the content of the training program, and its messages and concepts were determined by means of scientific resources, interviews with the participants, and information obtained from data collection. Based on the results of these 4 stages, convenient environmental and educational practices can be implemented to promote the use of early detection methods for cervical cancer (Figure 1).

Figure 1

Figure 1

The identification of factors preventing the use of early detection services for cervical cancer, as well as encouraging healthy lifestyle behaviors and beliefs among women, is important in preventing cervical cancer. Accordingly, studies revealing regional and cultural differences among countries are needed to prevent cervical-cancer–related mortality and morbidity. Although trainings using the PRECEDE-PROCEED education model to prevent certain diseases and health conditions have taken place in other countries,26–28 no previous use has been made of this model in these fields in Turkey. The results of this study could aid in the development of appropriate strategies and a course of action to prevent cervical cancer.

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Aim

This study aimed to determine the effect of education regarding cervical cancer and HPV on the healthy lifestyles and beliefs of Turkish women, using the PRECEDE-PROCEED education model. Study questions were the following:

  1. Are there any differences in the preeducation and posteducation scores of the study and control groups in terms of the SF-36 Health Status Questionnaire, Health Belief Model Scale for Cervical Cancer and Pap Smear Test, and Healthy Lifestyle Behavior Scale II?
  2. What are the retaining/preventing factors affecting women in the study and control groups in cervical cancer follow-up in the Turkish community?
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Methods

Study Design and Sampling Method

The study pool included all women taking courses (cookery, cloth dyeing, stitching, embroidery, carpet weaving, jewelry design, point lace, preparing decorative house accessories, etc) at the community training center; a total of 156 women agreed to participate in the study. Literate women with no oncologic cancer history (cervical cancer, breast cancer, etc) and no previous training regarding cervical cancer or HPV who agreed to participate in the study were included in the study sample. This study was performed in 2 stages: the first stage was conducted qualitatively to determine the knowledge and behaviors of women related to cervical cancer and HPV, and the second stage was conducted quantitatively (Figure 2).

Figure 2

Figure 2

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Data Collection

A semistructured interview form was used during the qualitative data collection. The SF-36 Health Status Questionnaire, Health Belief Model Scale for Cervical Cancer and Pap Smear Test, and Healthy Lifestyle Behavior Scale II were used during quantitative data collection to determine participants' sociodemographic characteristics and knowledge and practices related to cervical cancer and the HPV/HPV vaccine. The semistructured interview form and data collection tools were vetted by 5 experts (1 gynecologist and 4 nurse educators), and a pilot study was completed with 15 individuals to identify incoherent or unclear expressions before it was finalized.

During the qualitative data collection, focus group discussions were conducted with the 156 women to obtain detailed information regarding their quality of life, cervical cancer history, lifestyle behaviors, and beliefs. The following questions were asked: What do you think about the reasons for and possibility of contracting cervical cancer? Are you at risk for cervical cancer? If your answer is “no,” why do you not see yourself as being at risk of cervical cancer? What do you know about the methods used to detect cervical cancer during the early period? Have you ever had a Papanicolaou test? If your answer is “no,” what are your reasons for not having had a Papanicolaou test? What are the retaining/preventing conditions in regard to having a Papanicolaou test? Under what conditions would it be easier for you to have a Papanicolaou test? Focus group discussions were carried out in groups of 6 to 10 individuals per session.

Voice recordings were made during the face-to-face interviews after obtaining participants' informed consent. Interactions between participants were also noted by an observer. To ensure the data's internal validity, participants' answers were repeated and summarized to prevent misunderstandings and determine whether they were understood. Interviews were performed during 1 session. Content analysis of the research data was performed via deduction. This content analysis involved putting the data in writing, editing them, detecting significant data, forming an analysis matrix, reviewing the coded data in the analysis matrix to determine the factors inhibiting or enhancing early cervical cancer detection behavior, and analyzing and reporting the results. The results of the focus group discussion were used in preparing the content of the educational program on the basis of the PRECEDE-PROCEED education model.

At the second stage of the research, a real test model with pretest/posttest control groups was used. Using a table of random numbers, women who agreed to participate in the study were randomly assigned to 1 of 2 groups: the study group (n = 78) or the control group (n = 78). The same information form and scales were applied to the women in both groups. After the pretests, women in the study group received their first training for 60 minutes. Every other month, 2 additional trainings were provided for 60 minutes each. A month after the third educational program, the SF-36 Health Status Questionnaire, Health Belief Model Scale for Cervical Cancer and Pap Smear Test, the Healthy Lifestyle Behavior Scale II, and information tests were again administered to determine women's knowledge, attitudes, and beliefs about cervical cancer and HPV. At their first training, the women were provided with general information about female cancers, including cervical cancer; the risk factors for cervical cancer; the symptoms of cervical cancer; and cervical cancer and HPV. At the second training, they were informed about the prevalence and epidemiology of HPV, the types of HPV, the modes of transmission of HPV, risk factors related to genital HPV infection, techniques for diagnosing HPV, the prevention of HPV, treatment choices regarding HPV, and the HPV vaccine. At the third training, they were informed about how to protect themselves from cervical cancer and the importance of early detection, Papanicolaou testing, and healthy lifestyle behaviors, including healthy nutrition, physical activity, weight control, stress management, and abstaining from smoking, alcohol, substance abuse, and risky sexual behaviors. After the trainings and feedback, the degree of change in their quality of life and current knowledge, attitudes, and beliefs about cervical cancer and HPV were determined. Three months after the final training, the women were called via phone and evaluated in terms of whether their use of cervical cancer screening methods had increased. The number of women having had a Papanicolaou test was found to have increased from 7 to 69.

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Data Collection Tools

SF-36 HEALTH STATUS QUESTIONNAIRE

The SF-36 Health Status Questionnaire consists of 36 items measuring both negative and positive aspects of an individual's health status.29 It creates 8 scaled scores related to physical function (10 items), social function (2 items), role limitations related to physical functions (4 items), role limitations related to mental problems (3 items), mental health (5 items), energy/vitality (4 items), pain (2 items), and general health perception (5 items). The SF-36 also includes an item used to assess changes in the respondent's health status during the past year, which is not used in scoring the scales or summary measures. The SF-36 has been shown to be useful in estimating the average change in health status during the year before its administration.30 Each scale is evaluated with regard to the previous 4 weeks. Scores are calculated separately for each scale, instead of using a single total score. Health status is assigned a value between 0 and 100 via subscales. On this scale, “0” means poor health status, and “100” means good health status. A Turkish validity and reliability study of the SF-36 was performed by Kocyigit et al,31 and the scale was found to be valid and reliable for use in Turkey. The social norm values of the SF-36 in Turkish society were reported by Demiral et al.32 The Cronbach's α coefficient varies between .64 and .98 for the various subdimensions of the questionnaire in Demiral et al's32 study. In this study, the Cronbach's α values of the SF-36 Health Status Questionnaire were found to be .87, .63, .83, .61, .69, .66, .79, and .76 for physical function, social function, role limitations related to physical functions, role limitations related to mental problems, mental health, energy/vitality, pain, and general health perception, respectively.

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HEALTH BELIEF MODEL SCALE FOR CERVICAL CANCER AND PAP SMEAR TEST

The Health Belief Model Scale for Cervical Cancer and Pap Smear Test is a scale developed by Guvenc et al.12 It is based on the Health Belief Theory and consists of 35 items. The scale has 5 subdimensions: Papanicolaou test benefits and health motivation, Papanicolaou test barriers, perceived seriousness, perceived susceptibility, and health motivation. It is a Likert-type scale that is scored from 1 to 5. Each dimension is scored separately; there is no single total scale score. The number of scores is equal to the number of subdimensions for each individual. The minimum and maximum scores are 8 and 40 for Papanicolaou test benefits and health motivation, 14 and 70 for Papanicolaou test barriers, 7 and 35 for seriousness, 3 and 15 for susceptibility, and 3 and 15 for health motivation, respectively. The evaluation in the scores shows improvement in perceived susceptibility, caring, and health motivations. All subscales, except for a sense of obstacles, are positively related to Papanicolaou test screening behaviors. None of the items is scored negatively. In this study, the Cronbach's α value was .82; the Cronbach's α values of the subdimensions were .95 for Papanicolaou test benefits and health motivation, .82 for Papanicolaou test barriers, .84 for seriousness, .81 for susceptibility, and .77 for health motivation.

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HEALTHY LIFESTYLE BEHAVIOR SCALE II

The Healthy Lifestyle Behavior Scale evaluates individual behaviors related to having a healthy lifestyle. The scale, revised in 1996, was renamed the Healthy Lifestyle Behavior Scale II. The revised scale consists of 52 items and 6 subfactors: moral improvement, interpersonal relations, nutrition, physical activity, health responsibility, and stress management.33 It uses a 4-point Likert-type system. The minimum and maximum scores are 52 and 208, respectively. In this study, the Healthy Lifestyle Behavior Scale II's Cronbach's α reliability coefficient was found to be .93; the Cronbach's α values for the subdimensions were .79 for moral improvement, .81 for health responsibility, .84 for physical activity, .67 for nutrition, .75 for interpersonal relations, and .77 for stress management.

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ETHICAL CONSIDERATIONS

This study was initiated after receiving approval from the Ondokuz Mayis University Ethical Committee (27.06.2014/number B.30.2.ODM.020.08/1039). Informed consent was obtained from the institute and the women participating in the study. At the end of the study, the women in the control group were also educated about cervical cancer and HPV to eliminate ethical concerns and ensure that the women in both groups received this information.

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Data Analysis

The statistical analysis was performed using SPSS 22.0. The Shapiro-Wilk test evaluated the normality testing of the quantitative data. The Mann-Whitney U and Kruskal-Wallis tests were used for nonnormally distributed data; single-direction variance analysis and an independent sample t test were used for normally distributed data. The reliability of the scales was estimated using Cronbach's α statistic. The relationship among the scales was evaluated by using Spearman and Pearson correlation analyses. The results are presented as frequencies, means, standard deviations, and medians (minimum/maximum). The significance level was set at P < .05.

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Results

Sociodemographic Characteristics

A total of 156 women were included in the study (78 in the study group and 78 in the control group). Of these women, 75% were married, 46.1% had graduated high school, 76.9% were housewives, 58.4% had equal incomes and expenses, 75.6% were nonsmokers, 31.4% were exercising, 41.7% were overweight, and 87.8% were in good health. The mean age of the women was 40.9 ± 11.1 years (Table 1).

Table 1

Table 1

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Cervical Cancer and the Papanicolaou Test

All of the women in the study and control groups understood the importance of early cancer detection before the educational program. Among the women, 3.2% had a family member who had been diagnosed with cervical cancer; 28.2% indicated risk factors for cervical cancer, including a family history of cancer (n = 40), unsanitary vaginal hygiene (n = 32), multiple sexual partners (n = 30), and smoking (n = 28); none of them identified HPV as a risk factor for cervical cancer; 15.4% defined the method of cervical cancer screening as having a gynecological examination (n = 15) or Papanicolaou test (n = 7); and 58.3% did not know how to protect themselves from cervical cancer. Before the training, only 7 women have had a Papanicolaou test upon their doctors' recommendation, and 95.5% of the women did not know the benefits of having a Papanicolaou test (Table 2).

Table 2

Table 2

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HPV and the HPV Vaccine

In this study, 8.3% of the women in the study and control groups had previously heard about HPV. Their most valuable source of information about HPV was television health programs (n = 113). Among the women, 8.3% had information about how to protect themselves from HPV, and 11 recommended sexual monogamy as protection from HPV. Moreover, 39.1% of the women believed that it was possible to prevent cervical cancer through vaccination, one of them had heard about the HPV vaccine, none of the women had received the HPV vaccine, and 5.8% wanted to receive it. Of the women, 90.5% had inadequate information about the vaccine, 67.3% thought that it was unsafe, and 16.3% stated that it was expensive and not paid for by the government (Table 3).

Table 3

Table 3

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Barriers to Cervical Cancer Screening

Among the women in the research group, the “individual barriers” to cervical cancer screening were determined to be inadequate health-seeking behaviors, misinformation and misperceptions about the screening test and symptoms and etiology of cervical cancer, inadequate knowledge of Papanicolaou testing and current health services, fear of cancer and death, anxiety about having bad test results, not considering themselves at risk for cervical cancer, and ignoring cervical cancer screening (Table 4).

Table 4

Table 4

The “sociocultural barriers” to cervical cancer screening were being ashamed to receive a pelvic examination, public neglect of health issues as a cultural characteristic, not contacting healthcare institutions without an existing health problem, the unacceptability of extramarital affairs due to social and religious values (and therefore the lack of necessity for this test among single women), the unwillingness of women to speak to others about their sexual lives, considering the requirements of family members and their healthcare needs to be more important, being ashamed about participating in cervical cancer follow-up, and vacillating about attending follow-up (Table 4).

Among women in the research group, “healthcare system barriers” to cervical cancer screening were reported to be challenges in reaching and using qualified services, especially among those from villages and rural areas; the underestimation of an individual's need for privacy during pelvic examination on the part of healthcare professionals; rude behaviors by healthcare professionals during pelvic examinations; an inadequate number of female gynecologists; an unwillingness to be examined by male healthcare professionals; inadequate and poor consultancy services; and a lack of community-based approaches to cervical cancer (Table 4).

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Comparison of Scale Scores Before and After the Educational Program

When women in the study group were compared with those in the control group, the SF-36 Health Status Questionnaire's physical role limitations (P = .005), mental role limitations (P = .012), and general health perceptions (P = .001) were found to have increased after the educational program. No difference was identified in the median scores of women in the study group in terms of the Healthy Lifestyle Behavior Scale II's health responsibility, moral development, and stress management subdimensions; however, a statistically significant difference was detected in their physical activity (P = .001), nutrition (P = .001), and total Healthy Lifestyle Behavior Scale II scores (P = .002). The subdimension scores of the Health Belief Model Scale for Cervical Cancer and Pap Smear Test were found to be higher among women in the study group (cervical cancer seriousness, P = .001; health motivation, P = .001) as compared with those in the control group (Table 5).

Table 5

Table 5

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Discussion

Turkey reflects both the Islamic culture and a westernization process. This study provided a comprehensive understanding of Turkish women's knowledge of and attitudes toward cervical cancer, HPV, and HPV vaccination. The findings suggest that effective education strategies should be developed for women to increase their knowledge and awareness of cervical cancer risk factors and reduce the incidence of and mortality related to cervical cancer.

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Cervical Cancer and the Papanicolaou Test

In this study, the risk factors of the women in the study and control groups were a family history of cancer, unsanitary vaginal hygiene, having multiple sexual partners, smoking, and radiation. None of the women defined HPV as a risk factor for cervical cancer, and 58.3% were unaware of how to protect themselves from cervical cancer. Supporting this study's findings, the knowledge levels of women about cervical cancer, its seriousness, and their perceived susceptibility to it were found to be very low27,34,35; women did not know about the relationship between HPV and cervical cancer.34,35 These findings show that it is necessary to develop effective training strategies for women to reduce the incidence and mortality rate of cervical cancer and to improve women's knowledge, attitudes, and awareness of the risk factors for cervical cancer.

In this study, all the women agreed regarding the importance of early cancer detection. However, only seven had previously had a Papanicolaou test upon their doctors' recommendation, and 95.5% did not know the benefits of the Papanicolaou test. In certain studies, the ratio of those having had a Papanicolaou test was in the range of 23% to 79.4%.27,35–38 Compared with other studies, the ratio of those in this study having Papanicolaou tests is very low (4.5%) due to women's inadequate knowledge and awareness of this issue, their failure to consider themselves at risk for cervical cancer, and their failure to consider cervical cancer screening to be a necessity due to the Turkish community's disapproval of premarital sex.

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HPV and the HPV Vaccine

In this study, only 8.3% of the women in the study and control groups had heard about HPV, and their knowledge levels in this regard were low. Cermak et al14 also reported that awareness and knowledge levels regarding HPV were low among women, including the fact that HPV can be detected through abnormal Papanicolaou test results, and they reported that there was a lack of knowledge about HPV, even among women having had Papanicolaou tests. In a study of Turkish women having normal Papanicolaou results, the prevalence of HPV types was researched. Although the incidence of this virus was reported to be rare in Islamic cultures, HPV was common among women having normal cervical cytology, especially among young women. As a consequence, the benefits of receiving an HPV vaccination were stated in the national vaccination program.39

Lee et al40 studied the beliefs of Chinese women in Hong Kong about HPV and cervical cancer. They found that inadequate information about and misdetection of cervical cancer and HPV were common among women and that they would hide their conditions from the community because of their anxiety about stigmatization, even if they were infected by sexually transmitted HPV. In this study, only 1 woman has heard about the HPV vaccine before the training, none of the women received the HPV vaccine previously, and only 5.8% of the participants wanted to have the HPV vaccine. The reasons for their unwillingness to have the HPV vaccine were a lack of adequate information about the vaccine, not considering it to be safe, the vaccine fee, and the vaccine not being supported by the government.

Human papillomavirus vaccination is an effective method of preventing the most common types of HPV infection that cause cervical cancer.3 It is important to expand educational programs about HPV infection and the vaccine and to use health training and appropriate communication strategies to prevent illusions about the vaccine and improve awareness of it. The ratio of those having the HPV vaccine could likely be increased through educational programs about the etiology of cervical cancer and its relationship with HPV.17

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Barriers to Cervical Cancer Screening

Among the women in the research group, the individual barriers to cervical cancer screening were reported to be inadequate health-seeking behaviors, inadequate knowledge about the Papanicolaou test and current health services, fear of having bad test results, fear of death, failure to consider themselves at risk for cervical cancer, and failure to pay attention to cervical cancer scanning. In other studies, the factors affecting the participation of women in cervical cancer screening were found to be a lack of perspective on improving health and preventing disease, such as through Papanicolaou tests, and inadequate information about currently available services.41 Additional factors were an insufficient awareness of cervical cancer; cognitive and behavioral factors, such as a lack of healthcare research and poor attitudes; and sociocultural factors, such as religious, sexual, and cultural taboos.42

Because communities' cultural structures, knowledge, beliefs, and attitudes affect the participation of individuals in cancer screening programs, this issue must be evaluated in a sociocultural context. For example, gynecological examinations are considered to be confidential, women refrain from consulting healthcare institutions for their gynecological problems, and this type of cancer causes concern among women in conservative communities such as Turkey. The main reason for this concern is the necessity of women showing their sexual organs during examinations. According to the cultural values of Turkey, girls are raised with the idea of hiding and protecting their sexual organs; having negative perceptions about their bodies and sexual organs causes them to avoid gynecological examinations in later years.43

In this study, the sociocultural barriers to cervical cancer screening were identified as being ashamed of pelvic examinations, the unacceptability of extramarital affairs due to social and religious values and therefore considering it unnecessary for unmarried women to have this test, the unwillingness of women to speak to other individuals about their sexual lives, and embarrassment. In parallel research findings, Bethune and Lewis44 reported shame and hesitation, as well as the fear of screening and examination results. Lovell et al45 found that women's concerns about showing their bodies to another individual negatively affected their participation in cervical cancer screening and that shame and hesitation regarding the Papanicolaou test were common, especially among Maori and Pacific women.

According to this study's findings, the healthcare system barriers to cervical cancer screening were identified as the underestimation, on the part of healthcare professionals, of an individual's privacy needs during pelvic examinations, rude behaviors by healthcare professionals during pelvic examinations, the inadequate number of female healthcare professionals, and women's unwillingness to be examined by male healthcare professionals. In a study of the barriers to and benefits of cervical cancer screening among low-income women in Venezuela, Equator, Mexico, Peru, and El Salvador, Agurto et al46 found the barriers to be difficulties in reaching and benefitting from quality service, a lack of comfort and privacy, rude behaviors by healthcare professionals, poor services, the fear of cancer among women waiting for test results, and neglect. In other studies, women's levels of knowledge about cervical cancer risk factors have been found to be closely related to the gender of their doctors, with an examination by a male doctor having a negative effect due to women's preference of being examined by a female doctor.27,37 Matin and LeBaron47 investigated the attitudes of Muslim women toward cervical cancer screening, and they found that Muslim women resisted cervical cancer screening because of cultural and religious threats. Moreover, not only single women but also married women were highly conservative regarding genital examinations and the idea of young Muslim women having Papanicolaou tests and pelvic examinations after marriage.

The reasons for not having cervical cancer screening may be related to differences among the individuals' health beliefs and practices, cultural taboos, sexual taboos, fears about cancer, a lack of information, an unwillingness to undergo gynecological examinations, traditional and conservative community structures, concerns about the gender of the person who will perform the examination, and shame.10,43

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Efficiency of the Educational Program

No alteration was detected in the subdimension median scores among the women in the study group after the educational program in terms of the Healthy Lifestyle Behavior Scale II regarding health problems, moral development, and stress management; on the other hand, a statistically significant increase was determined in the total scores of the women in terms of physical activity, nutrition, and the Healthy Lifestyle Behavior Scale II. In certain studies, community education has been used to promote the adoption of healthy lifestyle behaviors. Positively changing the attitudes and behaviors of individuals helps to reduce cervical cancer risk23 and is highly beneficial in terms of improving culturally specific educational programs.21

In a study conducted by Laranjeiro34 to determine the knowledge and health beliefs of Portuguese women regarding cervical cancer and follow-up, most of the participating women believed that they could prevent cervical cancer by being healthy, performing regular exercise, reducing stress, having a positive attitude, and not worrying about getting cancer. In this regard, it is important to take responsibility for one's own health and to practice protective and beneficial health behaviors.48

In this study, when the women in the study group were compared with those in the control group, the subdimension score for the Health Belief Model Scale for Cervical Cancer and Pap Smear Test, cervical cancer seriousness, and health motivation was found to be higher in the study group after the educational program. However, improved health motivation and reduced perceptions of obstacles were found in the study group when compared with the pretest. Bebis et al49 reported significant differences in terms of cervical cancer susceptibility, Papanicolaou test benefits, and Papanicolaou test barrier dimensions, considering the subdimensions of the Health Belief Model Scale for Cervical Cancer and Pap Smear Test, among the women in their study and control groups, and they found that nurses could change the knowledge, attitudes, and beliefs of women by actively participating in educational programs about cervical cancer follow-up and Papanicolaou testing. Demirtas and Acikgoz50 found no differences related to the demographic and gynecological characteristics of women in the cervical cancer susceptibility, cervical cancer seriousness, and cervical cancer health motivation subdimension scores for the Health Belief Model Scale for Cervical Cancer and Pap Smear Test. They also stated that, as the awareness of Papanicolaou testing increased, the motivation to have a Papanicolaou test also increased, and different strategies were required to create behavioral changes. In another study, women had inadequate knowledge regarding cervical cancer screening.22

In conclusion, cervical cancer is a significant and growing health problem. Healthcare professionals have a substantial responsibility to increase awareness about the HPV virus and HPV vaccine to enable the participation of women in screening programs for cancer prevention and to increase women's healthy lifestyle behaviors. Nurses also play a significant role in motivating women who are not taking responsibility for their own follow-up to increase their participation in screening programs.

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Limitations

Although the strength of the study is the use of findings obtained from research on educational programs for women, the weakness of the study is that the research was conducted only on women and excluded their husbands. Therefore, it is recommended that further studies be planned that include women and their husbands from different geographical regions of Turkey.

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Conclusion

In this study, only 4.5% of the women participants have had a Papanicolaou test; none identified HPV as a risk factor for cervical cancer, and none have had an HPV vaccine before the training. Their reasons for not having received the HPV vaccine were determined to be inadequate information regarding the HPV vaccine and not considering it to be safe. The limitations preventing women's participation in cervical cancer screening were identified as neglect, shame, religious values, an unwillingness to speak to others about their sexual lives, rude behaviors by healthcare professionals and their underestimation of an individual's privacy needs during pelvic examinations, and the women's unwillingness to be examined by male healthcare professionals. The posteducational health motivations of women in the study group had improved as compared with the pretraining values, and perceptions preventing women from having a Papanicolaou test had decreased.

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ACKNOWLEDGMENTS

We would like to thank the women who took part in this study.

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Keywords:

Awareness; Behaviors; Belief; Cervical cancer; Education; Human papillomavirus; Knowledge; Papanicolaou test; Perception; Prevention

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