Introduction
Cervical cancer is a significant global health issue and that accounts for approximately 6.5% of cancers affecting women worldwide.1 It is the fourth most frequently diagnosed cancer among women of all ages worldwide,2 and the second leading cause of cancer-induced mortality among women at reproductive age.1 Interestingly, research evidence suggests that by 2030 cervical cancer will surpass other cancers and become the first leading cause of cancer-induced mortalities among women.3 As reported by the WHO, cervical cancer is also the second most common cancer in Asia.4
In 2020, there were an estimated 604 000 new cases of cervical cancer globally, with the highest proportion (58.2%) occurring in Asia.1 Furthermore, 91% of mortalities induced by cervical cancer occur in low-income and middle-income countries.4 5
Cervical cancer is the fourth most prevalent malignancy in women in Iran,3 and its age-standardised mortality rate was 2.3 per 1 00 000 women in 2020.5 Additionally, the average age at diagnosis is almost ten years lower than the global average.3
Fortunately, cervical cancer is among the most preventable and treatable types of cancer, as there is typically a 10–20 year lag between the development of pre-cancerous lesions and the onset of invasive cancer.6 Moreover, the survival rate of precancerous stages is approximately 100%.7 Effective prevention programmes and early-stage treatment led to an 80% reduction in cervical cancer cases in developed countries.8
With the implementation of the new WHO strategy, which aims for 90% vaccination, 70% screening, and 90% treatment, it is anticipated that over 40% of new cases of cervical cancer can be prevented by 2050.9 This could potentially save 60.8 million lives by the year 2120.10
The Pap smear (PS), a highly sensitive and specific screening method, is widely employed to detect premalignant cervical lesions.11 Since its introduction in 1950, the PS has proven to be one of the most effective and cost-effective screening tests for cervical cancer.12 Sexually active women aged 21 and above are recommended to take this test every 3 years.13
However, the average screening coverage for cervical cancer in less developed countries is only 19%, which is significantly lower than developed countries (63%).14 In developed countries, approximately 85% of women take the PS at least once in their lifetime, whereas this rate is only 5% in developing countries.10
According to the latest facts and figures reported by WHO in 2019, 49% of Iranian women had not had the PS test within the past 5 years.5 Various studies have reported the incidence rates of PS test between 34% and 66.6%.8 15–17 Only 8.23% of women who visited Mashhad health centres in the past 5 years ever had the test.18
Qualitative research methods provide researchers with the means to delve into questions of significance, find barriers and facilitators of change, and detect factors contributing to the success or failure of interventions.19 The majority of existing research on PS has been quantitative,17 20–22 with only a limited number of qualitative studies that used group interviews,3 12 23 interviews exclusively with women having the PS,3 individuals living with cervical cancer,24 and women residing in rural communities.25 These studies drew attention to some barriers to PS screening, including feelings of embarrassment, fear, high costs, false positives, cultural beliefs and limited knowledge.
Considering the statistically significant data, significance of the problem, multidimensional nature of cervical cancer prevention, and inadequate qualitative information to gain a more comprehensive understanding of barriers and facilitators of the PS, the present researchers tried to conduct qualitative research through individual interviews with all women (with or without a history of PS) to explore the barriers and facilitators of performing cervical cancer PS screening.
Methods
Study setting and design
The present qualitative content analysis was done using an inductive approach in Mashhad, Iran, from July to December of 2022. The women were selected through a purposive sampling. Initially, with the help of healthcare professionals, a list of eligible women was made from the provincial health system national portal. These women were contacted and provided with an explanation of the study’s objectives. If they agreed to participate, the time and place of interview were arranged. Out of the 58 individuals who were contacted, 50 consented to be interviewed. However, some individuals did not tur up for the interview. Some others did not have enough time to complete the in-depth interview; thus, they were excluded from the study.
Before the formal interviews, two pilot interviews were held with representatives of groups, who were not the primary research participants. The aim was to assess the validity of the tool and find any bias or inaccuracies in the interview process for the research team. The data were collected through semistructured in-depth interviews conducted by the first author (MSH: who is a PhD student in health education with an M.S. degree in midwifery).
Qualitative and quantitative papers on challenges and motivators of taking the PS in the world were reviewed to guide relevant questions. Then, the questions were modified according to the research team comments and the experience of one member of the research team. The guided questions are provided in online supplemental file 1 and a sample of them is shown in box 1.
Supplemental material
Samples of guided questions in interviews
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Do you believe that regular Pap smear testing is important for women? Why or why not? Please provide your explanation.
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What are your personal reasons for having (or not having) a Pap smear?
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Do you think that experiencing clinical symptoms is necessary to have a Pap smear? If so, what symptoms should one look out for?
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What factors have encouraged or motivated you to have Pap smear testing?
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What were the challenges or obstacles that you experienced during your Pap smear procedure?
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In your opinion, which people or organisations can have an impact on encouraging women to undergo Pap smear testing? How?
The inclusion criteria were: (1) women aged between 18 and 70 years, and (2) having been married for at least 3 years. In Iran, the minimum legal age of marriage for girls has been 15 years since 1934 and according to national guidelines for cervical cancer screening, the first PS should be performed 3 years after marriage. Thus, the age of 18 was selected as the lowest inclusion age for research. More specifically in this study, married women were included because in Iran premarital sexual activity is prohibited. It is generally assumed that sexual activity begins at the time of marriage.
The exclusion criterion was a refusal to continue participation in the research. The researchers aimed to achieve maximum diversity by selecting women from different parts of the town, in terms of demographic characteristics such as age, level of education, occupation, contraceptive method, parity and history of PS (at three levels of regularly screened, never-screened, and long-term-under screened women). Regularly screened women were those who had the PS according to the guidelines of the American College of Obstetricians and Gynecologists. Long-term-under screened women were defined as those who had had at least one PS, but were overdue for their next test.
Data collection continued until data saturation (ie, when no new data emerged or when redundancy occurred). A demographic information checklist was used in this study. The interviews were held in the healthcare centres. To promote social distancing and mitigate the risk of COVID-19 transmission in enclosed places, some interviews took place in public parks. Before appealing to a topic guide, two preliminary interviews were held to assess the validity of questions and identify any potential bias or inaccuracies in the interviewing process for the research group. Before initiating the interview, the purpose of study was revealed to the participants, and a written informed consent was obtained according to ‘The Declaration of Helsinki’.
The interview began with general open-ended questions by the first author to foster discussion and communication. Subsequently, probing questions were asked guided by the participants’ answers. The interviews ranged in duration between 25 and 35 min and were recorded with the participants’ consent.
The data were analysed at the same time of data collection, which enabled the researchers to detect emerging codes and themes. If necessary, for example, when a ‘new code’ was obtained from a subsequent participant or when words or phrases with ambiguous meanings were encountered, the researcher called the participant for further clarification and supplementary explanation before proceeding with the coding and analysis process.
Data analysis
Concerning the qualitative data analysis, the researchers employed the five-step approach proposed by Grandheim and Lundman,26 in MaxQDA (2020). These five steps were: (1) recording the interviews and immediately transcribing them verbatim in Persian, which served as the primary data of study (2) the researchers’ immersing themselves in data by listening to the recorded voices and reviewing the manuscripts again and again, finally dividing the textual content into semantic units, (3) dividing intensive semantic units based on explicit and implicit concepts in sentences to convey significant meanings, followed by coding and abstracting data (this third step of analysis also involved the substantiation of accuracy of codes by supervisors and research team), (4) assigning codes to singular topics based on similarities and differences in meaning to form subcategories, and (5) grouping subcategories at a higher level of abstraction, thereby classifying them and ultimately ascertaining the main theme.
Trustworthiness
To ensure the accuracy and robustness of study, the researchers followed Lincoln and Guba’s four evaluation criteria.27 These criteria provide a systematic approach for assessing the trustworthiness and rigour of qualitative research studies.
To establish credibility, member-check was used to seek feedback from three participants and the present authors. Additionally, enough time was spent on data collection, interpretation and continuous engagement with the data.
In terms of transferability, detailed descriptions were provided on the setting of study, participants and methods, which enabled readers to show the applicability of findings to other settings. Moreover, participants were selected with a variety of characteristics, and the findings were presented richly and comprehensively, accompanied by relevant quotations extracted from the interviewees’ accounts.
Confirmability was achieved by providing an audit trail, which included clear documentation of procedures of study, decisions and changes made during the study to ensure the findings can be traced and verified. The researchers avoided prolonging the duration of data collection (interviews) as much as possible and asked all participants about the same topic.
Dependability was achieved by providing clear and transparent documentation of procedures of study, data collection, analysis and theme extraction. The whole procedure of study was explained to several other researchers to confirm the accuracy.
Patientsand public involvement
There were no patients involved in this study.
Discussion
The present qualitative research was carried out to explore the barriers and facilitators of PS screening as perceived by the female population of Mashhad, Iran. The findings were divided into four categories, namely ‘individual challenges’, ‘environmental limitations’, ‘individual motivators’, and ‘supportive and efficient environment’.
The first theme, individual challenges, dealt with several significant factors that prevented women from taking the PS. An essential factor was the perceived assurance of one’s own health as there was no manifest clinical symptom or risk factor. In a study conducted by Intahphuak et al, the majority of participants had a false belief in their health and attributed the lack of perceived risk factors as the reason for not taking the PS.28 This finding is consistent with previous research that has consistently found inadequate knowledge and awareness of cervical cancer as a significant barrier to taking the PS.3 24 29 30 It is essential to remove this misconception and raise women’s awareness of the importance of regular PS screening, because cervical cancer often remains asymptomatic until it reaches an advanced stage.
Prioritising other aspects in life can dissuade women from taking the PS, as they may pay more attention to other things. Similar to previous studies, the present research showed that women often do the house chore, childcare and job-related duties.12 31 32 They are mostly pressed for time and are often too busy to go for a PS test.29 33 It is essential to remind women of the crucial role of the PS and emphasise the necessity of prioritising it.
Psychological factors, such as the fear of PS procedure and the result, previous negative experiences, and embarrassment were found as the main barriers to taking the PS. Previous studies consistently reported the fear of the potentially uncomfortable sampling process, misdiagnosis and previous positive results as psychological barriers to PS.23 31 32 34–36 The other perceived barriers found in the present study were the embarrassment in exposing intimate parts of body, specific examination positions and social stigma. These are consistent with the findings of a body of previous research.25 33 35 37 Darj et al31 reported that Nepali women predominantly regarded discussions about their reproductive system as shameful and, consequently, to be avoided.31 Fear and embarrassment can be reduced through perceiving the significance of PS, conversing freely with healthcare providers, enjoying the company of a supportive individual during the examination, and relaxation techniques.
Previous experience of the PS can significantly affect a woman’s willingness to take the test again. Negative experiences, such as pain, discomfort or a sense of violation during previous PS screenings, may cause reluctance or avoidance of later testing. This can act as a barrier to taking the PS, as pinpointed by participants of previous studies.28 38
Women who have a positive experience of PS, either by themselves or friends, are more likely to do the test again and can serve as a persuasive factor.28 31 37 Roux et al showed that the quality of care and satisfaction with previous screening are crucial factors affecting women’s willingness to take the PS again.39 Healthcare providers can provide more support and advice to make the test procedure less stressful and more comfortable.
Negligence or laziness of some women can cause the avoidance of PS, thereby exposing them to the risk of developing cervical cancer. This finding is consistent with previous studies conducted by Pakseresht et al and Mahalakshmi and Suresh .12 32 To proactively prevent women’s unintentional or careless attitude towards the PS, the use of reminders or making appointments can be effective strategies.
Awareness is essentially needed to change attitudes and behaviours.40 41 It serves to raise awareness of the importance of taking the test, the procedure and the potential consequences of not taking the screening test. Inadequate awareness and the disclosure of incorrect information have been found as the main causes of women’s unwillingness to take the PS in the existing literature.3 12 28 30–32 35 37 41 There are several ways to increase awareness of the PS, including public health campaigns, educating healthcare providers and community outreach. Counselling and education programmes that focus on community health can improve knowledge and awareness, remove misconceptions or stigma and make routine screening more accessible. Disseminating relevant information through different mass media, such as radio and television,12 23 32 37 38 social networks, women’s health campaigns,29 42 health volunteers,28 31 and local and religious leaders,28 37–39 are effective in increasing awareness and increasing the rate of regular screening.
The second category of barriers found in this study was environmental limitations, particularly within healthcare centres. Several factors within these establishments can prevent the PS test, including limited access, concerns about privacy and distrust in healthcare providers. Implementation of the PS has been observed to be prevented by overcrowded waiting areas, extended waiting time,34 inadequate resources,31 37 39 42 43 delayed test results35 and insufficient follow-up,3 as reported in similar studies.
Participants have also expressed concerns about the lack of professional competence and appropriate behaviour by healthcare providers, which can lead to unreliable test results, lower patient satisfaction and missed chances of screenings. To increase the rate of taking the PS, it is essential to enhance accessibility, ensure the provision of accurate and timely testing, and create a private and comfortable environment for screening. Healthcare providers should also receive comprehensive training and continuous education to ensure they have the required professional skills and knowledge to deliver effective PS.
Improvement of the healthcare system can be done by increasing access to healthcare services, and incorporating quality assurance measures. Shakibazadeh et al contended that easy and affordable access is a strong motivation for taking the PS.22 However, according to Tadler and Min, simply expanding healthcare services by adding facilities and broadening health programmes does not always lead to a better and increased use of the test.39 Consequently, a comprehensive approach is needed to effectively address the various factors that can influence the rate of taking the PS.
The lack of support by relatives, particularly the husband, can significantly affect women’s unwillingness to take the PS. Several researches have shown that women may lack the autonomy to make decisions about their well-being. Thus, they may require their husband’s permission to take the PS and cover the associated expenses.3 24 31 42 Having an open-minded husband who provides support and pays for the costs of test can serve as a motivation for women to take the PS. By raising men’s awareness through training programmes in their workplace and providing emotional and financial support for wives, women can be encouraged to take the PS test.
The support and recommendations of other important people in life, such as healthcare practitioners, gynaecologists, physicians, friends and family members, play a crucial role in promoting PS. These important others can cause positive influences, social support, encouragement and can help create trust in the healthcare system. The major motivators, as ratified in several studies, are reminders and recommendations from healthcare providers, friends and family members.3 12 28 29 35–38 The significance of family and social support, including women’s social groups, has been documented in some studies.3 31 36 Therefore, involving these important others in educational campaigns and outreach programmes can be an effective strategy to increase the rate of taking the PS.
For many women, economic challenges may present considerable barriers to taking the PS. Though many studies drew attention to the cost of PS as a barrier,3 12 23 29 31 32 34–39 41–43 the significance of this barrier in the present study seems to be inconsequential according to the frequency of the issue in interviewees’ accounts. This divergence can be due to the fact that a majority of participants had supplementary insurance coverage, which reduced their need to fully pay the cost of the test. Hence, providing financial support for women’s healthcare services, including the PS, can further ensure comprehensive access to these crucial services, regardless of the income level.
The primary cultural challenges that impede PS are the failure to establish the significance of women’s health in society. Induced gender inequality, which is perpetuated by social norms and traditional male-dominated values, as well as deep-rooted beliefs, contributed to this issue. Certain religious teachings and social norms strictly prohibit women from exposing their intimate parts of body, even to medical professionals.24 This is compounded by the prevailing cultural perspectives of destiny and the belief that a disease and its cure come directly from a superpower. These perspectives significantly influence the adoption of preventive behaviours.24 29 43 In case of extreme determinism, individuals hold the belief that cancer is an unavoidable destiny that cannot be prevented. Gele et al reported that Pakistani and Somali immigrants in Norway held the belief that Muslims were immune to the disease.38
Addressing cultural challenges is a complex and extensive effort that needs a comprehensive approach. Providing education and enhancing awareness, implementing community-based interventions, involving local communities in health-promoting activities and advocating for policies that promote gender equality and women rights make it possible to empower women and motivate them to prioritise their health. Undoubtedly, surmounting cultural barriers and increasing the rate of PS is not far-fetched.
Promoting the adoption of the PS can be a function of women’s health-related beliefs. These beliefs contribute to the promotion of consciousness, motivation, positive attitudes, perceived control, and greater adherence to healthcare recommendations. According to Darj et al31, prioritisation of one’s own body and health emerges as a key motivator for PS.31 There is resaerch evidence that interest in health and desire to acquire knowledge about one’s health are important drivers for Guatemalan and Thai women to take the PS.28 42 However, the findings also show that cultural challenges pose barriers to taking the PS. Healthcare providers should be aware of cultural barriers and try to provide culturally sensitive care to all patients.
The government and policy-makers can play a critical role in promoting the PS. This can be achieved through different strategies centred on education, access to healthcare services, provider incentives, policy and legislation, as well as data collection and surveillance. Some studies have also emphasised the significance of government policy change, such as mandatory screening, financial support and community outreach activities aimed at sensitisation, education and screening for cervical cancer.32 37 As the results showed, it is recommended that health policy-makers and planners enhance PS by offering free testing in healthcare centres, mandating cervical cancer screening for specific populations, providing education and incentives for healthcare providers to encourage them to recommend and provide the PS to patients, removing barriers to healthcare service access, disseminating health-based content through different channels including mobile phones, radios and television broadcasts, and particularly online sources. It is crucial to promote and update healthcare providers’ professional skills through in-service workshops.
Limitations
This study had certain limitations. It was conducted in only one city in Iran with a particular context, which limits the generalisability of findings to other populations or settings. Furthermore, the COVID-19 pandemic resulted in a relatively low willingness among women to participate in interviews about cervical cancer. Focus group discussions could have potentially provided deeper insights. Yet, this research method was not feasible due to the constraints of the pandemic. Consequently, face-to-face interviews were held, with some of them at a place other than the health centre as a precautionary measure to minimise the risk of disease transmission.
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