Low level of awareness among Iranian women concerning cervical cancer and screening: the role of knowledge, risk perceptions and cues to action

Background Iran has a low incidence of, but a higher rate of death from, cervical cancer (CC). The country is in the process of implementing an organized screening program including HPV testing and cytology. Studies show high drop-out in continued testing among eligible women. This qualitative study aimed to explore women’s awareness regarding CC and CC testing, and the role of knowledge, perceived risk and cues to action in this process. Methods We recruited 81 women aged between 25-65 years, who participated in 15 focus group discussions (FGDs) and two in-depth interviews in Tehran, the capital of Iran. Data were acquired through 11 open-ended questions and 32 related probe questions. All interviews were transcribed and independently analyzed by two researchers (Kappa and agreement testing respectively: 0.77, 97.11%). Results Coded texts were categorized under three themes and 13 subthemes. The three thematic areas referred to knowledge, cues to action and perceived risks regarding cervical cancer and screening. Results showed that women had inadequate and unspecified knowledge about cervical cancer and screening, compounded by misconceptions regarding infection and cancer prevention measures. Social and cultural barriers hindered proper communication between health system/providers and clients, and within communities on subjects related to cervical cancer and screening. Perceived risk of getting CC was low due to insufficient knowledge regarding the causes of cancer, difficulty in differentiating between cancer and sexually transmitted infections, and the absence of visible symptoms. Conclusions The results indicate a strong need to invest more efforts to improve health education and communication in the current national health program to promote awareness of the need to screen for CC, through, for example, establishing correct knowledge and risk perceptions among women. In addition, this intervention should address women’s social environment in order to prevent misconceptions being communicated to women.

6 countries, with limited awareness about cervical cancer considering cultural, social and religious sensitivities. In addition these findings will be helpful for developing effective health promoting interventions for Muslim women from Islamic countries living in the western or non-Islamic countries as well in order to provide them culturally tailored information suitable to their background. (43)(44)(45).

Methods
This qualitative study was conducted using Focus Group Discussions and In-depth interviews. We have used four-dimension criteria to ensure and explain trustworthiness of the study in all steps from design to implementation, analysis and interpretations. For this purpose we have used "the Four-Dimension Criteria" (46) which was summarized in table1 and explained in details subsequently. The semi structured interview guide for this study was composed of 11 main open-ended questions and 32 related probe questions (annex 1). The interview guide was based on the I-Change model (38) and focused on knowledge about cervical cancer (CC) and Pap smear testing, perceived susceptibility and severity of CC, cues to action, advantages and disadvantages of testing, as well as barriers and motivating factors, self-efficacy, and action plans. For this paper we focused only on awareness factors (pre-motivational components) and related constructs including knowledge, perceived risk and cues to action. The interview guide was reviewed by a group of experts and tested in two FGDs with eligible women (N=12) and it was used in the study after finalization regarding method and language. The study has received ethical clearance by Tehran University of Medical Science (TUMS) (reference number 24890, 11/08/2014) and was registered in Iran Clinical Trials (IRCT2014092918120N1) (47) .

Setting
The study was carried out in Tehran-Iran, a metropolitan city with 8 million inhabitants.
The municipality of Tehran has categorized its 22 districts (zones) into five categories using the Urban Health Equity Assessment and Response Tool (Urban HEART) which takes health and social determinants (48). A reference indicator for this classification was life expectancy at birth. We recruited our population study from randomly selected districts from all determined categories as shown in table 2. two in-depth interviews with employed women with higher education, which were introduced by PHC staff based on a request of the researchers.

Data collection and analysis
RTA (MD, MPH) and SZ (PhD in health education), both with good experience in qualitative research design and implementation, moderated all interviews during January to May 2015. Each interview was run by two researchers (always female and male together), one as interviewer/moderator and one as note taker., one as interviewer/moderator and one as note taker.
The interviewers are introduced to interviewees by PHC staff; then they gave a brief introduction of the interview and its objectives. Subsequently, the process and ground rules of the interview (time, role of facilitator and interviewees, respect and confidentiality) were explained and a consent form was read for all. The consent form clearly stated that results would be published for scientific purposes with consideration for confidentiality and anonymity of interviewees. Participants were informed that they could decide to stop and terminate the interview at any time without having to give an explanation. Before starting the interview, they were asked for consent for audio recording of the whole interview. All women who provided verbal consent continued participation in the interview. Each interview was continued with an introduction and collection of information on demographic characteristics (age, marital status, employment, literacy) and completed in approximately 60 minutes.
After finishing each interview, both the moderator and note taker reviewed the notes taken and consolidated them to be incorporated in the interview text when the audio file was transcribed. All audio files were transcribed literally by a typist and double-checked by the interview team and transcribed data descriptively reviewed to identify variation and similarity of information and expressions between FGDs while interviews were in progress. All names were coded in the interviews and finally transcribed data was used for detailed analysis.
All transcribed interviews were entered in NVIVO 10 and two interviewers applied inductive content analysis. Randomly selected four FGDs (4,5,9,11) Table 3 shows a summary of the demographic characteristics of interview participants. No illiteracy was reported and five out of 81 respondents (6%) reported having completed university education.

Knowledge about cervical cancer and cervical cancer screening
The results of the interviews revealed that women's knowledge and information about cervical cancer, the signs and symptoms of disease, as well as cervical cancer testing, was neither specific nor explicit. Tacit knowledge is embedded in practical experiences, not achieved through systematic or formal trainings, and not from standard documents, and it is nonspecific. By contrast, explicit knowledge is evidence-based, specific and precise knowledge which could be articulated and communicated systematically (50).
The results revealed different subthemes for this area, which are discussed below.

Lack of explicit knowledge on cervical cancer
Most of the women had heard about cervical cancer in general, but had not specifically mentioned the exact name of cervical cancer in the discussion. According to participants, older women have less knowledge than the younger generation. The majority of interviewees were also unable to differentiate between cervical cancer and other genital cancers (e.g. uterine cancer) and did not know the affected organ.

"We don't know anything about this (cervical cancer), we just know that a test is taken every six months or every year to see if a woman has uterine cancer or not." (participant 1, 56 yrs.)
Half of the participants (almost equally distributed over the socio-economic classes) referred to cervical cancer using nonspecific terms, mainly "women cancer" or "uterine cancer" without differentiating uterine and cervix.
"…among the general population, I don't hear anyone say cervical cancer, it is called uterine cancer." (participant 13, 56 yrs.).
Participants from low and lower-middle socio-economic groups (SEGs) reported the least accurate and explicit knowledge about cervical cancer in general, while inaccurate knowledge (content and frequency) was almost the same among all SEGs.

Limited knowledge about signs and symptoms
Most women did not recognize signs and symptoms of CC specifically and explicitly. They did not differentiate between CC and sexually transmitted infections (STIs), nor their signs and symptoms.

"I think this cancer is very silent and the one that is affected does not see any symptom
and cannot identify the disease herself." (participant 55, 50 yrs. Women in the upper and lower-middle SEGs expressed more accurate knowledge about signs and symptoms than the high and low SEGs. Inaccurately assigned STI-related signs and symptoms to cervical cancer were very frequent among all groups.

Lack of specific knowledge on testing purpose, frequency and timing
The majority of women knew about cervical cancer testing but their knowledge in most of the cases was nonspecific and inaccurate concerning the purpose and frequency (timing) of testing.

Deficit in knowledge about risk factors and causes
Most women wrongly mentioned cervical cancer as a consequence of STIs, more specifically prolonged/chronic infections, and also described family history as a main risk factor for CC. In addition, they listed other risk factors, including multiple partnerships, and misconceptions about hygienic measures for self-protection were highly stressed by almost all women.

Appropriate knowledge on conditions/ requirements for testing
The majority of women were aware of practical preparatory measures and recommended considerations required before attending CC testing. They stated practical terms and conditions for testing including sexual abstinence, avoiding the use of vaginal douche and vaginal treatments (gel and cream), and recommended scheduling testing when not the menstruating.

"In general no (vaginal) discharge should exist (at the time of testing) to avoid incorrect results of the test and a week should have passed after menstruation. Additionally, sexual intercourse should not have taken place in the previous 24 hours (before testing) and
(vaginal) ointments should not be used during the previous 48 hours. " (participant 74, 26 yrs.).
All groups excluding the high SEG elaborated on in detail the required preparedness before testing.

Limited and unspecified knowledge on preventive measures, care and treatment
Almost all women indicated not knowing how to prevent cervical cancer; they indicated that they were simply advised to perform the test.

"In fact, we don't know what to do or not to do, to avoid facing the problem (of getting cervical cancer) we do not know anything in this regard at all, we only know that a test is being taken, every six months or year, to identify if uterine cancer exists or not." (participant 1, 56 yrs.).
Most women understood that CC testing was a way to detect STIs early (without mentioning HPV) and they believed that STI prevention was essential in cervical cancer prevention. A few participants mentioned condom use as a preventive method. Only two women mentioned the availability of a vaccine and its preventive role; both women were highly educated.

Inaccurate perceived risk of cervical cancer and screening
In general, the proportion of women who very frequently cited their lack of perceived risk were almost the same in all SEGs. There was an overall low perceived susceptibility and high perceived severity among participants regarding cervical cancer. Most women believed that CC was a curable disease. However, extended social and cultural consequences of cervical cancer seem to lead to an increased perception of the severity of CC, causing some fear.
This theme was categorized under two subthemes which explain three main factors related to risk perception: misperception of cause, misconception about STIs and cervical cancer, and avoidance of negative thinking.

Low perceived susceptibility to CC due to misconceptions
Insufficient knowledge about the cause of cervical cancer resulted in misconceptions regarding vulnerability to cervical cancer. Overestimation of the role of heredity of cervical cancer was an important misconception among women; most women considered themselves not at risk because there was no (known) history of cervical cancer in their family. They specified insufficient hygiene as an important risk factor for CC and perceived an association between STIs and cervical cancer. As a majority of women evaluated their personal hygiene measures as being sufficient to prevent infections, they did not consider their CC risk as high. Those measures (e.g. changing underwear, washing themselves after sexual intercourse, not using toilet paper) pertain to cleanliness rather than specific hygienic measures.

Aggravated severity due to social and cultural misperceptions
Most women reported a high perceived severity of cervical cancer; severe consequences also included disruption of family life and social image.
"… (women are) concerned that when it is known that they have cervical cancer, their life will be disrupted." (participant 58, 43 yrs.).

Lack of perceived cues to action regarding cervical cancer
Most women reported few cues to action from their environment, also due to an existing stigma on CC in their community, and discrimination against women. Two different types of cues were mentioned, external cues and internal cues.

Culturally limited interpersonal and public communication about cervical cancer
All women strongly emphasized the need for health communication and education on cervical cancer and CC testing. Most women indicated that talking about issues related to the sexual organs including cervical cancer and testing is stigmatized according to cultural and social norms. In comparison to other groups, the low SEG indicated a lack of communication about cervical cancer more frequently as a barrier to awareness. Different information sources were listed, including HCPs, television, peers (relatives and volunteers) and others (internet, publications). Face-to-face counseling by public health services and health care providers (HCP) including physicians, midwives and others, was mostly preferred by women, as these consultations were mentioned as being transparent, and provided the opportunity to pose questions. The lack of interaction (i.e. posing questions and receiving answers) was regarded as the main disadvantage of health education through the public media (e.g. television).

"The Public Health Center is credible (for health education); when I am in a Public Health
Center I feel comfortable because I can ask my questions to doctors here, but in that case (TV education) I cannot ask questions to anybody." (participant 47, 35 yrs.).
Women indicated being confident about having the comprehensive knowledge about HCPs (particularly doctors) and trusting them. They were concerned that senior professionals spend less time with patients for health education. A need for health education was commonly expressed among all SEGs, with a higher frequency among high and upper-middle SEGs with the above-mentioned preference scheme.

Health Care Provider (HCP) as main external prompt
Being advised to go for screening by HCPs appears to be a very important cue encouraging attendance. Most of the women stated that they only participated in tests when their HCP advised them to do so; otherwise, they would not go for tests unless they had symptoms that might point to an STI.
"Whenever my doctor advises me to go for a test I go otherwise I would never go by myself, unless I had complaints. " (participant 39, 50 yrs.).
The advice of a health care provider was mentioned more often as the main motivation for testing among women in the upper-middle SEG than among women in the other SEGs

Socially imposed self-deprioritization and misinterpretation of symptoms
There was a general lack of perceived cues to initiate CC testing (apart from HCP advice); for most women, CC testing, and more generally personal health care, was not a main priority. Many women indicated that Iranian women prioritize family and household as a social value and criticize caring about personal health. Limited awareness of symptoms of CC is causing a misinterpretation of being healthy in the absence of visible symptoms, and neglecting routine examination and testing as follow-up. All groups very frequently expressed discrimination against women, self-deprioritization and misinterpretations of symptoms as barriers to participation in cervical cancer testing, with a slight dominance among high SEG.
A summary list for each main theme and related subthemes is provided in table 4.  (33,34,37,52). We found that women regarded themselves at risk concerning STIs; however, they had poor understanding of the purpose of CCS. In concurrence with other studies, our respondents considered CCS as an intervention for STI management (27,(56)(57)(58). A misconception was found concerning the role of cleanliness and hygiene to prevent STIs (HPV infection specifically) and cervical cancer, and similar findings have been reported by other studies (33,52). However, the absence of STI symptoms did not make women feel a need to go for screening.
Thirdly, with regard to cues to action, our respondents disliked discussing and thinking about cervical cancer and their existing symptoms, due to local beliefs about the consequences of such thinking and discussions, a finding reported in other studies (24,27,52,59). Consequently, receiving a cue to act as a result of discussions with others is rare in Iran. HCP advice on performing a CC test was found to be a crucial factor -if not the most crucial -for undergoing screening. Women emphasized that despite all existing barriers and lack of awareness regarding cervical cancer and testing, they attended CC screening when their physician advised them to do so. Other studies also reported this positive influence (20,60,61).
Previous local studies showed a positive correlation between health literacy for cervical cancer and income level (62), a higher concentration of cervical cancer among lower socio-economic groups in Tehran (63), and delayed diagnosis of CC among lower SEG (64).
However, our findings did not indicate a constant pattern and do not suggest differences in awareness, knowledge and risk perceptions between participants with different socioeconomic backgrounds. Health education and communication interventions are therefore suggested in all SEGs while further quantitative studies are recommended.
To our knowledge, this was the first comprehensive qualitative population study on this subject in Tehran conducted with the participation of a large number of participants from diverse SEGs (spread over the city). Moderating interviews by two experts of both genders and the openness shown by interviewees were other positive points of this study. The results of this study provide a wide range of comprehensive data on the above-mentioned thematic areas and advocate the development of health communication interventions to promote adequate uptake of cervical cancer testing in Iran. However, the status of sociocognitive factors related to CCS adherence should be further investigated to broaden understanding on this subject. In addition, quantitative studies are needed to identify statistical differences between groups and to identify which variables are most important for the realization of awareness of CC and CCS. and to explore the association of individuals' characteristics and identified factors with outcomes.
Although there is now a vaccine against cervical cancer, this is not yet available in Iran.
Future preventive actions could entail making this vaccine available and to provide information about this, a strategy which is advocated by the WHO suggesting to achieve a high coverage with both vaccine and a very sensitive screening test like a HPV test (18).

Conclusions
The results of our study indicate low and implicit knowledge about CC and the preventive role of cervical cancer testing. In addition, women reported a low level of perceived susceptibility along with misconceptions influencing their uptake of preventive measures.
Health communication campaigns, preferably using face-to-face methods in Public Health Centers, should therefore stress correctness, explicitness of knowledge and the importance of preventive measures and possible consequences of CC screening ignorance and late detection. Campaigns should emphasize that a negative family history of CC is no guarantee for not getting CC, as hereditary factors only play a minor role. HCPs and, more specifically, physicians were mentioned as trusted and preferred sources of education and their advice is one of the most influential factors for attendance, indicating that they can play a vital role in the success of health communication campaigns for CCS in Iran.

Authors' Contributions
RTA, HDV, NDV, LVO, KZ and MS designed the study, supervised the project, data abstraction, and data analysis; and FZ has contributed in data collection, abstraction and analysis. They prepared the initial draft and finalized it based on internal reviews and discussions among authors. All authors reviewed each manuscript draft, participated in interpreting the results, and approved the final version.