Barriers and facilitators to cervical cancer screening among under-screened women in Cuenca, Ecuador: the perspectives of women and health professionals

Women who had never or rarely been screened for cervical cancer were recruited during gynaecological consultations at the Sociedad de Lucha Contra el Cáncer (SOLCA) hospital in Cuenca and during outreach activities of the SOLCA mobile unit in rural areas. Inclusion criteria were being older than 30 years old, speaking Spanish and not having had a Pap smear test in the last 3 years.

The recruitment of participants was conducted by the project researchers. After verifying the inclusion criteria and providing verbal information about the project, the invitation for participation in the FDG was issued. Table 3 presents information about the settings and participants of FDGs for under-screened women.

Health professionals (HPs) were recruited from SOLCA hospital, the mobile unit of SOLCA and the Hospital del Niño y la Mujer (maternal and children’s hospital) in the municipality of Cuenca. All physicians and nurses working in cervical cancer screening as their main activity at the time were invited to participate.

Recruitment of HPs was done through a written invitation to the directors of SOLCA and the Hospital del Niño y la Mujer. Each hospital director passed an invitation to HPs who met the selection criteria. Table 4 presents information about the settings and participants of FDGs for HPs.

At the individual level, several main barriers were identified by both the HPs and the women: lack of knowledge, lack of risk perception, lack of time, discomfort and fear. In particular, all participants reported that cervical cancer is not well known or often discussed.

“Women do not know what a disease like cervical cancer means. That is why they don’t consider Pap smears important... They do not have the correct information ... to be able to get screened. It is an unknown world for many people.” – Medical doctor, 27 years

“About cervical cancer … . Not in my family, and neither with my daughter, who is 20 years old. We have not dealt with this issue. None of us are familiar with this issue. The only thing we know is that it is dangerous.” – Woman, 50 years

A lack of risk perception, caused by a lack of knowledge, means that some women only seek medical attention when they feel symptoms. For many women, feeling healthy is synonymous with being healthy; therefore, they do not see any reason to get screened.

“I got screened because I felt bad, so I took it, the exam [Pap smear] to see if I had cancer of the uterus.” – Woman, 47 years

“There are some adult women who say: ‘I've never had a Pap smear and I'm not going to get it, because I never feel anything and I'm fine and nothing has ever happened to me.’” – Woman, 49 years

In general, the participants, especially the women, reported a lack of time as a significant barrier. They are expected to first finish all their household obligations before accessing health care. If they work, they need to ask permission to attend a health centre.

“So we go to the supermarket, we go to work, we pick up the child, we go to the meeting, we go to pay the bills, … and of course, we are busy, we do not have time to get a Pap smear.” – Woman, 49 years

Women also feel that they do not have the time for screening because they usually have to take care of others first and put their needs last, focusing on the well-being of their children and other priorities in their lives.

“Culturally, we as women have been left behind – that is, if you get sick, you are the last on the list and you have to heal yourself practically. That is the first mental barrier: we have to think about others and not think about ourselves.” – Woman, 45 years

Discomfort with the procedure was mentioned as a major barrier by both groups of participants. Several different aspects of discomfort were identified, the first of which was related to the fear of feeling pain during the examination.

“When that machine [speculum] is introduced, it hurts there, and ... I don't even know why, those things have always hurt me.” – Woman, 62 years

Another discomfort they mentioned was embarrassment. Women perceived cervical cancer screening as an uncomfortable and even denigrating experience.

“I think it's like one of the most degrading exams that one can have. It does not feel good. Yes, like degrading, uncomfortable. I think that sometimes it doesn't even hurt, but [it is uncomfortable] because of the tension and stress.” – Woman, 48 years

For some women, it is even more embarrassing if a male doctor performs the gynaecological examination: they would feel more comfortable if a female doctor were to do it.

“Maybe I can say that I would have more confidence with a female doctor because when it’s a male doctor, … I don't know. No, well, speaking for myself, since I live alone, I always get nervous when I am going to see a male doctor.” – Woman, 62 years

Participants even reported that they fear being mistreated or sexually abused during the consultation. Some women mentioned that some doctors flirt during consultations, while others even expressed fear of being raped.

“I have heard from friends that the gynaecologist, when he takes the Pap smears, touches her and puts his fingers in on purpose, that he does it roughly on purpose and that she feels that it gives him a certain pleasure … I saw him when he put his fingers in: he closed his eyes and yuck, that is horrible, and my husband was not there because he [the doctor] told him to stay out.” – Woman, 49 years

In addition, women reported poor communication between patients and physicians, claiming that some HPs do not take enough time to explain the procedure step by step. As a result, they do not understand the procedures and even fear them.

“The doctor did not explain or anything. He told me, ‘Well, go and lie down [on the gynaecological chair], and I'll do it [take the sample].’ From then on I was afraid to go. I said, ‘Now I'm not going to do anything again’, because it was horrible.” – Woman, 49 years

Finally, some women expressed fear of a possible positive result. Consequently, some women prefer not to be screened, ignoring the fact that early detection could save lives.

“For fear of the result. She had never had a Pap smear in her life until now, because of fear of the result. [Imagine that] suddenly [the doctor is] saying that she is going to die!" – Woman, 33 years

Empowering women to take control over their own health was considered important to improve uptake of cervical cancer screening.

“When you love yourself, you take care of yourself, you protect yourself, and you don't expect anyone to protect you as you protect yourself.” – Woman, 49 years

All HPs agreed that improving women’s health literacy is a priority to improve their knowledge and awareness regarding cervical cancer prevention. Sensitization should start at school and will motivate women to get screened.

“I think that with education and motivation it should start even at school and then at college and, well, at university.” – Medical doctor, 78 years

The lack of family support was considered an important barrier to cervical cancer screening. HPs reported that in some traditional rural communities, women need to ask their husband’s permission to get a gynaecological examination. This machismo (sexism) prevents women from getting screened, since men are often reluctant and women follow their advice.

“A woman of about 42 years old says, ‘I don't know, doctor, because my husband does not want me to do it.’” – Medical doctor, 40 years

Another reason why men might not approve is because sexually transmitted infections such as HPV could be detected during the medical consultation; this could be a proof of infidelity, for both men and women, and lead to divorce.

“When she had a positive human papillomavirus test, ... she was obviously a person of a certain level [of education], she asked, ‘How is this transmitted?’ And the doctor told her how it was transmitted, and she said [to her husband], ‘I want a divorce.’ It was like that. The doctor tried to explain, and calm her down, but the patient reacted like that … I will never forget.” – Nurse, 52 years

Facilitators linked to providing information were reported most commonly by HPs. They considered that increasing awareness of cervical cancer screening in communities and households will increase the acceptance of Pap smears and reduce the stigma. In particular, targeting husbands in preventive programmes could improve uptake of cervical cancer screening, since it would help break down barriers caused by the lack of knowledge regarding screening and the machismo in those communities.

“I say, ‘Bring him here [to the health centre] to convince him’, like a joke. I say, ‘Bring him to convince him’ [the husband].” – Medical doctor, 40 years

Cultural beliefs, even if they are based on misconceptions, constitute a barrier to examinations, as, for example, some women are afraid of getting sick or becoming infected during screening. Some women had experienced bleeding after having a Pap smear; therefore, they suspected that the material used in the procedure was not sterilized well. One participant even mentioned experiencing symptoms of a sexually transmitted infection after the screening.

“I was fine, and two days after I returned from the exam, it began to feel bad, … [I felt] itching, then a very ugly discharge. I got a very strong infection.” – Woman, 44 years

According to HPs, women who live in rural areas are screened less often due to the great distance they have to travel to reach health centres. They also believe that these women might be more afraid of having a Pap smear.

“In rural areas people are still afraid of going to the doctor to have a sample taken.” – Medical doctor, 61 years

In general, stigma related to Pap smears is a significant barrier, as some women thought that screening is mainly for women who have multiple sexual partners, such as sex workers, or for women who are victims of sexual abuse. As such, getting screened is not considered necessary for a ‘respectable woman’, and participating in regular screening could lead to discrimination by the community.

“Maybe sex workers [should go for routine screening] because they are in more contact with their clients, let’s say. For their safety they should, they should ... And women or adolescents who are already sexually active ... or girls who are raped, girls who are raped should also already have a Pap test.” – Woman, 56 years

Overall, some women believed that the main cause of the lack of adherence to routine screening is social inequity. Women who live in poverty, with a low educational level, have less access to screening.

“Social inequalities exclude more women, and women who are socially excluded – those who we consider more vulnerable in society – have less access to screening tests.” – Woman, 40 years

Moreover, Spanish is not the first language in some rural communities. HPs recognized that they themselves are not fluent in the local languages; hence poor communication is a bigger problem in these areas.

“In my indigenous community, we should look for possibilities to do [promotion] in Quichua [an indigenous language], because we try to involve them a lot, although I do not speak it [Quichua] 100 per cent.” – Medical doctor, 40 years

According to the HPs, including the community in health promotion activities – for example, through peer education or disseminating flyers in local languages – would not only increase knowledge about cervical cancer screening but would also help increase its acceptance.

“A great advantage in our community is that health promoters are indigenous, so they do not have language barriers, so they can help us with this type of promotion. We have even used some brochures in Quichua.” – Medical doctor 40 years

Also, the support of political and religious leaders in the community could help spread positive messages and might encourage the population to attend screening. Participants considered young community leaders more open to collaborating with this type of health promotion.

“We involved leaders. Some of them are young and very open to promote this type of procedure.” – Medical doctor, 40 years

“Talking with the priest. Maybe if the priest talks in the same church [during a religious service] it would be spectacular.” – Nurse, 52 years

HPs and women reported barriers related to both access to health centres and the quality of the health care services provided. In particular, they identified difficulties and challenges at every step of the cervical cancer screening process: from making the appointment to obtaining follow-up care.

Getting an appointment was described as a major difficulty, since the waiting time can be up to 3 months. In addition, once an appointment is made, it can still be changed, and women only find out when they arrive for their appointment on the day originally scheduled. As a result, many women are discouraged from returning to the health centre.

“I was going to my appointment one day, but they gave me another appointment for the next day, and then again [the next day]. They said, ‘Come tomorrow.’ I kept going all week, but no, [every time] they gave me an appointment for another day.” – Woman, 41 years

“If you call and they answer, you are lucky. If not, you spend a week calling and they never answer. If you are able to make an appointment, they give you one in three months: ‘Come on in on that date’, and so we go that day, and sometimes the doctor has gone on vacation, and there is no one to replace him.” – Woman, 41 years

Because of these problems, some women opt for cervical cancer screening at private clinics or non-governmental organizations. However, both the HPs and the women reported that due to the cost this is only accessible for those women who can afford this type of care.

“Because in the countryside it is very complicated for the mothers, so they are selling eggs or exchanging things to get money … They have to see how they can support the family. If they have to pay for their [cervical cancer screening] test and it has a very high cost, they do not go.” – Nurse, 54 years

The women also reported that the COVID-19 pandemic increased waiting times. In addition, they considered that HPs prioritized COVID patients, which made it is even more difficult to get an appointment at that time.

“If you get sick right now, they tell you, ‘Go to the health centre.’ But they don't attend to you. Right now it's more – because of COVID – ‘Go, or call the hospital’, yet they don't attend to you.” – Woman, 41 years

According to the women, the waiting does not end after getting an appointment. Once they have an appointment, they spend an entire morning at the health centre actually getting screened.

“Going to have a Pap smear at a health centre takes all day! The whole morning. People just don’t have that time.” – Woman, 47 years

After the sample is taken, patients wait another one or 2 months, which is the minimum time it takes to process the samples and share the results with the health centre. Participants thought that this delay compromises treatment if cancer is found.

“The result is given after three months.” A Pap smear is taken, and they say, ‘Come back for the results. You can come in about three months.’ And we go back after three months, and what if you have cancer? It will already be worse by then.” – Woman, 49 years

While some women reported that it took months before they received their test results, others even mentioned that they never received them, which of course hampers their trust in the health system. The HPs confirmed that indeed sometimes samples and/or results do get lost and that some women, therefore, have lost interest in cervical cancer screening.

“I went to the hospital to get screened. I swear I waited one, two, three, four, five, six months for the results, but they never came, and he [the doctor] told me that he is going to take another sample.” – Woman, 35 years

In general, the women showed little trust in the quality of health services; for example, some women were afraid of getting sick or becoming infected during screening. Some participants had actually experienced bleeding after having a Pap smear; therefore, they suspected that the material used in the procedure was not sterilized well. One participant even mentioned experiencing symptoms of a sexually transmitted infection after the screening. Unclean examination rooms also contributed to this general feeling of mistrust.

“I have been very suspicious of having to lie down and spread my legs on a stretcher where the sheet shows that it is completely dirty. There were hairs and black dots from the previous patient.” – Woman, 50 years

With regard to the quality of the test, the HPs also added that false negative results have made them lose trust in the sensitivity of the Pap smear.

“She was getting a Pap smear every year, and has had over 15 or 20 or 30 tests, or more, and … the next year she died with advanced cancer, and there is nothing that can be done.” – Medical doctor, 50 years

The HPs felt that this misinterpretation of Pap smears is caused by a lack of training of HPs in either obtaining or managing the samples, or due to poor reading skills of pathologists, resulting in a high number of false negatives.

“Doctors, not all of them, don’t know how to take a Pap smear. As the doctor said [referring to another participant], it is true, and we have seen here [in the hospital] that the Pap smear is poorly taken, poorly fixed and also poorly analysed.” – Medical doctor, 37 years

Finally, the HPs considered that there is in general a lack of investment in high-quality cervical cancer screening services. They mentioned that when additional examinations, such as HPV detection or colposcopy, are required, they need to refer patients to specialized health centres, as most health centres do not offer these services. Many of those patients then get lost to follow-up, since there is no system in place to manage or keep track of them at community health centres.

“I think we fall short in the treatment. We do a Pap smear and find an abnormality, so we need to do an HPV test or we need colposcopy and biopsy, so we send them [the patients] to another place and lose track of the patients.” – Medical doctor, 40 years

The women and HPs identified some options that have shown good results in improving access to health services. For example, both groups mentioned that mobile units can improve access to cervical cancer screening by removing barriers such as distance to health centres or lack of time.

“Mobile units that offer Pap smears, because, for example, women want to get screened, but because they live far away, first comes the economic aspect, second the time.” – Woman, 33 years

Reducing the cost of getting screened was also considered important to increase uptake, especially in poor communities where women do not have access to the public health system.

“Any test that is recommended in the communities should be free of charge, because if people already hear that there is no cost, they will go [for screening].” – Nurse, 42 years

Nurses also suggested that health centres could dedicate 1 day per week to Pap smears, to increase uptake and reduce waiting times.

“Health centres should do Pap smears at least once a week; on that day Pap smears are taken for all patients who want one.” – Nurse, 59 years

They also proposed linking cervical cancer screening with other health services, to increase uptake. They also suggested offering it opportunistically when women come in for other reasons, such as for pre-surgical examinations.

“On the surgery floor, before they go to have breast surgery or whatever, first thing you do is take a Pap smear.” – Nurse, 50 years

Furthermore, the HPs recommended using an appointment card to remind women when the next Pap smear should be done.

“When the Papanicolaou result is given, the next Pap test could be scheduled and written down on a card so that the patient does not miss her appointment and returns.” – Nurse, 35 years

Some nurses already applied a more active follow-up strategy by calling women who are lost to follow-up.

“We started calling patients who get lost. People leave us their numbers.” – Nurse, 54 years

In addition to these rather practical facilitators, the women also emphasized that HPs’ kindness and confidence in HPs would encourage them even more to go for cervical cancer screening. They pointed out that improved communication skills of physicians would contribute to increasing uptake of Pap smears.

“The respect and explanation that the doctor gives before the procedure. No matter if it is a man or a woman, it’s just that the doctor should always try ... to explain well.” – Woman, 35 years

Barriers to cervical cancer screening at policy level were mainly mentioned by the HPs. In their opinion, the national strategy for cervical cancer prevention is not well known by HPs in the field and therefore poorly implemented at operational level. Physicians added that there is no effective health promotion policy, including for cancer screening, which leads to poor knowledge among the population.

“There is some policy on cervical cancer, but in practice it has not been used as it should be.” – Medical doctor, 78 years

“Many of the patients have not been adequately sensitized regarding early detection, and there are no government screening programmes either.” – Medical doctor, 28 years

Moreover, the HPs mentioned that the current evaluation system inhibits cervical cancer prevention: they are expected to take a certain number of Pap smears per month, rather than being incentivized to reach under-screened women. As a result, some women are over-screened to reach numeric goals, while a large group of women are never invited.

“We do cytology or Pap smears among the same women ... We can't see the ones who live further away [never-screened women], because all we want is to meet the three or six patients they ask of us [on the target list] at the end of the month.” – Medical doctor, 37 years

Both the women and HPs believed they cannot influence political decisions, but some suggestions were made to improve cervical cancer screening programmes. First, all participants mentioned that national media campaigns could help to encourage women to get screened, by providing information on preventive medicine and how and where they can get screened for cervical cancer.

“Campaigns, so that the population knows about the exam [cervical cancer screening] or what they have to do in general.” – Medical doctor, 26 years

Women also suggested that offering screening in the workplace could remove various barriers such as limited time and a lack of engagement.

“I can tell you that I have done it [getting screened] periodically, because I worked in a public company, and they made us [get screened] practically every year.” – Woman, 58 years

Others even mentioned that the government should set up health programmes in which certain other benefits are conditional on getting screened. Even mandatory screening was considered an option, with a Pap smear a prerequisite for obtaining certain permissions at government level. In addition, some women had the experience of being screened in the workplace through occupational health programmes. Those initiatives reduce absence from work and the need to ask for permission to seek medical attention.

“It should be a programme that motivates [women to take up screening] and gives conditions and permission [to get screened at work]. It should be an obligation to take these exams annually.” – Woman, 50 years