Cervical cancer knowledge and barriers and facilitators to screening among women in two rural communities in Guatemala: a qualitative study

Background Approximately 80% of deaths due to cervical cancer occur in low- and middle-income countries. In Guatemala, limited access to effective screening and treatment has resulted in alarmingly high cervical cancer incidence and mortality rates. Despite access to free-of-cost screening, women continue to face significant barriers in obtaining screening for cervical cancer. Methods In-depth interviews (N = 21) were conducted among women in two rural communities in Guatemala. Interviews followed a semi-structured guide to explore knowledge related to cervical cancer and barriers and facilitators to cervical cancer screening. Results Cervical cancer knowledge was variable across sites and across women. Women reported barriers to screening including ancillary costs, control by male partners, poor provider communication and systems-level resource constraints. Facilitators to screening included a desire to know one’s own health status, conversations with other women, including community health workers, and extra-governmental health campaigns. Conclusions Findings speak to the many challenges women face in obtaining screening for cervical cancer in their communities as well as existing facilitators. Future interventions must focus on improving cervical cancer-related knowledge as well as mitigating barriers and leveraging facilitators to promote screening.

alarmingly high cervical cancer incidence rate of 20.3 per 100,000 and a mortality rate of 11.9 per 100,000 women in 2018 [2]. Surprisingly, given the high burden of cervical cancer in the country, cervical cancer screenings are provided free-of-cost through the Guatemala Ministry of Health (MOH) [3], both through local women's health clinics and contracts with nongovernment organizations (NGOs) [4]. In the early 2000s, NGOs in Guatemala introduced visual inspection with acetic acid (VIA) and cryotherapy as an alternative to cytology-based screening (i.e. Pap smears) [4]. VIA was formally integrated into the national cervical cancer screening program in 2008 and now accounts for the majority of cervical cancer screenings in the country [4]. In 2015, the MOH launched a pilot implementation trial for human papillomavirus (HPV) testing in urban settings to evaluate its feasibility as an alternative to traditional screening methods [5].
Despite these services, approximately 64% of women in Guatemala report lifetime cervical cancer screening, with lower rates among indigenous and rural women [6]. This disconnect suggests the need for a more nuanced exploration of the barriers women in Guatemala face in obtaining cervical cancer screening. Extant literature in other LMIC settings suggests that limited cervical cancer knowledge [7], fear of the procedure [7] and possible positive test results [8], embarrassment [7,9] and competing costs [8,9] present significant barriers to cervical cancer screening. In Guatemala in particular, cost and distance, permission required to attend, not wanting to attend screening alone, and language discordance with providers were found to be associated with never being screened [6]. In addition to these barriers, even if women are able to access screening, its effectiveness in reducing cervical cancer incidence and mortality further depends upon access to follow-up care and treatment, which are also often lacking [10].
In August 2020, the World Health Assembly adopted the Global Strategy for the elimination of cervical cancer to reduce the age-adjusted incidence rate of cervical cancer to less than 4 per 100,000 women-year in all countries by the end of the century through the promotion of HPV vaccines, screening, and treatment [11]. In light of this global effort, a better understanding of the reasons why free-of-cost screening in Guatemala has not resulted in improved cervical cancer outcomes is warranted. To our knowledge, the present study is the first to utilize in-depth, qualitative interviews to elucidate barriers and facilitators to cervical cancer screening among women in two rural communities in Guatemala.

Study setting Santiago Atitlán, Sololá
Santiago Atitlán (Santiago) is a majority Maya-Tz'utujil community on the southern shore of Lake Atitlán. Santiago's roughly 45,000 inhabitants live in 20 cantones or neighborhoods, located in the town's center and spreading out to more rural, surrounding neighborhoods. Nearly all of Santiago's inhabitants speak Tz'utijil as their first language and Spanish as a second language. A small proportion speak only Tz'utujil [12].

Livingston, Izabal
Livingstonl is situated on the Caribbean coast of Guatemala and is accessible only by boat. Livingston is an ethnically diverse community with a large Garifuna (Afro-Caribbean) population as well as Maya-Q'eqchi and Ladino (mixed-race) populations. Most inhabitants speak Spanish and either Garifuna or Q'eqchi [13].

Study population
Participants were recruited from a larger pool of women who had been sampled to participate in the HPV multiethnic study (HPV MES), which involved completing a quantitative survey on prior screening behavior and acceptability of Human Papillomavirus (HPV) self-collection sampling to screen for cervical cancer, as well as the opportunity to participate in self-collection HPV-based screening [13]. In brief, participants in Santiago were randomly sampled through stratified multilevel sampling based on maps and population counts. Due to lack of census data, participants in the larger study in Livingston were recruited through convenience sampling. Details and main results of this study are described elsewhere [13,14]. Following completion of the quantitative survey, women consented to be contacted for an in-depth, semistructured interview. Interview participants in both communities were sampled purposively by neighborhood.

Community partners
The study team worked collaboratively with community partners at both study sites. In Santiago, the team worked with local health clinic, Rxiin T'Namet, which provides family and reproductive health services to residents, including workshops and community outreach. In Livingston, research was supported by a local HIV-focused health clinic, Iseri Ibagari. The clinic provides HIV testing, referrals for treatment, and health education workshops focused on reproductive health. Both community partners helped to publicize the study to the larger community and provided private spaces for in-depth, semistructured interviews.
All study procedures were approved by the Institutional Review Boards at the University of Michigan (HUM00096559) and the Instituto de Nutrición de Centro America y Panamá (INCAP) (MI-CIE-16-009), located in Guatemala City.

Data collection
Interviews were conducted privately in the women's homes or spaces provided by community partners. Interviews were conducted in Spanish by the lead qualitative investigator and began with the administration of informed consent in the participant's preferred language. An interpreter provided real-time translation for participants in Santiago Atitlán who completed the interview in Tzu'tujil. Interviews lasted 60-90 min and followed a semi-structured interview guide to better understand the barriers and facilitators to cervical cancer screening faced by participants (Table 1). Interviews were conducted until common themes suggested data saturation as it related to our major research questions. All interview were recorded and transcribed verbatim by native Spanish speakers. Those conducted in Tzu'tujil were translated and transcribed into Spanish by a native Tzu'tijil speaker.

Analysis
Utilizing an adapted Framework Analysis approach [15], the transcribed data were analyzed by three Spanish-speaking study team members who independently reviewed five transcripts for emergent themes that related to the original research questions. Codes were created to characterize emergent themes and revised in an iterative process to ensure coverage and reliability between coders. The resulting final codebook included 56 codes, their definitions, and examples of each code ("Appendix A"). The remaining 16 transcripts were each coded by two of the three Spanish-speaking study team members; coding inconsistencies were reconciled by the lead qualitative investigator and organized using NVivo 9 (QSI International). Data were then organized by theme using an analytic matrix, which was reviewed by the lead investigator and a fourth Spanish-speaking study team member. Illustrative quotes were selected relating to salient themes and subthemes and translated into English. Translations were reviewed by two native-Spanish speaking members of the research team for consistency with their original significance.

Results
Twenty-one women (Santiago Atitlán, n = 10; Livingston, n = 11) were interviewed. Participant demographics, stratified by community, are provided in Table 2. Women in Livingston had higher average household incomes, educational attainment, and literacy. Marriage rates in both communities were comparable. About 80% of women in both communities reported having ever been screened for cervical cancer.

Cervical cancer and screening knowledge and beliefs
Cervical cancer knowledge discussed in qualitative interviews was variable across sites and across women. Overall, women in Livingston shared greater cervical cancer knowledge than women in Santiago, though several women at both sites reported no cervical cancer-related knowledge. This knowledge difference is supported by previously published quantitative findings among the larger HPV MES sample, which found higher knowledge of HPV and perceived severity of cervical cancer in Livingston [13]. In Livingston, the majority of interview participants had heard of cervical cancer and several women reported knowledge related to cervical cancer development and symptomology, including that it is often asymptomatic, resulting in later-stage diagnoses and poor prognoses for women who are not regularly screened. Women at both sites, including those self-reporting lower levels of knowledge spoke of the connection between cervical cancer and sex, though few mentioned HPV. Many discussed this relationship in terms of male partners engaging in extra-relational sex with other women or with sex workers, as well as women themselves having multiple sex partners. In turn, women discussed the need to "cuidarse" or take care of oneself within the context of sexual relationships. When asked what it mean to take care of oneself in relation to cervical cancer, one Santiago participant explained through an interpreter: She has heard that to take care of herself, she shouldn't sleep with other men. Because she heard that when men have sexual relations with a lot of women…it's possible that you get infected with this illness. (Santiago, Tzutujil, Age 30-35, Neverscreened) Knowledge related to cervical cancer screening also differed greatly across participants. In both Santiago Atitlán and Livingston, several women reported no knowledge of cervical cancer screening but familiarity with Pap smears specifically, suggesting that women may obtain screening without understanding its purpose. When asked if she had heard of a test to detect cervical cancer, one participant in Santiago responded:

Barriers to cervical cancer screening
Women across both communities expressed similar barriers to obtaining cervical cancer screening. Barriers generally fell into one of three, often intersecting, categories: individual, interpersonal and system-level. At the individual level, cost was the most commonly cited barrier. Though all women in Guatemala are entitled to free cervical cancer screening through publicly run women's health clinics, in practice ancillary costs including transportation, food, and loss of income pose significant barriers to screening. Women also perceived the cost of future tests and treatment that may result from a diagnosis as a barrier to seeking screening. When asked why she had never been screened, one participant in Livingston explained: Women understood this both abstractly and from personal experience. Among those who had previously received screening, two women shared their own stories of being unable to afford treatment after a positive screening. One participant from Livingston recalled being unable to afford a biopsy after doctors found a lesion on her cervix during a routine Pap smear: At the interpersonal level, several women cited male partners as a potential barrier to obtaining screening among women, citing a culture of "machismo" in which women are seen as subordinate to men [16]. This barrier was twofold: men who exert economic control over their female partners may refuse to provide the money for screening or male partners may withhold permission, explicitly or tacitly, for their female partners to obtain a screening. Women described how knowledge acquisition related to cervical cancer was also informed by gender norms.
I also think it's machismo. The majority of women live with machista men, they demand order, food, everything in the house. So I think this also influences the lack of knowledge. (Livingston, Garifuna, Screened) Fear was also a barrier commonly expressed by women in both communities. At the individual level, fear of pain or discomfort during the screening itself was common among screening-naïve women.
[ Women in both communities expressed fear of embarrassment or vergüenza of being seen by a doctor or other healthcare worker. Notably, this fear often presented a barrier to seeking screening even when free-of-cost screening was available. Often this fear centered on the need for a healthcare provider to view intimate body parts to conduct the screening. Fear of disclosure of personal information was another barrier. In both communities, women cited personal experience or experiences among their friends and family in which their medical confidentiality was violated. This fear stemmed, in part, from the fact that healthcare workers were often well known in the community or even related to their patients. Further, general concerns about treatment by providers presented a barrier to screening for many women. In Santiago in particular, indigenous-identifying participants described experiences of discrimination when obtaining screening at the local health center.
[ Due to shortages, women often sought screenings through traveling health campaigns or "jornadas"; however, these options also presented challenges. When describing the process for obtaining a free screening at health campaign in Livingston, one participant explained: Barriers to obtaining a free or low-cost screening in turn, create a tiered system in which those women who could afford to pay out of pocket for a screening at a private clinic, were more likely to seek care. Speaking about healthcare more broadly, one woman in Santiago Atitlán explained:

Facilitators to cervical cancer screening
Despite significant barriers to screening, a large proportion of our sample reported being screened at least once in her lifetime and women described several facilitators to screening. In both communities, the desire to know one's health status motivated women to obtain screening. Women also described interpersonal and system-level facilitators that promoted cervical cancer screening. Though not consistent across participants, some women expressed that provider-communicated screening guidelines prompted them to obtain screenings. When asked how she knew to obtain her first screening, one Livingston resident replied: At the system level, health campaigns, or "jornadas", outside of the public health system also facilitated screening. Women often traveled to nearby towns hosting health campaigns for a variety of health services. However, as discussed above, several women described health campaigns as irregular, lacking follow-up and often tied to some other event. In one extreme example, a participant from Santiago obtained her first and only Pap smear during the aftermath of Hurricane Stan in 2005, which resulted in mudslides that killed over 1000 residents.

I got my Pap smear after the accident caused by
Hurricane Stan. That day, they set up shelters for people and they came from the health center to do a health campaign and I took advantage to get my Pap smear. (Santiago,Tzutujil,(30)(31)(32)(33)(34)(35)Screened) In this way, such health campaigns may facilitate access for individual women, but their irregularity may also present barriers to care if they are women's only screening option.

Discussion
Cervical cancer is a major public health concern for women in LMICs, where barriers to screening often prevent early diagnosis and treatment [6,17,18]. The present study sought to examine the cervical cancer knowledge and barriers and facilitators to screening among a sample of women in two rural communities in Guatemala. Barriers and facilitators at the individual, interpersonal, and system levels were identified by women in both communities.
Limited knowledge related to cervical cancer was common but differed across women and site. These findings are in line with previous quantitative and qualitative research in Guatemala [19] and other LMIC contexts [20][21][22]. Notably, while some women reported no knowledge of cervical cancer screening in general, they were aware of and, in some instances, had obtained screening. This discordance suggests that women may be screened by healthcare providers during other health care visits without adequate explanation of the purpose of the procedure or its risks. This is congruent with other provider-related interpersonal barriers to screening reported by women in our sample, including poor communication, experiences of discrimination and distrust of healthcare providers as well as earlier research which found patient/provider language discordance to be a barrier to screening [6]. In contrast, community health workers (CHWs) and workshops were identified by women as facilitators to screening. CHWs have been found to be effective in increasing cervical cancer knowledge among women in other LMIC settings [23] and task shifting from physicians to CHWs has been found to be an effective strategy for the management of non-communicable diseases, including screening [24]. Our results suggest that interventions to improve screening may include promoting the integration of CHWs in clinical settings to facilitate patient-provider communication and to ensure women understand screening recommendations and the risks and benefits of cervical cancer screening.
Resource limitations were also a major barrier to screening for most women. Despite the availability of free-of-cost screening to women in Guatemala through government-funded women's health clinics, few women reported being able to access these services due to the associated costs of travel or food, barriers that have been identified in other LMIC settings [8,9,25,26]. Cost of future procedures associated with a positive screening was also a concern and several women described personal experiences in which they were unable to afford follow-up care associated with a positive screening. Gender norms related to economic control also presented a barrier to women whose male partners were unwilling to provide needed funds to obtain screening. Interventions to limit ancillary and future costs, including minimizing the need for and/or subsidizing the cost of travel, must be considered when developing future screening programs to promote utilization of free or low-cost screening and to reduce help minimize potential interference by partners.
At the system level, shortages of materials, long wait times and irregularities in service also hindered women's ability to access government subsidized services. Through formal agreements with the Guatemalan government, non-governmental organizations (NGOs) provide a significant proportion of healthcare services throughout Guatemala, including approximately 15% of cervical cancer screenings [4]. Though health campaigns implemented by NGOs helped supplement governmental programs, irregular scheduling, shortages of tests and similar cost-related barriers also plagued these programs. As such, the implementation of less resource-intensive screening methods [5] by governmental programs and NGOs is an important step to addressing these barriers.
Despite significant barriers to screening, most participants reported at least one previous cervical cancer screen and women identified several important facilitators to screening, including internal motivation to maintain one's health, health campaigns and formal or informal conversations with other women. Programs to improve cervical cancer screening should leverage women's own desire for good health and the power of interpersonal relationships in fostering health promotive behaviors, while reducing financial and logistical barriers to screening. For example, at-home self-screening for HPV has been proposed as one method to improve cervical cancer outcomes in LMICs, as this type of screening can assuage barriers such as cost (test can be performed in home) and embarrassment (test can be performed by in private, by women themselves) [14].

Limitations
The findings of this study should be understood in the context of its limitations. Women who chose not to enroll in the larger HPV MES cohort and those who did enroll but chose not to participant in the qualitative interview may be systematically different from those who agreed to participate. With 21 interviews, our sample is relatively small; however, interviews were conducted until saturation was reached [27] and guidelines suggest that 20 interviews may be sufficient for qualitative convenience samples [28]. Social desirability bias may have impacted women's responses during interviews. The sensitive nature of the interview was described to participants during recruitment and steps taken to ensure participant privacy were explained in detail at the start of each interview and throughout conversations.

Conclusions
The World Health Organization has identified the "robust understanding of the social, cultural, societal and structural barriers to the uptake of services" as a strategic action necessary to achieve the elimination of cervical cancer [29]. This study is the first to our knowledge to qualitatively examine cervical cancer knowledge and barriers and facilitators to screening among women in two rural communities in Guatemala. Our findings speak to the many challenges women face in obtaining screening for cervical cancer in their communities but also to existing facilitators that may be leveraged for future interventions. Future research must focus on mitigating barriers through education and alternative screening methods.