Barriers to uptake of cervical cancer screening services in low-and-middle-income countries: a systematic review

1What is already known: Low-and-middle-income countries (LMICs) bear a disproportionate burden of cervical cancer mortality and there is limited knowledge on barriers to cervical cancer screening uptake across LMICS.

2Findings: Women in LMICs face individual level, cultural/traditional and religious, societal, health system, and structural barriers to cervical cancer screening. The underlying reasons for these barriers include limited information about cervical cancer and screening as a preventive strategy, poorly resourced health systems without screening policies, poorly implemented policies, generalised limited access to health services, and gender norms that deprioritize the health needs of women.

3What the findings imply: There is a need for education, information dissemination, and advocacy to dispel myths about cervical cancer, and implementation of clear cervical cancer policies and guidelines with prerequisite structures and resources across diverse health settings. Policies that support sexual and reproductive health and the rights of women should be strengthened and expanded and account for inequities in access for diverse groups of women. Education and awareness initiatives should be driven by local and community contexts, and engage community members and multiple stakeholders, including traditional and religious figures. In addition, the introduction and roll out of more modern screening approaches in LMICs should be prioritized to ensure more women are reached.

4Cervical cancer, although preventable and curable, is the fourth most common cancer among women globally. The burden is greatest in low-and-middle-income countries (LMICs) with age-standardized incidence rates varying from 75/100000 women in highest-risk countries to less than 10/100000 women in lowest risk countries. In 2018, approximately 90% of deaths occurred in LMICs. The remarkable geographic contrasts in cervical cancer incidence and mortality reflect differences in social and structural contexts associated with cervical cancer, and inequities in access to information about cervical cancer, prevention, screening, and effective cancer treatment facilities and thus indicate areas with the greatest need for interventions. Consequently, the World Health Organization’s (WHO) global strategy to accelerate the elimination of cervical cancer proposes a vision of a world where cervical cancer is eliminated as a public health problem by employing measures that are sensitive to women’s needs, their social circumstances, and the personal, cultural, social, structural and economic barriers hindering their access to health services.

5With almost all cervical cancer cases (99%) linked to human papillomaviruses infection (HPV), HPV vaccination is a key primary preventive strategy, with secondary prevention – screening - remaining a key component of the cervical cancer elimination toolkit, especially where there is low HPV vaccination availability, access, and uptake. Screening coverage of eligible women in most LMICs is on average 19%, compared to 63% in high income countries, and thus it is important to review identified barriers to screening uptake to address the burden in LMICs.

6We conducted a systematic review on barriers to uptake of cervical cancer screening services (including poor provision of services) in LMICs. The objectives of the review were to i) document and investigate the underlying reasons for poor uptake of cervical cancer screening services in LMICs, ii) identify research gaps, and iii) provide evidence for decision-making and policy interventions for improved programmes and actions to support the elimination of cervical cancer in LMICs. We used Brofenbrenner’s social ecological model to understand the dynamic interrelations among personal and environmental factors. First introduced in the 1970s as a conceptual model, the social ecological model was formalized as a theory in the 1980s and underwent revisions by Bronfenbrenner until his death in 2005. In his initial theory, Bronfenbrenner proposed that to understand human development, the entire ecological system in which growth occurs needs to be considered. In subsequent revisions, the model examines how human beings develop according to their environment, which includes society and the context which impacts behavior and development.

7The review was conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines and included LMICs, as defined by the World Bank based on per capita gross national income in 2020. The research question was framed using the broad population, concept and context (PCC) framework recommended by the Joanna Briggs Institute for Scoping Reviews and was defined as: “What are the barriers to the uptake of cervical cancer screening services in LMICs?”. The population was women (15 years and older) eligible for cervical cancer screening. Studies that examined HPV vaccination and included girls younger than 15 years old together with older girls and women were also included.

8Two authors (AJ and ZP) developed the search strategy. A comprehensive literature search was conducted in February 2021 in Scopus, Web of Science and Pubmed. No language or date restrictions were applied in the initial search. A search in Google Scholar using the keywords ‘cervical cancer screening’ and ‘barriers to cervical cancer screening’ was also conducted, aimed at finding studies that may not have been included in the findings from the major databases that were searched. We also searched the websites of the WHO, the International Agency for Research on Cancer (IARC), and the reference lists of all included studies for additional relevant articles. The search was initiated with keywords and refined by adapting search terms from relevant literature to include a variation of the terminology used in different countries. The detailed search strategy for the three databases is shown in Table 1.

9Studies addressing barriers to and uptake of cervical cancer screening in LMICs and published in English over 10 years (1 January 2010 to December 2020) were eligible for inclusion. Project and academic reports including Master’s and Doctoral theses were also eligible while editorials, commentaries, and abstracts where we could not access full-text articles were ineligible. Working in pairs, the authors independently screened the titles and abstracts of the search output and retrieved the full texts of those considered eligible. The authors then independently assessed the full texts for inclusion and resolved disagreements through discussion and consensus.

10A standardized data extraction tool was used. Information was extracted on the country of study, aim/s, design, population, sample size, participant ages, screening type, documented barriers, reported findings, and recommendations. Discrepancies were resolved through discussion and consensus. Two authors assessed the quality of the studies included using the Critical Appraisal Skill Program(CASP) tool. See Appendix 1, Quality Assessment of studies.

11The literature search yielded a total of 2148 articles: 385 from PubMed, 1280 from Scopus, and 461 from Web of Science, 18 from Google and Google scholar. After removing 20 duplicates, we screened titles for eligibility and 1882 irrelevant articles were excluded (Fig. 1). Full texts of the 246 remaining articles were assessed for eligibility, and 92 met the inclusion criteria. Thirteen review articles were excluded, leaving 79 articles based on individual studies.

12The included studies were undertaken in 28 LMICs; with 61% undertaken in Africa, 21% in Asia, 5% in North America, 9% in South America, 1% in Oceania and 3% in Europe. The characteristics of the included studies are shown in Table 2. Of the included individual studies, 45 (57%) were quantitative, 27 (34%) qualitative and 4 (5%) used a combination of qualitative and quantitative methods. Four studies were based on secondary data analysis. The quantitative studies were largely cross-sectional surveys, while the qualitative studies involved focus group discussions, in-depth and semi-structured interviews (Table 2).

13Patients were not directly involved or recruited into this study. We reviewed published articles that investigated the barriers to cervical cancer screening uptake by women in LMICs. The results will be disseminated through a publicly available research report and a manuscript and in conferences and webinars. They will also be distributed through the WHO and the institutions involved in the project.

14The individual studies included participants from rural and urban areas, women living with and without HIV, women in the general public, women attending antenatal services, university students, and healthcare workers. Four studies included men and in two of the studies, they were partners of women participants while in the others they were university male students. Thirteen studies included healthcare workers exclusively or with non-healthcare workers. Eight studies included participants younger than 18 years old including one study that included girls from the age of 10 years together with older women -36. In 17 studies, age details were not specified (Table 2). Frequently missing information was age of the participants, type of screening and when the study was conducted. The sample sizes of studies ranged from 15 participants to 15,317 participants in a study that analysed secondary data.

15Forty eight percent of studies were about Papanicolaou (pap) smears exclusively or in combination with other screening methods, 25% about visual inspection with acetic acid (VIA) or visual inspection with Lugol’s iodine (VILI), 5% on HPV screening (through self-sampling or using DNA based tests) exclusively or in combination with other screening methods, while a total of 30% of studies did not specify the type of screening method (Table 2).

16Since most studies identified were descriptive or qualitative in design, we analysed and summarized the main findings using a descriptive narrative, based on themes identified as levels of the social ecological model. During the thematic analysis six authors in groups of two grouped the barriers that were identified into five categories, as defined below.Individual/personal level barriers – obstacles experienced at individual levelCultural/traditional and religious barriers – cultural, traditional, and religious views, norms, and expectationsSocial barriers – community and societal obstaclesHealth system barriers – factors in the design, function and implementation of health systems that make it difficult for some individuals to access, use or benefit from careStructural barriers– macroscale obstacles that affected some women disproportionately

17Individual/personal level barriers – obstacles experienced at individual level

18Cultural/traditional and religious barriers – cultural, traditional, and religious views, norms, and expectations

19Social barriers – community and societal obstacles

20Health system barriers – factors in the design, function and implementation of health systems that make it difficult for some individuals to access, use or benefit from care

21Structural barriers– macroscale obstacles that affected some women disproportionately

22These categories are not entirely distinct or mutually exclusive as factors in one category overlap and are influenced by those in other categories (Refer to Fig. 2 for a visual diagram depicting barriers across each level).

23The barriers to uptake of cervical cancer are interconnected and operate across and within the various levels of the social ecological model. The following category levels include factors that contribute to barriers to cervical cancer screening, spanning the patient/individual level to the structural level. The studies reviewed included quantitative and qualitative input from both women and men (including patients, women from the community, male and female students, female teachers and male partners), as well as from the health service-level (including nurses, doctors, community health workers, policy makers, NGO staff and district coordinators). Information about the different categories of barriers that were identified across the articles included in this review are provided in Table 3.

24Most studies reported individual or personal level barriers to screening. The most common individual level barriers were lack of knowledge and information about cervical cancer and cervical cancer screening, and its benefits, including women who did not understand the value of screening – i. e., health examination in the absence of symptoms or ill health. Another commonly reported individual level barrier was fear of receiving positive screening results with many women believing that a cancer diagnosis was terminal.

25Studies also reported that women had misconceptions about screening and the screening process. Women feared pain from the screening procedure and had misconceptions about possible harms such as contracting cancer, or damage to the uterus or cervix during screening. In Nigeria, women reported being afraid of contracting infections from the screening equipment or from other sources within the health facility. In Ethiopia, most women offered self-sampling for HPV thought that the process would be painful, while some feared using the Evalyn brush, and in South Africa, some women reported fear of concurrent HIV testing during screening for cervical cancer.

26In 33% of studies conducted in Africa, Asia, and South America many women reported being embarrassed to be screened or to undergo pelvic examination. Embarrassment was associated with the activity of going to a facility for screening, the pelvic examination itself, and being examined by a male or young healthcare worker.

27Studies also reported that women, regardless of geography or employment status, faced competing priorities and responsibilities and thus often had limited time to attend screening.

28Cultural/religious/traditional, and social barriers were closely intertwined in the studies evaluated. Eleven studies reported that women were not screened because of religious or traditional reasons and prohibitions. Two studies reported on possible clashes between western and traditional views of cervical cancer screening, and mistrust of western medicine and preference for traditional medicine was reported in Ghana, and South Africa. In Ecuador, there were competing interpretations of health between healthcare workers and the community. Some studies (21%) also reported that men disapproved of cervical cancer screening, with some refusing for their wives to be screened. Other studies reported that women’s health issues, including sexual and reproductive health, were deprioritized and not awarded the same urgency as other health issues, while others reported that cervical cancer screening was viewed as a private and taboo topic (culturally embarrassing) not to be discussed, due to its connection to sexual and reproductive health.

29Social barriers were related to community disapproval or negative community perceptions about the health system, the screening process, lack of peer support, and stigmatization of cervical cancer and the screening process. In some studies stigma was related to cervical cancer being viewed as a terminal disease by some, while in others stigma was due to association with sexual transmission, with women attending screening sometimes assumed to be engaged in infidelity or promiscuity. In South Africa where concurrent HV testing was offered, stigma was related to the association of cervical cancer with HIV infection.

30Heath system barriers included lack of capacity, poor organization of services, lack of knowledge about cervical cancer amongst healthcare workers, lack of promotion of screening, poor (negative and unfriendly) attitudes of healthcare workers when interacting with patients, and lack of public confidence in the health system. Lack of capacity included limited numbers of healthcare facilities in general, but especially in rural areas, few healthcare facilities providing screening services, limited staff, brief and rushed consultations, and shortage of equipment and materials which often led to women being referred for screening far from where they live resulting in costly, and lengthy screening and diagnostic pathways.

31Capacity barriers also included reports of poor knowledge of cervical cancer among healthcare workers, poor technical skill to perform screening procedures, limited supervision leaving staff uncertain about technique, and limited specialized experts such as gynaecologists for guidance and management of some patients. In Kenya and Ethiopia, clinic operating times and unavailability of services on weekends also limited screening uptake. In studies conducted in Uganda and South Africa, women reported that lack of privacy in healthcare facilities was a barrier to screening, while in Malawi, Munthali et al., identified a lack of space for screening services in healthcare facilities as a barrier. Lack of confidence in the health system was reported in Nigeria and Uganda.

32Eleven studies, seven in Africa (n = 7), Asia (n = 3) and South America (n = 1) found that poor, negative and discriminatory attitudes of healthcare workers towards women discouraged women from screening. A study conducted in Nigeria, reported that discrimination toward Muslim women hindered access to healthcare facilities and screening. Two studies also found that communication and language barriers between women and healthcare workers left women with unanswered questions and limited screening uptake.

33Long wait times in healthcare facilities were a barrier to screening in South Africa, Uganda, Kenya and China. This may partly also explain why women reported competing priorities for their time (work and family responsibilities) when they considered attending screening services.

34Several studies reported on policy and guideline implementation barriers. Studies in Uganda, Indonesia, Brazil, and China found poor organisation of the services with limited information available about screening services leaving women without information about screening sites, and procedures for booking screening appointments. In Bolivia, healthcare workers reported that lack of dissemination of screening guidelines, and lack of educational campaigns and infrastructure for screening limited screening uptake. In Oceania, screening guidelines were not implemented while Bulgaria had no screening policy. In Argentina and China, the screening policy excluded unmarried women from free screening (in China), thus limiting screening for some women since out-of-pocket screening costs were frequently identified as a barrier to uptake. Healthcare workers also often failed to promote, recommend or offer screening and related cervical cancer information during other consultations.

35Structural barriers were mainly related to geographic distance to screening facilities, associated travel costs, poor transport systems, and screening costs where screening was not a free service in the absence of health insurance. Screening costs were a barrier in all continents, with travels costs a barrier in Africa, Asia and South America. Long waiting times were also associated with additional costs for meals, and this increased overall screening costs. Women in rural areas were disproportionately affected by distance, and travel costs. In South Africa, Uganda and Nigeria, additional barriers were crime (which hindered free and safe travel), poor road networks and unreliable and inconvenient transport schedules to screening facilities. One study reported lack of infrastructure for women with disabilities. Other structural issues included low levels of education and low socioeconomic status, common among women living in conditions of poverty or limited resources.

36Based on the descriptive analysis of the main findings of the studies included in this review, we identified four underlying reasons for barriers to cervical cancer screening uptake that should be addressed when considering interventions and policies for remedial action. Firstly, poor or ineffective messaging about cervical cancer, screening and prevention evidenced by limited information and education about cervical cancer and screening as a preventive strategy and misconceptions about the cause of cervical cancer, and the screening process, is a key underlying reason for poor screening uptake. Many women are not aware of screening and its value, and there are many misconceptions about screening in many communities. Secondly, health systems are poorly resourced to provide screening, lack clear policies on cervical cancer and screening, or poorly implement any existing policies. Thirdly, there is limited access to health care services more generally, because of lack of universal health coverage and affordability, a common feature in many LMICs and a notable barrier to screening uptake. Women often must travel to facilities far from where they live for screening services, indicating limited access in many geographic areas which is worsened by transport and other additional costs.

37Finally, gender norms that deprioritize the health needs of women both at institutional, community and household levels also underly poor screening uptake. Patriarchal norms which value the needs of men and boys over women and girls are often upheld in institutions and communities, which shapes political will and decision-making regarding investment in women’s health and creates inequitable health and access to care for women. In many studies, women reported a lack of partner approval, permission, or support, as well as religious, cultural, or traditional prohibitions as a barrier to uptake, indicating the breadth and depth of the impact of gender norms.

38This review provides a broad overview of the barriers to uptake of cervical cancer screening in LMICs. The barriers were generally the same across countries and continents and different study designs, and are attributable to interacting individual, social, cultural, health system and structural factors.

39At the individual level, lack of knowledge and information about cervical cancer, the screening process, and its value, were frequently reported. This suggests that failure to address the knowledge and information gaps, will likely continue to limit uptake even in the absence of other barriers. The literature also reports poor uptake among well-informed women, who reported other barriers rooted in societal religious, cultural health system and structural barriers. Another common individual level barrier was fear which encompassed a wide range of issues. Limited information about the screening process (how it is done and by whom), may result in fear of what to expect. In Switzerland, women preferred to screen themselves using the self-HPV test kit since it reduced discomfort, embarrassment and maintained privacy compared to the traditional pap smear test. Appropriate and careful introduction and scale up of such self-testing could expand screening in LMICs. Fear of the screening outcome could indicate anxiety around stigmatization, related to discrimination of women with cervical cancer. In a Ugandan study, cervical cancer patients were abandoned by their families, while in a Zambian study, cervical cancer was associated with shame. Stigma has also been reported in high income countries. Muslim women in London were hesitant to screen due to embarrassment and fear because they were unmarried and did not want to send implicit messages about being sexually active. Another study also in the United Kingdom found that cervical cancer screening was stigmatized because of its association with HPV, and the perception that it shows failure of women’s responsibility for their health. This emphasizes the urgent need for strengthened information dissemination, attention to gender-related discrimination, and dispelling of myths, about cervical cancer.

40Cultural/traditional, religious, and social barriers were identified across many studies in all continents, but mainly in Africa and Asia. Lack of spousal and or family support were key barriers, and these may be driven by misconceptions about cervical cancer and traditional, cultural, or religious beliefs about pelvic examination and cancers, and this has also been reported in high income countries. Overlapping with cultural/traditional and religious barriers were other social factors including misconceptions and stigmatization of screening and cervical cancer, largely shaped by gender norms. The impact of gender norms and inequality were common barriers. When men hold decision-making power, women and girls can have limited access to the social, economic and health resources necessary for their well-being. At the household level, men often shape the logistical, educational, and psychosocial factors that directly affect women’s ability to access cervical cancer services. Women who are emotionally and financially supported by their families and partners are more likely to get screened. Conversely, family and partners can play a key role in stigmatizing, isolating, and prohibiting women from accessing screening.

41Well-functioning health systems with accessible services are critical for successful and effective health programmes. We found significant gaps in cervical cancer screening services in the health systems of LMICs ranging from a lack of high-level elements such as policies and guidelines, poor referral systems, limited points of service, inadequate resources (human and equipment/materials), to local level factors including poor attitudes of healthcare workers. Poor attitudes and discrimination by healthcare workers while inexcusable may be fuelled by staff overload and challenging and constrained conditions, areas in need of urgent attention of policy makers and implementers.

42Access to screening services was also hindered by geography and cost. Travel costs are significant for women with limited financial means. Women with low levels of education – who often have limited financial means – were less likely to be screened, hence, investing in women’s education in combination with other equity-promoting interventions is likely to improve uptake, given the known benefits of education.

43This review includes a wide range of studies (both qualitative, quantitative, and mixed method study designs) and grey literature published over the period 2010 and 2020, enabling an extensive investigation of barriers to cervical cancer screening in LMICs. However, a potential limitation is that studies may have been overlooked due to the search terms used. For example, if studies used terms other than “Vaginal Smears”, “Papanicolaou”, “pap smear”, “pap stain”, “pap test” or “vaginal smear” to describe this specific screening test, they may not be included in the search results. We also included studies where barriers to cervical screening uptake was not a primary objective, and this may limit generalizability of some findings. However, the common barriers were corroborated by many different studies, looking at multiple level barriers to screening in LMICs.

44To increase screening uptake and support the elimination of cervical cancer as a public health problem in LMICs, there is a need for implementation of clear cervical cancer policies and guidelines with the prerequisite structures and resources required across diverse health settings. Countries should review their cervical cancer policies and related programs, and fully implement screening guidelines which prioritize structured screening, rather than rely on opportunistic screening that is patient driven. Policies – both within and beyond the health sector – should also actively account for and work to eliminate stigma and all forms of disadvantage and discrimination that shape inequities in communities and within the healthcare system. There is also need for education, information dissemination, engagement, and advocacy about cervical cancer at the community and health facility level. This creation of knowledge and awareness amongst community members and providers around how to proactively reduce barriers to care is crucial for ensuring more women receive screening, and is central to addressing misconceptions, myths, and fears that are prevalent in many communities. Education and awareness initiatives should be grounded in accessible language, driven by local and community contexts and needs, and meaningfully engage diverse groups of women, men, boys and girls as well as multiple sector stakeholders (including a community health worker component focused on women’s health and counselling). Policies that support the sexual and reproductive health and rights of women and girls should be strengthened and expanded and account for inequities in access to care for diverse groups of women. This can include culturally appropriate interventions with a dedicated focus on promoting women’s health, taking into account the social and financial needs of communities. Further priorities at the health facility level includes adequately addressing issues around staff-patient ratio, staff capacities and competencies, organization and integration of facility services, and health promotion efforts aimed at attracting community members for screening. To engage women and communities effectively and consistently, outreach efforts should be conducted in a manner that recognises the different contexts with regards to physical access, affordability, culture, tradition, and competence of health providers to provide high quality and friendly services. Community and religious leaders, non-governmental organizations (NGOs), women who have been screened, and other stakeholders need to reinforce and advocate the message that screening saves lives. This would be an important step in combatting the stigma related to cervical cancer screening.

45Future research should focus on generating robust data on which groups are under-screened and why. This must account for the differential experiences of women across diverse categories (e.g., age, socioeconomic status, geography, disability, etc.) and look at the multiple level barriers that converge to create or reinforce barriers to health and screening.

46This review highlights some of the key issues highlighted in the literature to date, but there remains a dearth of information as to the multi-level barriers to screening that women face across axes of inequity, including gender, age, income, migrant status, ability, etc.

47Finally, the introduction of more modern screening approaches in LMICs should also be supported. It is better information, better resources, and input from women themselves, that can ground how barriers are addressed and how access is improved moving forward.

48This review identified a wide range of barriers to cervical cancer screening in LMICs. Urgent implementation of clear policies and programs, supported by health system capacity to implement them is required to address these barriers. The policies should support the promotion of women and girls’ health and rights, and gender equality. In addition, community-wide information dissemination, engagement and advocacy, and targeted further research on barriers to care across diverse groups and contexts are needed to effectively address the inequitable burden of cervical cancer in LMICs. It is only in reducing the barriers to cervical cancer screening that so many women continue to face, that the aims of the WHO’s global strategy to eliminate cervical cancer as a public health problem will be fulfilled.