A Qualitative Analysis of Factors Contributing to Cervical Cancer Screening Implementation in Health Care Facilities in Uganda

Abstract

Introduction

Cervical cancer prevalence and incidence are high in sub-Saharan Africa, especially in Uganda, where screening rates are low, despite government policy recommending screening for all women aged 25-49 every three years. Most prior research focuses on client-related barriers to screening, including women’s fears about the screening procedure, lack of partner support, and community-level stigma. Fewer studies elaborate on inner context factors related to health care systems, facilities, and providers. The aim of this study was to use qualitative methods to explore inner context factors that may affect cervical cancer screening in Uganda.

Methods

We recruited 20 health care facility administrators, 6 providers of cervical cancer screening, 2 district health officers, 2 division medical officers, and one government health official for key informant interviews, and 69 women (31 screened and 38 not screened for cervical cancer) for focus group discussions. Participants were recruited from four health care facilities that varied by urbanicity and funding source: one urban public facility, one urban private non-profit facility, one rural public facility, and one rural private non-profit facility.

Results

Inner context themes emerged around infrastructure needs (insufficient space, equipment, and supplies) and staffing issues (inadequate staff quantity and training), which contributed to lower quality of care (e.g., long wait-times; painful, rushed exams). Women described privacy concerns as well as discomfort with male and young providers. Women with HIV were prioritized for screening based on funding streams and inability to serve all women given infrastructure and staffing issues. Despite barriers, many stakeholders were committed to providing cervical cancer screening services, and many women saw the value of screening.

Conclusion

This study identified inner context barriers related to resource shortfalls, which affected quality of care. Low cost solutions are needed to improve health care readiness and increase reach of cervical cancer screening in Uganda.

Keywords

cervical cancer screening inner context implementation science qualitative methods Uganda women’s health

Introduction

In sub-Saharan Africa, prevalence and incidence of cervical cancer are among the highest globally^1-3: In 2022, multiple countries across the continent—in Eastern (Burundi, Tanzania, Uganda), Western (Guinea), and Southern (Eswatini, Lesotho, Mozembique, Zambia, Zimbabwe) Africa showed the highest level of standardized incidence rates worldwide (from 45.3-95.9 per 100,000). In Uganda in particular, cervical cancer is the leading cause of cancer-related deaths among women; the age-standardized incidence and mortality rates are 53.8 and 40.6 per 100,000, respectively.⁴ Ugandan government policy states that all women aged 25 to 49 years-old should be screened for cervical cancer every 3 years.⁵ Evidence-based visual inspection with acetic acid (VIA) screening and thermal cryotherapy for pre-cancerous lesions are available at low or no cost to women, mostly through midwives and nurses in health care facilities.⁶ However, a minority of women in sub-Saharan Africa are estimated to have ever screened for cervical cancer,^7,8 and late-stage presentation for screening is common.⁹ In a five-country analysis of data from 2011 to 2018 across sub-Saharan African regions (Benin, Ivory Coast, Kenya, Namibia, Zimbabwe), 19% of women on average (95% confidence interval = 18.5% to 19.5%) were estimated to have ever screened for cervical cancer.⁸ In Uganda, across different samples, an estimated 5-35% of women have been screened, and an estimated 80% have advanced cancer when initiating care.^6,10 Moreover, most women diagnosed with cervical cancer cannot afford treatment and do not live near treatment centers. Thus, early detection and prevention through screening are critical.

Consistent with the implementation science literature suggesting that inner context factors (within clinics) and outer context (extra-clinic) factors (e.g., policy, community norms, client attitudes) impact implementation of evidence-based practices,^11,12 research has identified factors at multiple levels that affect cervical cancer screening implementation in sub-Sanahan Africa.^13-15 Prior research across sub-Saharan African has primarily focused on outer context factors related to client barriers to cervical cancer screening, including low knowledge and awareness, misconceptions and fear regarding cervical cancer screening (e.g., perceptions that it damages the uterus, causes infertility, and is painful), stigma around cervical cancer and the screening process, and lack of partner support.^13,14,16-23 Stigma can stem from fear of having cancer (and anticipated cancer stigma), shame around having symptoms of a sexually transmitted infection and advanced disease (e.g., bleeding, discharge), as well as embarrassment from the screening procedure itself (including disrobing), especially with male providers. Women may need to get permission for screening and treatment from male partners, who may be unsupportive, especially if the woman needs to abstain from sexual intercourse when healing after treatment.

Socio-demographic outer context factors at the client level, such as poverty and geographic location also may hinder screening in Uganda as well as sub-Saharan Africa as a whole: those who live far from screening facilities, who do not have access to financial support for medical care, and who live in rural areas are less likely to get screened,^{13,14,16,17,22,24} suggesting that transport costs are a barrier. In sub-Saharan Africa, women with HIV also have been more likely to be screened, potentially because some donor and partner organizations provide funds for services for people with HIV only.^16,17,25,26 In addition, insufficient funding for cervical cancer screening and management overall greatly hinders implementation in sub-Saharan Africa.¹³

Relatively less research in sub-Saharan Africa has described organizational barriers to cervical cancer screening in the inner context (i.e., at the health care facility and provider levels).^13,24 In sub-Saharan Africa as well as Uganda specifically, inner context factors at the organizational level include insufficient or lack of resources and equipment, long wait-times, and staffing shortages.^{13,14,17,24,25,27} At the provider level, studies have identified inadequate knowledge and skills, in part due to high staff turn-over and lack of training opportunities, as well as lack of recommendation or encouragement to screen.^13,18,28,29 Research in several sub-Saharan African countries also has found poor patient experience to be an issue^13,14; for example, in a focus group study of screening-eligible women in Uganda, some participants noted that screened women’s stories of providers causing pain or being rude during the screening process deterred other women in the community from getting screened.²⁰

In sum, prior research on barriers to cervical cancer screening implementation in sub-Saharan Africa has mainly focused on outer context factors related to client characteristics. Thus, the purpose of the present paper was to explore implementation factors at the inner context health care system, facility, and provider levels that contribute to low cervical cancer screening levels in Uganda. We collected data across multiple levels of stakeholders: health care facility administrators, screening providers, government officials, women who had been screened for cervical cancer, and women who had not been screened.

Methods

Setting

This study was conducted in four health care facilities offering cervical cancer screening that varied by urbanicity and funding source: two urban clinics, one public and one private non-profit, in Kampala, Uganda, and two rural clinics, one public and one private non-profit, near Jinja, Uganda. A substantial percentage of the Ugandan population utilizes public and private non-profit facilities (about 40% each), increasing this study’s external validity.³⁰

Study Design and Implementation Framework

We conducted a cross-sectional qualitative study in four health care facilities that used key informant interviews with health care workers and policymakers, and separate focus groups with female clients who had and had not been screened for cervical cancer. Our research was guided by the Exploration, Preparation, Implementation and Sustainability (EPIS) implementation framework,¹¹ which highlights inner and outer contextual factors and dynamic phases of implementation; this qualitative study, which was conducted under the Preparation phase of EPIS, aimed to identify inner context barriers to easy access to and delivery of CC screening. This qualitative analysis represents the first step of a larger study on a social network intervention to increase cervical cancer screening demand among women in Uganda.³¹ After this qualitative phase, following EPIS’s dynamic phases, the team remediated barriers uncovered in the qualitative analysis in Plan-Do-Check-Act (PDCA) cycles,³² evaluated intervention implementation, and then observed sustainment of the social network intervention in the same four facilities.

Participants and Procedures

A total of 31 individuals participated in 60-minute audio-recorded qualitative key informant interviews; individuals were eligible if they were a healthcare administrator or provider in one of the study clinics, or a relevant government health official. A total of 20 health care facility administrators, including directors, department heads, and managers (4-6 per facility; physician specialists, nurses, and other types of senior managers), 6 providers of cervical cancer screening (1-2 per facility; 5 midwives, 1 assistant nursing officer), 2 district health officers, 2 division medical officers, and one government health official. The majority of interview participants were women (n = 17, 56.7%), and their average age was 45.7 years (SD = 8.5, range = 32-63); they had worked in health care an average of 14.8 years (SD = 9.8, range = 1-36).

Using a purposive (selective) sampling method, study team members attended health care facility staff meetings and offered participation to staff; the government official was known by members of the research team and thus called directly. Interview participants were told that the purpose of the study was “to explore how to best ensure that women have access to and are utilizing cervical cancer screening services here at the clinic.” All interviews were conducted in English in a private facility space or office by trained local Ugandan Co-Investigators with MDs, PhDs, or both (one man and four women). Participants were given the equivalent of $8 cash (in Ugandan Shillings). Interviews took place from October, 2023-January2024.

A total of 69 women were recruited across the targeted health care facilities to participate in focus group discussions in October, 2023: 31 women who were screened for cervical cancer (range = 6-9 per facility) and 38 women who were not screened for cervical cancer (range = 8-11 per facility). Individuals were eligible for the focus groups if they were a woman aged 25 years-old or older and a client at the health care facility. Using a convenience sampling strategy, providers of gynecological care, HIV care treatment and support, and family planning services told clients who had never been screened about the study, and providers of cervical cancer screening told clients who were recently screened for cervical cancer (who screened negative as well as those who were treated for pre-cancerous lesions) about the study. They were told that the purpose of the study was “to explore how to best ensure that women get periodically screened for cervical cancer risk.” Interested women were contacted and offered participation by the local study coordinator. Two focus group discussions by two local team Co-Investigators (both women, one with MD/MPH training and one with PhD training) were conducted in a private room at each facility (eight total): Four focus groups with women who had been screened for cervical cancer and four different focus groups with women who had not been screened. The 60-minute focus groups were audio-recorded and conducted in Luganda by trained bilingual local staff. Women were provided with refreshments during the discussion and the equivalent of $8 in transport reimbursement.

The team did not conduct interim analyses to inform saturation and sample size; instead, the team pre-determined sample sizes based on standard guidance for code and meaning saturation in qualitative research,^33,34 as well as the number of relevant health care workers at each facility who served unique roles in the cervical cancer screening process.

Qualitative Guides

The qualitative guides contained parallel questions for interviews and focus groups, and were developed collaboratively by the Ugandan and American investigators. The guides included questions designed to elicit narratives on health care barriers to cervical cancer screening, with a focus on inner context subdomains described by the EPIS framework (facility organizational characteristics, organizational staffing processes, individual characteristics; see Table 1). Although the focus on the study and this analysis was on inner context barriers, some prompts asked about outer context factors (e.g., funding) to obtain a comprehensive understanding of the interplay of factors that affect cervical cancer screening processes.

Table 1.

Example Qualitative Questions to Elicit Information About Health Care System, Facility, and Provider Factors in Cervical Cancer Screening, by EPIS Subdomain

EPIS subdomains	Example questions: Health care provider/Administrator/Policymaker interviews	Example questions: Screened and unscreened women focus groups
Organizational Characteristics (Inner Context): Clinic processes that affect cervical cancer screening implementation	What is the process or workflow for how cervical cancer screening is provided here at the clinic?	How easy or hard was it to access cervical cancer screening here? Why?
	Some clinics can get very busy and need to turn away clients for cervical cancer screening. How often has the clinic staff had to turn women away who wanted to be screened? Why?	How willing would you be to get screened for cervical cancer here at the clinic again? What concerns do you have about getting screened, if any?
Organizational Staffing Processes (Inner Context): Clinic procedures related to staff hiring and training regarding cervical cancer screening	To what extent are staffing/resources for cervical cancer screening an issue in screening all women?	What have healthcare providers told you about cervical cancer screening in the past, if anything?
	How prepared do you think staff would feel, if they were asked to provide cervical cancer screening to the majority of female clients here at the clinic? Why or why not?
Individual Characteristics (Inner Context) (No formal probes; emerged in response to broad questions): Shared or unique characteristics of clients that influence the process of implementation of cervical cancer screening	What factors keep women from getting screened for cervical cancer?	What concerns do you have about getting screened, if any?
Outer Context (Funding): Fiscal support from outside entities for cervical cancer screening	How does external funding impact provision of CC screening services?	N/A

Qualitative Data Collection, Management, and Analysis

The team used a deductive directed content analysis strategy, in which broad categories of inner context factors affecting implementation under the EPIS framework (facility organizational characteristics, organizational staffing processes, individual characteristics) guided construction of the codebook and the analysis.³⁵ Members of the Uganda team transcribed the interviews and focus groups, and used standard methods to translate and back-translate focus group discussions into English. Two members of the US team (PhD Co-Principal Investigator and MPH Project Coordinator, both women) first read all transcripts, and then, with input from a Ugandan Co-Investigator (a woman), wrote preliminary summaries of overall and health care facility-specific results. These summaries were refined with Uganda team input, after which Ugandan and U.S. study team co-authors discussed and refined the facility-specific results with administrators and providers in all four facilities in separate in-person meetings.

After the health care facility meetings, the PhD Co-Principal Investigator and MPH Project Coordinator from the U.S. developed a codebook, which was refined iteratively with two non-Ugandan graduate students in public policy (who served as coders) and then uploaded along with all transcripts into Dedoose³⁶ (qualitative data management software). The coding team met to refine the codebook, iteratively coding transcripts and revising the codebook as needed. Once the codebook was fully refined, the two coders coded approximately 13% of the transcripts (n = 3 or 10% of interviews; n = 2 or 25% of focus groups), randomly selected by Microsoft Excel random function. After satisfactory interrater reliability was established (Cohen’s Kappa = 0.774),³⁷ the two coders reviewed and updated all previously coded transcripts to align with the final codebook, and then divided the coding between the remaining transcripts. The coders continued to meet weekly, with the PhD Co-Principal Investigator and MPH Project Coordinator resolving any coding differences as needed. The PhD Co-Principal Investigator reviewed all final codes, after which the MPH Project Coordinator reviewed coded transcripts and updated the preliminary summary, focusing on key themes that strongly emerged across participant groups and facilities. Because no clear differences in themes emerged by type of facility, and to preserve confidentiality and reduce potential for identifiability in urban and rural locations, specific quotations are identified by facility funding source only rather than the cross of urbanicity by funding source.

All participant details have been de-identified. The reporting of this study conforms to the COREQ guidelines.³⁸ The team ensured trustworthiness,^39,40 including: credibility through triangulating themes across multiple data sources (i.e., different types of stakeholders) and methods (key informant interviews and focus groups), and validating findings (i.e., presenting and discussing results) in meetings with health care workers at the facilities where data collection occurred; transferability through comprehensive description of the methods (participants, setting, procedures), such that applicability of the results to other contexts can be determined; dependability through documentation of all research steps (e.g., qualitative analysis, interrater reliability) with a standards of procedures manual and weekly study updates; and confirmability through discussions about data interpretation with multiple levels of relevant stakeholders in Uganda (e.g., policymakers, health care providers, local community advisory board members) and the Uganda study team.

Ethical Approvals

Study procedures were approved by the RAND Human Subjects Protection Committee (HSPC#2023-N0111; May 4, 2023) in the U.S., and Makerere University School of Public Health Higher Degrees, Research, and Ethics Committee (HDREC#SPH-2023-412; May 26, 2023) and the Ugandan National Council of Science and Technology (HS SS1873ES; July 13, 2023) in Uganda. The study was conducted in accordance with the Helsinki Declaration of 1975, as revised in 2024. Interview participants provided verbal informed consent and focus group participants provided written informed consent.

Results

Overview

Key inner context barriers varied by health care facility and included infrastructure needs (regarding space, equipment, and supplies), which exacerbated staffing issrues (insufficient staff quantity and training), reducing quality of care. Outer context funding and policy factors interacted with inner context factors, such that insufficient funding to screen all women was a root cause of scarce resources and led health care workers to prioritize some subpopulations for screening. Representative quotes are shown in Table 2.

Table 2.

Exemplary Quotes by Theme and Subtheme Representing Inner Context Implementation Factors in Cervical Cancer Screening in Uganda

Theme	Sub-theme	Health care providers/Administrators/Officials	Screened and unscreened women
Organizational Characteristic	Physical Infrastructure: Need for Space	“The challenge is space. We need a bigger space around here, at least which can accommodate two beds. We have one room which is down, so we need more space here.” - female screener/midwife in public facility	N/A
	Physical Infrastructure: Need for Space	“The barrier we have is the delays that we have, the delays that are caused when one clinic overflows because we use the same space like for three activities… We use it for antenatal, and we use it for [Elimination of Mother-to-Child Transmission and] for cervical cancer. So, when we have an overflow for one activity, then it keeps other services lagging a bit so there is a delay.” - male physician specialist/administrator in private non-profit facility	N/A
	Physical Infrastructure: Layout Challenges	“Clients go unattended at times…some get lost and they don’t come back” - female nurse midwife/administrator in public facility	“When we came and asked the gatekeeper, where they do cancer screening from…he did not respond to us. We greeted him and he kept quiet.” - unscreened woman in private non-profit facility
	Physical Infrastructure: Stigma and Privacy Concerns	“I think because maybe it is nested in the cancer ward, maybe some people, they think by sending them there, you have already condemned them that you have seen cancer.” - male physician specialist/department head in private non-profit facility	“These prying eyes are terrible; people around will be whispering to each other when they see you coming out. They will say, maybe she has a problem, don’t you see how she looks? Everyone’s eye will be on you as you get out; and you too will feel small.” - screened woman in private non-profit facility
Organizational Characteristic	Equipment & Supply Shortages	“The equipment is not autoclaved in time. They have nowhere to autoclave the reusable equipment. And even the replacement of a lamp, the lamp that is used blows and it takes more time.” - male specialist/administrator in private non-profit facility	“Mine is about the equipment. That thing which they use to clean down. At first, they used a chemical and another time it was just cotton. I did not blame them; I just knew that there was a shortage.” - screened woman in public facility
Organizational Characteristic	Equipment & Supply Shortages	“…being that we have one machine also it cannot do, even though now they have screened many, the one who will do the VIA is one, then the machine is also one then you end up having none.” - female nurse/administrator in public facility
Organizational Staffing Processes	Too Few Trained Staff	“We have those deficiencies because you find a facility one staff is trained and may be others do not have that skill. So, you need to train several people at the facility.” - male health worker (officer) for private non-profit facility	“When I came to screen, we were so many women and we made a queue and yet the screener was alone. It was 4pm and then she had to tell us to come another day.” - screened woman in public facility
		“The work is really much… you find yourself working through the day without anything to put in the stomach.” - female screener/midwife in public facility
			“I lost my pregnancy and they brought me here. They did not treat me. They made me to sit and wait, they took of a test and they told me that I was still pregnant but they cannot see it. They told me to wait and come back on a Tuesday. But I did not come back here.” - unscreened woman in private non-profit facility
		“We at the moment do not have enough manpower, sometimes you find it is only one staff handling the entire team, so, she is doing family planning, she is also doing cervical cancer screening, besides he is also engaged in other duties in the facility. Even people were trained, you find he was trained but deployed elsewhere because of the shortage of manpower… Sometimes he has been transferred, others are on maternity leave, sick leave, trainings and all that. So, it is an issue.” - government official
	Counseling/Education Insufficiencies	“When women don’t feel welcomed, they are scared to expose themselves, like here we have the word oncology which means cancer, so they are scared they don’t know what to expect and the health workers do not welcome them. The processes of the hospital are inhumane sometimes. So the health workers do not give women a talk before, what to expect and sometimes they don’t even show the women the equipment to be used, the women then will sort of back off. We have had reports of women telling us that the nurses have been rude.” - male physician specialist in private non-profit facility	“[Facilitator: What would you advise on how to improve on the services here in case someone would like to be screened?] Handling us well before we get up the bed, explaining to us the whole process. We even do not know what they inserted in us down there.” - screened woman in private non-profit facility
	Counseling/Education Insufficiencies	“After educating them, they like it because they have heard over the radio, that cancer is now common, cancer of the cervix is common, so when you offer the chance they come for screening after all they say it is not evasive, so they don’t fear. After counselling they always accept.” - male health worker (officer) for public facility	“What I heard about cervical cancer made me come here to be screened. The nurse from here at [study site] told us that once you get screened early enough, you can be helped when they discover early enough when you have a sign or maybe you contracted the virus, you can be helped. But the moment you do not get screened early enough, it does not heal and yet it is a very painful disease. That is what made me get screened to just see if I have any sign, I may be helped.” - screened woman in private non-profit facility
	Improper Exam Technique	“The assumption is that the midwives who know how to put a speculum, she could put a speculum, can’t see the cervix and still say that everything is okay because may be they have other tasks to take care of. The next thing you hear that the woman has come back with a problem.” - male physician specialist in private non-profit facility	“I also request the providers that when we come on such a big and serious disease. I request them to calm us down and handle patients well. Because there are some providers who are very tough, it demoralizes the patient. It adds to the fear that she came with and this makes the condition worse.” - screened woman in public facility
	Improper Exam Technique	“But it’s also true, we have health workers or midwives and doctors who are not good at communication or just how to insert it. There’s small things that you can do to make it comfortable and less traumatic. But if you just insert..., many women will find it uncomfortable.” - male physician specialist/administrator in private non-profit facility
	Mistreatment/Disrespect	“If a client comes today and not being worked on, I don’t expect that client to come back next time. So, you may find that the service will fade out. Because when this client goes back in the community she will tell them what has happened. Even others will not be inspired to come.” - female screener/midwife in private non-profit facility	“I request that the providers improve on the way the handle us. Even when it is for free but we can improve because when you become tough on her, she will not come the next day. She will say that the providers are impossible and I will not manage this treatment and she goes away silently.” - screened woman in public facility
Individual Characteristics	Provider and Client Characteristics (Provider sex, age, training; client community)	“Woman to woman is better than man to woman because that is where religions don’t want a male who is not your husband to talk about the privacy of the genital areas.” - female assistant nursing officer in public facility	“For me what I saw was that, in that screening room, there is no privacy. There are many nurses. They surround the whole place. But worst of all they even allow in male medical workers. You look at a boy fit to be your child. Then you feel like dying on the inside. You feel shy opening up to this male child.” - screened woman in public facility
		“I was trained, but due to gender issues … there are those who also say they want a [NURSE] who is a lady.” - male physician specialist in private non-profit facility	“For me, I would find it difficult, because almost all the nurses and medical personnel here know me and I know them. So I feel I can’t screen from here. Am I allowed to screen from somewhere else? The truth is that the service here is very good and the providers are also perfect but for me as me, I can imagine sister [NAME] working on me yet she knows me and I know her. Then when I leave, she might tell another sister they start discussing about me how am created. So that’s where I can find a problem with screening from here otherwise, I would have no problem.” - unscreened woman in public facility
	Client HIV Status	“It’s fair for the limited resources to first go to where the burden is so heavy, which is the HIV-positive.” - female health worker (medical officer) for public facility	“Looking at what I have been going through, what helped was that it is mandatory to screen all the HIV-positive mothers who come to government facilities are screened for cervical cancer. If you come to get your drugs, they have to screen you for cervical cancer.” - unscreened woman in public facility
		“As a starting point the [cervical cancer screening] program was geared towards HIV-positive clients because the prevalence is quite high. And because our partners, they also wanted to pursue that direction. But ideally it is not proper and it is not called for to send away clients whatever the case. … The policy direction we are taking on is I think is to screen all mothers who are HIV-positive or -negative. So, there is no justification to turn away the mothers.” – government health official
		“The positives are referred, after the initial encounter that proves them that they are positive, whereas what we are looking at is having everybody that is coming in to be given a chance to be screened. The positives are given priority because of the perceived high risk of getting cancer of the cervix. So, somewhere along the way, unintendedly, they are given priority.” - male hospital director in public facility
	Commitment to Screen	“We are few staffs but committed, we don’t turn away any woman from screening because of the numbers that we are understaffed. We endeavor to come very early and leave very late to make sure that we screen everybody that comes on board.” - female screener/midwife in public facility	“Because we all know that cancer can’t be cured, for us we always know that cancer is not curable. We know that cancer disease is never curable. But when they say that there’s a way it can be done to treat you, you have to come when it is still early and that’s how it was. When I heard that I can be treated I said let me go and get tested.” - screened woman in private non-profit facility
	Commitment to Screen	“I think, in my opinion, the current staff who are there are just people who are really interested in making sure that people get services. It’s a personal thing. I’m not so sure that it's going to be permanent if the staff changes. Currently the staff who are there are really passionate about cervical cancer screening services. They have been trained and they offer support supervision to other health clinics beyond [CLINIC], so it’s like a passion they have.” - female health worker (medical officer) for public facility	“When I realized it was so easy, I reached out to some friends and told them about my experience. And truly they came and were screened. They were saying that if a timid me could encourage them, then there is no issue to worry about. Just go and get screened.” - screened woman in private non-profit facility

Note. The number of exemplary quotes shown per theme vary when relevant to demonstrate different perspectives on the same theme among a range of stakeholders.

Organizational Characteristics

Space Issues (Need for space, layout challenges, stigma and privacy concerns): Physical infrastructure, including space quantity, quality, and layout, limited the number of women who could be screened. Most staff across all clinics expressed the need for larger and more spaces to conduct multiple screening procedures simultaneously. Two facilities did not have a dedicated space that was only used for cervical cancer screening. Staff and clients also mentioned facility layout as a hindrance. For example, in a public facility, women had difficulty finding the screening area. In addition, infrastructure contributed to stigma and privacy concerns: In a private non-profit facility, screening was done in the oncology unit, which deterred clients from attending, and in a private non-profit facility, people in the waiting room could hear discussions in the screening room and see clients who were leaving the screening room. Overall, infrastructure issues contributed to clients’ difficulties navigating the facility as well as concerns that their health information would be kept confidential.

Equipment and Supply Shortages: Many spoke of inadequate stocks of equipment and supplies—a result of insufficient funding. Except for those in the private non-profit facility, most staff reported equipment issues. They described regular stockouts of speculums, testing kits, ascetic acid, thermocoagulators, and basic supplies like gloves and pipettes, because of insufficient funding. One public facility had only one thermocoagulator; the other public facility did not have any.

Inadequate equipment and supplies affected clients negatively. Screened women in two focus groups in public clinics commented on the effects of equipment and supply shortages on the screening experience. Some providers discussed turning clients away or long wait times, if there was insufficient time to sterilize speculums in between screenings. A screener mentioned that facilities tend to stock one standard speculum size only, which could lead to discomfort and pain, such as if the speculums were too large for nulliparous women.

Staffing Processes (too few trained): Across all facilities, an insufficient number of staff were trained. Health care providers generally saw a need to increase the quantity of staff trained to perform cervical cancer screening. Many providers discussed overworked staff and burnout, with few staff available to handle large number of screening clients. Limited number of staff also created problems when one staff member was called to another department, needed to spend an unexpected amount of time with one client, or was absent. As a result of these staffing issues, screened women similarly described long wait-times or being told to return for the service on another day. Some unscreened women explained that long wait-times for other services deterred them from coming back to the clinic for screening or other services.

Staffing Processes (counseling/education insufficiencies, improper exam techniques, mistreatment/disrespect): Some participants described negative screening experiences, suggesting a need to retrain existing screening staff. In addition to training new staff to conduct cervical cancer screening, participants emphasized the need to retrain some existing staff to improve quality of care. Although some women across focus groups had positive experiences with well-trained staff, providers and clients described instances of disrespect as well as lack of clear communication and education about the screening procedure.

Clients complained of discomfort, and staff said that discomfort can be a training issue, because some staff do not employ correct techniques. For example, some screeners do not prepare speculums appropriately (to be correct size, warmed, and lubricated)—although, as noted above, some facilities stocked only one speculum size. Low skill or lack of proper attention could result in painful screening. Moreover, women who experienced pain or who felt disrespected might not return for screening or treatment, or might discourage other women from screening.

Individual Characteristics

Provider and Client Characteristics (provider age, sex, training; client community): Women’s reluctance to be screened was heightened by some types of staff and staffing patterns. Women expressed concerns when the provider was younger and male, and when groups of observers (usually medical trainees) were present. Some women were reluctant to screen at facilities in their own community, when they knew screening staff from their social circles. Health care workers were aware of such concerns and recognized some women’s discomfort with male providers based on cultural norms.

Client HIV Status: Inner context issues combined with insufficient funding led to prioritization of women with HIV. In practice, given limited resources in the inner context, all women aged 25-49 could not be screened. As a result, some providers prioritized women with HIV for screening because of their higher risk of progression to cervical cancer. Some funding partners required that women with HIV screen for cervical cancer to access antiretroviral therapy. Government officials, however, emphasized that all women should be screened, both women living with HIV and women who were HIV-negative.

Provider and Client Commitment to Screen: Despite substantial challenges, many stakeholders were committed to ensuring that women were screened—and many women were committed to getting regular screenings. A number of staff, especially in the public facility, described intrinsic motivation to ensure that all women are screened. Some discussed staying late and showing empathy to clients despite the overwhelming workload. Notably, in the face of their fears and experienced difficulties, women across groups, especially those who had been screened and treated for pre-cancerous lesions, still viewed screening as important and necessary—and some spread this message in their social networks. Moreover, with proper counselling and information ahead of time, women felt prepared and were willing to be screened. Staff and clients across facilities observed that provider encouragement and education around screening facilitated screening uptake, and thus saw a need for community-wide sensitization regarding screening and cervical cancer.

Discussion

This qualitative study in a low-income country with high cervical cancer prevalence and low screening rates uncovered inner context health care system, facility, and provider challenges to screening implementation. Across urban and rural public and private non-profit facilities, multiple types of stakeholders described how resource issues related to space, equipment, supplies, and staffing (in the inner context) could lead to inability to screen all women aged 25-49 every three years, per government policy. In most clinics, stakeholders noted that the demand for screening sometimes exceeded available staffing and infrastructure resources, consistent with prior research in sub-Saharan Africa.^13,14,24 Our research extends prior studies in Uganda and sub-Saharan Africa as a whole,^14,17,24 which have established client-related (outer context) barriers such as misconceptions and fears about the screening process, community stigma around cancer, and male partner barriers, and rarely include perspectives of health care providers, administrators, and policymakers.

Prior research in sub-Saharan Africa, including in Uganda, has found that women may be reluctant to be screened because they are concerned about discomfort and pain, as well as long wait times; they also may have misconceptions and lack of awareness about the procedure.^14,16-23 Our research indicates that such client fears may have some basis in truth. Screeners may rush through examinations and not have time to provide sufficient counseling or to warm instruments; screeners also may not have access to resources that would allow them to serve more women, including additional equipment to sterilize more speculums, or access to different size speculums to lower the discomfort of the procedure. Such resource limitations may reduce providers’ motivation to offer screening and increase their workload.¹³

Our research suggests cause for optimism in overcoming barriers. Despite substantial inner context barriers to cervical cancer screening, policymakers, administrators, and providers persevered, supporting screening for as many women as resources would allow. Women too believed in overcoming their fears and navigating difficult clinic experiences to get screened. Across narratives, stakeholders shared their commitment to improving the screening process, given the high rates of cervical cancer, combined with few treatment options for advanced disease, in the country.

Based on our results, we propose several specific recommendations for increasing cervical cancer screening in this low-resource environment. As prior qualitative research suggests that compassionate, respectful care facilitates retention,^41,42 policymakers and health care administrators could require trainings for cervical cancer screening providers to improve their skills and to practice client-centered care; such training seems critical to increase demand for screening, given the inherent discomfort of the screening procedure. Training could include preparing clients by telling them what to expect, ensuring that speculums are warmed and available in different sizes; clinics could also stock plastic disposable speculums (that do not need to be sterilized in between clients) as a back-up, to decrease waiting time or ability to serve all clients. Moreover, improved infrastructure and greater resources (i.e., expanding space, increasing staff, and ensuring sufficient supplies and equipment) from public and private funders would address many of the barriers detailed in the present study, but such changes can be unrealistic for low-resource settings if cost is prohibitive and supply stockouts are beyond the control of individual facilities. Creative, cost-effective solutions could include reconfiguring space and adding appropriate signage for easier navigation to screening rooms, and training more clinic staff on screening procedures, even if their daily responsibilities are in other departments, so that more staff are available when demand is high.

Consistent with prior research,^23,25 stakeholders mentioned the need for community sensitization about cervical cancer and screening, to raise awareness, overcome misconceptions, and convince male partners of the high need—which in turn would help women to feel more prepared and knowledgeable about the screening process prior to the clinic visit. However, standard community education strategies have not consistently increased screening uptake.⁴³ Social network interventions, in which pre-existing social ties with known others in the community are leveraged to diffuse health information in communities, have shown promise for cervical cancer prevention.^44,45 For example, in the Game Changers for Cervical Cancer Prevention group-based intervention, originally developed for HIV and adapted for cervical cancer,^31,46,47 women who have been screened for cervical cancer are trained to engage in peer advocacy. Results of a pilot study showed significantly increased cervical cancer knowledge and uptake of cervical cancer screening among social network members.⁴⁷ Although such community-based interventions can be effective, local health care facilities first need to be prepared for the surge in demand for screening that result from such interventions, by addressing the inner context factors described above.³¹

Limitations of this study include qualitative data collection in only four clinics in a lower-income country—one of each type representing the cross of urbanicity and funding source. Results may not be generalizable to other countries, especially those of higher income, or other health care facilities. We triangulated results across data collection sources at multiple levels, reducing the likelihood of bias from any one individual source. Moreover, we did not systematically collect facility-level quantitative data on the number of health facilities providing cervical cancer screening services in the study areas or on the number of women screened for cervical cancer in the clinic catchment areas, which would have provided useful contextual information for our analysis.

Conclusion

In this qualitative study of cervical cancer screening implementation factors in Uganda, multiple types of stakeholders were engaged, including at the national policy level. The similarity of our findings with other studies on cervical cancer screening barriers in Uganda and sub-Saharan Africa lends credence to our results. Furthermore, by elucidating the inner context factors that can impede smooth cervical cancer screening, our research can help to determine solutions to address outer-setting factors related to lack of community demand for screening.

Footnotes

Acknowledgments

We are grateful for the participants who shared their stories and the community advisory boards who contributed their insights.

ORCID iD

Laura M. Bogart

Ethical Considerations

Study procedures were approved by the RAND Human Subjects Protection Committee (HSPC#2023-N0111; May 4, 2023), Makerere University School of Public Health Higher Degrees, Research, and Ethics Committee (HDREC#SPH-2023-412; May 26, 2023), and the Ugandan National Council of Science and Technology (HS SS1873ES; July 13, 2023).

Consent to Participate

Interview participants provided verbal informed consent and focus group participants provided written informed consent.

Author contributions

Conceptualization (Bogart, Beyeza-Kashesya, Gwokyalya, Ober, Wagner, Wanyenze), Methodology (Bogart, Ober, Wagner), Validation (Bogart, Rukundo, Timmins, Whitaker), Formal Analysis (Bogart, Rukundo, Timmins, Whitaker), Investigation (Beyeza-Kashesya, Gwokyalya, Matovu, Nakami, Namisango), Data Curation (Gwokyalya, Whitaker), Funding Acquisition (Bogart, Wagner, Wanyenze), Project Administration (Gwokyalya, Nakami, Namisango, Whitaker), Writing – Original Draft (Bogart, Whitaker), Writing – Review & Editing (Bogart, Beyeza-Kashesya, Green, Gwokyalya, Matovu, Nakami, Namisango, Ober, Timmins, Rukundo, Wagner, Wanyenze, Whitaker).

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the National Cancer Institute of the U.S. National Institutes of Health (Grant # R01CA282284).

Declaration of Conflicting Interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Data Availability Statement

Representative quotes are shown in . Because of the small number of participating clinics (and participants within each clinic) and risk of identifiability, full qualitative transcripts are not being made available.*

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