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Abstract

Introduction

Cervical cancer screening literacy among rural women living with HIV (WLHIV), the ability to access, understand, appraise, and apply cervical cancer screening information to use cervical cancer screening services, is affected by individual factors including low educational attainment, low socioeconomic status, poor cervical cancer risk perception, fear, misconceptions, and beliefs, as well as interpersonal, community, and health facility barriers. However, rural public health facilities have limited resources that limit their ability mitigate these challenges. This research identified barriers and facilitators of healthcare providers’ responsiveness to cervical cancer screening literacy needs of rural WLHIV in Eastern Uganda.

Methods

This was a descriptive qualitative study that involved conducting 15 Key Informant Interviews with all individuals involved in planning, communicating, and providing cervical cancer screening services at 4 purposively selected rural public health facilities in Eastern Uganda. Data were collected using a guide developed based on the organizational Health Literacy responsiveness framework. This framework was used to derive deductive categories (domains and sub-domains) during thematic analysis, and barriers and facilitators were inductively identified from the interviews.

Results

Barriers included non-involvement of health workers and affected women in planning, limited funding, few trained health workers, long waiting times, limited space, limited communication modalities, inadequate Information Education and Communication (IEC) materials, IEC materials not translated to the local language, challenges with addressing misconceptions, and language barriers. Facilitators included support from implementing partners, free cervical cancer screening services, integration of cervical cancer screening into HIV care, consumer-centered care, clear pathways and navigation support, using peers during health education, availability of IEC materials, using simple, local language during education sessions, and health worker facilitation.

Conclusion

Strategies targeted at the identified factors can improve health care providers’ responsiveness to the cervical cancer screening literacy needs of rural WLHIV in Eastern Uganda.

Keywords

cervical cancer screening literacy barriers facilitators health care providers’ responsiveness rural women living with HIV

Introduction

Cervical cancer is the fourth most common cause of cancer among women. Globally, 570 000 cases and 311 000 deaths are reported annually, of which 85% are from low- and middle-income countries, mostly sub-Saharan Africa.^1,2 Cervical cancer is the most common cancer in Uganda, with an incidence rate of 54.8 per 100 000 women per year.³

The majority of cervical cancers can be prevented through early detection of cervical cancer by screening women of ages with maximal incidence; age 25-40 years, followed by treatment of detected precancerous lesions.^4,5 Women living with HIV (WLHIV) require more frequent cervical cancer screening than HIV-negative women because they have a shorter period from HPV acquisition to invasive cervical cancer.⁶ In Uganda, cervical cancer screening services are mainly provided through visual inspection with acetic acid (VIA)⁷ followed by treatment of precancerous lesions with cryotherapy.⁸ The Ministry of Health recommends screening among women 25-49 years, once every 3 years for HIV-negative women following a negative screening test, and once every year for WLHIV.⁹ However, there is low uptake of cervical cancer screening services among Ugandan women, with lifetime screening rates ranging from 4.8% to 30%^10,11 owing to various multi-level barriers.¹² As a result, over 80% of Ugandan women are diagnosed with advanced cervical cancer¹³ and experience poor treatment outcomes and high mortality rates.¹⁴

The integration of cervical cancer screening services into HIV care is the major strategy for improving the uptake of cervical cancer screening services among WLHIV in Uganda.¹⁵ However, despite integration, low levels of cervical cancer screening services have been reported among WLHIV in Uganda (30.3%.¹⁶ Since 2021, the Makerere University Joint AIDS Program (MJAP) USAID Local Partner Health Services – Eastern Region, LPHS-EC has supported the integration of cervical cancer screening services into HIV care in 12 districts in the Eastern region through training health workers, providing supplies, and providing health education sessions. This led to a general improvement in the uptake of cervical cancer screening services among WLHIV in the region from 36% by the end of March 2022 to 64% by mid-September 2022. However, several public health facilities still in the region had sub-optimal levels of uptake of cervical cancer screening services, ranging between 49% and 25% within the same period.¹⁷ This indicates that rural WLHIV who have access to cervical cancer screening services cervical cancer do not screen for cervical cancer.

The low uptake of cervical cancer screening services among Ugandan WLHIV has been attributed to the lack of knowledge about cervical cancer and cervical cancer screening.¹⁸ Health literacy, the knowledge, motivation, and competence to access, understand, appraise, and apply health information,¹⁹ is a predictor of knowledge of cervical cancer screening.²⁰ Accessing, understanding, and using health information result from interactions among individual, interpersonal, community, and health facility factors.¹⁹ The complexity of health information and health services and the demands they place on individuals also affect individuals’ health literacy.^21,22 “Cervical cancer screening literacy” among rural WLHIV, ability to access, understand, appraise and apply cervical cancer screening information to seek and use cervical cancer screening services is affected by individual factors including low educational attainment, low socioeconomic status, poor cervical cancer risk perception, fear, misconceptions, and beliefs as well as interpersonal, community and health facility barriers.¹¹ Therefore, improving and sustaining the uptake of cervical cancer screening services among rural WLHIV requires interventions targeting these multilevel factors. In addition, strategies aimed at improving health literacy should reduce health systems and organizational demands on people in order to ensure responsiveness to individuals’ health literacy needs.^23,24 Health literacy responsiveness is defined as “the provision of services, programs, and information in ways that promote equitable access and engagement that meet the diverse health literacy needs and preferences of individuals, families, and communities, and that support people to participate in decisions regarding their health and social well-being.²³ The 2016 World Health Organization Shanghai Declaration acknowledges health literacy as a critical determinant of health, a key driver of citizen empowerment and health equity, and establishes a mandate for developing, implementing, and monitoring strategies to strengthen health literacy in all populations.²⁵ There is a need for strategies that extend beyond the health literacy of individuals to reduce health systems and organizational demands on people to ensure responsiveness to their health literacy needs.^23,24 Hence, cervical cancer screening information, interventions, and services should be provided in ways that respond to the cervical cancer screening literacy needs of these women by mitigating the challenges they face in accessing, understanding, and applying cervical cancer screening information. However, rural public health facilities are unable to mitigate these challenges owing to limited resources.

There has been a focus on research on barriers and facilitators of the uptake of cervical cancer screening services among Ugandan women¹² and Uganda WLHIV.¹⁸ We identified barriers and facilitators of cervical cancer screening literacy among rural WLHIV from the perspective of these women.²⁶ However, there is a paucity of information on the factors that affect healthcare providers’ responsiveness to the cervical cancer screening literacy needs of rural WLHIV, which could explain the barriers faced by rural WLHIV and inform interventions. In this study, we explored barriers to and facilitators of healthcare providers’ responsiveness to the cervical cancer screening literacy needs of rural WLHIV in Eastern Uganda to identify actionable areas and interventions.

Theoretical Framework

This study adopted the organizational health literacy responsiveness (Org-HLR) framework.²³ According to this framework, the health literacy skills individuals need to interact effectively with health services depend on the complexity of those services and the demands they place on people. The Org-HLR framework recognizes the responsibility of healthcare organizations to provide health services and information in ways that promote equitable access and engagement by responding to the diverse needs of people to support their decisions and abilities to use these services. It comprises 7 domains of organizational health literacy responsiveness: (1) external policy and funding environment; (2) leadership and culture; (3) systems, processes, and policies; (4) access to services and programs; (5) community engagement and partnerships; (6) communication practices and standards; and (7) the workforce. The 7 domains of the Org-HLR framework have 24 corresponding sub-domains.²³ These domains and subdomains of the Org-HLR framework suggest areas to be considered in endeavors to identify and address system-level factors that impact health literacy.²³

Methods

Study Design

This study is part of a larger study titled “Improving cervical cancer screening literacy among rural women living with HIV in selected districts in Eastern Uganda”. This study is part of formative research aimed at identifying demand- and supply-side barriers and facilitators to cervical cancer screening literacy among rural WLHIV in East Central Uganda. We have reported the demand-side barriers and facilitators.²⁶ We describe a descriptive phenomenological qualitative study²⁷ that identified supply-side barriers, facilitators of cervical cancer screening literacy, and the needs of rural WLHIV in Eastern Uganda to complement and explain the barriers and facilitators identified among the women.

Setting and Sites

The study setting was selected districts in Eastern Uganda: Bugiri, Bugweri, Busia, Buyende, Iganga, Jinja, Kaliro, Kamuli, Luuka, Mayuge, Namayingo, and Namutumba. Cervical cancer screening services using VIA were integrated into HIV care at 42 rural public health facilities, Health Center IIIs, and Health Center IVs in these districts in 2020 and 2021, requiring WLHIV aged 25-49 years to be screened once per year. The overall prevalence of precancerous lesions among WLHIV screened for cervical cancer from October 2021 to September 2022 in these districts was 5%.¹⁷

The study sites were 4 purposively selected rural public health facilities in Mayuge and Namayingo districts of Eastern Uganda. Wabulungu HCIII and Malongo HCIII in Mayuge district and Banda HCIII and Mutumba HCIII in Namayingo District. These health facilities were selected because they represent the integration of cervical cancer screening services into HIV care at rural public health facilities in Eastern Uganda and exhibit varying levels of uptake. Between October 2021 and September 2022, the level of achieving health facility cervical cancer screening targets among WLHIV at these health facilities was as follows: Wabulungu HCIII 82% (209/254), Malongo HCIII 43% (286/671), Banda HCIII 143% (504/352), exceeded the target by 43% and Mutumba HCIII 39% (173/443).¹⁷

Participants, Recruitment, and Data Collection

We conducted 15 Key Informant Interviews with purposively selected healthcare providers involved in planning, communicating, and providing cervical cancer screening services at selected health facilities. All health care providers involved in planning, communicating, and providing cervical cancer screening services at selected health facilities were contacted by telephone to participate in the study, and none declined. These included health facility in-charges, ART clinic in-charges, volunteers, counsellors, and midwives. All participants were recruited for consultation with the ART clinic in-charges. Data were collected in June 2023 by 5 female researchers, the Principal Investigator (JN) with a Master’s training in research, and 4 research assistants with undergraduate degrees in social sciences programs and training and experience in collecting qualitative data. Researchers ensured that their credentials did not bias the data collection. Interviews were conducted in areas convenient for the participants within the health facility premises. These included the participants’ offices, under trees, and building sheds. Only the interviewer and the participant were present during each interview. Participants provided written informed consent and demographic characteristics prior to the start of each interview. Data were collected using interview guides developed based on the Org-HLR framework²³ targeting different participant categories. The interview guides were pretested among healthcare providers at a health facility not included in the study, Baitambogwe HCIII in Mayuge, prior to data collection. All other interviews were conducted in English, except for interviews with volunteers, which were conducted in the native Lusoga language and lasted between 45 minutes to 1 h and 20 minutes. Table 1 provides the sample questions for each domain.

Table 1.

Sample Questions From the Key Informant Guides

Domain	Sample questions
External policy and funding environment	How do you access funds or other support for providing cervical cancer screening services? What challenges do you face in accessing support for providing cervical cancer screening services to WLHIV?
Leadership and culture	How is improving access to cervical cancer screening services among WLHIV included in the health facility operational plans? How is improving access to cervical cancer screening information among WLHIV included in the health facility operational plans?
Systems, processes and policies	How do you identify barriers to uptake of cervical cancer screening services among WLHIV? How do you monitor, evaluate, and report on activities for ensuring access to cervical cancer screening services among WLHIV?
Access to cervical cancer screening services	What pathways do WLHIV go through to access cervical cancer screening services? What challenges do rural WLHIV face in the process of accessing cervical cancer screening services? How are WLHIV supported to navigate pathways for accessing cervical cancer screening services?
Community engagement and partnerships	How do you consult with WLHIV to develop an understanding of their needs for cervical cancer screening services? How do you work collaboratively with other organizations in the provision of cervical cancer screening services?
Communication practices and standards	What tools do you use while providing cervical cancer screening information to WLHIV? How do you tailor available cervical cancer screening tools to the specific needs of rural WLHIV?
Workforce	How are you supported to develop knowledge and skills relevant communication of cervical cancer screening to rural WLHIV? How are you supported to develop knowledge and skills relevant to providing cervical cancer screening services?

Data Management and Analysis

All interviews were audio-recorded, and each interview was labelled with a unique identifier comprising the participant’s identification number, participant category, interview date, and interviewer. Interviewers also took notes during the interviews. Each interviewer transcribed and translated the interviews they conducted within a short time. The interviews that were conducted in the local language were directly transcribed into English. Transcripts were exchanged among interviewers who listened to the audio recordings to ensure that no meaning was lost during transcription.

All interviews and transcripts were assigned unique identifiers and could not be traced back to the participants. Coding and data analysis were conducted manually in Excel by JN and an independent Research Assistant. The initial coding was done by the independent research Assistant and reviewed by JN, and both coders met to discuss and address any inconsistencies. Both coders used Template analysis for coding because it allows flexibility in coding structure and the use of a predetermined coding template.^28,29 A codebook was developed using a previously developed coding template, based on the Org-HLR framework. We used both deductive and inductive categorizations during the analysis. Deductive categorization was used for pre-determined domains and sub-domains, whereas inductive categorization was used to derive barriers and facilitators from healthcare providers’ statements. The steps in the analysis included: (1) developing a codebook based on the coding template; (2) reading each transcript to familiarize ourselves with the data; (3) coding systematically across all transcripts while ensuring that we identify important quotations and capture the source and participant identification number; (4) sorting the data by domain, sub-domain, and barriers and facilitators to retain only coded data; and (5) combining all transcripts in 1 Excel sheet and using the same criteria (by domain, sub-domain, and barriers and facilitators). The reporting of this study conforms to the Consolidated criteria for Reporting Qualitative research (COREQ) guidelines.³⁰

Ethical Approval and Consent to Participate

This study was approved by the Makerere University School of Public Health Research Ethics Committee (Protocol Number: SPH-2022-355) on 23.02.2023. We sought written permission from the authorities in the two districts and permission to conduct the study from the Uganda Council for Science and Technology (Registration Number: HS2753ES). All participants provided written informed consent. We used unique identifiers to ensure that the information collected was not linked to the participants. The study was conducted in accordance with the Helsinki Declaration of 1975, as revised in 2024.

Results

The participants included 3 health facility in-charges, 4 ART clinic in-charges, 2 volunteers, 2 counsellors, and 4 midwives. Most of the participants were female. The age range was 28-59 years, with most participants falling into the 35-and 44-year age category. Table 2 provides details of the participants’ characteristics.

Table 2.

Characteristics of Participants

Characteristics of participants (N = 15)
Variable	Frequency (n)
Sex
Male	5
Female	10
Age (years)
Age range (28-59)
25-34	4
35-44	7
45-54	3
55+	1
Health facility
Malongo HCIII	3
Wabulungu HCIII	4
Mutumba HCIII	4
Banda HCIII	4
Position
Health facility in-charges	3
ART clinic in-charges	4
Midwives	4
Counsellors	2
Volunteers	2
Highest education level
Degree	2
Diploma	7
Certificate	1
Upper secondary	2
Lower secondary	3
Years of working experience
Range (4-32)
1-9	5
10-19	5
20-29	4
30+	1
Years worked in current position
Range (1-15)
1-4	10
5-9	3
10-14	1
15+	1

Barriers to Health Care Providers’ Responsiveness to Cervical Cancer Screening Literacy Needs of Rural WLHIV

External Policy and Funding Environment

The non-involvement of health facilities in planning for cervical cancer screening services and limited funding for cervical cancer screening communication and services were identified as barriers under external policies and the funding environment.

...They (implementing partners) don’t normally involve us in the planning phase…. They come with their activities stipulated, so it is hard to change them. So, for us, when we see they are supporting us, we go with what they are saying. (Participant, category one)

There is no specific support for that (cervical cancer screening communication), but we have been integrating in giving information with the actual screening services. (Participant, category two)

Consumer-Centered Philosophy, Leadership and Culture, and Performance Monitoring and Evaluation

Non-involvement of affected women in planning for cervical cancer screening services and high workload were identified as barriers to providing consumer-centered cervical cancer screening services under the leadership and culture domain, whereas missing data was the only barrier identified under the performance monitoring and evaluation subdomains of the systems, processes, and policies domain.

When it comes to the plans, one challenge at times we don’t involve these clients when we are planning for them (Participant, category one).

……They come when we have a tight schedule, and then the one she is looking for is not in place, so it’s quite challenging to call this person to come and work on this client … (Participant, category one).

Service Environment and Initial Entry and Ongoing Access

Long waiting times and limited space were identified as barriers in the service environment subdomain. Barriers to supporting initial entry and ongoing access among rural WLHIV included long distances, challenges with follow-up on women, and limited support from implementing partners.

It can be one midwife on duty, doing other services like family planning and ANC, and you have clients who want to screen, but they are being told to wait longer… someone will get tired and walk away. (Participant, category four)

…… Where they screen from is a labor suit, so you will find there are women in labor, and yet you have referred women there for screening…… it is small, and you can’t tell the one in labor to first wait because they are going to give birth, so that is our problem. (Participant, category four)

Outreaches

The inability to screen women for cervical cancer during outreach and limited facilitation were identified as barriers to providing outreach services.

… We integrate screening in outreaches. But now we realize that the equipment we use needs a special place at the community level, which you may even miss if you go there. So, it is somehow challenging. (Participant, category two)

Provision of Cervical Cancer Screening Information

Structural barriers to providing cervical cancer screening information include a lack of trained healthcare providers, limited knowledge among healthcare providers, limited funding and space, a lack of IEC materials, inadequate IEC materials, and IEC materials not translated into the local language.

A few were trained in cervical cancer screening; they came back and gave us Continuing Medical Education (CME), but not every member of staff was there that day. So those who missed the information now lack it, creating a knowledge gap in delivering the message. (Participant, category two)

…. There is no permanent place to accommodate those women we teach; there is a room for screening them from, but a place where we can sit and teach about cervical cancer is not available. (Participant, category five)

There are no IEC materials for cervical cancer. Maybe they are there in the health facility and I don’t have but I have not seen any IEC material on cervical cancer screening. (Participant, category four)

… We still need teaching guides; we have very few. We have only one chart and a guide, so we have very few teaching guides. (Participant, category five)

IEC, that chart, then we have the SOPs, which are not in the local language. If you come here and you don’t know how to interpret them in this local language, it may be hard for you…. (Participant, category two)

Barriers encountered by health care providers in the process of providing cervical cancer screening information include limited modalities of communicating cervical cancer screening information, language barriers, challenges in addressing misconceptions and beliefs among women, and ensuring that women understand the information.

…… Those who come late may not have a chance to be educated…and those categories are also many. (Participant, category one)

Apart from the talk, if we had brochures, we would add on…. but today we have one mode of health education at the facility. (Participant, category two)

...This place is a multilingual area because we have the Samya, the Basoga, the Japadhola, and the Itesots, so at times language is a problem ……. (Participant, category one)

Removing incorrect information from a client can be a bit hard, but we do our part by giving them the facts. We give them facts, and some refuse to believe them, as if there were people in denial forever. (Participant, category one)

One challenge I have faced in teaching is that most of our women didn’t know about it (cervical cancer screening), so you must educate them for a long time, talk to them, keep on talking to them. (Participant, category five)

Workforce

Barriers in the workforce domain include a shortage of trained healthcare providers, insufficient supplies, high workload, inadequate training, insufficient facilitation, and low motivation among healthcare providers.

We have midwives who are not screening for cervical cancer, not because they don’t want to, but because they lack the skill since they were not trained. The people screening might be off; they might be on leave. So who is going to screen? (Participant, category two)

….. At times we run out of stock of gloves, and when you tell a mother to go and buy gloves, it becomes a problem…” (Participant, category three)

…. You may find only one midwife or two, and they have a lot of mothers on the other side; they may say, 'You tell those mothers to come back next week…' You know the patient has gone without a service, and getting this patient back is really hard. .…. (Participant, category two)

... I learnt tips of screening, but tips of treatment I have not gone too deep much as they have mentored me. (Participant, category three)

In terms of cervical cancer screening...No, I have not been facilitated. (Participant, category five)

Facilitators of Health Care Providers’ Responsiveness to Cervical Cancer Screening Literacy Needs of Rural WLHIV

External Policy and Funding Environment

Following the Ministry of Health guidelines, support from implementing partners was identified as a facilitator under the external policy and funding environment, respectively.

Of course, there is MOH, the guidelines, so basically here we screen mothers who are HIV positive, and they are between 25 and 49 years, that’s our age bracket. Because we screen, and they are positive, some of them we treat by thermal coagulation, and the bigger cases, like the suspects for cancer, those with cancerous …, we refer them. (Participant, category two)

.... It has been MJAP funding this program. I think, as the major funder, but also, there are other interested partners like Rays of Hope, which have also been occasionally conducting camps here for cervical screening. (Participant, category two)

Leadership and Commitment

Health facility goals to achieve cervical cancer screening services, provide cervical cancer screening education and services, and commitment by health managers to support cervical cancer screening services were identified as facilitators under the leadership and commitment subdomains.

… We set targets at the beginning of this financial year in October 2022, running up to September, and, according to the data, we exceeded our targets by more than 100% because we aimed to have all eligible women take the service screening for CA cervix. (Participant, category one)

...We make sure that mothers are aware of the benefits of screening for cervical cancer. If they are aware of the benefits, it can pull them to come for screening …... (Participant, category two)

As far as cervical cancer screening is concerned, my role is to organize the staff…… I educate them on the importance of screening for cancer at the facility. It’s also my role as the in-charge to look around and mobilize for resources as we plan together as a facility…. Also, I must make sure that those who have been found with cancer are followed up with and they get treatment. (Participant, category one)

Consumer-Centered Philosophy

Facilitators under the consumer-centered philosophy subdomain included autonomy in making decisions to screen for cervical cancer, consent before screening for cervical cancer, not coercing women, and provision of patient-centered services.

We don’t decide for them… we openly provide information about cervical cancer screening services and how they should receive them. So, women understand the information and then make informed choices or decisions (Participant, category two)

Informed consent for the woman that you are trying to give the screening of the cervix involves discussing with them the procedure itself, the advantages, and then the possible side effects….. We also discuss confidentiality issues associated with the screening process with them; they consent after understanding. (Participant, category two)

We are not supposed to force them; the client must do it voluntarily. You ask her if we would like to test you for cervical cancer, then she can say, Musawo [health worker], today I am not going to test, I will come back on another day. You ask her, Why don’t you do it? no, I came without that program. You leave and let her go away. You don’t have to force her. (Participant, category five)

... If this one wants a specific health worker, for example, I need a lady, I need a sister, so we must call that Sister and tell her there is a client here who wants your services, please come.... (Participant, category one)

Data Collection and Needs Identification

Facilitators of data collection and needs identification included the use of health facility records and feedback from women, while documenting and reporting performance were identified as facilitators of performance monitoring and evaluation.

… We didn’t know that there was a need among HIV clients. For us, we were waiting for someone who was coming with signs and symptoms of cervical cancer. However, after getting this surge, we saw that there was a need for cervical cancer screening. There is a positivity rate. From October, we now have 24 positives from the 229 we have screened. We have 24 positives (almost 10%), yes, so this caused an alarm… (Participant, category two)

…… In the process of giving them information, we also allow them to share with us what they think, they ask questions and we give them feedback so through this we get to know for example the misconceptions about the service (cervical cancer screening) then also how individuals feel about the procedure and maybe how better they may really need this service to be offered to them. (Participant, category two)

…… We got some community workers for cervical cancer who help us get the feedback from the community so that we can link up that communication feedback for cervical cancer patients at the facility … (Participant, category two)

……. We report on cervical cancer screening among WLHIV weekly, so if the data clerk says this week, you people didn’t screen cervical cancer, we start monitoring that indicator to find out why the screening was not there … (Participant, category two)

Service Environment

Facilitators in the service environment subdomain included integrating cervical cancer screening into HIV care and ensuring the availability of cervical cancer screening services.

We have embarked on offering health services and screening services (for cervical cancer) together with the rest of the services within HIV care and treatment cascade….. (Participant, category two)

We have been making sure the services (cervical cancer screening) are readily available so that WLHIV can access them. (Participant, category two)

Initial Entry and Ongoing Access

Facilitators of women’s initial entry and ongoing access to cervical cancer screening services included free cervical cancer screening, provision of information, commitment from health workers, coercing women to screen for cervical cancer, using peers to share the benefits of cervical cancer screening, clear pathways and support to navigate cervical cancer screening services, consumer-centered care, follow-up, and referral.

...It (cervical cancer screening) is free of charge so long as someone is in the age bracket…because we have eligibility criteria. (Participant, category four)

...During health education, we talk about cancer (cervical cancer) screening, and for those who are eligible, we give them more information as they agree to get the services. (Participant, category four)

……. we take away their books…. because she will not get the drugs …… she has been dodging, so you confiscate her book, and then you end up with her acceptance to screen. (Participant, category three)

….. we make sure that we mix the ones who tested positive with those who don’t want to go for screening …… so that a person who has gone, has the experience and is positive, shares that experience with others……. that positivity, in a way, has helped us change many patients here. (Participant, category two)

As they come, we usually screen them (for eligibility). After screening them, they are health educated, and those who are eligible for screening are screened if they don’t opt out. (Participant, category one)

We have our lay volunteer or linkage facilitator who always escorts them (to go for cervical cancer screening) …. (Participant, category two)

….. You don’t just send them there; you must also follow up to confirm with the midwives whether the women you sent have been screened. (Participant, category four)

…… If they are screened and found to have cervical cancer, they are referred to Mayuge (HCIV) and are given the phone numbers of the health workers they are supposed to meet in Mayuge. (Participant, category four)

Outreach Services

The integration of cervical cancer screening services into outreach, confidentiality during outreach, and working with community health workers were identified as facilitators of outreach services.

...If we are going for an outreach, we integrate the cancer screening component to at least make sure the community is sensitized. (Participant, category two)

...In our community outreaches, the mobilization is not usually labeled in a way that indicates we are looking for WLHIV, because we understand the issues of confidentiality… (Participant, category two)

Community Engagements and Partnerships

Facilitators in the community engagement and partnership domains include the use of community health workers and partnerships with other organizations.

...We are working with the community, facilitating staffs …… they get feedback, they visit those who were screened to get the challenges, so they link the facility and the community…. (Participant, category two)

…There is an organization called Mother to Mother…... it supports us in making sure that they bring these mothers on board. (Participant, category one)

Provision of Cervical Cancer Screening Information

Structural facilitators of providing cervical cancer screening information included health worker training and the availability of IEC materials. Facilitators of providing cervical cancer screening information included interactive health education sessions, one-on-one health education sessions, peer sharing of experiences with cervical cancer screening, use of local language, ensuring that women have understood, using simple language, consumer-centered communication, addressing misconceptions, fears, beliefs, and teamwork during health education sessions.

….. Since we were trained through CME, we also give health education talks to the mothers before they are screened. (Participant, category two)

….. You see, with rural mothers, when you talk to them a lot, some of them don’t understand, so we have a tool that extracts the information. We make sure that whatever is there has been dispersed...... Midwife

...... During the health education sessions, we don’t monopolize; we make it interactive, a dialogue talk, we give opportunity to each person …. (Participant, category two)

..... Others have their own issues as individuals, and then she comes to see you in person to ask more questions and better understand. Others are afraid, and cannot ask a question in public, then she comes looking for you... If you are not busy, you give her time. (Participant, category three)

...we say, “If you know you were screened, raise your hand.” “Are you willing to share your experience with this other team?” Then she will begin to share her experience, so we have to make sure that at least the information gets out of the client’s mouth... (Participant, category two)

….. You must use the language everyone understands, not being in our villages and using English to teach. (Participant, category five)

You should use the easiest language, easy such that anybody can understand it, don’t bring your terminologies…… no, use the simplest language such that even the last person in the village can understand. (Participant, category three)

My role as a volunteer is to provide information, so I am very friendly with these people. Most of them know us as community members, so they are very open with us. (Participant, category five)

As we are doing health education, we first probe and find out how much they know…. Then, based on what they have discussed, you pick out the myths and misconceptions and clear them up. (Participant, category three)

……. When I am talking to them, the ART clinic in charge is usually present, so if they ask something I can’t explain in detail, she helps and gives explanations… (Participant, category four)

Workforce

Facilitators in the workforce domain included trained and dedicated healthcare providers and supplies. Training, Continuing Medical Education (CME), and mentorship were identified as ways healthcare providers receive ongoing professional development, whereas other types of support include supervision and facilitation.

….. We have about three midwives who know how to screen for cervical cancer, and in case they are available, the work moves on smoothly. (Participant, category five)

What we have is enough because we have enough cotton and acetic acid, and we actually give some out to other centers to start screening. (Participant, category three)

…… We have held capacity-building sessions with various professional organizations, right from the facility … (Participant, category two)

…. They only train clinicians and midwives; counsellors were not trained, so it was the midwives who came back and did a CME for the counsellors. (Participant, category four)

We offer mentorship for staff; the only difference between us and them is that we have the skill for screening. We involve them, pass on the information, and they are also part of the health education. (Participant, category two)

Our HSD (Health Sub-district) comes and mentors these midwives on how they are doing it and how they should manage the cases that they have, including referrals. (Participant, category four)

Table 3 shows facilitators and barriers of health care providers’ responsiveness to cervical cancer screening literacy needs of rural WLHIV mapped onto the Org-HLR.

Table 3.

Barriers and Facilitators of Health Care Providers’ Responsiveness to Cervical Cancer Screening Literacy Needs of Rural WLHIV

^b Sub-domain	^c Barriers	^c Facilitators
^a Domain 1: External policy and funding environment
External policies and funding environment	Non-involvement of health facilities in planning for cervical cancer screening services	Following Ministry of health guidelines Support from implementing partners
External policies and funding environment	Limited funding
^a Domain 2: Leadership and culture
Leadership and commitment		Goal to achieve cervical cancer screening targets
		Goal to provide cervical cancer screening education and services
		Commitment by health facility managers
Consumer-centred philosophy	Non-involvement of affected women in planning for screening services	Autonomy in making decisions to screen for cervical cancer
	High workload	Consent before screening for cervical cancer
		Not coercing the women to screen
		Patient-centered services
^a Domain 3: Systems, processes, and policies
Data collection and needs identification		Using health facility records
Data collection and needs identification		Feedback from the women
Performance monitoring and evaluation	Missing data	Documenting and reporting performance
^a Domain 4: Access to cervical cancer screening services
Service environment	Long waiting time	Integration of cervical cancer screening services into HIV care
Service environment	Limited space	Availability of cervical cancer screening services
Initial entry and ongoing access	Long distances
	Challenges follow-upLimited support from implementing partners	Cervical cancer screening is free of charge
		Provision of information
		Commitment from health workers
		Coercion (not ethically accepted)
		Using peers to share the benefits of cervical cancer screening
		Clear pathways for accessing cervical cancer screening services
		Support navigating cervical cancer screening pathways
		Consumer-centered services
		Follow up
		Referral
Outreach services	Inability to screen for cervical cancer during outreaches	Integration of cervical cancer screening communication and services into outreaches
Outreach services	Limited facilitation	Confidentiality during outreachesWorking with community health workers
^a Domain 6: Cervical cancer screening communication practices and standards
Cervical cancer screening information provision	Lack of trained health workers	Health worker training
	Limited funding	Availability of IEC materials
	Limited space	Using community health workers
	Inability to reach all women	Interactive health education sessions
	Limited communication modalities	One-on-one health education sessions
	Lack of IEC materials	Peers sharing their experiences
	IEC materials have not been translated into the local language	Use of local languageUsing simple language
	Language barrier	Ensuring that women have understood
	Challenges with addressing misconceptions and beliefs	Addressing misconceptions, fears, and beliefs
	Challenges with ensuring that women understand the information	Consumer-centered communicationTeamwork during health education sessions
^a Domain 7: Workforce
Practice tools and resources	Few trained health workersLack of supplies	Availability of trained health care providersDedicated health care providers
Practice tools and resources	High workload	Availability of supplies
Ongoing professional development	Inadequate training	Training
		Continuing Medical education
		Mentorship
Supportive working environment	Lack of facilitation	Support supervision
Supportive working environment	Lack of motivation among health care providers	Facilitation

Discussion

This study applied the Organizational Health Literacy Responsiveness (Org-HLR) framework to identify barriers and facilitators of healthcare providers’ responsiveness to the cervical cancer screening literacy needs of rural WLHIV in Eastern Uganda. Based on the existing literature, the identified factors can be categorized into 5 broad categories: (1) policy, funding, and leadership support, (2) infrastructure, (3) resources and health worker facilitation, (4) accessibility of cervical cancer screening information and services, and (5) patient-centered communication and services.

Lack of funding for cervical cancer screening communication and services was identified as a barrier under policy, funding, and leadership support. Inadequate funds have been previously reported as a barrier to implementing patient-centered interventions and motivating staff.³¹ Facilitators in this category included health facility goals and commitment by health facility managers, which have been reported in other studies to promote patient-centered care.^31-33

Limited infrastructure, in terms of space, has been reported as a barrier to providing a conducive environment for cervical cancer screening. This finding agrees with previous studies that reported physical resources and environmental constraints as barriers to patient-centered care³³ and limited space as a health system barrier to the uptake of cervical cancer screening services.^18,34

Barriers identified under resources and health worker facilitation included a limited number of trained health workers, inadequate training, insufficient supplies and IEC materials, high workload, limited facilitation, and lack of motivation among health care providers. A lack of trained staff has been reported as a barrier to providing cervical cancer screening services in previous studies in Uganda.^18,34,35 These studies also reported inadequate training and a lack of supplies^18,34,35 as barriers to providing cervical cancer screening services. Our findings on the lack of IEC materials and the inadequacy of those available are in line with a Ghanaian study, which found that adequate cervical cancer screening education tools are important for addressing the information needs of WLHIV.³⁶ Previous studies have reported that high workload³³ and time constraints³⁷ are barriers to providing patient-centered care and that high workload is a barrier to providing cervical cancer screening services.¹⁸ Staff satisfaction has previously been reported as a facilitator of patient-centered care,^32,33 whereas unsupportive staff attitudes have been reported to impede its provision.³³ Facilitators identified under resources and health worker facilitation included the availability of trained and dedicated healthcare providers, health worker training, availability of supplies, IEC materials, and facilitation. Health worker training, logistical support, and health workers’ commitment³¹ and staff satisfaction^32,33 have been reported to facilitate patient-centered care, whereas adequate communication tools are important for addressing the cervical cancer information needs of WLHIV.³⁶

We identified long distances, long waiting times, challenges with following up on women, and language barriers as barriers to the accessibility of cervical cancer screening information and services. Previous studies have also reported that long distances are a barrier to patient follow-up³⁷ and access to cervical cancer screening services.³⁴ Similar studies have reported that long waiting times³⁴ and lack of proper follow-up mechanisms¹⁸ are health system barriers for providing cervical cancer screening services, whereas language differences impede health workers’ ability to communicate with patients.³¹ Facilitators identified under accessibility of cervical cancer screening information and services included the provision of cervical cancer screening information, integration of cervical cancer screening services into HIV care, proving cervical cancer screening services free of charge, availability of cervical cancer screening services, clear pathways and support to navigate cervical cancer screening services, community outreach, the use of community health workers, and follow-up. Receiving information and counselling has been reported to alleviate anxiety among WLHIV during cervical cancer screening.³⁶ Previous studies have reported that coordination to address multiple patient needs on a single visit is important for delivering patient-centered care³⁷ and the integration of cervical cancer screening services into HIV care improves access to cervical cancer screening services among WLHIV.^15,38,39 The cost of cervical cancer screening services has been previously reported as a barrier to uptake of cervical cancer screening services.⁴⁰ Patient support has been reported to facilitate patient-centered care,³³ and support for WLHIV in navigating cervical cancer screening services is important for addressing barriers to cervical cancer screening.⁴¹ Previous studies have also recognized the importance of outreach,³¹ community engagement,⁴² and follow-up³⁷ in providing patient-centered care, overcoming social barriers to the uptake of cervical cancer screening services, and ensuring continuity of care, respectively.

Non-involvement of affected women in planning for cervical cancer screening services and challenges in ensuring that women understand the information were identified as barriers to patient-centered cervical cancer screening communication and services. Our finding on the Non-involvement of affected women in planning for cervical cancer screening services is supported by a finding from a Ghanaian study that engaging patients in coming up with solutions and improving the quality of care facilitates patient-centered care.³¹ A study conducted at a large HIV clinic in Uganda also reported that inadequate information and the inability to adequately explain to women were barriers to the uptake of cervical cancer screening services.¹⁸ We identified women’s involvement through consent, autonomy in decision-making, non-coercion, using peers to share experiences, interactive health education sessions, consumer-centered communication, use of local language, use of simple language, addressing misconceptions, and obtaining feedback from women as facilitators of patient-centered communication and services. In line with our findings, previous studies have also recognized the importance of patient participation in decision-making,⁴³ peer-to-peer education,⁴² interactive health education,^31,44 adapting communication to patients’ needs³⁷ and receiving feedback from patients.^31,32

Our research identified context-specific barriers such as non-involvement of health facilities in planning for cervical cancer screening services, lack of a direct relationship with some partners, missing data for monitoring performance, inability to reach all women with information, IEC materials not translated to the local language, inability to screen for cervical cancer during outreaches, and challenges in ensuring that women have understood and facilitators, including coercion (not ethically accepted), and addressing misconceptions and fears that have been previously reported in the literature.

Identified barriers, lack of IEC charts, IEC charts not translated into the local language, misconceptions among women and peers, and lack of partner support and facilitators, providing health education, peers sharing experiences, and using local language during health education sessions were also reported by rural WLHIV.²⁶ However, unlike healthcare providers who reported coercing women to screen for cervical cancer as both a barrier and facilitator, rural WLHIV women reported that coercing them was a barrier to cervical cancer screening.²⁶ This highlights the need to identify demand-side and supply-side factors that affect cervical cancer screening literacy among these women to inform effective multi-level strategies.

Limitations and Strengths of the Study

Few previous studies have assessed the barriers and facilitators of health care providers to the cervical cancer screening needs of rural WLHIV. This study included rural public health facilities in Eastern Uganda that had both high and low levels of uptake of cervical cancer screening services among WLHIV. This enabled us to identify the barriers to and facilitators of health care providers’ responsiveness to the cervical cancer screening needs of rural WLHIV. We interviewed different categories of healthcare providers: healthcare facility in-charges, ART clinic in-charges, midwives, counsellors, and volunteers involved in the planning, communication, and provision of cervical cancer screening services. This allowed for triangulation of information and, therefore, improved the validity of our findings. Our data collection, analysis, and reporting of the results were based on the organizational Health Literacy responsiveness framework. This framework enabled us to obtain detailed information on the barriers and facilitators of health care providers’ responsiveness to the cervical cancer screening literacy needs of rural WLHIV.

Our study was restricted to only 4 rural public health facilities in Eastern Uganda and a small sample of 15 KIIs. This constrains the generalizability and representativeness of the findings. We assessed the barriers and facilitators of healthcare providers’ responsiveness to the cervical cancer screening literacy needs of rural WLHIV from the perspective of healthcare providers. Therefore, our findings may not reflect the needs of all women. Investigation of cervical cancer screening literacy needs of rural WLHIV is necessary. Our focus on applying the Org-HLR framework in developing the interview guides and data analysis may have introduced confirmation bias and underreporting of themes beyond this framework. Recruiting participants through consultation with the ART clinic in-charges may have introduced selection bias by favouring more engaged or available health care providers. Using data from 1 month, June 2023, provided a cross-sectional view that did not capture temporal changes in service provision, staffing, and funding. We relied on double coding and consensus without member checking or any other reliability checks. This may have affected the quality of the analysis. We included only cadres involved in planning, communication, and the provision of cervical cancer screening services at the selected health facilities. Therefore, the perspectives of cadres at levels beyond the health facilities may be underrepresented.

Conclusion

The identified barriers included non-involvement of health workers and women in planning, limited funding, few trained health workers, long waiting times, limited space, challenges with following up women, limited communication modalities, inadequate IEC materials, IEC materials not translated to the local language, challenges with addressing misconceptions, and ensuring that women understand, and language barrier. The identified facilitators included following MOH guidelines: support from implementing partners, free cervical cancer screening services, integration of cervical cancer screening into HIV care, outreach, consumer-centered care, clear pathways and support to navigate, follow-up, referral, coercion (not ethically accepted), using peers, availability of IEC materials, using simple and local language during education sessions, obtaining feedback from women and health worker training, facilitation, and supervision. These barriers and facilitators can be targeted through attitudinal changes among health care providers and interventions by health facilities, implementing partners, and the Ministry of Health. Strategies targeting these factors may help rural public health facilities in the study setting and other rural public health facilities in Uganda improve their responsiveness to the cervical cancer screening needs of rural WLHIV. This may lead to an improved uptake of cervical cancer screening services and a reduction in disparities in the cervical cancer burden among these women.

Footnotes

Acknowledgements

We thank the Makerere University Joint AIDS Program USAID Local Partner Health Services – East Central Region Project for giving us the opportunity to use their data to inform us of this research. We thank the healthcare providers who participated in our study and openly answered our questions. We thank our research assistants, Prossy Aliweebwa, Resty Nakayima, Virginia Viola Bangi, and Lilian Tabwenda, for their efforts during data collection and transcription. We thank Amanya Leo for his support during data analysis.

ORCID iD

Juliana Namutundu

Ethical Consideration

Consent to Participate

All participants provided written informed consent. We used unique identifiers to ensure that the information collected was not linked to the participants. The study was conducted in accordance with the Helsinki Declaration of 1975, as revised in 2024.

Author Contributions

Conception: JN and FM, writing the proposal: JN, RKW, FCS, ENJ, JK, MLO, DN, MN Data analysis and interpretation: JN, ENJ, JK, MN Drafting the manuscript: JN. All authors reviewed and approved the final version of the manuscript.

Funding

This study was funded by NIH U54 award 1U54CA254518-01 (U54CA25458). The research reported in this publication was also supported by the Fogarty International Center, the National Institute of Mental Health, and the Office of AIDS Research of the National Institutes of Health under Award Number D43 TW010037 which funded Juliana Namutundu’s PhD Scholarship. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

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

Data in form of transcripts may be availed by the corresponding author upon request.*

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“Correcting Misinformation is Challenging”: Exploring Barriers and Facilitators of Health Care Providers’ Responsiveness to Cervical Cancer Screening Literacy Needs of Rural Women Living With HIV in Eastern Uganda

Abstract

Introduction

Methods

Results

Conclusion

Keywords

Introduction

Theoretical Framework

Methods

Study Design

Setting and Sites

Participants, Recruitment, and Data Collection

Data Management and Analysis

Ethical Approval and Consent to Participate

Results

Barriers to Health Care Providers’ Responsiveness to Cervical Cancer Screening Literacy Needs of Rural WLHIV

External Policy and Funding Environment

Consumer-Centered Philosophy, Leadership and Culture, and Performance Monitoring and Evaluation

Service Environment and Initial Entry and Ongoing Access

Outreaches

Provision of Cervical Cancer Screening Information

Workforce

Facilitators of Health Care Providers’ Responsiveness to Cervical Cancer Screening Literacy Needs of Rural WLHIV

External Policy and Funding Environment

Leadership and Commitment

Consumer-Centered Philosophy

Data Collection and Needs Identification

Service Environment

Initial Entry and Ongoing Access

Outreach Services

Community Engagements and Partnerships

Provision of Cervical Cancer Screening Information

Workforce

Discussion

Limitations and Strengths of the Study

Conclusion

Footnotes

Acknowledgements

ORCID iD

Ethical Consideration

Consent to Participate

Author Contributions

Funding

Declaration of Conflicting Interests

Data Availability Statement

Appendix

References