Improving cervical cancer continuum of care towards elimination in Ethiopia: a scoping review

Introduction: Cervical cancer is the second-leading cause of death among all cancers in Ethiopia. Ethiopia plans to eliminate cervical cancer as a public health problem by 2030, following the World Health Organization’s call for action. A scoping review was conducted on the status of the cervical cancer continuum towards elimination in Ethiopia. Methods: We searched articles in PubMed, Scopus and Google Scholar. All studies conducted on cervical cancer in Ethiopia, irrespective of date of publication, type of article, or language of publication were included. However, conference abstracts, commentaries, and letters to the editors were excluded. We used EndNote x9 software to merge articles from different databases and automatically remove duplicates. Screening of titles, abstracts, and full texts was performed by two co-authors independently. The cancer care continuum was employed as a framework to guide data synthesis and present the findings. Results: Of the 569 retrieved articles, 159 were included in the review. The found most of articles were about knowledge, attitude, and practice. There were few studies on health-seeking behaviour, perception and acceptability to cervical cancer services and availability and readiness of a screening programme. The review identified that there was inadequate knowledge, attitude and perception about cervical cancer. Screening for cervical cancer is not widely used in Ethiopia. Knowledge and attitude, education status, and income were repeatedly reported as precursors for cervical cancer screening. Most studies concluded a high prevalence of precancerous lesions and cervical cancer, as well as high mortality rates or short survival times. The review also identified that there is huge heterogeneity in findings under each component of the cancer care continuum across time and geographic settings. Conclusions: Overall, there is inadequate knowledge, perception, health seeking behaviour, screening and treatment services. This implies that the country is lagging behind the targets towards eliminating cervical cancer despite the availability of effective interventions and tools. We argue that an implementation research is needed to identify implementation issues, challenges and strategies to scale up both primary and secondary prevention services so that cervical cancer will not anymore be a public health problem.


Introduction
Cervical cancer is a signi cant global health problem, with an estimated 604,127 new cases and 341,831 deaths worldwide in 2020, making it the fourth-most prevalent cancer among women (1). Almost 90% of these deaths occur in low-and middle-income countries (2). Africa has seen the highest incidence and mortality rate of cervical cancer, and countries in the region have bear a greater burden compared to others (3). For instance, in Ethiopia, there were 7,445 new cases of cervical cancer and 5,338 deaths in 2020 (4). Cervical cancer has a huge impact women's disability-adjusted life years, nancial burden, and life expectancy (5,6). Cognizant of its impact, global and national policy strategies have been set as a guide to halt the incidence and deteriorating effects of cervical cancer (7).
There is ample evidence that vaccination, early identi cation, and treatment are effective to prevent cervical cancer (7). In line with this, the World Health Organization (WHO) launched a plan to eliminate cervical cancer as a public health problem by 2030 through targets including 90% of girls fully vaccinated with human papilloma virus (HPV vaccine) by age 15 years, 70% of women are screened with a highperformance test by 35 years of age and again by 45 years of age, and 90% of women identi ed with cervical disease receive treatment (90% of women each precancer treated and invasive cancer managed) (8). The Economist Intelligence Unit has proposed recommendations to eliminate cervical cancer as a public health treat, including generating local data to inform health nancing design and decision-making (9). The Union for International Cancer Control also supports prevention, multi-cancer early detection, and treatment in support of the WHO cervical cancer elimination policy (10).
Despite these global initiatives and recommendation, the progress towards cervical cancer elimination is still lagging behind those targets. A study in Ethiopia found that women had a relatively poor awareness of cervical cancer and favoured traditional remedies as a treatment option for the early stages of the disease (11). Inadequate awareness is one of the challenges to receiving health care services (12).
The strategic plan for cervical cancer elimination calls for countries to adopt a full-continuum approach, encompassing prevention, screening, diagnosis, treatment, psychosocial care, and outcomes (13).
However, there is scarcity of evidence about these cancer continuum indicators, making it di cult to determine the status of program implementation towards elimination. We argue that an in-depth understanding of the overall cervical cancer continuum, including epidemiology, promotion, prevention services, as well as outcomes and impacts will help countries to develop mid-and long-term strategy towards elimination.
In Ethiopian context, this scoping review was conducted to assess the cervical cancer continuum in Ethiopia, including prevalence of cervical cancer, knowledge, attitude, perception, health-seeking behavior, prevention services, and outcome and impacts of cervical cancer.

Reporting
The review was conducted based cancer care/control continuum model (13). The rst component is health promotion and disease prevention services/domains. These are: behavioural interventions (awareness, knowledge, attitude, and perception), vaccination, and the health-seeking behaviour of women. Screening and diagnosis are the second phase in the continuum. Psychosocial care encompasses the cancer patient's experience with treatment, satisfaction, and general happenstance during their interaction with the health system. Furthermore, treatment outcome and disease impact are important section of the continuum (Figure).

Search strategy
A literature search was conducted using the term cervical cancer associated with Ethiopia, irrespective of language, settings, and date of publication. We searched articles indexed in PubMed and Scopus from inception to March 15, 2023. We searched Ethiopia with 'AND' Boolean operator in the title and abstract of records in PubMed, and in the title, abstract, and keywords of records in Scopus. Additional records were searched on Google Scholar.

Inclusion and Exclusion criteria
Inclusion criteria were any kind of studies conducted on cervical cancer in Ethiopia. There was no restriction on the date of publication, type of article, or language of publication. However, conference abstracts, commentaries, and letters to the editors were excluded.

Screening, selection and data extraction
We used EndNote x9 software to merge search results from different databases and remove duplicates. Screening of articles by titles, abstract and full text was conducted independently by two of the coauthors (AE and HA). Any disagreement was solved by discussion. A data extraction sheet was prepared and approved in consultation with the last author (YA). The data extraction sheet included rst author, publication year, study setting, region, study design, major category (based on the cancer care continuum), and main ndings.

Data synthesis
The characteristics of the articles were described using frequency distribution. Data synthesis began with a thematic category of available articles based on the cancer care continuum. These themes were knowledge and attitude or perception towards cervical cancer or prevention services, HPV, health seeking behaviour, diagnosis (prevalence of cervical cancer lesions), treatment (health care experience), and outcome (mortality).

Characteristics of articles
The search identi ed a total of 569 articles: 248 from Scopus, 158 from PubMed, and 164 from Google Scholar. After title, abstract and full-text screening, 159 articles were included (supplementary le on characteristics of articles) in the review. Eleven articles were on HPV vaccination, with different proportions in the regions. There were 36 articles on knowledge, attitude, and practice about cervical cancer screening. The willingness and acceptability of women for cervical cancer screening were examined by one study each in Amhara and Addis Ababa. Four articles assessed health-seeking behaviour and demand for cervical cancer screening (2 articles in Addis Ababa and one article each in Oromia and Tigray). Five articles assessed women's intention to undergo cervical cancer screening in Amhara (3 articles) and Oromia (2 articles). Forty-two articles were available on cervical cancer screening uptake. In 26 articles, the epidemiology of precancerous cervical lesions is described, and the prevalence of cervical cancer is assessed in 6 articles. Ten articles were found on cervical cancer patients experiences when interacting with the health system or due to the disease mechanism. Ten articles (seven studies in Addis Ababa and three in the Amhara region) were found on mortality or survival of patients with cervical cancer. This review ndings presented based on the cancer care continuum model in the subsequent sections.

Health Promotion and Prevention
Knowledge, attitude/perception and practice The ndings related to knowledge, attitude, perception and practice are heterogeneous among populations and locations. Among university/college students good knowledge about cervical cancer/and/or screening ranged from 9.3% (14) to 35.6% (15). Knowledge about the cause and risk factors of cervical cancer was also low among health care providers; only 43.8% of female healthcare providers were knowledgeable (16), while 51.6% of urban health extension workers were nonknowledgeable (17). Among women who attended health facilities, 21.2% in the Amhara region (18) and 86.9% in the Southern Nations Nationalities Region (SNNPR) (19) were knowledgeable. According to community-based studies, around 20% of women in Amhara region (20) and 46.4% of women in Tigray region (21) had knowledge about cervical cancer.
The review ndings were also observed in attitude towards cervical cancer and/or screening among college or university students, health care professionals, women in the community, and those who attended health care facilities. It ranged from 44.1% at Wollega University (22) to 71.7% at Adama Science and Technology University (23). About 30.7% of female health care providers had unfavourable attitude in the Amhara region (16). Based on community-based studies, the lowest result (53.3%) and highest (64%) of women had a favourable attitude towards cervical cancer in Tigray (21) and Amhara regions (24), respectively. A lower level (46.1%) of favourable attitude was reported among women who attended health facilities (25). More than one-third (34.8%) of women in the SNNPR had unfavourable attitude towards cervical cancer (26).
Few studies assessed the perception of university students, women, and men, as well as community leaders on cervical cancer and/or screening. For example, 33.2% of female students in higher education perceived to be at risk of cervical cancer (15). According to a qualitative study, women in the community perceived that they were not vulnerable to the disease and believed cervical cancer screening was not necessary (27). Socioeconomic and demographic barriers are available in supplementary table (sTable  1).

Health seeking behaviour
A qualitative study among men, women, and community leaders in rural settings in Oromia region revealed that study participants preferred traditional healers over modern medicine (28). Women's health seeking behaviour was also found to be low in Addis Ababa (29). It was found that only 14.2% of women had good health seeking behaviour in the southern part of Ethiopia (30). Lack of information and awareness, or poor knowledge, were the common barriers or reasons that women and community leaders were unable to attend health care (28-30) (sTable 2).

Human Papilloma Virus Vaccination
The review found that that HPV vaccines acceptance rate of parents varied from 44.8% (31) to 94.3% (32). The HPV vaccination status among female students ranged from 44.4% (33) to 66.5% (34). Higher acceptance of vaccine was associated with media exposure and parents' perceptions of positive behavioural control (35). On the other hand, lack of knowledge (11,36), unfavourable attitudes toward the vaccine (37, 38), living in rural area, poor socioeconomic status, and being a member of an unidenti ed target population for HPV vaccination (31) were identi ed as challenges of the vaccination programme (sTable 3).

Early detection and diagnosis
Cervical cancer screening A meta-analysis, based on the articles published before 2020, estimated that 14.8% of women utilized cervical cancer screening services in Ethiopia, with the lowest in the Amhara region (13.6%) and the highest in the SNNPR (18.6%) (39). Another meta-analysis showed 18.2% of women living with human immunode ciency virus (HIV) underwent cervical cancer screening in 2020 (40). There were studies that reported that 2.5% (14) or none (22) of university students were screened for cervical cancer. About 20.3% of female sex workers responded that they had received cervical cancer screening (41).
One nationwide study among 632 health facilities using service availability and readiness assessment 2016 and 2018 involving 'equipment', 'reagent', 'training' and 'guideline' as tracer items. This study found that 21% and 33% of the health facilities delivered cervical cancer screening in 2016 and 2018, respectively; none of health facilities have ful lled all four components (42). Moreover, health care providers have rare exposure to demonstrate cervical cancer screening skills. For example, only 8.7% of female health care providers had exposure to regular cervical cancer screening practises in Amhara region (16).
The review also identi ed effective strategies to scale up the cervical cancer screening programme. These were a cervical cancer screening campaign assisted by robust technology (43), health education at the coffee ceremony (44) and other settings (45), and 'single-visit approach'/ 'Addis Tesfa Project' (46). Individual and social determinants that encouraged utilization of cervical cancer screening were having symptoms of vaginal bleeding, physician recommendation (47), women having attended formal education and having good knowledge toward cervical cancer screening, a history of sexually transmitted infections (39), a favourable attitude about cervical cancer and screening (48) and higher sexual autonomy (49). Another study involving health workers also identi ed barriers such as low community and provider awareness of cervical cancer, lack of space and equipment to offer screening, and lack of support from leaders (50), social and religious in uence (51). The detail characteristics of the studies and additional ndings are available in sTable 4.

Precancerous cervical lesion and cervical cancer
The overall prevalence of oncogenic HPVs (HPV 16/18) and the VIA-positivity rate, possibly indicative of cervical lesions, were 7.1% and 13.1%, respectively (52). Another study using VIA estimated that 10.3% (53)  Only 41% of women who underwent cervical cancer screening in Addis Ababa were satis ed with the services (62). Women with cervical cancer faced interruptions of social cohesion, felt stressed, and struggled with work and daily life (63); Care givers were also less satis ed with 'physical patient care' and 'provision of information' (64). Cervical cancer results in social impact on patients, including social discrimination (61.8%), loss of body image (63%), loss of sexual functioning (78%), loss of femininity (89%) and nancial crises by loss of income (45.7%), medical and non-medical expenditure (71%), and work and employability challenges (66.8%) (65). The quality of life of women diagnosed with cervical cancer was low due to poor physical functioning, emotional functioning, pain, and symptom experience (66). Two studies showed the nancial costs of cervical cancer (63, 67). One of the two articles that reported nancial crises qualitatively explored women's experiences during their follow-up care in Tikur Anbessa Specialized Hospital, Addis Ababa in 2022 (63). The latter study estimated the direct outpatient and inpatient costs that women with cervical cancer incur for health care was US$334.2 and US$329, respectively, in 2013 (67).

Outcome
Mortality due to cervical cancer There are reviews on mortality due to cervical cancer that assessed using document reviews in hospitals. In Addis Ababa, only 28% of study participants survived in ve years (68). Another study estimated that 38.6% of women survived for ve years (69). The incidence of mortality was 15.6 per 100 per year (70). In contrast, the overall incidence of mortality was estimated to be 31 per 100 person-years of follow-up (71). In the Amhara region, 36.6% of women died in a study conducted at the University of Gondar Hospital from 15 May 2018 to 15 May 2022; they also estimated that the median survival time was 42 months (72). Another study in the same setting estimated that probability of women to death was increased with an increased tumor size (73). Another study in Felegehiwot Comprehensive Specialised Hospital in the Amhara region estimated that the mean survival time was 40.1 months from 25 June 2017 to 31 March 2021 (74). Adherent patients were more likely to survive (75), while older age groups and women with advanced disease stages and low baseline anaemia were more likely to die (76) (sTable 6).

Discussion
This scoping review, conducted based on the cancer continuum care model on women's knowledge, attitude, and perception, health seeking behaviour, uptake of cervical cancer prevention services (HPV and screening), prevalence of cervical cancer, women's experience in health care, and treatment outcome (e.g., mortality) in Ethiopia.
The majority of the articles reported that about 50% and more of the study participants were not knowledge about cervical cancer, prevention, and services (19,22,77,78). Similarly, about half or more women had an unfavourable attitude except in a few studies that reported better attitude coverage (14,23,77,79,80). Knowledge was frequently reported as a precursor to a favourable attitude (16, 26, 81). A meta-analysis nding among women living with HIV in Africa revealed a comparable estimate to knowledge (43.0%) and attitude (38.0%) towards cervical cancer (82). Lack of information and awareness, or poor knowledge, was also the common barrier or reason that women and community leaders were unable to attend health care (28-30) and the reason for unacceptability of screening services (83, 84). In contrast, a meta-analysis nding in Africa claimed that 'school-based education' improves knowledge, perception, attitude, intentions toward and uptake of cervical cancer screening services (85). The review also found that women's and communities' health-seeking behavior was low, including among those living in the capital city, Addis Ababa. Cervical cancer screening acceptability was low among women with HIV in Addis Ababa (83) and a rural small city in Amhara region (84) that were conducted before nine and six years, respectively, which needs recent research. Additionally, further triangulated evidence, including men, women, and key informants from several sectors, on knowledge, attitude, and perception would support the implementation of whole-of-society and whole-of-government approach to strengthen and scale up cervical cancer prevention activities. at all levels (86).
A higher HPV vaccination coverage was observed among students; both were above the global estimation; global HPV vaccination coverage was 12.2% in 2018 (87). Another meta-analysis nding in low-and middle-income countries (45.48%) (88) is comparable with vaccination uptake based on one study in Oromia region in Ethiopia (44%) (33), but lower than a single district study in Amhara region Ethiopia (66.5%) (34). However, HPV vaccination coverage was high in routine or administration programmes (89.0%) (88). Those female adolescents who had prior information, good knowledge, and a favourable attitude were more likely to be vaccinated and show a willingness to be vaccinated (33, 34).
HPV vaccination coverage was further improved by narrative education, outreach plus reminders, nancial incentives plus reminders, brief motivational behavioral interventions, training plus assessment and feedback, and multicomponent interventions in high-income countries (89). These are relevant interventions that could assist the scale up of vaccination program in Ethiopia. However, it should be guided by implementation studies that evaluate the effectiveness, e ciency, and acceptability of these interventions in Ethiopia. Though few studies found a higher percentage of women showing willingness to get their children vaccinate in Ethiopia (32), many women did not participate in health care interventions for their own health, as a higher percentage of women were not screened for cervical cancer (90).
The review found that the national coverage of cervical cancer screening was low (39,48,91). Cervical cancer screening was slightly higher among women with HIV (40) than other women (39,91); this might be because women with HIV have better exposure to health services due to long-term adherence with HIV treatment. A worldwide review showed that about 67% of women aged 30-49 years have never been screened for cervical cancer, which is very low in low-income countries (11%) (92). Women's income was associated with cervical cancer screening (93) as were knowledge, attitude, and health-seeking behavior (17,19,21,94). The cost-effectiveness of cervical cancer screening methods (cytology-based screening and provider-collected HPV testing, or VIA) was assessed in low-and middle-income countries (95), which identi ed that HPV test was cost e cient and effective that cytology-based screening. Similar evidence is needed in Ethiopia to identify effective and cost-effective interventions for cervical cancer screening and treatment. It is worrisome that this low and unsatisfactory cervical cancer screening happens despite the high rate of precancerous cervical lesions and cervical cancer in Ethiopia. There have been well-known effective strategies, including technology assisted screening campaign (43), health education at the coffee ceremony (44) and a health education intervention (45), and 'single-visit approach' (46). Implementation of these strategies could be challenged by low-community and provider awareness, lack of infrastructure, lack of screening machine, and high staff turnover in Ethiopia (50). In another lower-income country, Bangladish, there are similar supply-side barriers, for instance, lack of skilled screening providers, lack of advocacy and health promotion, resource constraints, lack of effective leadership (96). These strategies to be implemented and barriers to be solved should be evaluated further for their acceptability and cost-effectiveness.
The review also found that the prevalence of cervical cancer was high in Ethiopia (54,97) compared to many low-income countries (98). Cervical cancer, including precancerous lesions, is high in a country where a higher percentage of women practised multiple sexual intercourse and had a history of sexual transmission diseases (56, 99). Women's diagnosis of cervical cancer is a turning point that requires the women to be linked to cancer clinics or start receiving cancer care. Women face several challenges (e.g., self-image and personality, nancial challenges) in the health care system after being diagnosed with cervical cancer in Ethiopia. Similarly, a systematic review in low-and middle-income countries identi ed that cervical cancer results in nancial insecurity among women and children (100). The impact of cervical cancer on children and families, on employment, education, and household income, needs further study in Ethiopia. Many women are unsatis ed with services, have an impaired quality of life, and face nancial crises; they interrupt treatment and unattended health care. As a result, women with con rmed cervical cancer had a high chance of mortality or a low chance of survival in Ethiopia (72).
As to future research implications, there are several crucial topics that were not examined in the previous research. For example, the extent and effectiveness of community engagement and multisectoral collaboration towards cervical cancer service uptake and outcome improvement. The available evidence did not also provide insight about the acceptability and applicability of interventions which are beyond HPV and screening. There are a few interventional studies on knowledge and service uptake improvement that should be evaluated further to transform the response to cervical cancer towards its elimination. Almost all studies used a quantitative approach, and the participants of these studies were women. It is also crucial getting data from men, key informants, religious leaders, traditional healers, and policy document review.

Strength and Limitation
This scoping review provides a comprehensive assessment of the literature on cervical cancer prevention and outcomes. As scoping reviews do not typically require quality appraisal of article, the authors did not evaluate the quality status of the included studies.

Conclusions And Recommendation
Overall, there is inadequate knowledge, perception, health seeking behaviour, screening and treatment services. This implies that the country is lagging behind the targets towards eliminating cervical cancer. It is therefore crucial that the country identi es the key implementation issues, challenges and strategies to scale up both primary and secondary prevention services so that cervical cancer will not anymore be a public health problem. This requires a whole-of-society and a whole-of-government response based on the primary health care approach.