Cervical cancer screening utilization and predictors among eligible women in Ethiopia: A systematic review and meta-analysis.

BACKGROUND: Despite a remarkable progress in the reduction of global rate of maternal mortality, cervical cancer has been identified as the leading cause of maternal morbidity and mortality, particularly in sub-Saharan African countries. The uptake of cervical cancer screening service has been consistently shown to be effective in reducing the incidence rate and mortality from cervical cancer. Despite this, there are limited studies in Ethiopia that were conducted to assess the uptake of cervical cancer screening and its predictors, and these studies showed inconsistent and inconclusive findings. Therefore, this systematic review and meta-analysis was conducted to estimate the pooled cervical cancer screening utilization and its predictors among eligible women in Ethiopia. METHODS AND
FINDINGS: Databases like PubMed, Web of Science, SCOPUS, CINAHL, Psychinfo, Google Scholar, Science Direct, and the Cochrane Library were systematically searched. All observational studies reporting cervical cancer screening utilization and/ or its predictors in Ethiopia were included. Two authors independently extracted all necessary data using a standardized data extraction format. Quality assessment criteria for prevalence studies were adapted from the Newcastle Ottawa quality assessment scale. The Cochrane Q test statistics and I2 test were used to assess the heterogeneity of studies. A random effects model of analysis was used to estimate the pooled prevalence of cervical cancer screening utilization and factors associated with it with the 95% confidence intervals (CIs). From 850 potentially relevant articles, twenty-five studies with a total of 18,067 eligible women were included in this study. The pooled national cervical cancer screening utilization was 14.79% (95% CI: 11.75, 17.83). The highest utilization of cervical cancer screening (18.59%) was observed in Southern Nations Nationalities and Peoples' region (SNNPR), and lowest was in Amhara region (13.62%). The sub-group analysis showed that the pooled cervical cancer screening was highest among HIV positive women (20.71%). This meta-analysis also showed that absence of women's formal education reduces cervical cancer screening utilization by 67% [POR = 0.33, 95% CI: 0.23, 0.46]. Women who had good knowledge towards cervical screening [POR = 3.01, 95%CI: 2.2.6, 4.00], perceived susceptibility to cervical cancer [POR = 4.9, 95% CI: 3.67, 6.54], severity to cervical cancer [POR = 6.57, 95% CI: 3.99, 10.8] and those with a history of sexually transmitted infections (STIs) [POR = 5.39, 95% CI: 1.41, 20.58] were more likely to utilize cervical cancer screening. Additionally, the major barriers of cervical cancer screening utilization were considering oneself as healthy (48.97%) and lack of information on cervical cancer screening (34.34%).
CONCLUSIONS: This meta-analysis found that the percentage of cervical cancer screening among eligible women was much lower than the WHO recommendations. Only one in every seven women utilized cervical cancer screening in Ethiopia. There were significant variations in the cervical cancer screening based on geographical regions and characteristics of women. Educational status, knowledge towards cervical cancer screening, perceived susceptibility and severity to cervical cancer and history of STIs significantly increased the uptake of screening practice. Therefore, women empowerment, improving knowledge towards cervical cancer screening, enhancing perceived susceptibility and severity to cancer and identifying previous history of women are essential strategies to improve cervical cancer screening practice.

Background

Despite a remarkable progress in the reduction of maternal mortality, cervical cancer is the second most commonly diagnosed cancer and the leading cause of cancer related death among African women [1]. There were approximately 236,000 deaths from cervical cancer worldwide and it was the most common cancer in east and middle Africa [2, 3]. About 90% of cases and 85% of these deaths have occurred in Low and Middle-Income Countries (LMICs); the highest has occurred in Sub-Saharan Africa (SSA) and approximately 311,000 women died from cervical cancer [2]. The incidence, the death rate and morbidities associated with cervical cancer significantly varies across the world; higher in the developing nations compared to the developed countries [4]. The high burden of cervical cancer is mainly due to the early onset of sexual intercourse, multiple sexual partners, human immunodeficiency virus (HIV) infection, history of sexually transmitted infections (STIs), human papilloma virus (HPV) infection, cigarette smoking, limited resources for early detection and poor HPV vaccination coverage [5, 6].

Almost all of the maternal deaths associated with cervical cancer could be prevented if early and effective interventions mechanisms to cervical cancer control were available to all women. In particular, a comprehensive approach such as prevention, early diagnosis, effective screening and treatment programmes of pre-cervical lesions are essential for prevention of cervical cancer [7]. Visual inspection with Acetic Acid (VIA) and Visual Inspection with Lugol’s Iodine (VILI) are commonly used in low-resource settings [6]. VIA combined with the immediate treatment of women who tested positive at the first visit was cost saving and was the next most effective strategy, with a 26% decrease in the incidence of CC, further reduce mortality due to CC. A large-cluster randomized trial from rural India showed that a single round of HPV screening could reduce the incidence and mortality from CC of approximately 50% [8].

The guidelines of the World Health Organization (WHO), the United States Preventive Services Task Force (USPSTF) and the American Cancer Society (ACS) recommends that all eligible women should have cervical cancer screening at least once every three years [9]. Ethiopia adopted WHO’s recommendation that woman aged 30 and above should begin screening for cervical cancer at least one to three years of age with a see- and -treat approach. However, sexually active and HIV-positive women (start screening at HIV diagnosis) are suggested to be screened every 3 years regardless of their age [10]. The prevalence of cervical cancer screening is much higher at the Western countries than SSA [11, 12]; 85.0% in the United States, 78.6% in the United Kingdom [13], and ranges from 2% in Ethiopia, 6% in Kenya [14], to 8% in Nigeria [15]. The lower rate of cervical cancer screening programme at LMICs may be related to the complexity of the screening process and the common inherent barriers in the setting such as poverty, limited access to information, lack of knowledge of cervical cancer, lack of healthcare infrastructure required, lack of trained practitioners and the absence of sustained prevention programmes [16].

The government of Ethiopia launched a cervical cancer screening service and has given more emphasis on programs focusing on the early detection of cervical cancer using advocacy efforts by different stakeholders such as academia, professionals, media and partners. However, the prevalence of cervical cancer remains a major problem, and it is one of the leading causes of morbidity and mortality among women in the country [17, 18]. Evidence show success of cervical screening initiatives depend on high participation of the target population, which in turn is determined by the women’s knowledge, perceptions, health orientations and other socio-cultural issues. It is also affected by factors including early marriage, early sexual practice, delivery of the first baby before the age of 20, multiple sexual partners and low socio economic status. Therefore, addressing the different barriers for poor utilization of cervical cancer screening is essential component of intervention. Although, there were previous pocket studies conducted on these issues in Ethiopia, the studies showed fragmented, inconsistent and inconclusive findings. Even the studies were fragmented in different specific population characteristics like among HIV positive women and reproductive age women. Therefore, this systematic review and meta-analysis aimed to estimate the pooled cervical cancer screening utilization and its predictors among all eligible women in Ethiopia. It also aimed to address the common barriers of cervical cancer screening.

Methods

Registration of systematic review, data sources and search strategies

The purpose of this systematic review and meta-analysis was to estimate the pooled utilization level of cervical cancer screening and its predictors among women of reproductive-aged in Ethiopia. The protocol has been registered with the International Prospective Register of Systematic Review (PROSPERO), the University of York Center for Reviews and Dissemination (https://www.crd.york.ac.uk/), registration number CRD42019119626. The findings of this review have been reported as recommended by the Preferred Reporting Items for Systematic Review and Meta-Analysis (PRISMA-P) 2009 statement checklist [19] (S1 Table). All published articles were searched from major international databases like PubMed, Cochrane Library, Psych Info, Scopus, CINAHL, Web of Science, Science Direct, Google Scholar and African Journals Online. Additionally, Google hand searches were used mainly for unpublished studies. A search was also made for the reference list of studies already identified in order to retrieve additional articles. The Population, Exposure, Comparison and Outcomes (PECO) search formula was used to retrieve articles.

All eligible women for cervical cancer screening Ethiopia were the population of interest for this study. The outcome of interest was the utilization of cervical cancer screening among women. The predictor variables of cervical cancer screening utilization included in this study were age of women, educational status, and occupational status, knowledge of cervical cancer screening, perceived susceptibility and severity to cervical cancer and history of sexually transmitted infections. Comparisons were defined for each predictor based on the reported reference group for each predictor in each respective variable.

For each of the selected components of PECO, electronic databases were searched using the keyword search and the medical subject heading [MeSH] words. The keywords include “utilization, uptake, cervical cancer, screening, and women of reproductive age as well as Ethiopia”. The search terms were combined by the Boolean operators "OR" and "AND. The specific searching detail in PubMed was putted in S1 Appendix.

Eligibility criteria and study selection

This review included studies that reported either the use of cervical cancer screening or the cervical cancer screening predictors in Ethiopia. All published and unpublished studies through April 7, 2020 and reported in English language were retrieved to assess eligibility for inclusion in this review. However, this review excluded studies that were case reports of populations, surveillance data (demographic health survey), and abstracts of conferences, articles without full access and the outcome of interest not reported. The article selection underwent several steps. Two reviewers (MD and TE) evaluated the retrieved articles for inclusion using their title, abstract and full text review. Any disagreement during the selection process between the reviewers was resolved by consensus. Full texts of selected articles were then evaluated using the prior eligibility. During the encounter of duplication; only the full-text article was retained.

Quality assessment and data collection

The Newcastle-Ottawa Scale (NOS) quality assessment tool was used to assess the quality of the included studies. The tool contains three components- selection of the study groups, comparability of the study groups, and ascertainment of exposure or outcome [20]. The main component of the tool was graded from five stars and mainly emphasized on the methodological quality of each primary study. The other component of the tool graded from two stars and mainly concerned with the comparability of each study. The last component of the tool was graded from three stars and was used to evaluate the results and statistical analysis of each original study. The NOS included three categorical criteria with a maximum score of 9 points. The quality of each study was assessed using the following score algorithms: ≥7 points were considered as “good”, 4 to 6 points were considered as “moderate”, and ≤ 3 point was considered as “poor” quality studies. In order to improve the validity of this systematic review result, only primary studies of fair to good quality have been included. The two reviewers (MD and TE) independently assessed articles for overall study quality and extracted data using a standardized data extraction format. The data extraction format included primary author, year of publication, region of the study, sample size, prevalence, and the selected predictors of cervical cancer screening utilization.

Publication bias and statistical analysis

The publication bias was assessed using the Egger’s [21] and Begg’s [22] tests with a p-value of less than 0.05. The I statistic was used to assess heterogeneity between studies and a p-value of less than 0.05 was used to detect heterogeneity. As a result of the presence of heterogeneity, a random-effects model was used as a method of analysis [23]. Data were extracted in Microsoft Excel and exported to Stata version 11 for analysis. Subgroup analysis was conducted by geographic region, population’s characteristics and design or type of study. Moreover, a meta-regression model based on sample size and year of publication was used to identify the sources of random variations in the included studies. The effect of selected determinant variables was analyzed using separate categories of meta-analysis [24]. The findings of the meta-analysis were presented using forest plots and Odds Ratio (OR) with its 95% Confidence intervals (CI). In addition, we conducted a sensitivity analysis to assess whether the pooled prevalence estimates were influenced by individual studies.

Results

Study identification and characteristics of included studies

This systematic review and meta-analysis included both published and unpublished studies on the use of cervical cancer screening in Ethiopia. A total of 850 articles were found from the review. Of these, 250 duplicated records were removed and 581 articles were excluded by screening using their titles and abstracts. Subsequently, a total of 38 full-text papers were assessed for eligibility on the basis of the inclusion and exclusion criteria. Thus, four studies were excluded due to lack of the outcome of interest [25-30], three due to low quality [31-33], five due to difference in the study population [34-39] and only one study was excluded due to lack of access to the full text [40]. Finally, 25 studies were included in the final quantitative meta-analysis (Fig 1).

Fig 1

PRISMA flow diagram of cervical cancer screening utilization in Ethiopia.

All of the included studies were cross-sectional. From this, twelve studies were facility- based cross sectional studies (FBCS) and thirteen were community- based cross-sectional studies (CBCS). The review was conducted among 18,067 women to estimate the pooled prevalence of cervical cancer screening. Publication of articles was between 2016 and 2020. The largest sample size was 5,823 women in a national level study [41] and the smallest sample was 250 women from a study conducted in Oromia region [42]. All studies were conducted in five geographic regions of Ethiopia. Four studies (16%) were from Addis Ababa [43-46], nine (36%) were from Amhara [47-55], four (16%) were from Southern Nations, Nationalities and Peoples Representative (SNNPR) [56-60], four (16%) were from Oromia [42, 61–63], two (8%) were from Tigray [64, 65], and the remaining one study [41] was a national- level study. Twelve studies were conducted among eligible women with no specific characteristics of their HIV status [44, 47], five studies on HIV-positive women [43, 48, 53, 61, 63], four studies among healthcare workers [59, 63, 65, 66] and the remaining one study [51] was conducted among women who were commercial sex workers (Table 1).

Table 1

Characteristics of the included studies in the meta-analysis, Ethiopia.

Author	Year	Region	Prevalence	Design	Sample	Population
Shiferaw H et al. [43]	2018	AA	10.8	FBCS	598	HIV+
Getachew S et al. [44]	2018	AA	25	FBCS	520	All
Bante SA et al. [47]	2019	Amhara	20.9	CBCS	577	All
Aweke YH et al. [56]	2017	SNNPR	9.9	CBCS	583	all
Nega AD et al. [48]	2018	Amhara	10	FBCS	496	HIV+
Nigussie T et al. [49]	2019	Amhara	15.5	CBCS	737	all
Bayu H et al. [64]	2016	Tigray	19.8	CBCS	1186	all
Assefa AA et al. [57]	2019	SNNPR	40.1	FBCS	342	all
Gebreegziabher M et al. [65]	2016	Tigray	10.7	FBCS	225	all
Solomon K et al. [61]	2019	Oromia	25	FBCS	475	HIV+
Tefera and Mitiku [50]	2017	Amhara	11	CBCS	620	All
Muluneh BA et al. [51]	2019	Amhara	13.28	CBCS	467	CSWs
Seyoum T et al. [58]	2017	SNNPR	9.6	FBCS	281	all
Geremew AB et al. [26]	2018	Amhara	no data	1152	98.7
Michael E et al. [42]	Unpub	Oromia	17.6	CBCS	250	all
Galibo T et al. [41]	2017	National	2.9	CBCS	5823	all
Kassa AS et al. [52]	2018	Amhara	7.3	CBCS	735	all
Erku DA et al. [53]	2017	Amhara	23.5	FBCS	302	HIV+
Woldetsadik AB [45]	2020	AA	12.2	FBCS	425	All
Aynalem BY et al. [54]	2020	Amhara	5.4	CBCS	822	All
Asres T [55]	Unpub	Amhara	18	FBCS	322	Healthcare
Dulla D et al. [59]	2017	SNNPR	11.4	FBCS	367	Healthcare
Heyi WD et al. [62]	2018	Oromia	5.8	CBCS	845	All
Berhanu T et al. [66]	2019	AA	9.3	CBCS	291	Healthcare
Tekle T et al. [60]	2020	SNNPR	22.9	CBCS	520	All
Ashagrie A [63]	Unpub	Oromia	16	FBCS	318	HIV+

AA: Addis Ababa; CSWs: Commercial sex workers.

CBCS: community based cross-sectional study; FBCS: facility based cross-sectional study.

Meta-analysis of cervical cancer screening utilization in Ethiopia

The highest cervical cancer screening utilization was observed in SNNPR, a study conducted at ART health facilities of Hawassa, 40% [57] and Wolayita hospitals, 22.9% [60]. Whereas, the lowest was 2.9% in a national level study [41] and 5.4% from a study conducted in Amhara region [54].

The meta-analysis of twenty-five studies showed that the pooled national level of cervical cancer screening utilization was 14.79% (95% CI: 11.75, 17.83). A random-effect model of analysis was used due to significant heterogeneity (I = 97.9%, p-value<0.05) (Fig 2). Publication bias was assessed using Eggers test and it was statistically significant, p-value less than 0.0001. To account for publication bias, the duval and trimmed full analysis was performed. The univariate meta-regression model was also used to identify possible sources of heterogeneity using different covariates like year of publication and sample size. However, none of these variables were found to be statistically significant, p-value > 0.05. Moreover, the sensitivity analysis using a random-effects model showed that no single study had unduly influenced the overall estimate of the use of cervical cancer screening among Ethiopian women (S1 Fig). The funnel plot also showed that there was symmetrical distribution (Fig 3).

Fig 2

The pooled utilization of cervical cancer screening among women in Ethiopia.

Fig 3

Funnel plot of the prevalence of cervical cancer screening utilization in Ethiopia.

Subgroup analysis

The subgroup analysis was conducted based on region of studies, the study design and women’s characteristics. Therefore, this random effect meta-analysis based on the geographic region revealed that the highest cervical cancer screening utilization was observed in the SNNPR, 18.59 (95% CI: 9.65, 27.53) followed by Oromia region, 16.00% (95% CI: 16.00% (95% CI: 6.31, 25.7) and lowest occurred in Amhara region, 13.62% (95% CI: 9.92, 17.32) (Table 2). In addition, the pooled subgroup analysis showed that cervical cancer screening was highest in studies that were institution- based cross-sectional studies, 17.54% (95% CI: 13.16, 21.93). The highest cervical cancer screening was among HIV- positive women, 20.71% (95% CI: 12.8, 28.63) and the lowest was among reproductive age women, 11.54% (95% CI: 8.00, 15.05) (Table 2).

Table 2

Sub-group analysis of cervical cancer screening utilization in Ethiopia: A meta-analysis.

Subgroup type	Category	No of studies	Prevalence(95%CI)	I2	P-value
Study design	FBCS	12	17.54 (13.16,21.93)	94.6%	<0.0001
	CBCS	13	12.29 (8.70,15.88)	98.0%	<0.0001
Region	Addis Ababa	4	14.32 (8.09,20.56)	93.7%	<0.0001
	Amhara	9	13.62 (9.92,17.32)	94.5%	<0.0001
	SNNPR	5	18.59 (9.65,27.53)	97.3%	<0.001
	Oromia	4	16.00 (6.31, 25.7)	97.1%	<0.001
	Tigray	2	15.41 (6.5, 24.32)	93.3%	<0.001
	National level	1	2.9 (2.47,3.33)	-
Women characteristics	HIV positive	5	20.71 (12.8,28.63)	96.6%	<0.0001
	All women	12	11.54 (8.00, 15.05)	97.9%	<0.0001
	Healthcare workers	4	12.21 (8.71,15.71)	72.4%	0.012
	Commercial sex worker	1	13.28 (10.2,16.36)	-	-

Predictors of cervical cancer screening utilization

Association of educational status and utilization of cervical cancer screening

In regard to the social inequities, the effects of three predictors on cervical cancer screening utilization were estimated. Thus, age of women and occupational status were not significantly associated with cervical cancer screening utilization (S2 and S3 Figs). While, women’s educational status was significantly associated with utilization of cervical cancer screening. Accordingly, the pooled random effect of eight studies [48–50, 54, 57, 62, 63, 60] found that women who have no formal education were 66% (POR:0.33, 95% CI: 0.23,0.46) times less likely to utilize cervical cancer screening than those who attended any formal education (Fig 4).

Fig 4

Association of educational status with cervical cancer screening in Ethiopia.

Association of knowledge and perception of cancer and screening utilization

The meta-analysis of 14 studies revealed [42, 45, 49–51, 53, 54, 57, 58, 60, 62–65] that women’s knowledge of cervical cancer screening uptake was the commonest predictor of screening utilization. Women who had good knowledge of cervical cancer screening reuptake were 3.97 times (POR: 3.49, 95% CI: 1.67, 7.33) more likely to have cervical cancer screening than women who had poor knowledge (Fig 5).

Fig 5

Association of knowledge of the screening with cervical cancer screening utilization.

The pooled effect of six studies [33, 42, 45, 49, 53, 64] also revealed that the perceived susceptibility to cervical cancer was another major predictor of cervical cancer screening utilization in Ethiopia. Women who had perceived susceptibility to cervical cancer were 5.5 times more likely to reuptake cervical cancer screening than their counterparts (POR = 5.54, 95% CI: 4.28, 7.16) (Fig 6). Similarly, women who had perceived severity of cervical cancer were more likely to utilize cervical cancer screening (POR = 6.57, 95% CI: 3.99, 10.82) (Fig 7).

Fig 6

Association of perceived susceptibility to cervical cancer with cervical cancer screening.

Fig 7

Association of perceived severity of cancer and cervical cancer screening utilization.

Association of history of sexual transmitted infection and cervical cancer screening uptake

Based on the pooled analysis of four studies [47, 51, 54, 64], women who had history of sexual transmitted infection were more likely to utilize cervical cancer screening (POR: 3.32, 95% CI: 1.07, 10.34) (Fig 8).

Fig 8

Association of history of sexual transmitted infection with cervical cancer screening utilization.

Barriers of cervical cancer screening uptake

The pooled analysis also revealed that the most common reasons that hinder the use of cervical cancer screening were associated with women considered to be healthy, 48.97% (95% CI: 38.3, 59.59) and lack of information on screening, 34.34% (95% CI: (17.93, 50.75) (Table 3).

Table 3

Barriers of the cervical cancer screening utilization in Ethiopia: A meta-analysis.

Barriers	Studies	Prevalence [95% CI]	I2	P-value
Consider as healthy	11	48.97% [38.3, 59.59]	98.7%	<0.0001
Fear of screening	11	15.25% [6.77,23.73]	99.4%	<0.0001
Lack of information	7	34.34% [17.93, 50.75]	99.4%	<0.0001
Embarrassment	8	11.16% [5.76,16.56]	99.3	<0.0001
Long waiting time	7	21.58% [6.87,36.28]	99.6	<0.0001
Don’t know place	5	10.06% [3.53,16.59]	97.0	<0.0001

Discussions

The uptake of cervical cancer screening services in Ethiopia is not well established. Despite, WHO recommends cervical cancer screening tests to be included as part of well-planned and implemented programs in every country’s health care policy. This systematic review and meta-analysis was conducted to estimate the pooled level of cervical cancer screening and its associated factors in Ethiopia. Accordingly, the pooled national level of cervical cancer screening utilization was 14.79 (95% CI: 11.75, 17.83). This was lower than 85% from a study conducted in United States [13], 21.4% in China national population based survey [67], 19.4% in Kenya [68], 19% - 63% from studies conducted in 54 countries [69], 48.9% in Malaysia [70], and also lower than 67% from a national-based study conducted among Vietnamese women [71]. The difference could be explained by the variation in the population characteristics, study settings and quality of health care services and screening programs. Besides, this could be explained by socio-economic inequalities, higher birth order and poor access to reproductive health care service utilization in Ethiopia could lower the cervical screening utilization. Previous report also showed that women with high birth order and poor women are less likely to receive cervical screening service [69]. In Ethiopia, a small proportion of women are in contact with obstetric or gynecological health services and that the health system may not have the capacity to provide effective screening to a larger number of women. Therefore, intervention programs to improve the quality of cervical cancer screening clinics are essential.

The findings of this meta-analysis also showed that the highest prevalence of cervical cancer screening occurred in the SNNPR followed by Oromia region and the lowest was in Amhara region. Regional variation in the burden of cervical cancer screening in Ethiopia might be explained by the difference in maternal health care service utilization that could be explained by in the difference in spousal support, cultural and linguistic diversity across the regions and societal stigmatization. Additionally, health service-related reason like cost of access to services, proximity to facilities, navigation of the facilities, waiting time and attitude of the health care staff may be the reasons for the regional difference and lower use of cervical cancer screening in the country.

The highest screening utilization in SNNPR and Oromia may be due to the nature of included studies in the respective regions. For example, 60% of the studies from SNNP region were institutional based cross-sectional studies and 50% of the included studies from Oromia region were conducted among HIV-positive women. Such differences may have contributed to the higher prevalence of cervical cancer screening in SNNPR and Oromia regions. Furthermore, socio-demographic characteristics and lifestyle activities could also be mentioned as reasons for the variation in screening across the different regions in the country. The pooled cervical cancer screening was also highest among HIV- positive women (20.71%). This may be due to the fact that these women may be given information about the disease during their follow-up visit to antiretroviral therapy [57], which may improve their knowledge about cervical cancer, and therefore, increase service utilization.

This systematic review and meta-analysis found that educational status of women was one of the significant predictors of cervical cancer screening utilization. No formal education reduces the cervical cancer screening uptake by 67%, and this finding was supported by a study done in China [67] and a meta-analysis conducted in developed countries [72]. The possible justification for this might be due to the fact that women who have no formal education are less likely to have gynecological examinations and maternal health service utilization. As the result, they are likely to have limited exposure to visit health institution for antenatal care, health facility delivery and post-natal care.

Uneducated women also have lower possibilities to read and fully understand the information and instructions provided by healthcare providers, and therefore, reduce the rate of cervical cancer screening. Cervical cancer educational interventions and provider recommendation for screening increases the rates of cervical cancer screening [73]. Therefore, more integrated interventions to improve women’s empowerment should be done at national level to improve the rate of cervical cancer screening utilization, and therefore, reduce cervical cancer related morbidity and mortality.

This study also found that women’s knowledge of screening for cervical cancer was a significant predictor of cervical cancer screening service uptake. The finding was supported by studies done in Uganda [74], Malaysia [70], a review done in LMICs [75] and among Arab women [76]. This could be explained by the fact that those women who had good knowledge for cervical cancer screening are more likely to give priority to the issue and improves their decisions on health- seeking screening behavior. Accordingly, findings in Ethiopia, Malawi, Tanzania and Thailand [64, 77–79] have shown that a good flow of information and awareness creation campaigns about cervical cancer increase the uptake of cervical cancer screening.

This meta-analysis also showed that women with a history of STI were more likely to use screening for cervical cancer compared to those with no history of STI. This result was supported by the findings of other studies [64, 80]. This may be explained by the fact that women who have STIs and history of STI will have an increased chance of visiting health institutions for treatment and medical check-ups, and therefore, more likely to get the screening information from the healthcare provider.

This systematic review and meta-analysis also found that perceived susceptibility and severity were also predictors of the use of cervical cancer screening as supported by Wanyenze et al. [74]. This may be those who perceive their susceptibility or severity of cancer may be aware of the severity of the cancer and higher level of education about the disease as a result of the increased screening rate. As a result, those women who have an increased perception of susceptibility or severity of the disease may have higher education that has increased adherence to the cervical cancer screening [68]. These may include those women who are perceived to be more acutely aware of their risk, more interested and knowledgeable about health and behavioral issues, and better access to health information and resources [81]. This finding was also supported by recent studies done in Ghana [82] and Kenya [83] which found that women who perceived the severity of disease were more likely to accept screening due to increased perception of the benefits and barriers to cervical cancer, which increases their cancer screening.

Furthermore, the results of this systematic review and meta-analysis found that the common barriers to the utilization of cervical cancer screening were considered healthy and lack of information by women. This is supported by additional studies [47, 49, 51, 56, 64]. This may be due to the fact that those who consider their status to be healthy and who have poor knowledge are less likely to perceive the benefits of screening and the severity of cervical cancer., Therefore, multi-disciplinary interventions across the life course, community education and social mobilization on cervical cancer risk and its screening should be improved and emphasized to increase the cervical cancer screening utilization.

This review’s strengths include the very extensive systematic search conducted and the inclusion of articles identified without specifying the population characteristics and period of publications. Our review adopted the international standard definitions to measure the quality of studies. This meta-analysis has its strengths because it has used a pre-specified protocol for search strategy and data abstraction and used internationally accepted tools for a critical appraisal system for the quality assessment of individual studies.

However, the results of this review should be interpreted with some limitation. The high heterogeneity in the characteristics of the studies might lead to insufficient statistical power to detect significant association. However, a meta-regression analysis revealed that there was no variation due to sample size and publication year. This meta-analysis was also unable to assess the type of screening, and therefore, an area of research for future studies. Additionally, the studies included in this review were from only five regions out of the nine regional states and the two administrative cities that might reduce its representativeness for the country. Some studies have small sample size, affect the estimation.

Conclusions

This meta-analysis found that cervical cancer screening rate was lower than the WHO recommendations. Only one in every seven eligible women were screened in Ethiopia, and there was a significant variation in the screening level based on geographical regions and characteristics of women. Women’s educational status, knowledge towards cervical cancer screening, perceived susceptibility and severity to cervical cancer and history of sexual transmitted infections significantly increased uptake of the screening practice. Therefore, women empowerment, improving knowledge towards cervical cancer screening, enhancing perceived susceptibility and severity to cervical cancer and identifying previous history of women are an essential strategy to increase utilization of cancer screening. Moreover, adoption of the better strategies and addressing the barriers of cervical cancer screening uptake mainly improving of the provision of adequate information on cervical cancer screening has a paramount importance to improve cervical cancer screening among reproductive age women.

Sensitivity analysis of cervical cancer screening utilization.

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Association of women’s age and cervical cancer screening utilization.

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Association of occupational status and cervical cancer screening utilization.

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PRISMA check list.

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Included studies for the barriers of cervical cancer screening.

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Quality assessment of included studies.

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Specific searching on PubMed database.

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16 Dec 2020

PONE-D-20-22948

Cervical cancer screening utilization and predictors among reproductive-age women in Ethiopia: a systematic review and meta-analysis

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The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

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2. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

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Reviewer #1: Yes

Reviewer #2: Yes

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Reviewer #1: Yes

Reviewer #2: Yes

**********

5. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: General comment: Very good and useful review that could provide evidence on barrier to CC screening in Ethiopia

Specific comments

IN the abstract as well as under background section, it is stated “Despite a remarkable progress in the reduction of maternal mortality, cervical cancer is the 73 second most commonly diagnosed cancer and the leading cause of cancer related death among 74 African women”. I agree with the reduction of MM. However, in view of the fact that CC is a major public health challenge and with its continued pressure, is it not naïve to argue about reduction of maternal mortality without showing how CC screening has contributed to that or contrary to this maintained MM in consequence higher.

Mention is made “The incidence, death rate and morbidities associated with cervical cancer is 79 significantly varies across the world; higher in the developing nations than compared to the 80 developed countries”(4), while again it is stated “The prevalence of cervical cancer screening is much higher at the Western countries than SSA” (11, 12); The two statements looks contradictory

Method

There is no clarity on whether this review is ‘systematic’ or ‘met-analysis’ or ‘both’. If it is both, it is imperative to clarify which part of it is systematic and meta-analysis OR clarify why both were considered.

From the statement “All published and unpublished studies through April 7, 2020” there were quite few concerns. Firstly what was the lower time frame. Could it be any document from time immemorial to April 7, 2020? Secondly, how were the unpublished reports captured? Were there any criterion set to identify those?

While WHO’s recommended age of CC screening is 30-50, it is not clear why in this study age 18-49 years was chosen? Is it not contradictory?

Results

The studies were drawn from five geographic regions: Addis Ababa, Amhara, Southern Nations, Nationalities and Peoples, Oromia and Tigray with only one from the national- level study. Couple of concern here. Firstly, how was the 18,067 women considered to estimate the pooled… proportionated in light of population size. Given the fact that studies are not proportional to the population of the regions, it would be difficult to reach conclusion as desired – this is about comparability of results. Secondly, I am wondering if this study could mirror realities for the country at large. Perhaps clarifying those and stating limitations may help.

I am not convinced that what are stated as ‘most common reasons that hinder the use of cervical cancer screening’ in the result section and conclusion section are aligned. This needs to be checked against the finding and corrected

Discussion

The fact that it was not clear on what of this review is meta and systematic, the discussion suffers much missing what is being discussed. Perhaps with clarification on how the two contributed to this review may

Reviewer #2: Generally a good paper, congratulations, however, the work needs some grammatic revision for clarity. I have listed some below but kindly revise the entire paper checking for grammatic and punctuation errors.

Line 74- Update the reference and use more recent data than 2013

Line 77- Be consistent in presenting figures i.e 311000 should have a comma as with other figures

Line 78- Correct the grammar of the sentence which start as "The incidence, death ......"

Line 85-6- Correct the grammar of the sentence

Line 97-98- Correct grammar

Line 99-100- Correct grammar

Line 103- Correct the punctuation

Line 292-295- Sentence needs revision for clarity, attend to the grammar

Line 295-298- Sentence needs some revision for clarity

Line 307 - Clarify what "tall reproductive age" refers, sentence may need some revisions

Line 309- Add reference of relevant papers to support your interpretation

Line 367- Replace "representative" with representativeness

**********

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Reviewer #1: Yes: Mirgissa Kaba

Reviewer #2: Yes: Dr. Oscar Tapera

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Submitted filename: CC meta-systematic analysis-Review comment.docx

Click here for additional data file.

8 Apr 2021

Dear editors and reviewer of Plos One

We would like to extend our deepest appreciation for devoting your time to review our manuscript entitled “cervical cancer screening utilization and predictors among eligible women in Ethiopia: a systematic review and meta- analysis”. Cervical cancer is the second most commonly diagnosed cancer and the leading cause of cancer death in African women. In 2013, there were approximately 236,000 deaths from cervical cancer worldwide and it is the most common cancer in east and middle Africa. Cervical cancer screening is an important intervention to redcue cervical cancer and its associated maternal mortality. Even though, the utilization of the screening is inconsistent across the country and affected by different barrier. Therefore, this systematic review and meta-analysis estimates the pooled utilization of cervical cancer screening and its predictors in Ethiopia. Overall the main finding of this review is means of an intervention based on the pooled cervical cancer screening utilization and its predictors, which might be used to improve maternal adverse outcomes in Low and middle income countries, subsequently means of achieving SDGs.

Dear reviewer, there has been a major revision of the whole structure of the manuscript (Abstract, introduction, methods, results, discussion and conclusions) mainly with a correction of grammar errors. The further details regarding the choice of age range as well as outlining the limitations of the study and it's generalizability for the study areas are addressed. The reproductive group is substituted by eligible women as the global and who recommendations. We hope now the manuscript is clear and more acceptable than its previous version. We tried to state the limitations and generalizability issues in the limitation and strength section of the discussion. We have tried to present the response for each reviewer according to your comment what to suppose to do so. For this, here we have given our responses to each of the concerns you raised, highlighted by red color. Again, we would like to remind our strongest gratitude for your effort for the improvement of this manuscript and the response for each the points were addressed in the response to reviewers’ section. For this, I kindly request you to consider the paper for publication. Again, we would like to remind our strongest gratitude for your effort for the improvement of this manuscript.

Regards

Reviewer #1

1. Abstract

1.1. In the abstract as well as under background section, it is stated “Despite a remarkable progress in the reduction of maternal mortality, cervical cancer is the 73 second most commonly diagnosed cancer and the leading cause of cancer related death among 74 African women”. I agree with the reduction of MM. However, in view of the fact that CC is a major public health challenge and with its continued pressure, is it not naïve to argue about reduction of maternal mortality without showing how CC screening has contributed to that or contrary to this maintained MM in consequence higher.

Response: thank you for the highly valuable scholarly comments and suggestions. Revision was made on the abstract and background section stating that maternal mortality reduction achieved with cervical cancer screening.

1.2. Mention is made “The incidence, death rate and morbidities associated with cervical cancer is significantly varies across the world; higher in the developing nations than compared to the 80 developed countries”. While again it is stated “The prevalence of cervical cancer screening is much higher at the Western countries than SSA” (11, 12); the two statements looks contradictory.

Response: Thank you for the comments, but, the two statements is non-contradictory. Hence, the incidence, death rate and morbidities associated with cervical cancer is significantly varies across the world, which is higher in developing countries like SSA. This is explained due to high prevalence and severity of the problem among in low income countries and the fact that it is the only gynaecologic cancer which can be prevented and treated through early screening and follow-up, and the cervical cancer screening practice in low income countries is significantly low. Therefore, the two statements support each other.

#2. Method

2.1. There is no clarity on whether this review is ‘systematic’ or ‘met-analysis’ or ‘both’. If it is both, it is imperative to clarify which part of it is systematic and meta-analysis OR clarify why both were considered.

Response: Thank you for the valuable comments. We used the PRISMA diagram or recommendations of the systematic review and meta-analysis including the report of this study like the search strategy and the overall written was based on the recommendations. The meta-analysis commands and software were used based on the meta-analysis Cochrane handbooks. The meta-analysis was done to get the pooled estimate using Stata 14 using a meta-analysis written command. To do a good review and meta-analysis it should be searched systematically and other quality measures should be addressed what we have tried.

2.2. From the statement “All published and unpublished studies through April 7, 2020” there were quite few concerns. Firstly what was the lower time frame? Could it be any document from time immemorial to April 7, 2020? Secondly, how were the unpublished reports captured? Was there any criterion set to identify those?

Response: accepted and specific lower time frame was putted (2016) and the criteria used to identify unpublished articles were those fully access during manual search, found in university repositories and those studies fulfilling quality score to be included in this study.

2.3. While WHO’s recommended age of CC screening is 30-50, it is not clear why in this study age 18-49 years was chosen? Is it not contradictory?

Response: Thank you for the highly valuable comments. I completely agree what you supposed to do so and revision was made throughout the manuscript. The reproductive age group is not representative for all the all age eligible women for cervical cancer screening for the population charactertics we included. The recommendation was for the general population Evidence show success of cervical screening initiatives depend on high participation of the target population, which in turn is determined by the women’s knowledge, perceptions, health orientations and other socio-cultural issues. It is also affected by factors including early marriage, early sexual practice, delivery of the first baby before the age of 20, too many or too frequent childbirths, multiple sexual partners and low socio economic status. Women with early sexual practice, multiple partners, having HIV AIDS and sexual transmitted disease should have more screening schedule.

According to world health organization (WHO) guideline, every sexually active woman aged 30–49 years should undergo cervical cancer screening at least every 5 years. However, sexually active and HIV-positive women are suggested to be screened every 3 years regardless of their age. HIV positive women Ethiopia adopted the WHO recommendation in 2015 and recommended HIV positive women to start screening at HIV diagnosis, regardless of age once the woman is sexually exposed. In this meta-analysis age all age eligible women or from different population charactertics for cervical cancer screening such as women from 30-50 years old, HIV positive women, healthcare workers, and commercial sex workers were included. Thus, eligible women are better than reproductive age and we have accepted your comment.

#3. Results

3.1. The studies were drawn from five geographic regions: Addis Ababa, Amhara, Southern Nations, Nationalities and Peoples, Oromia and Tigray with only one from the national- level study. Couple of concern here. Firstly, how was the 18,067 women considered to estimate the pooled… proportionated in light of population size. Given the fact that studies are not proportional to the population of the regions, it would be difficult to reach conclusion as desired – this is about comparability of results. Secondly, I am wondering if this study could mirror realities for the country at large. Perhaps clarifying those and stating limitations may help.

Response: accepted and revision was made. The limitations were stated in regard to the less representativeness of five studies out of nine regions in Ethiopia in our meta-analysis.

3.2. I am not convinced that what are stated as ‘most common reasons that hinder the use of cervical cancer screening’ in the result section and conclusion section are aligned. This needs to be checked against the finding and corrected

Response: thank you for the comments suggest being.

We have checked it and the barriers in the result section and conclusion section are aligned

#4. Discussion

4.1. The fact that it was not clear on what of this review is Meta and systematic, the discussion suffers much missing what is being discussed. Perhaps with clarification on how the two contributed to this review may help refine the discussion section.

Response: Highly valuable comment, I completely agree what you supposed and revision was made. In the last two paragraphs of the discussion section narrates about the meta-analysis and systematic review mainly the strength and weakness.

Reviewer #2

1. Generally a good paper, congratulations, however, the work needs some grammatical revision for clarity. I have listed some below but kindly revise the entire paper checking for grammatical and punctuation errors.

Response: Thank you for your scholarly comments.

The major grammatical errors were revised and seen by sinor experts.

2. Line 74- update the reference and use more recent data than 2013

Response: Accepted and data published in 2016 by WHO and Bruni et al 2017 was cited.

3. Line 77- Be consistent in presenting figures i.e. 311000 should have a comma as with other figures

4. Response: accepted and revision was made. Comma as with other figures is putted.

5. Line 78- Correct the grammar of the sentence which starts as "The incidence, death ......"

Response: accepted and the grammar error was revised.

6. Line 85-6- Correct the grammar of the sentence, Line 97-98- Correct grammar, Line 99-100- Correct grammar, Line 103- Correct the punctuation, Line 292-295- Sentence needs revision for clarity, attend to the grammar, Line 295-298- Sentence needs some revision for clarity.

Response: all grammar and punctuation errors was corrected

7. Line 307 - Clarify what "tall reproductive age" refers, sentence may need some revisions

Response: valuable comment and revised. The editing "tall reproductive age" is an error, we want to instead want to spell as all reproductive age and revision was made. Fortunately, hence, it was not clear for reader we remove from the document.

8. Line 309- Add reference of relevant papers to support your interpretation

Response: reference number 73 was cited.

9. Line 367- Replace "representative" with representativeness

10. Response: representative" was replaced by with representativeness.

Submitted filename: Point by Point reponse .docx

Click here for additional data file.

19 Oct 2021

Cervical cancer screening utilization and predictors among eligible women in Ethiopia: a systematic review and meta-analysis

PONE-D-20-22948R1

Dear Mr Desta,

We’re pleased to inform you that your manuscript has been judged scientifically suitable for publication and will be formally accepted for publication once it meets all outstanding technical requirements.

Within one week, you’ll receive an e-mail detailing the required amendments. When these have been addressed, you’ll receive a formal acceptance letter and your manuscript will be scheduled for publication.

An invoice for payment will follow shortly after the formal acceptance. To ensure an efficient process, please log into Editorial Manager at http://www.editorialmanager.com/pone/, click the 'Update My Information' link at the top of the page, and double check that your user information is up-to-date. If you have any billing related questions, please contact our Author Billing department directly at authorbilling@plos.org.

If your institution or institutions have a press office, please notify them about your upcoming paper to help maximize its impact. If they’ll be preparing press materials, please inform our press team as soon as possible -- no later than 48 hours after receiving the formal acceptance. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information, please contact onepress@plos.org.

Kind regards,

Gizachew Tessema, PhD

Academic Editor

PLOS ONE

Additional Editor Comments.

I would suggest to shorten the description related to key words and search terms. Instead put the details search terms and key words presented in lines 158-172 in a supplementary appendix. Revise the statement in the methods section of the abstract. Indicate that databases were searched for peer-review articles whereas Google scholar was used to search grey literature

Reviewers' comments:

Reviewer's Responses to Questions

Comments to the Author

1. If the authors have adequately addressed your comments raised in a previous round of review and you feel that this manuscript is now acceptable for publication, you may indicate that here to bypass the “Comments to the Author” section, enter your conflict of interest statement in the “Confidential to Editor” section, and submit your "Accept" recommendation.

Reviewer #1: All comments have been addressed

Reviewer #2: (No Response)

**********

2. Is the manuscript technically sound, and do the data support the conclusions?

The manuscript must describe a technically sound piece of scientific research with data that supports the conclusions. Experiments must have been conducted rigorously, with appropriate controls, replication, and sample sizes. The conclusions must be drawn appropriately based on the data presented.

Reviewer #1: Yes

Reviewer #2: Yes

**********

3. Has the statistical analysis been performed appropriately and rigorously?

Reviewer #1: Yes

Reviewer #2: Yes

**********

4. Have the authors made all data underlying the findings in their manuscript fully available?

The PLOS Data policy requires authors to make all data underlying the findings described in their manuscript fully available without restriction, with rare exception (please refer to the Data Availability Statement in the manuscript PDF file). The data should be provided as part of the manuscript or its supporting information, or deposited to a public repository. For example, in addition to summary statistics, the data points behind means, medians and variance measures should be available. If there are restrictions on publicly sharing data—e.g. participant privacy or use of data from a third party—those must be specified.

Reviewer #1: (No Response)

Reviewer #2: Yes

**********

5. Is the manuscript presented in an intelligible fashion and written in standard English?

PLOS ONE does not copyedit accepted manuscripts, so the language in submitted articles must be clear, correct, and unambiguous. Any typographical or grammatical errors should be corrected at revision, so please note any specific errors here.

Reviewer #1: Yes

Reviewer #2: Yes

**********

6. Review Comments to the Author

Please use the space provided to explain your answers to the questions above. You may also include additional comments for the author, including concerns about dual publication, research ethics, or publication ethics. (Please upload your review as an attachment if it exceeds 20,000 characters)

Reviewer #1: Authors revised the manuscript following the comments. They considered the comments useful which helped them to refine the manuscript

Reviewer #2: Great paper that contribute to knowledge in LMICs. Please see a few comments below:

-Some grammar and punctuation corrections are needful throughout the paper to aid clarity

-Line 74 Use more recent data e.g GLOBOCAN 2020

-Line 77 Be consistent in presentation of figures use the format 311,000

**********

7. PLOS authors have the option to publish the peer review history of their article (what does this mean?). If published, this will include your full peer review and any attached files.

If you choose “no”, your identity will remain anonymous but your review may still be made public.

Do you want your identity to be public for this peer review? For information about this choice, including consent withdrawal, please see our Privacy Policy.

Reviewer #1: Yes: Mirgissa Kaba, School of Public Health, Addis Ababa University

Reviewer #2: Yes: Oscar Tapera

26 Oct 2021

PONE-D-20-22948R1

Cervical cancer screening utilization and predictors among eligible women in Ethiopia: a systematic review and meta-analysis

Dear Dr. Desta:

I'm pleased to inform you that your manuscript has been deemed suitable for publication in PLOS ONE. Congratulations! Your manuscript is now with our production department.

If your institution or institutions have a press office, please let them know about your upcoming paper now to help maximize its impact. If they'll be preparing press materials, please inform our press team within the next 48 hours. Your manuscript will remain under strict press embargo until 2 pm Eastern Time on the date of publication. For more information please contact onepress@plos.org.

If we can help with anything else, please email us at plosone@plos.org.

Thank you for submitting your work to PLOS ONE and supporting open access.

Kind regards,

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on behalf of

Dr. Gizachew Tessema

Academic Editor

PLOS ONE