https://orcid.org/0000-0003-1505-9390
Figures
Abstract
Introduction
Cervical cancer is a major public health problem, particularly in resource-limited settings. The use of vaccination and screening tests has reduced the burden of cervical cancer in developed countries. However, the situation is quite the reverse in developing countries, including Ethiopia. Hence, this study aimed to estimate the pooled impact of knowledge and attitude on the prevalence of cervical cancer screening service utilization rates among Ethiopian women.
Methods
Studies that examined cervical cancer screening service utilization among women in Ethiopia were searched from five international databases. Cochran’s Q chi-square and the I-squared test statistics were used to check the presence of heterogeneity among the included studies. The funnel plot and Egger’s regression tests were also used to assess the presence of publication bias. A weighted DerSimonian and Laird random-effects model was employed. Subgroup analysis was performed by the study population concerning the prevalence of cervical cancer screening service utilization rates. Sensitivity analysis was also conducted to assess the effect of a single study on the pooled estimates. Data analysis was performed using STATA™ Version 14 software.
Results
A total of 44 studies with 28,186 study participants were included. The estimated pooled prevalence of cervical cancer screening service utilization was 8.11% (95% CI: 7.26, 8.97). After adjustment for publication bias with the trim and fill analysis, the estimated prevalence rate appeared to be 5.47% (95% CI: 4.66, 6.28). The prevalence of cervical cancer screening service utilization was higher among HIV-positive women, 16.85%, and in studies conducted among health care workers, 10.24%, than the general population. The pooled effect of knowledge on the utilization of cervical cancer screening tests among Ethiopian women was statistically significant (AOR = 3.20, 95% CI: 1.63, 6.31). Similarly, the pooled estimated odds of utilizing cervical cancer screening tests were 6.1 times higher (AOR = 6.09, 95% CI: 1.09, 34.36) among women who had a favorable attitude towards the screening tests.
Conclusion
Knowledge and attitude had a significant impact on the prevalence of cervical cancer screening test utilization rates among women in Ethiopia. However, the prevalence of cervical cancer screening service utilization among Ethiopian women is very low. Hence, large-scale awareness programs and situation-based strategies need to be designed to increase the uptake of cervical cancer screening services in the country.
Citation: Kassie AM, Abate BB, Kassaw MW, Aragie TG, Geleta BA, Shiferaw WS (2020) Impact of knowledge and attitude on the utilization rate of cervical cancer screening tests among Ethiopian women: A systematic review and meta-analysis. PLoS ONE 15(12): e0239927. https://doi.org/10.1371/journal.pone.0239927
Editor: Jonah Musa, University of Jos, NIGERIA
Received: May 11, 2020; Accepted: September 15, 2020; Published: December 8, 2020
Copyright: © 2020 Kassie et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the article and its supporting information files.
Funding: The author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: AOR, Adjusted Odds Ratio; CI, Confidence Interval; HPV, Human Papilloma Virus; JBI, Joanna Briggs Institute; SNNPR, Southern Nations, Nationalities, and Peoples Region; PRISMA, Preferred Reporting Items for Systematic Reviews and Meta-Analyses
Introduction
Globally, the incidence and mortality rates of cervical cancer have increased with 0.6 and 0.46% estimated annual rates respectively in the past 3 decades [1, 2]. The new cases of cervical cancer more often occur in all age groups of women in developing countries than in developed countries [2, 3].
Cervical cancer is the most common type of cancer and the leading cause of cancer-related deaths in women in several low and middle human development index countries [4]. Africa is hardly affected by the disease [3]. This is a source of great concern because cervical cancer is preventable and curable using the currently available methods [5, 6].
The onset of the HIV/AIDS epidemic that is highest in the region has also raised the problem of cervical cancer to a serious level [6]. In 2018, cervical cancer was the leading cause of cancer-related mortality among women in the southern, western, middle, and eastern Africa regions [7].
Cervical cancer costs the world billions of dollars [8, 9]. Cervical cancer-related costs are estimated at $407.2 per patient for outpatient services in Ethiopia and the mean inpatient cost for hospitalized patients is estimated to be $404.4 [10]. This is very huge and unimaginable for many to get treatment given the socioeconomic status of the community [10, 11].
Human papillomavirus (HPV) which is a sexually transmitted infection-causing organism is the main cause for cervical cancer [12, 13]. Currently, highly effective vaccines are available against HPV infection [14–16]. However, early detection through screening and treatment of pre-cancerous lesions remains the best possible protection against cervical cancer in resource-limited settings [17].
Human papilloma virus-based screening coupled with immediate treatment with cryotherapy has reduced both cervical cancer precursors and cervical cancer cases in many countries though HPV-based screening has been indicated to be more effective than cytology for the detection of cervical cancer precursors and prevention of cervical cancer [18].
Nevertheless, the rate of cervical cancer screening tests is reported to be low across literatures in many low and middle-income countries [19–21]. It is indicated that on average, cervical cancer screening rate is three times higher in high-income countries (63%) than in low and middle-income countries (19%) [22].
The Ethiopian cervical cancer prevention and control guidelines recommend every woman starting from the age of 30 to be screened every five years unless HIV-positive and if there is an indication starting from the age of 25 years. If a woman is HIV positive, it recommends starting screening at HIV diagnosis, regardless of age once the woman is sexually exposed [23].
In line with global guidelines, the Ethiopian cervical cancer prevention and control guidelines recommend the human papillomavirus test and cytological tests such as the use of visual inspection of the cervix with acetic acid and Pap smear tests to be used for screening depending on their availability in the health care systems nearby to the woman [23, 24].
However, the uptake of cervical cancer screening tests is unsatisfactory in Ethiopia. A study has indicated that based on the World Health Organization (WHO) non-communicable steps survey conducted in Ethiopia in 2015, the rate of cervical cancer screening tests was extremely low (2.9%) [25].
The low uptake rate of cervical cancer screening tests in many low- and middle-income countries is thought to be related to multiple barriers, including the lack of awareness and knowledge about the risk factors and the prevention methods of cervical cancer and the women's unwillingness to be tested [26].
Therefore, knowing the impact of knowledge and attitude on the utilization rate of cervical cancer screening tests is paramount in designing effective strategies. However, primary studies on the utilization rate of cervical cancer screening tests and the associated barriers in Ethiopia are inconsistent. Hence, this systematic review and meta-analysis aimed to determine the impact of knowledge and attitude on the prevalence of cervical cancer screening service utilization rates among Ethiopian women.
Methods
Literature search strategy
The Cochrane Library, Joanna Briggs Institute (JBI), and PROSPERO databases were searched to check whether a systematic review and meta-analysis studies exist or for the presence of ongoing project works related to the utilization of cervical cancer screening tests and the associated barriers in Ethiopia. The relevant articles were searched using PubMed, Scopus, Google Scholar, and African journals online.
For this study, relevant articles were identified using the following terms: “Cervical cancer screening”, “utilization”, “uptake”, “practice”, “factors”, “barriers” and “Ethiopia”. The key terms were used in combination using Boolean operators of “OR” or “AND”. The searches were restricted to full texts, free articles, English language publications, and human studies. This search involved articles published from January 1st, 2010 to April 10th, 2020.
Gray literature, such as surveillance reports, academic dissertations, and conference proceeding abstracts, were also examined and included when they deemed low risk. In addition, the reference lists of included articles in this systematic review and meta-analysis were used for hand searching to identify any relevant additional articles.
Article screening for eligibility and selection for inclusion
Studies were included in this systematic review and meta-analysis if they followed the following guidelines: (1) all observational study designs (cross-sectional, case-control, and cohort studies) that reported the utilization rate of cervical cancer screening tests and the associated barriers; (2 published from 2010 to 2020; (3) published in the English language; (4) abstract and, or full text available for this review; and (5) conducted in Ethiopia. Unpublished works were also considered and included when low risk was deemed. Studies were excluded if they (1) possessed a poor quality score as per the stated criteria and (2) failed to determine the desired outcomes (utilization of cervical cancer screening services and its association with knowledge and attitude of women). Furthermore, citations without abstracts and/or full texts, anonymous reports, editorials, and qualitative studies were excluded from the analysis.
Outcomes of interest
The main outcomes of interest were the utilization rate of cervical cancer screening services and its association with the knowledge and attitude of women. The outcome variables of interest were operationally defined as follows for the study participants of the included studies in the systematic review and meta-analysis.
Cervical cancer screening service utilization.
A woman who has been screened for the detection of any possible abnormal cells in the cervix in their lifetime. In this study, screening refers to the use of a human papillomavirus test, and/or the use of visual inspection of the cervix with acetic acid [27, 28] and, or the use of a Pap smear test [28].
Knowledge.
Studies were included for knowledge analysis if participants’ knowledge of cervical cancer and/or about cervical cancer screening tests were reported with outcomes categorized as good and poor or other analogous binary classifications. For studies that have presented the knowledge of participants in sections, the knowledge category that covers questions about cervical cancer screening was considered. For studies that used more than 2 categories to describe the participant’s knowledge of cervical cancer and screening services, the 2 categories of good and poor were selected and included in this study. That means we selected the lowest and compared it to the highest in terms of the likelihood of attending screening tests.
Data extraction
The authors have developed a data extraction platform on the Excel sheet that consists of the name of authors, year of study, year of publication, study design, study setting, participant type, sample size, prevalence rate of cervical cancer screening service utilization, participants’ knowledge and attitude towards cervical cancer and screening tests. The data extraction sheet was piloted using 6 papers randomly. Then, the extraction form was adjusted after having the piloted template. Two of the authors independently extracted all the necessary data from each article using the data extraction sheet. The third author checked the correctness of the data independently. Any disagreements between authors who extracted the data were resolved through discussions with the third reviewer and fourth reviewer when required. For articles that did not provide details of their study background, corresponding authors were contacted through e-mail and asked for relevant information, such as study time, region, or others.
Quality assessment
Two independent authors assessed the methodological quality of all of the potential studies to be included in the analysis. Any failure to reach an agreement between the authors on whether to include or exclude studies was resolved through discussion or, if consensus could not be reached, consultation with a third independent author was considered. The quality of each included study was assessed using the JBI quality appraisal checklist for case-control and cross-sectional studies because the articles included in this study were case-control and cross-sectional in design [29].
The JBI quality appraisal checklist has several key criteria to appraise case-control studies, including [1] group comparability other than the presence of disease in the cases or the absence of disease in the controls [2], matching appropriateness of cases and controls [3], similarity of criteria used for identification of cases and controls [4], exposure measurement in a standard, valid and reliable way [5], similarity of exposure measurement for cases and controls [6], identification of confounding factors [7], clarity of strategies to deal with confounding factors [8], outcome assessment in a standard, valid and reliable way for cases and controls [9], meaningfulness of period of exposure and [10] appropriateness of statistical methods used.
The items in the checklist used to appraise cross-sectional studies were [1] clarity of inclusion criteria definitions [2], extent of study participant and setting description [3], valid and reliable exposure measurement [4], presence of clear objective, and use of standard criteria for measurement of the condition of interest [5], identification of confounding factors [6], clarity of strategies to handle confounding factors [7], valid and reliable way of outcome measurement and [8] appropriateness of statistical methods used [29]. Studies were considered low risk when scored 50% and above of the JBI quality assessment indicators.
Statistical analysis
To obtain the pooled estimated impact of knowledge and attitude on the prevalence of cervical cancer screening service utilization rates among Ethiopian women, a meta-analysis using the random-effects model was performed due to the presence of heterogeneity [30].
Cochran’s Q chi-square statistic and the I2 tests were run to assess the random variations between primary studies [31]. In this study, heterogeneity was interpreted as an I2 value of 0% = no heterogeneity, 25%-50% = low, 50%-75% = moderate, and ≥ 75% = high [31]. In the case of high heterogeneity, subgroup and sensitivity analyses were run to identify possible moderators for the heterogeneity.
Potential publication bias was assessed by visually inspecting funnel plots and objectively using Egger’s bias test [32]. The trim and fill analysis was performed to assess for any publication bias based on the assumption that the effect sizes of all the studies are normally distributed around the center of a funnel plot in the absence of publication bias. The meta-analysis was performed using STATA™ Version 14 software [33]. Finally, for all analyses, a p-value of less than 0.05 was considered to declare statistically significant values.
Presentation and reporting of results
The results of this systematic review and meta-analysis were reported based on the Preferred Reporting Items for Systematic Review and Meta-Analysis statement (PRISMA) guidelines [34]. The entire process of study screening, selection, and inclusion are shown with the support of a flow diagram. Moreover, tables and narrative summaries are used to report the risk of bias for every eligible study.
Results
Search results
In the first step of article searches, 1,548 studies that were published from 2010–2020 were retrieved from four international databases. Fifteen studies (n = 15) were retrieved through manual searches from grey literature. Of the 1,563 retrieved studies, 327 duplicate records were identified, and after duplication removal, a total of 1,236 articles remained for screening. Then, 1,184 studies were excluded after reading their title and abstracts because either these studies were not conducted in Ethiopia or they were not in line with the objective of this systematic review and meta-analysis. Finally, 52 studies were screened for full-text review, and 44 studies with 28,186 study participants were included. The remaining 8 articles were excluded because they failed to report the outcomes of interest (prevalence of cervical cancer screening tests or impact of knowledge and attitude on the utilization rate of cervical cancer screening tests). The detailed steps in the screening process are shown in the PRISMA flow chart below (Fig 1).
Baseline characteristics of the included studies
In this systematic review and meta-analysis, a total of 44 studies with 28,186 study participants were included to estimate the pooled impact of knowledge and attitude on the prevalence of cervical cancer screening service utilization rates among Ethiopian women.
Among the included studies, 42 had reported the prevalence of cervical cancer screening service utilization, 24 had reported the level of association between participants’ knowledge and cervical cancer screening service utilization, and 12 studies had also reported the effect of attitude on the utilization rate of cervical cancer screening services.
Concerning the study design, 42 of the studies included were cross-sectional, and the remaining 2 were case-control in design. The studies included in this systematic review and meta-analysis varied substantially in sample size, ranging from 202 to 5,823.
Overall information regarding the prevalence of cervical cancer screening service utilization was obtained from various regions of the country. Ten of the studies involved participants from the Amhara region [35–44], eleven from the Oromia region [45–55], nine from the SNNPR [56–64], four from Tigrai [65–68], eight from Addis Ababa [69–76], one study involving participants from the Amhara, SNNPR and Afar regions [77], and another study involving participants countrywide [25]. Regarding sampling, all of the studies used the probability sampling technique (Table 1).
The pooled estimate of cervical cancer screening service utilization in Ethiopia
The prevalence of cervical cancer screening service utilization reported in the included studies ranges from 0% [53] to 40.1% [56]. For the study with zero prevalence, a continuity correction formula that is 0.5 was considered [53].
The possible reason for the zero prevalence might be due to differences in the setting because the study conducted by Tilahun T. et al. was conducted among university students who are usually young aged [53]. Therefore, the result might be due to the age of participants because screening is recommended in Ethiopia starting from the age of 30 years unless there is another clear indication [23].
In this meta-analysis, the random-effects model revealed that the estimated pooled prevalence of cervical cancer screening service utilization in Ethiopia was 8.11% (95% CI: 7.26, 8.97). There was a significant level of heterogeneity among the included studies (I2 = 97.8%; p ≤ 0.001) (Fig 2).
Subgroup analysis
Subgroup analysis was performed through stratification using the study population to identify the sources of heterogeneity for the pooled prevalence of cervical cancer screening service utilization rate in Ethiopia.
In the subgroup analysis, the prevalence of cervical cancer screening service utilization was found to be 16.85% in studies conducted among HIV-positive women, 10.24% in studies conducted among health care workers, 8.42% in the general population of women, and 3.73% in studies conducted among college or university students (Fig 3).
Sensitivity analysis
To evaluate the effect of individual studies on the pooled prevalence of cervical cancer screening service utilization in Ethiopia, a sensitivity analysis was performed using the random-effects model. The results from the sensitivity analysis revealed that a study conducted by Gelibo T. et al. influenced the pooled estimated prevalence of cervical cancer screening service utilization rates among Ethiopian women. The exclusion of the Gelibo et al. study increased the overall rate from 8.11% (7.26, 8.97) to 9.66 (8.40, 10.92). This might be due to the large number of participants included in the Gelibo T. et al. study because unlike the other studies, the Gelibo T. et al. study was conducted on 5,823 study participants and involved participants from the entire country [25] (Fig 4).
Publication bias test
There was a publication bias among the studies included to estimate the pooled prevalence of cervical cancer screening service utilization among Ethiopian women, as illustrated by the asymmetrical distribution of funnel plot tests (S1 Fig). Similarly, the result of Egger’s tests for the funnel plot was statistically significant for the presence of publication bias (P ≤ 0.001).
Trim and fill analysis
A trim and fill analysis was performed to estimate the number of missing studies that might exist, thereby reducing and adjusting publication bias in the included studies. After adjustment for publication bias, the estimated pooled prevalence of cervical cancer screening service utilization among Ethiopian women was 5.47 (95% CI: 4.66, 6.28), with a very low level of heterogeneity among the studies (I2 = 4.31%; p ≤ 0.001) (Fig 5).
The effect of knowledge on utilization of cervical cancer screening services
According to this meta-analysis, the pooled estimated effect of knowledge on the utilization of cervical cancer screening services in Ethiopian women was statistically significant. The odds of utilizing cervical cancer screening tests were 3.2 times higher among women who had good knowledge regarding cervical cancer and its screening tests than those who had poor knowledge (AOR = 3.20, 95% CI: 1.63, 6.31, I 2 = 90.5% with p ≤ 0.001) (Fig 6).
Egger’s regression test also showed that there was no publication bias for the studies included to estimate the pooled effect of knowledge on cervical cancer screening service utilization among women (P = 0.062).
The effect of attitude on the utilization of cervical cancer screening services
Ethiopian women with a favorable attitude towards the utilization of cervical cancer screening tests were 6.1 times more likely than those with poor attitudes to have a test (AOR = 6.09, 95% CI: 1.09, 34.36, I2 = 97.4%, p ≤ 0.001). However, a very high odds ratio of 46.49 was observed under the Andargie A, et al. study row. This could be due to the difference in the reporting of odds ratios in the original studies. Unlike other studies that have reported adjusted odds ratios, the study conducted by Andargie A et al. did not report the adjusted odds ratio on the effect of attitude [44]. As a result, the crude odds ratio was used in the case of Andargie A et al.’s study (Fig 7).
In the publication bias assessment, Egger’s regression test indicated that there was no publication bias for the studies included to estimate the pooled effect of attitude on cervical cancer screening service utilization (P = 0.776).
Discussion
The World Health Organization recommends cervical cancer screening tests to be included as part of well-planned and implemented screening programs in every country's health care policy [78]. However, the uptake of cervical cancer screening services in Ethiopia is not well established. Hence, this systematic review and meta-analysis were conducted to estimate the pooled effect of knowledge and attitude on the prevalence of cervical cancer screening service utilization rates among Ethiopian women.
In this study, the estimated pooled prevalence of cervical cancer screening service utilization among Ethiopian women was 8.1%. However, after adjustment with the trim and fill analysis for publication bias, the estimated pooled prevalence of cervical cancer screening service utilization rate appeared to be 5.5%. This finding is higher than a previously estimated rate of screening in Ethiopia, which is 0.8 [79]. It is also higher than another study conducted based on the population-based WHO Steps survey that the utilization rate of cervical cancer screening services in Ethiopia was found to be 2.9% [25]. This suggests that the uptake of cervical cancer screening rates is increasing in Ethiopia though still too low. A consistent finding has been reported in Nigeria (8.0%) [80].
However, the result is lower than a finding from European countries that the coverage of cervical cancer screening tests ranges from 10% to 79% [81]. Consistent with the European report, a study in Minnesota, United States of America, showed that 60.8% of women had received Pap-HPV co-test screening with a significant increment among women aged 30–65 years, from 10.0% in 2007 to 60.8% in 2016 [82]. It is also lower than other findings across the literature: Kenya, 16.4% [83], India, 29.8% [84], South Africa, 52% [85], and China, 20.7% [86].
These discrepancies might be due to differences in the developmental level of the countries. Unlike developed countries, the availability of cervical cancer screening programs is limited in developing countries [87, 88]. In addition, cervical cancer screening services are opportunity-based in many low- and middle-income countries [19]. This can be justified by the lack of adequate infrastructure and the availability of many other public health problems that need prioritization [89]. It might also be due to differences in the educational level and the knowledge of women in these countries because education is one of the major tools and has an immense contribution to increasing the uptake of cervical cancer screening tests [90, 91].
In the subgroup analysis, the prevalence of cervical cancer screening service utilization was higher among HIV-positive women (16.85%) and in studies conducted among health care workers (10.24%) than in the general population. This could be due to differences in the knowledge of participants. It is obvious that health care workers will have better knowledge and information on cervical cancer screening services. In addition, people with HIV are not only closer to healthcare-related information but also at a higher risk of cervical cancer and might obtain better opportunities and recommendations from their health care providers [92]. Furthermore, the Ethiopian cervical cancer prevention and control guidelines recommend that if a woman is HIV positive, screening should be started at HIV diagnosis regardless of age once the woman is sexually exposed [23].
A consistent finding has been reported that in South Africa, 25.3% of the women who attended a health care facility were screened for cervical cancer [93]. Similarly, higher screening rates were seen in a more educated woman (25.2%) in the Kenyan study [83]. The possible reason could be that people who attend health care facilities have a higher chance of getting information from their health care workers and other sources. Likewise, women who have higher educational levels might obtain information from different sources and might have a better understanding of the benefits of using cervical cancer screening tests [90, 91, 94].
The pooled odds of being screened among women who have better knowledge about cervical cancer and its screening services was 3.2 times higher than those who have poor knowledge. Similarly, Ethiopian women who had a favorable attitude towards the utilization of cervical cancer screening tests were 6.1 times more likely to have a test than those with poor attitude. This is encouraging. However, various studies in different parts of Ethiopia have shown that the majority of women not only have insufficient knowledge about cervical cancer screening tests but many of them also do not have information about the disease itself [64, 95, 96]. This suggests that awareness programs need to be implemented strategically on a regular basis.
Strength and limitations
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.
As a limitation, it is difficult to determine if the results from various regions are representative of the entire country because the majority of the data were found from four (Oromia, Amhara, SNNPR, Tigray) of the 9 regions and the country's capital city Addis Ababa. Only one study was found involving participants from all regions of the country.
Furthermore, all the included studies in this systematic review and meta-analysis were either institution-based or were conducted in urban settings. Hence, the results of this study may not represent rural women in Ethiopia.
Conclusion
Knowledge and attitude had a significant impact on the prevalence of cervical cancer screening test utilization rates among Ethiopian women. However, the prevalence of cervical cancer screening service utilization among Ethiopian women is very low. Hence, large-scale awareness creation programs and situation-based strategies need to be designed to increase the uptake of cervical cancer screening services in the country. Furthermore, addressing women living in rural areas is highly recommended, as no sufficient evidence has been found on their involvement in screening programs.
Supporting information
S1 Fig. Funnel plot test for publication bias in cervical cancer screening service utilization.
https://doi.org/10.1371/journal.pone.0239927.s001
(DOCX)
References
- 1. Luciani S, Cabanes A, Prieto-Lara E, Gawryszewski V. Cervical and female breast cancers in the Americas: current situation and opportunities for action. Bulletin of the world health organization. 2013;91:640–9. pmid:24101780
- 2. Forouzanfar MH, Foreman KJ, Delossantos AM, Lozano R, Lopez AD, Murray CJ, et al. Breast and cervical cancer in 187 countries between 1980 and 2010: a systematic analysis. The lancet. 2011;378(9801):1461–84. pmid:21924486
- 3. Torre LA, Bray F, Siegel RL, Ferlay J, Lortet‐Tieulent J, Jemal A. Global cancer statistics, 2012. CA: a cancer journal for clinicians. 2015;65(2):87–108. pmid:25651787
- 4. Bray F, Jemal A, Grey N, Ferlay J, Forman D. Global cancer transitions according to the Human Development Index (2008–2030): a population-based study. The lancet oncology. 2012;13(8):790–801. pmid:22658655
- 5. Tota J, Ramana–Kumar A, El-Khatib Z, Franco E. The road ahead for cervical cancer prevention and control. Current oncology. 2014;21(2):e255. pmid:24764711
- 6. Louie KS, De Sanjose S, Mayaud P. Epidemiology and prevention of human papillomavirus and cervical cancer in sub‐Saharan Africa: a comprehensive review. Tropical Medicine & International Health. 2009;14(10):1287–302. pmid:19772550
- 7. Arbyn M, Weiderpass E, Bruni L, de Sanjosé S, Saraiya M, Ferlay J, et al. Estimates of incidence and mortality of cervical cancer in 2018: a worldwide analysis. The Lancet Global Health. 2020;8(2):e191–e203. pmid:31812369
- 8. Subramanian S, Trogdon J, Ekwueme DU, Gardner JG, Whitmire JT, Rao C. Cost of cervical cancer treatment: implications for providing coverage to low-income women under the Medicaid expansion for cancer care. Women's Health Issues. 2010;20(6):400–5. pmid:21050999
- 9. Campos NG, Sharma M, Clark A, Lee K, Geng F, Regan C, et al. The health and economic impact of scaling cervical cancer prevention in 50 low‐and lower‐middle‐income countries. International Journal of Gynecology & Obstetrics. 2017;138:47–56. pmid:28691334
- 10. Hailu A, Mariam DH. Patient side cost and its predictors for cervical cancer in Ethiopia: a cross-sectional hospital-based study. BMC cancer. 2013;13(1):69. pmid:23391288
- 11.
Messay H. The Right to Social Security of Public Servants in Ethiopia: Assessing The Challenges and Prospects: Addis Ababa University; 2019.
- 12. Denny L. Cervical cancer: prevention and treatment. Discovery medicine. 2012;14(75):125–31. pmid:22935209
- 13. Sankaranarayanan R, Nessa A, Esmy PO, Dangou JM. Visual inspection methods for cervical cancer prevention. Best practice & research Clinical obstetrics & gynecology. 2012;26(2):221–32. pmid:22075441
- 14. Steben M, Tan Thompson M, Rodier C, Mallette N, Racovitan V, DeAngelis F, et al. A Review of the Impact and Effectiveness of the Quadrivalent Human Papillomavirus Vaccine: 10 Years of Clinical Experience in Canada. Journal of obstetrics and gynecology Canada: JOGC. 2018;40(12):1635–45. pmid:30341021
- 15. Drolet M, Bénard É, Pérez N, Brisson M. Population-level impact and herd effects following the introduction of human papillomavirus vaccination programs: updated systematic review and meta-analysis. Lancet. 2019;394(10197):497–509. pmid:31255301
- 16. Ng SS, Hutubessy R, Chaiyakunapruk N. Systematic review of cost-effectiveness studies of human papillomavirus (HPV) vaccination: 9-Valent vaccine, gender-neutral, and multiple age cohort vaccination. Vaccine. 2018;36(19):2529–44. pmid:29625764
- 17. Dillner J. Primary human papillomavirus testing in organized cervical screening. Current Opinion in Obstetrics and Gynecology. 2013;25(1):11–6. pmid:23299089
- 18. Chrysostomou AC, Stylianou DC, Constantinidou A, Kostrikis LG. Cervical Cancer Screening Programs in Europe: The Transition Towards HPV Vaccination and Population-Based HPV Testing. Viruses. 2018;10(12):729. pmid:30572620
- 19. Sancho-Garnier H, Khazraji YC, Cherif MH, Mahnane A, Hsairi M, El Shalakamy A, et al. Overview of cervical cancer screening practices in the extended Middle East and North Africa countries. Vaccine. 2013;31 Suppl 6:G51–7. pmid:24331820
- 20. Ebu N, Sylvia C. Mupepi S, Mate-Siakwa P, Sampselle C. Knowledge, practice, and barriers toward cervical cancer screening in Elmina, Southern Ghana. Int J Women's Health. 2015;7:31–39 https://doi.org/10.2147/IJWH.S71797.
- 21. Al Eyd GJ, Shaik RB. Rate of opportunistic pap smear screening and patterns of epithelial cell abnormalities in pap smears in Ajman, United Arab emirates. Sultan Qaboos Univ Med J. 2012;12(4):473–8. pmid:23275844
- 22. Gakidou E, Nordhagen S, Obermeyer Z. Coverage of cervical cancer screening in 57 countries: low average levels and large inequalities. PLoS medicine. 2008;5(6). pmid:18563963
- 23.
The Federal Democratic Republic of Ethiopia, Ministry of Health. Guideline for Cervical Cancer Prevention and Control in Ethiopia, January 2015. Available at: https://www.iccp-portal.org/system/files/plans/Guideline%20Eth%20Final.pdf.
- 24.
Organization WH. WHO guidelines for screening and treatment of precancerous lesions for cervical cancer prevention: World Health Organization; 2013.
- 25. Gelibo T, Roets L, Getachew T, Bekele A. Coverage and factors associated with cervical cancer screening: results from a population-based WHO steps Study in Ethiopia. Journal of Oncology Research and Treatment. 2017;2(1):1–5.
- 26. Chidyaonga-Maseko F, Chirwa ML, Muula AS. Underutilization of cervical cancer prevention services in low and middle-income countries: a review of contributing factors. Pan Afr Med J. 2015;21:231. pmid:26523173
- 27. Poli UR, Bidinger PD, Gowrishankar S. Visual Inspection with Acetic Acid (VIA) Screening Program: 7 Years Experience in Early Detection of Cervical Cancer and Pre-Cancers in Rural South India. Indian J Community Med. 2015;40(3):203–7. pmid:26170547
- 28.
WHO Guidelines Approved by the Guidelines Review Committee. WHO Guidelines for Screening and Treatment of Precancerous Lesions for Cervical Cancer Prevention. Geneva: World Health Organization Copyright © World Health Organization 2013.; 2013.
- 29. Institute JB, Institute JB. Critical appraisal tools. The University of Adelaide See: joannabriggs org/research/criticalappraisal-tools html (accessed 20 January 2017). 2017.
- 30. Huedo-Medina TB, Sánchez-Meca J, Marín-Martínez F, Botella J. Assessing heterogeneity in meta-analysis: Q statistic or I2 index? Psychological methods. 2006;11(2):193. pmid:16784338
- 31. Higgins J, Green S. Assessing risk of bias in included studies. Cochrane Handbook for Systematic Reviews of Interventions Version 5.1. 0; 2011. 2008.
- 32.
Egger M, Davey-Smith G, Altman D. Systematic reviews in health care: meta-analysis in context: John Wiley & Sons; 2008.
- 33.
StataCorp L. Stata statistical software (version release 14). College Station, TX: Author. 2015.
- 34. Moher D, Liberati A, Tetzlaff J, Altman DG. Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Annals of internal medicine. 2009;151(4):264–9. pmid:19622511
- 35.
Abebe Dires Nega et.al. Self-Perceived Risk of Cervical Cancer and Associated Factors among HIV Positive Women Attending Adult HIV/AIDS Care and Follow Up Clinic in Gondar University Referral Hospital, Northwest Ethiopia, 2016.
- 36. Kasa AS, Tesfaye TD, Temesgen WA. Knowledge, attitude, and practice towards cervical cancer among women in Finote Selam city administration, West Gojjam Zone, Amhara Region, North West Ethiopia, 2017. African health sciences. 2018;18(3):623–36. pmid:30602995
- 37. Muluneh BA, Atnafu DD, Wassie B. Predictors of cervical cancer screening service utilization among commercial sex workers in Northwest Ethiopia: a case-control study. BMC women's health. 2019;19(1):162. pmid:31842845
- 38. Aynalem BY, Anteneh KT, Enyew MM. Utilization of cervical cancer screening and associated factors among women in Debremarkos town, Amhara region, Northwest Ethiopia: Community based cross-sectional study. PloS one. 2020;15(4):e0231307. pmid:32255807
- 39. Erku DA, Netere AK, Mersha AG, Abebe SA, Mekuria AB, Belachew SA. Comprehensive knowledge and uptake of cervical cancer screening is low among women living with HIV/AIDS in Northwest Ethiopia. Gynecologic oncology research and practice. 2017;4(1):20. pmid:29276611
- 40. Tefera F, Mitiku I. Uptake of cervical cancer screening and associated factors among 15–49-year-old women in Dessie town, Northeast Ethiopia. Journal of Cancer Education. 2017;32(4):901–7. pmid:27075197
- 41. Geremew AB, Gelagay AA, Azale T. Uptake of pre cervical cancer screening service and associated factors among women aged 30–49 years in Finote Selam town Northwest Ethiopia. International Journal of Collaborative Research on Internal Medicine & Public Health. 2018;10(2):0-.
- 42. Bante SA, Getie SA, Getu AA, Mulatu K, Fenta SL. Uptake of pre-cervical cancer screening and associated factors among reproductive-age women in Debre Markos town, Northwest Ethiopia, 2017. BMC public health. 2019;19(1):1102. pmid:31412831
- 43. Getahun T, Kaba M, Derseh BT. Intention to Screen for Cervical Cancer in Debre Berhan Town, Amhara Regional State, Ethiopia: Application of Theory of Planned Behavior. Journal of cancer epidemiology. 2020;2020. pmid:32256590
- 44. Andargie A, Reddy P. Knowledge, attitude, practice, and associated factors of cervical cancer screening among women in Dessie referral hospital and Dessie health center, Northeast Ethiopia. Glob J Res Anal. 2016;4.
- 45. Boka Abdisa and Nigatu Dessalegn. "Cervical cancer screening and associated factors among women attending gynecology outpatient department and maternal and child health at Mettu Karl referral hospital, South West, Ethiopia, 2019" International Journal of Current Research in Life Sciences, 8, (01), 2934–2944.
- 46.
Ashagrie A. Knowledge and screening practice on cervical cancer and associated factors among HIV positive women in Adama, Ethiopia: Addis Ababa University; 2017. https://doi.org/10.1186/s13104-017-2887-z pmid:29110731
- 47. Bulto G, Demmissie D, Daka K. Knowledge about Cervical Cancer, Screening Practices, and Associated Factors among Women Living with HIV in Public Hospitals of West Shoa Zone, Central Ethiopia. J Women's Health Care. 2019;8.
- 48.
Michael E. Cervical cancer screening utilization and its associated factors among women aged 30 years and above in Woliso town, South West Showa Zone, Oromia region, Ethiopia: Addis Ababa Universty; 2018.
- 49. Haile EL. Evaluation of cervical cancer screening uptake and risk factors knowledge: HEALTH BELIEFSMODEL (HBM). GSJ. 2018;6(12).
- 50. Solomon K, Tamire M, Kaba M. Predictors of cervical cancer screening practice among HIV positive women attending adult anti-retroviral treatment clinics in Bishoftu town, Ethiopia: the application of a health belief model. BMC Cancer. 2019;19(1):989. pmid:31646975
- 51. Nigussie T, Admassu B, Nigussie A. Cervical cancer screening service utilization and associated factors among age-eligible women in Jimma town using the health belief model, South West Ethiopia. BMC women's health. 2019;19(1):127. pmid:31660938
- 52. Kassa R, Gurmessa T, Lemma T, Abebe W. Cervical Cancer, and Screening Method: Knowledge, Attitude, and Practice among Women Living in Adama Town. J Women's Health Care. 2019;8(458):2167–0420.1000458.
- 53. Tilahun T, Tulu T, Dechasa W. Knowledge, attitude, and practice of cervical cancer screening and associated factors amongst female students at Wollega University, western Ethiopia. BMC research notes. 2019;12(1):518. pmid:31426860
- 54. Heyi WD, Bekabil TT, Ebo GG. Knowledge, attitude, and practice of cervical cancer screening among women aged 15–49 years in Bishoftu town, east Shewa zone, Oromia region, Ethiopia, 2016. Ethiopian Journal of Reproductive Health. 2018;10(2):10–.
- 55.
Tadesse A. Knowledge, attitude, and practice (KAP) towards screening for cervical cancer among Adama University female students, Adama, Ethiopia, 2014: Addis Abeba University; 2015.
- 56. Assefa AA, Astawesegn FH, Eshetu B. Cervical cancer screening service utilization and associated factors among HIV positive women attending adult ART clinic in public health facilities, Hawassa town, Ethiopia: a cross-sectional study. BMC health services research. 2019;19(1):847. pmid:31744548
- 57. Dulla D, Daka D, Wakgari N. Knowledge about cervical cancer screening and its practice among female health care workers in southern Ethiopia: a cross-sectional study. International journal of women's health. 2017;9:365. pmid:28579837
- 58. Abamecha F, Tena A, Kiros G. Psychographic predictors of intention to use cervical cancer screening services among women attending maternal and child health services in Southern Ethiopia: the theory of planned behavior (TPB) perspective. BMC public health. 2019;19(1):434. pmid:31023306
- 59. Deresse M, Yosef K, Aebra B. Study on Knowledge, Attitude and Practice towards Cervical Cancer and Screening among Women in Butajira Town: A Cross-Sectional Study.
- 60. Tekle T, Wolka E, Nega B, Kumma WP, Koyira MM. Knowledge, Attitude and Practice Towards Cervical Cancer Screening Among Women and Associated Factors in Hospitals of Wolaita Zone, Southern Ethiopia. Cancer management and research. 2020;12:993. pmid:32104081
- 61. Seyoum T, Yesuf A, Kejela G, Gebremeskel F. Utilization of cervical cancer screening and associated factors among female health Workers in Governmental Health Institution of Arba Minch town and Zuria District, Gamo Gofa zone, Arba Minch, Ethiopia, 2016. Arch Cancer Res. 2017;5(4):165.
- 62. Gebru Z, Gerbaba M, Dirar A. Utilization of cervical carcinoma screening service and associated factors among currently married women in Arba Minch town, southern Ethiopia. J Women’s Health Care. 2016;5(297):2167–0420.1000297.
- 63. Mulatu K, Motma A, Seid M, Tadesse M. Assessment of knowledge, attitude, and practice on cervical cancer screening among female students of Mizan Tepi University, Ethiopia, 2016. Cancer Biol Ther Oncol. 2017;1(1):1–5.
- 64. Aweke YH, Ayanto SY, Ersado TL. Knowledge, attitude, and practice for cervical cancer prevention and control among women of childbearing age in Hossana Town, Hadiya zone, Southern Ethiopia: Community-based cross-sectional study. PLoS One. 2017;12(7).
- 65. Gebregziabher D, Berhanie E, Birhanu T, Tesfamariam K. Correlates of cervical cancer screening uptake among female undergraduate students of Aksum University, College of Health Sciences, Tigray, Ethiopia. BMC research notes. 2019;12(1):520. pmid:31426848
- 66. Gebreegziabher M, Asefa NG, Berhe S. Factors affecting the practices of cervical cancer screening among female nurses at public health institutions in Mekelle town, Northern Ethiopia, 2014: a cross-sectional study. Journal of Cancer Research. 2016;2016.
- 67. Bayu H, Berhe Y, Mulat A, Alemu A. Cervical cancer screening service uptake and associated factors among age-eligible women in Mekelle zone, northern Ethiopia, 2015: A community-based study using the health belief model. PloS one. 2016;11(3):e0149908. pmid:26963098
- 68. Teame H, Gebremariam L, Kahsay T, Berhe K, Gebreheat G, Gebremariam G. Factors affecting utilization of cervical cancer screening services among women attending public hospitals in Tigray region, Ethiopia, 2018; Case-control study. PloS one. 2019;14(3). pmid:30870497
- 69. Woldetsadik AB, Amhare AF, Bitew ST, Pei L, Lei J, Han J. Socio-demographic characteristics and associated factors influencing cervical cancer screening among women attending St. Paul's Teaching and Referral Hospital, Ethiopia. BMC women's health. 2020;20:1–9. pmid:31898500
- 70. Gamshe EN, Demissie DB. Assessment of Risky Sexual Behavior, Pap Smear Uptake, and Predictors of Pap Smear Uptake among Female Students in Addis Ababa University College Health Science, Ethiopia. EC Gynaecology. 2019;8:540–53.
- 71.
Eyerusalem G. Knowledge Attitude and Practice on Cervical Cancer and Screening among Reproductive health Service Clients. Addis Ababa, Ethiopia: Ethiopia Addis Ababa University. 2015.
- 72.
Abdulkadir IR. Level of knowledge toward human papillomavirus/cervical cancer & practice of Papanicolaou test screening among female Addis Ababa university students in Ethiopia: California State University, Northridge; 2013.
- 73. Abebaw T, Emru K, Abaerei A. Role of awareness on cervical cancer screening uptake among HIV positive women in Addis Ababa, Ethiopia. A cross-sectional study. 2019.
- 74. Belete N, Tsige Y, Mellie H. Willingness and acceptability of cervical cancer screening among women living with HIV/AIDS in Addis Ababa, Ethiopia: a cross-sectional study. Gynecologic oncology research and practice. 2015;2(1):6.
- 75. Shiferaw S, Addissie A, Gizaw M, Hirpa S, Ayele W, Getachew S, et al. Knowledge about cervical cancer and barriers toward cervical cancer screening among HIV‐positive women attending public health centers in Addis Ababa city, Ethiopia. Cancer medicine. 2018;7(3):903–12. pmid:29441700
- 76. Berhanu T, Mamo E, Tewolde T, Beshir M. Knowledge of Cervical Cancer and Its Screening Practice among Health Extension Workers in Addis Ababa, Ethiopia. Primary Health Care: Open Access. 2019;9(1):1–5.
- 77. Chaka B, Sayed A-R, Goeieman B, Rayne S. A survey of knowledge and attitudes relating to cervical and breast cancer among women in Ethiopia. BMC public health. 2018;18(1):1072. pmid:30157813
- 78.
Organization WH, Zdrowia ŚO, Control PoC, Health WHOR. Cervical cancer screening in developing countries: report of a WHO consultation: World Health Organization; 2002.
- 79.
ICO/IARC Information Centre on HPV and Cancer; Human Papillomavirus and Related Cancers in Ethiopia, Fact Sheet 2018. Available at: https://hpvcentre.net/statistics/reports/ETH_FS.pdf.
- 80. Idowu A, Olowookere SA, Fagbemi AT, Ogunlaja OA. Determinants of cervical cancer screening uptake among women in Ilorin, North Central Nigeria: a community-based study. Journal of cancer epidemiology. 2016;2016. pmid:26880916
- 81. Anttila A, von Karsa L, Aasmaa A, Fender M, Patnick J, Rebolj M, et al. Cervical cancer screening policies and coverage in Europe. European Journal of Cancer. 2009;45(15):2649–58. pmid:19699081
- 82. MacLaughlin KL, Jacobson RM, Radecki Breitkopf C, Wilson PM, Jacobson DJ, Fan C, et al. Trends over time in Pap and Pap-HPV Co-testing for cervical cancer screening. Journal of Women's Health. 2019;28(2):244–9. pmid:30614380
- 83. Nyangasi M, Nkonge NG, Gathitu E, Kibachio J, Gichangi P, Wamai RG, et al. Predictors of cervical cancer screening among Kenyan women: results of a nested case-control study in a nationally representative survey. BMC public health. 2018;18(3):1221.
- 84. Assam M, Nagaland S. Establishing Baseline Cervical Cancer Screening Coverage—India, 2015–2016.
- 85. Phaswana-Mafuya N, Peltzer K. Breast and cervical cancer screening prevalence and associated factors among women in the South African general population. Asian Pacific journal of cancer prevention: APJCP. 2018;19(6):1465. pmid:29936716
- 86.
ICO/IARC Information Centre on HPV and Cancer, Human Papillomavirus, and Related Cancers in China, Fact Sheet 2018. Available at: https://hpvcentre.net/statistics/reports/CHN_FS.pdf.
- 87. Pimple S, Mishra G, Shastri S. Global strategies for cervical cancer prevention. Current Opinion in Obstetrics and Gynecology. 2016;28(1):4–10. pmid:26642063
- 88. Olson B, Gribble B, Dias J, Curryer C, Vo K, Kowal P, et al. Cervical cancer screening programs and guidelines in low-and middle-income countries. International Journal of Gynecology & Obstetrics. 2016;134(3):239–46.
- 89. Catarino R, Petignat P, Dongui G, Vassilakos P. Cervical cancer screening in developing countries at a crossroad: Emerging technologies and policy choices. World journal of clinical oncology. 2015;6(6):281. pmid:26677441
- 90. Agide FD, Garmaroudi G, Sadeghi R, Shakibazadeh E, Yaseri M, Koricha ZB, et al. A systematic review of the effectiveness of health education interventions to increase cervical cancer screening uptake. European journal of public health. 2018;28(6):1156–62. pmid:30346504
- 91. Staff PO. Correction: Effect of cervical cancer education and provider recommendation for screening on screening rates: A systematic review and meta-analysis. Plos One. 2017;12(12):e0190661. pmid:29287125
- 92. Roman L, Meghea C, Ford S, Penner L, Hamade H, Estes T, et al. Individual, provider, and system risk factors for breast and cervical cancer screening among underserved Black, Latina, and Arab women. Journal of Women's Health. 2014;23(1):57–64. pmid:24283674
- 93. Akinyemiju TF, McDonald JA, Lantz PM. Health care access dimensions and cervical cancer screening in South Africa: analysis of the world health survey. BMC Public Health. 2015;15(1):382. pmid:25886513
- 94. Abiodun OA, Olu-Abiodun OO, Sotunsa JO, Oluwole FA. Impact of a health education intervention on knowledge and perception of cervical cancer and cervical screening uptake among adult women in rural communities in Nigeria. BMC public health. 2014;14(1):814. pmid:25103189
- 95. Mengesha A, Messele A, Beletew B. Knowledge and attitude towards cervical cancer among reproductive age group women in Gondar town, North West Ethiopia. BMC Public Health. 2020;20(1):209. pmid:32046681
- 96. Getahun F, Mazengia F, Abuhay M, Birhanu Z. Comprehensive knowledge about cervical cancer is low among women in Northwest Ethiopia. BMC Cancer. 2013;13:2. pmid:23282173