https://orcid.org/0000-0002-9174-7120
Figures
Abstract
Background and aims
Globally, cervical cancer is the fourth most common cancer among women, and more than 90% of all cervical cancer-related deaths worldwide are recorded in resource-limited countries. The present review investigated the uptake rate of cervical cancer screening and identified the factors associated with screening service utilisation in the female populations of least developed countries (LDCs).
Methods
Five electronic databases (EMBASE, Ovid MEDLINE, CINAHL, Cochrane Library, and PubMed) and grey literature were searched for relevant literature using the keywords of the included studies. Both qualitative and quantitative studies were included. Three reviewers performed critical appraisals using the Mixed Methods Appraisal Tool. Meta-analysis was performed to pool the quantitative results from comparable studies.
Results
A total of twenty-five studies were included in the review. The cervical cancer screening uptake rate in LDCs ranged from 4% to 21%. Multiple factors were associated with screening service utilisation among women in the LDCs, namely socio-demographic characteristics, including employment status (odds ratio (OR): 2.72; 95% CI: 1.97–3.76; p < 0.001); knowledge of cervical cancer and its screening (OR: 3.39; 95% CI: 2.00–5.75; p < 0.001); sexual and reproductive health-related factors such as parity status (OR: 2.73; 95% CI: 1.61–4.64; p = 0.002); healthcare providers’ recommendations (OR: 5.32; 95% CI: 2.44–11.58; p < 0.001); perceived risk of developing cervical cancer (OR: 3.76; 95% CI: 2.62–5.38; p < 0.001); use of media for cervical cancer screening promotion, including radio; cultural factors; and myths and misconceptions about cervical cancer and its screening.
Conclusions
The uptake of cervical cancer screening among eligible women in the LDCs was notably low. The governments of these countries are advised to invest and allocate additional resources to advance policies and develop cervical cancer prevention programmes that are accessible, affordable, and acceptable.
Citation: Rana T, Chan DNS, Law BMH, Choi KC, Shrestha S, So WKW (2025) Determinants of cervical cancer screening utilisation among women in the least developed countries: A systematic review and meta-analysis. PLoS One 20(6): e0321627. https://doi.org/10.1371/journal.pone.0321627
Editor: Emmanuel Kokori, University of Ilorin, NIGERIA
Received: August 28, 2024; Accepted: March 10, 2025; Published: June 24, 2025
Copyright: © 2025 Rana 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 paper 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.
Introduction
In 2022, cervical cancer was the fourth most common cancer in women, with an estimated 660,000 newly diagnosed cases and 350,000 deaths globally, representing 6.6% of all female cancers [1,2]. More than 90% of all cervical cancer-related deaths worldwide are recorded in low- and middle-income countries (LMICs) [3–9]. It is estimated that the incidence of global cervical cancer will increase by 44.4 million cases between 2020 and 2069, nearly two-thirds of which will be diagnosed in least-developed countries (LDCs) [10]. The United Nations defines LDCs as low-income countries that face considerable structural impediments to sustainable development; the criteria for being defined as an LDC include a gross national income per capita of USD 1,088 or below, a human assets index of 60 or below, and an economic and environmental vulnerability index of 36 or above [11]. As of 2024, 44 countries were classified as LDCs worldwide [11]. In 2020, the World Health Organisation (WHO) launched a global strategy to eliminate cervical cancer as a public health problem by reducing the number of new cases per year to four or fewer per 100,000 and set three targets: 90% coverage of human papillomavirus (HPV) vaccination for girls (by 15 years of age); 70% coverage of cervical cancer screening (screening of 70% of women by 35 and 45 years of age using high-performance tests); treatment of 90% of precancerous lesions; and management of 90% of invasive cancer cases by 2030 [6,12,13]. Evidence indicates that nearly 80% of cervical cancer cases can be prevented and detected early with routine screening and early treatment [14,15]. Primarily, cervical cancer can be prevented by adopting healthy lifestyles and vaccinating with HPV among girls aged 9–14 [5]. Further, various types of screening tests, including HPV-based testing, conventional cytology (Papanicolaou [Pap] test), liquid-based cytology, and Visual Inspection with Acetic acid (VIA), can detect any precancerous changes in the cervix or early-stage cancer in adult women [5,16]. According to the WHO, HPV-based screening is superior to the Pap test or VIA in terms of the early detection and prevention of cervical cancer [7,17]. The HPV-based screening test detects the high-risk strains of HPV that are responsible for causing almost all cervical cancer cases and helps save more women’s lives than the Pap test or VIA [17]. It is a cost-effective screen-and-treat approach, and women aged 30 years or above are strongly advised to take regular HPV-based screening tests every 5–10 years [15]. The utilisation of self-sampling methods is also encouraged and can increase adherence among under-screened women, with acceptance rates ranging from 90.5% to 97.3% [18]. However, HPV-based testing programs are not yet operational in many countries, particularly in LDCs, due to suboptimal resources and the unavailability of affordable and clinically validated HPV tests, where VIA is recommended as a primary screening test [7,13,17,19]. The VIA involves an inspection of the cervix after applying 3%–5% acetic acid (vinegar) directly to the cervix to detect any abnormalities in it [20]. After the application of vinegar, abnormal cells in the cervix temporarily turn white (aceto-white), indicating the need for further assessments [20]. Most importantly, this screening provides instant results, allowing women to undergo screening and treatment in a single visit if any abnormalities have been detected [5,14,21]. The VIA method has an average sensitivity of 77% and an average specificity of 86% to detect precancerous and cancerous cells of the cervix [22].
Despite the wide availability of these effective cervical cancer screening tests, some screening tests, such as the Pap test, are not commonly available in LDCs due to a lack of resources, the sub-optimal performance of cytology, lack of quality control, and inefficient processes of investigation and treatment in healthcare systems; as a result, the uptake of cervical cancer screening in LDCs is significantly lower than that in developed countries [7,23]. The WHO estimated that only around 5% of the women in LDCs have been screened for cervical cancer compared with 60% in high-income countries [20,23]. For example, only 1%, 6%, 12%, and 16% of age-eligible women in Ethiopia, South Africa, Bhutan, and Nepal, respectively, have undergone cervical cancer screening [24–26].
Several reviews have identified that cervical cancer screening utilisation is associated with various factors. For example, Yimer et al. (2021) found that cervical cancer screening utilisation was positively associated with knowledge of the disease but negatively associated with a lack of formal education. Bruni et al. (2022) and Bogdanova et al. (2022) identified being older, being diagnosed with a sexually transmitted disease, fear of a negative result after the screening, the lack of a national screening programme that is accessible to women, inadequate training for healthcare providers, and stigma associated with the screening procedures as other factors associated with cervical cancer screening utilisation [7,19]. The absence of a routine screening programme for cervical cancer and a lack of official recommendations for screening also discourage screening service utilisation among women. More than 60% of low-income countries and almost 45% of LMICs still lack official recommendations for cervical cancer screening [7].
In LDCs, understanding the coverage of and factors associated with the uptake of cervical cancer screening is essential to address the barriers to implementing effective interventions and thereby reducing the cervical cancer burden. Although previous systematic reviews and meta-analyses have explored the barriers to and factors associated with cervical cancer screening utilisation in LMICs, sub-Saharan Africa, and Ethiopia, none have focused on LDCs [8,9,27]. Thus, our systematic review and meta-analysis aimed to examine the cervical cancer screening uptake rate and identify its associated factors among women in LDCs.
Methods
The review followed the Preferred Reporting Items for Systematic Reviews and Meta-analysis (PRISMA) guidelines, and the relevant parts are reported [28]. The review protocol has been registered in the International Prospective Register of Systematic Reviews (PROSPERO; registration number CRD42022330199).
Search strategy
A literature search was conducted in December 2023 across five databases, EMBASE, MEDLINE (Ovid), CINAHL, Cochrane Library and PubMed, and grey literature. The relevant studies were searched using combinations of keywords, such as ‘cervical cancer, screening or prevention or early detection of cancer or cervical smear or Pap smear test or Pap test or Visual Inspection with Acetic Acid or Papanicolaou test’, ‘factor or predictor, least developed countries or low-income countries and ‘women or female’. Various Medical Subject Headings, such as ‘uterine cervical neoplasms’, ‘early detection of cancer’, ‘poor’ and ‘women’, were also used to search for relevant studies. Regarding the types of screening test, both the Pap test and VIA screening are used in the LDCs; thus, both were used as key terms to identify relevant studies [11]. The reference lists of the retrieved studies were also searched to identify further relevant studies. Studies conducted in countries other than LDCs and published in languages other than English were excluded [11]. To include all relevant studies conducted in the LDCs, no restriction was placed on the year of publication [29] (see S1 Table).
Study selection
Initially, the identified studies were imported into Endnote, and duplicate studies were removed [30]. The three reviewers independently screened the studies based on their abstracts and titles. The full texts of the studies were then systematically reviewed and assessed for eligibility against the inclusion and exclusion criteria. Any disagreements were resolved through discussion until a consensus was reached.
Data extraction
Both qualitative and quantitative studies that examined cervical cancer screening uptake and its associated factors in LDCs were included in the review. Two reviewers extracted and recorded the key characteristics of the included studies, namely the lead author name, study year, country, design, population, sample size, cervical cancer screening uptake rate, and factors associated with cervical cancer screening utilisation, in a Microsoft Excel sheet. Discrepancies were resolved through discussion until a consensus was reached.
Quality assessment of included studies
To assess the quality of the studies, the Mixed Methods Appraisal Tool (MMAT) version 2018 was used [31]. This tool is used to appraise the quality of primary research studies based on experiment or observation, and it has been validated for its content and tested for its reliability [32]. This assessment tool allows for appraisal of the methodological quality of studies with different designs, including quantitative, qualitative, and mixed-method studies. Every criterion is rated on a categorical scale of ‘yes’, ‘no’, and ‘cannot tell’. Based on the suggestions made in the previous version of the MMAT, the overall quality score for the methodological items can be presented using descriptors such as stars (*) or % (5***** or 100% quality criteria met, 4**** or 80% quality criteria met, 3*** or 60% quality criteria met, 2** or 40% quality criteria met and 1* or 20% quality criteria met) [33]. The critical appraisal was performed by three independent reviewers, and any disagreement was resolved through discussion and consensus.
Data synthesis
We combined the quantitative and qualitative findings to present a comprehensive synthesis of the evidence. The results of quantitative studies included in the review were pooled for meta-analysis if appropriate. Meta-analysis was conducted using the Cochrane Collaboration’s Review Manager (RevMan 5.4.1) [34]. The generic inverse variance method was used to pool the results of individual studies with effect size estimates, whose standard errors were reported or could be estimated from other reported parameters. The standard error is needed to calculate the inverse variance weight, which is used to compute the pooled effect estimate and its 95% confidence interval (CI). In view of the heterogeneity of the study populations, a random-effects model was used for all of the meta-analysis [35]. Odds ratios (ORs) and 95% CIs were used to summarise the effect sizes of associated factors for cervical cancer screening uptake of the included studies. Heterogeneity among studies was assessed using I2 with I2 < 25%, 25 ≤ I2 < 50%, and I2 ≥ 50%, categorising heterogeneity as low, medium, and high, respectively [35]. Sensitivity analysis was used to identify the reasons for the heterogeneity and evaluate the robustness of the results by excluding the studies one by one [36]. The qualitative data were synthesised narratively to ensure empirical faithfulness to the original data and allow their integration with the quantitative data [37].
Results
Search results
A total of 965 articles were retrieved from the five databases, the grey literature, and the manual search of the reference lists of the retrieved articles. Among them, 439 articles were found to be duplicates and hence removed. After screening the titles and abstracts of the remaining 526 articles, 62 relevant articles were found, and their full texts were reviewed. A total of 37 articles were further removed after assessing against the inclusion and exclusion criteria. Finally, 25 articles were included in this review (Fig 1).
Study characteristics
Of the 25 studies, 22 were quantitative [25,38–58] and 3 were qualitative [24,59,60]. The studies included in the present review were published between 2010 and 2022. One of these studies was conducted in multiple LDCs, including Chad, Mali, Congo (Brazzaville), Comoros, Laos, Zimbabwe, Burkina Faso, Mauritania, Myanmar, Ghana, Malawi, Ethiopia, and Bangladesh (n = 1) [39], while the rest were conducted in single LDCs, namely Nepal (n = 4) [24,38,54,60], Ethiopia (n = 11) [25,40–42,44,45,48,52,55,57,58], Bangladesh (n = 1) [47], Burkina Faso (n = 1) [43], Tanzania (n = 3) [49,50,53], Uganda (n = 2) [46,51], Lao People’s Democratic Republic (n = 1) [56], and Malawi (n = 1) [59]. The sample size in the individual studies ranged from 72 to 10,021 and the women’s ages ranged from 15 to 72 years. The eligible participants in these studies were recruited from the community (n = 19) [25,38–41,45–53,56,58–60], hospitals (n = 5) [43,44,54,55,57], or both settings (n = 1) [24] (see S2 Table).
Critical appraisal results
The included studies were appraised using the MMAT. Of the 25 studies, 17 met 100% of the quality criteria; six met 80% of the quality criteria, as they did not report the non-response rate; and two met 60% of the quality criteria, as they did not clearly explain the sampling strategy or sample representativeness of the target population and reported inadequate information about the risk of non-response bias (Table 1). Methodologies and study designs, such as the use of appropriate methods to answer the research questions, sampling strategies, and adherence of different study components to the quality criteria of each method, were well described in the majority of the included studies. Based on the present review question, the identified factors associated with utilising cervical cancer screening services among eligible women in LDCs were categorised into various themes and subthemes.
Cervical cancer screening uptake
Seventeen of the 25 included studies reported the uptake rates of cervical cancer screening among eligible women in LDCs [24,25,38,40–42,44–52,54,55]. Of these studies, nine were conducted in Ethiopia and reported cervical cancer screening uptake rates ranging from 4% to 21% [25,40–42,44,45,48,52,55], and two were conducted in Uganda and reported cervical cancer screening uptake rates of 4.8% and 20.6% [46,51]. Similarly, two studies conducted in Nepal reported screening uptake rates of 18.3% and 13.6% [38,54], one conducted in Bangladesh reported an uptake rate of 8.3% [47], and two studies conducted in Tanzania reported screening uptake rates ranging from 8.2% to 21% [49,50]. Lastly, one study reported a cervical cancer screening rate as low as 4.1% among eligible women from low-income countries [39].
Factors associated with the uptake of cervical cancer screening
Socio-demographic factors.
Age.
Nine studies reported that older age was significantly associated with women’s increased uptake of cervical cancer screening [25,40–43,45,47,53,55]. In contrast, one of the included studies reported that younger age was associated with increased uptake of cervical cancer screening [49] and two studies did not find a significant association between age and cervical cancer screening uptake among women from LDCs [38,54].
Residential areas.
All four quantitative studies that reported on the association between women’s residential areas and cervical cancer screening uptake were pooled in the meta-analysis [39,43,47,55]. The findings demonstrated that women living in rural areas were less likely to undergo cervical cancer screening than those living in urban areas (OR: 0.70; 95% CI: 0.31–1.58; p = 0.39; I2 = 83%); however, statistical significance was not reached (Fig 2a). Similar findings were observed in qualitative studies indicating that women from rural areas were less likely to have undergone cervical cancer screening than those from urban areas, due to the inadequate availability of healthcare facilities, including screening services for cervical cancer [39,59,60]. In rural areas, poorly equipped examination rooms in healthcare facilities and lack of privacy during examination, e.g., conducting screening on floor mats and examining many women simultaneously, were found to deter women from utilising screening services [58].
Financial status.
Six studies examined women’s financial status and uptake of cervical cancer screening [39,43,46,51,53,55]. Four of these six studies reported that women of lower socio-economic status were less likely to undergo cervical cancer screening [39,43,46,55]. In contrast, one study reported that those women who encountered financial barriers were more likely to undergo cervical cancer screening tests than their counterparts [53]. A study by Ndejjo et al. (2016) [51] reported that the financial status of the women had no association with cervical cancer screening uptake.
Employment status.
Five studies that investigated women’s employment status were pooled for the meta-analysis [42,43,47,52,55]. The findings demonstrated that employed women were 2.72 times more likely to have undergone screening for cervical cancer than unemployed women (OR: 2.72; 95% CI: 1.97–3.76; p < 0.001; I2 = 0%) (Fig 2b).
Educational status.
Thirteen studies, namely 12 quantitative studies [40,41,43–45,47–49,51,54,55,58] and one qualitative study [38], examined the association between women’s educational background and cervical cancer screening uptake. All the quantitative studies that reported on this association were pooled in the meta-analysis [40,41,43–45,47–49,51,54,55,58]. The pooled results demonstrated that women with higher educational backgrounds were 1.34 times more likely to have undergone screening than those without such backgrounds (OR: 1.34; 95% CI: 0.70–2.53; p = 0.37; I2 = 90%), however, statistical significance was not reached (Fig 2c). In contrast, Acharya et al. [38] reported that women’s educational backgrounds were significantly positively associated with their cervical cancer screening uptake (p = 0.01).
Knowledge of cervical cancer and its screening.
Thirteen studies that investigated women’s knowledge of cervical cancer and its screening were pooled for the meta-analysis of this factor [25,40–42,44,46,48,50–52,55]. The findings showed that women who were knowledgeable about cervical cancer and its screening were more likely to have undergone screening than those with poor or no knowledge (OR: 3.39; 95% CI: 2.00–5.75; p < 0.001; I2 = 82%) (Fig 3). Consistent findings were observed in all the qualitative studies included in this review, which reported that a lack of, or inadequate, knowledge of cervical cancer and its screening was directly related to low uptake of cervical cancer screening [24,59,60].
Myths and misconceptions about cervical cancer and its screening.
Darj et al. [24] reported several misconceptions about cervical cancer and its screening held by many women in LDCs, which contributed to the reduced uptake of cervical cancer screening: (i) cervical cancer is a deadly and unusual disease with no cure other than surgery and causes substantial stress and emotional and physical suffering to both the patients and their family members; (ii) cervical cancer screening is only used for the detection of cancer that is already present or is usually provided for sick women and those with other uterine complications; (iii) screening should be completed every six months at the nearest health centre; (iv) negative results from preliminary screening suggest that an individual will never develop cervical cancer; (v) cervical cancer can be diagnosed and treated simultaneously during screening; and (vi) cervical cancer might show signs and symptoms even at an early stage. Accordingly, most women believed that if they were not experiencing any symptoms, abnormal discharge, or difficulties during sexual intercourse, they did not need to seek screening services [24].
Sexual and reproductive health-related factors.
Parity status.
Only three studies assessed the parity status of women and cervical cancer screening uptake in women from LDCs [49,55,58]. These three studies were pooled into a meta-analysis, and the pooled results demonstrated that multiparous women were approximately three times more likely to have undergone screening than nulliparous women (OR: 2.73; 95% CI: 1.61–4.64; p = 0.002; I2 = 0%) (Fig 4a).
Visiting healthcare facilities.
Women who had visited gynaecology units for other examinations were more likely to have undergone screening than those who had never visited gynaecology units (OR: 4.53; 95% CI: 1.51–13.62; p = 0.007; I2 = 65%) (Fig 4b) [42,52]. Baley et al. (2020) [42] reported that women who visited private healthcare facilities for reproductive healthcare services and cervical cancer screening uptake were more likely to undergo screening than those who visited public health facilities (OR: 8.9; 95% CI: 2.8–28.9; p ≤ 0.05). In contrast, women who visited government facilities to receive reproductive healthcare were more likely to undergo cervical cancer screening than women who visited private facilities (OR: 9.71; 95% CI: 1.33–71.11, p = 0.025) [51]. Similarly, women who visited non-governmental organisations (NGOs) were less likely to undergo cervical screening tests than those who visited government or private clinics (OR: 0.33, 95% CI: 0.23–1.49; p ≤ 0.05) [39]. Regarding women’s mode of travel to health facilities, two included studies demonstrated that women who travelled to facilities by car were more likely to be screened for cervical cancer than those who travelled by motorbike or foot (OR: 1.33, 95% CI: 0.30–5.97; p = 0.71; I2 = 93%) (Fig 4C) [39,56].
History of multiple sexual partners.
Five of the included studies investigated women’s history of multiple sexual partners and uptake of cervical cancer screening, and their results were pooled into a meta-analysis [25,40,48,49,57]. The findings of the meta-analysis demonstrated that women with a history of having multiple sexual partners were 2.39 times more likely to have undergone screening than those without a history of multiple sexual partners (OR: 2.39; 95% CI: 1.63–3.51; p < 0.001; I2 = 32%) (Fig 4D).
History of sexually transmitted diseases and other illnesses.
Eight studies evaluated the association between previous history of sexually transmitted diseases and uptake of cervical cancer screening [25,40,41,45,48,51,54,56]. The meta-analysis showed that women with a history of sexually transmitted diseases were more likely to have undergone screening than those who had no history of sexually transmitted diseases (OR: 2.10; 95% CI: 1.16–3.83; p = 0.01; I2 = 84%) (Fig 4E). This finding is consistent with a qualitative study that demonstrated that women who had chronic abdominal pain were more likely to have undergone screening for cervical cancer than their counterparts [59].
Healthcare provider-related factors.
Seven studies that evaluated healthcare provider-related factors and uptake of cervical cancer screening were pooled in a meta-analysis [41–44,51,52,56]. The results showed that women who had received recommendations from healthcare providers were 5.32 times more likely to have undergone cervical cancer screening than those who had never received such recommendations (OR: 5.32; 95% CI: 2.44–11.58; p < 0.001; I2 = 85%) (Fig 5). Furthermore, three qualitative studies reported that lack of trust in healthcare providers due to previous uncomfortable screening experiences, inappropriate behaviour by some healthcare providers, and service providers’ negligence and incompetence tended to discourage women from utilising screening services [24,59,60].
Decision-making.
The review found that due to the patriarchal nature of society, women in LDCs lack decision-making power, often depending on their husbands and in-laws to decide whether they should access healthcare facilities, including to undergo cervical cancer screening [24,60]. Moreover, women tend to be reluctant to talk about and express their feelings to their husbands and family members because they do not receive permission and encouragement to do so and are afraid of abuse, discrimination, and rejection, which in turn prevents them from seeking screening services [24,60]. In contrast, an included study by Kileo et al. [49] found that women who had not involved their husbands in decision-making regarding healthcare service utilisation were more likely to have undergone cervical cancer screening than those who had involved their husbands in decision-making (OR: 3.73; 95% CI: 2.22–6.26; p < 0.005).
Perceptions of cervical cancer and its screening.
A total of eight studies reported the association between women’s perceptions of cervical cancer and screening uptake [25,38,41,44,45,52,55,59]. Of these eight studies, six were pooled for meta-analysis, and the results demonstrated that women who perceived a high risk of developing cervical cancer were more likely to undergo screening for cervical cancer test than those who perceived a low risk (OR: 3.76; 95% CI: 2.62–5.38; p < 0.001; I2 = 37%) (Fig 6) [25,41,44,45,52,55]. Moreover, women who perceived higher severity and more cues to action were more likely to undergo cervical cancer screening [44,59]. In addition, two studies reported the association between women’s self-efficacy and uptake of cervical cancer screening, and these two studies were pooled for a meta-analysis [44,45]. The finding of the meta-analysis showed that women with high self-efficacy were 4.76 times more likely to have undergone cervical cancer screening than those with low self-efficacy (OR: 4.76; 95% CI: 2.46–9.23; p < 0.001; I2 = 0%) (Fig 6). Similarly, the findings also demonstrated that women with lower perceived barriers had higher cervical cancer screening utilisation than their counterparts (OR: 3.42; 95% CI: 1.26–9.28; p = 0.02; I2 = 70%) (Fig 6) [25,44]. However, Acharya et al. [38] and Fort et al. [59] reported that cervical cancer screening behaviour was not associated with women’s perceptions of severity, benefits, or barries.
Cultural factors.
Various cultural factors, such as fear of discrimination and exclusion from society, influenced women’s decision to undergo cervical cancer screening [24,59,60]. Another factor that prevented women from undergoing screening tests was that male healthcare providers might perform the examinations. Women tended to feel ashamed and embarrassed about showing their genitals to healthcare providers, particularly if they were male [24,59,60]. Moreover, women expressed a sense of discomfort and shame at the idea of other people knowing that they might be ‘sick’ [24]. They feared that people would suspect and assume that they had been cheating on their husbands with multiple sexual partners and were thus ‘being punished for what they had done’ [24]. Women also feared being excluded from social activities such as gatherings for festivals; thus, fear of social rejection was a major barrier to cervical cancer screening utilisation [24,59,60]. These findings suggest that it is imperative to develop and implement culturally appropriate and women-friendly interventions to educate women and their family members regarding the importance of cervical cancer screening and encourage them to participate in such screening to reduce the burden of cervical cancer across the local, community, national, and global levels [24,59,60].
Use of mass media.
Women who tended to listen to the radio regularly or at least 1–3 times a week were more likely to have undergone screening than those who never listened to the radio (OR: 24.76; 95% CI: 11.49–53.33; p < 0.001) [53].
Discussion
To the best of our knowledge, this systematic review and meta-analysis is the first to synthesise current evidence regarding cervical cancer screening uptake and its associated factors among women in LDCs worldwide. The findings revealed that the cervical cancer screening uptake rates among eligible women in LDCs were notably lower, ranging from 4% to 21%, than those in developed regions/countries such as Hong Kong (48%) [61] and England (85.7%) [62]. Screening coverage in LDCs is significantly lower than the WHO’s target screening rate of 70% among women aged 35–45 years by 2030 [13]. Our systematic review and meta-analysis further identified multiple factors associated with the low cervical cancer screening uptake rate among eligible women in LDCs, relating to socio-demographic factors, knowledge of cervical cancer and its screening, sexual and reproductive health-related factors, healthcare providers’ recommendations, decision-making power, perceived beliefs and misconceptions regarding cervical cancer and its screening, cultural factors, and use of mass media. Among these factors, knowledge and awareness of cervical cancer and screening tests were positively and significantly associated with cervical cancer screening uptake among women in LDCs. Previous reviews have similarly reported that women with good knowledge of cervical cancer and its screening are more likely to undergo screening than those with poor or no knowledge [9,27]. Thus, it is critical to plan and implement context-specific and culturally appropriate educational programmes targeting women and their family members, including their husbands and community members, to increase screening coverage. It is suggested that women be involved in leading cervical cancer programmes and that these programmes be integrated into various national, community, and school programmes to reach the WHO 2030 target of 70% cervical cancer screening coverage [9,13,63,64]. Our systematic review and meta-analysis also found that factors such as a lack of nationally recommended screening programmes, inadequate standard screening facilities in rural areas, lack of time to travel, and poverty also prevented women from utilising the screening services [7,27,65,66]. These findings indicate that the availability of nationally recommended screening services with well-functioning healthcare facilities that are accessible and affordable to women from rural areas is crucial for enhancing women’s participation in screening [8]. Our review also found that women’s sexual and reproductive health status was associated with screening uptake. For instance, multiparous women and women with a history of various illnesses, including sexually transmitted diseases, were more likely to undergo screening than their counterparts [9,63]. Moreover, as women with multiple sexual partners were more likely to be infected with various sexually transmitted diseases, such as HPV, these women were at a higher risk of developing cervical cancer than their counterparts. This finding echoes that of a previous review [15]. As such women frequently visit healthcare facilities, the screening uptake rate is higher among them than women with no history of sexually transmitted diseases [9,15]. The review also revealed several myths and misconceptions related to cervical cancer and its screening that affect women’s screening uptake. These stemmed from patriarchal social beliefs, a fatalistic view of cervical cancer, shame about being sick, fear of social exclusion, embarrassment, and fear of abuse and rejection. These findings are supported by previous studies [9,27,49]. The barriers and factors associated with stigma and cultural beliefs that prevent cervical cancer screening utilisation could be addressed by introducing HPV self-sampling [13,19]. HPV self-sampling is a comfortable and reliable screening test for cervical cancer, which is well accepted by women from rural areas [64]. Some women prefer to receive screening using the HPV self-sampling technique because the technique is easy to perform, reduces discomfort and embarrassment, and maintains privacy while giving reliable results [8]. Therefore, promoting and introducing HPV self-sampling in LCDs using community resources, such as community health workers, could improve screening participation, particularly among women from stigmatised backgrounds [8,10,19,67].
Moreover, healthcare providers’ recommendations were found to be an important factor encouraging women’s utilisation of screening services. This is consistent with another review’s finding that advice from healthcare providers is a major facilitator of cervical cancer screening uptake in LDCs [15]. In contrast, a lack of trust in healthcare providers due to discomfort experienced while undergoing screening was negatively associated with screening service utilisation [60]. It is vital to provide continued training and professional development for the healthcare providers involved in cervical cancer screening [19]. Furthermore, the results of our systematic review and meta-analysis revealed that women who had decision-making power regarding the utilisation of healthcare services were more likely to utilise screening services than those whose family members, particularly their husbands, were involved in making these decisions. This finding is in line with the results of a study by Petersen et al. (2022) [8].
Moreover, this review identified perceived susceptibility, severity, low perceived barriers, cues to action, and self-efficacy as predictors of cervical cancer screening utilisation. Women who perceived higher susceptibility to or severity of cervical cancer, fewer barriers to undergoing screening, cues to action, and higher self-efficacy in accessing screening may have had higher education, more knowledge of the benefits of screening, and a better understanding of the consequences of cervical cancer, which might have encouraged them to participate in screening. A similar finding was reported in a previous review [9]. Lastly, this review revealed that the use of media, such as radio, plays an important role in promoting the utilisation of cervical cancer screening services. Therefore, it is important to utilise social media to promote or disseminate health messages rapidly at a low cost to a large number of people across geographical locations [68].
Limitations
This present review has several limitations. First, the studies included in the review covered only one-third of the LDCs worldwide, so the review findings may not be generalisable to women from all LDCs and may not reflect all of the characteristics of women from all LDCs. Second, as the cervical cancer screening uptake was self-reported by women in some studies, their screening uptake rates and effect size estimates of associated factors might be subject to self-report bias. In addition, only studies published in English were included in this review, which may limit understanding of some factors influencing cervical cancer screening uptake; and the results of our review might be subject to publication bias, as studies without significant findings are less likely to be published. Lastly, a high degree of heterogeneity was observed in the included studies as a result of variation in the study populations with different cultural and social backgrounds. Future studies should explore the reasons for this variability and address the issue of heterogeneity to generate robust evidence and guide the development of effective interventions to increase the uptake of cervical cancer screening by women from LDCs.
Recommendations
The current review has some recommendations for improvements at the research, government, policy, and community levels. At the research level, future studies should explore the effectiveness of culturally tailored interventions in LDCs using behavioural science approaches to understand barriers to and identify strategies for increasing the uptake of cervical cancer screening. At the government level, it is essential for governments of LDCs to invest additional resources in the development of evidence-based, comprehensive national cervical cancer elimination strategies, which should involve all relevant stakeholders, including academia, policymakers, and communities, and be implemented at all levels, from national to local, to reduce the burden associated with cervical cancer [69]. At the policy level, policymakers from the LDCs should work closely with national and international organisations, such as the WHO, to call for the immediate enforcement of accessible and well-structured national guidelines for cervical cancer screening and prevention programmes. Screening programmes should be incorporated into various other health-related programmes, such as women’s health programmes, national immunisation programmes, and family planning programmes, to educate the public about the importance of early cancer detection and regular screening. However, implementing national recommendations is not sufficient to reduce the cervical cancer burden [7]. Effective screening, which involves proper diagnosis, follow-up, and management of positive cases, is crucial to prevent cervical cancer [7,19].
The government should also provide education and training for healthcare providers, including community healthcare workers, to build their capacity to promote cervical cancer screening (based on national guidelines). At the community level, it is crucial to conduct various women-friendly awareness campaigns, such as age-specific educational interventions, health camps, and school-based health programmes, to educate community members about the benefits of routine screening for and early treatment of cervical cancer [21,70]. In addition, awareness and educational programmes should be widely promoted through social media platforms, such as Facebook, and news programmes and advertisements on television and radio. It is crucial to educate family members, particularly husbands, because family support and permission to attend cervical cancer screening tests are essential to encourage women in LDCs to undergo screening [19].
Conclusions
This review found that the uptake of cervical cancer screening among eligible women in LDCs was significantly low. The low utilisation of cervical cancer screening services was found to be associated with various factors, such as lack of knowledge of cervical cancer screening. It is imperative to develop and implement women-friendly and culturally appropriate health interventions to reduce the healthcare burden of cervical cancer among women in LDCs. It is recommended that the governments of all LDCs invest additional resources in policy advancement and development of cervical cancer prevention programmes that are affordable, acceptable, and accessible to improve screening uptake and thereby reduce cervical cancer morbidity and mortality in their female populations.
Supporting information
S4 Table. List of full-text excluded articles (titles and reasons).
https://doi.org/10.1371/journal.pone.0321627.s004
(DOC)
S5 Table. All the included studies identified during the literature search (after duplicate studies removed).
https://doi.org/10.1371/journal.pone.0321627.s005
(DOCX)
Acknowledgments
The authors would like to acknowledge Dr. Chura Bahadur THAPA, Dr. Khanh Thi NGUYEN, and Mr. Aristo Anselmus, PARUT for their assistance in preparing the manuscript. We would also like to thank AsiaEdit (asiaedit.com) for providing professional English language editing support.
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