Barriers to and Facilitators of Cervical Cancer Screening among Women in Southeast Asia: A Systematic Review

In Southeast Asia, cervical cancer is the second most common cancer in women. Low coverage for cervical cancer screening (CCS) becomes a roadblock to disease detection and treatment. Existing reviews on CCS have limited insights into the barriers and facilitators for SEA. Hence, this study aims to identify key barriers and facilitators among women living in SEA. A systematic literature review was conducted on Pubmed, Embase, PsycINFO, CINAHL, and SCOPUS. Primary qualitative and quantitative studies published in English that reported barriers and facilitators to CCS were included. The Mix Methods Appraisal Tool was used for the quality assessment of the included studies. Among the 93 included studies, pap smears (73.1%) were the most common screening modality. A majority of the studies were from Malaysia (35.5%). No studies were from Timor-Leste and the Philippines. The most common barriers were embarrassment (number of articles, n = 33), time constraints (n = 27), and poor knowledge of screening (n = 27). The most common facilitators were related to age (n = 21), receiving advice from healthcare workers (n = 17), and education status (n = 11). Findings from this review may inform health policy makers in developing effective cervical cancer screening programs in SEA countries.


Introduction
In 2018, approximately 570,000 women developed cervical cancer and 311,000 women died from it [1]. Approximately 84% of all cervical cancers and 88% of all deaths caused by cervical cancer occurred in lower-resource countries [1]. Over the past four decades, a significant reduction in mortality and incidence of cervical cancer have been observed with preventive strategies such as cervical cancer screening (CCS) and vaccination against the human papilloma virus (HPV) [2]. Screening modalities for cervical cancer include a pap smear, HPV test, and visual inspection with acetic acid (VIA). Despite the proven effectiveness of screening, worldwide coverage of these preventive strategies remains poor, especially in developing countries [3].
The Southeast Asia (SEA) region comprises of 11 countries of diverse religions, cultures, and history: Brunei, Cambodia, Indonesia, Laos, Malaysia, Myanmar, Philippines, Singapore, Timor-Leste, and Vietnam. There are approximately 330 million women in SEA, equivalent to 4.3% of the world's population [4]. Cervical cancer is the second most common cancer among women in the region [5]. In 2020, SEA was ranked seventh for cervical

Data Collection and Analysis
Two independent reviewers (BC and AL) performed the search strategy and study selection, while two independent reviewers (BC and MM) executed the data extraction and quality assessment of the included studies. A manual search of the reference list for all included studies was done to identify additional studies for inclusion. All citations were uploaded on Endnote for the removal of duplicates and exported to Microsoft Excel for screening studies for inclusion.
The following information were abstracted from eligible articles: Study title, authors, publication year, study design, screening instrument used, population size, age of study participants, and proportion of patients with history of CCS. In addition, for quantitative studies, data extracted included barriers and facilitators that were statistically significantly associated (p < 0.05) with CCS intention or uptake, as well as proportions of participants reporting a barrier or facilitator. When univariate and multivariable analyses were both conducted, only results from multivariable analyses were extracted. For qualitative studies, data extracted included all reported barriers and facilitators.
Thematic analysis with an inductive approach was performed to classify barriers and facilitators into major categories [13], with a focus on context and commonalities across included studies. Data extracted from included studies were first assigned a code and patterns were searched amongst the coded data. Similar codes were subsequently categorized into descriptive themes, and themes were clustered into higher-ranking themes (major categories subsuming the themes). Finally, the number of studies supporting each theme were summed up for each SEA country. The Mixed Methods Appraisal tool (MMAT) was used to conduct a quality assessment of the included studies [14]. The MMAT has different rized into descriptive themes, and themes were clustered into higher-ranking themes (major categories subsuming the themes). Finally, the number of studies supporting each theme were summed up for each SEA country. The Mixed Methods Appraisal tool (MMAT) was used to conduct a quality assessment of the included studies [14]. The MMAT has different scoring criteria for different types of studies: Mixed methods, qualitative, quantitative non-randomized, and quantitative descriptive. Each type of study was assessed based on five criteria with a "yes", "no", or "unsure" response, with a maximum score of 5. Any discrepancies for study inclusion, data extraction, analysis, and quality assessment were resolved through consensus or by referral to a third reviewer (VM or WHL).

Results
A total of 3025 records were retrieved from the databases. After the removal of 1610 duplicates, 1415 records underwent title and abstract screening resulting in the exclusion of 1270 articles (Figure 1). After a full text review of 145 studies, 75 articles met the inclusion criteria. In addition, we identified 18 studies that met inclusion criteria from manual search. Therefore, the final number of original research articles for data extraction, analysis, and synthesis was 93.

Quality Assessment
A majority of the studies (68.8%, n = 64) scored 4 or 5 out of 5 based on the MMAT. All qualitative (n = 9) and mixed-methods studies (n = 3) scored either 4 or 5 points. Among 73 quantitative non-randomized studies, the lack of description of the sampling process or population (n = 38), and the lack of description of tools for an outcome and exposure measurement (n = 20) were common. Four studies were not clear on the completeness of screening data. Among eight quantitative descriptive studies, five studies lack description on sampling or target population, where non-response bias becomes difficult to assess. The complete quality appraisal can be found in Table S2.

Factors Associated with Cervical Cancer Screening in Southeast Asia (n = 91)
A total of 63 barriers from 63 studies were reported across seven countries in SEA (Table S3), while 71 facilitators from 73 studies were reported across nine countries (Table S4). The top three barriers to CCS in SEA by the number of publications include embarrassment (n = 33), busyness or time constraints (n = 27), and poor knowledge of screening (n = 27). The top three CCS facilitators include age (n = 21), healthcare workers' advice for CCS (n = 17), and higher education status (n = 11). Figure 2 summarizes 29 factors that were described both as barriers and facilitators of CCS across studies in SEA (full details by country level are available in Figure S1). two studies in Thailand referred to the Reproduction Health Survey 2009 [62,70], data were only extracted from the more recent publication [70]. Two studies from Singapore analyzed the same study cohort but reported unique barriers and facilitators separately for each study [89,90]. Hence, both studies were included in this analysis.

Quality Assessment
A majority of the studies (68.8%, n = 64) scored 4 or 5 out of 5 based on the MMAT. All qualitative (n = 9) and mixed-methods studies (n = 3) scored either 4 or 5 points. Among 73 quantitative non-randomized studies, the lack of description of the sampling process or population (n = 38), and the lack of description of tools for an outcome and exposure measurement (n = 20) were common. Four studies were not clear on the completeness of screening data. Among eight quantitative descriptive studies, five studies lack description on sampling or target population, where non-response bias becomes difficult to assess. The complete quality appraisal can be found in Table S2.

Common Barriers and Facilitators in Cervical Cancer Screening Across Countries in Southeast Asia
The barriers to and facilitators of CCS were also summarized by the number of countries in Tables S3 and S4, respectively, to allow for commonalities across countries to be drawn. The barrier categories reported by most countries (n = 6) were demographics, knowledge, risk perception, and health system. Poor awareness to screening was the most common barrier reported by countries in SEA (n = 6). Other common barriers (n = 5) include poor knowledge of screening, poor perceived susceptibility, having no symptoms, factors related to health center characteristics (manpower, operations, and location), embarrassment, fear of results, fear of pain, and costs related to CCS. Most countries in SEA (n = 7) reported facilitators in the category of demographics. This is followed by knowledge, financial access, and health system-related facilitators (n = 6). Specific facilitators common across countries include age (n = 6), followed by good awareness of screening, and the receipt of healthcare worker advice (n = 5).
The commonalities among the top three barriers and facilitators for each country were also assessed. Embarrassment (n = 4) and poor knowledge to screening (n = 3) were the two most common barriers in SEA. Other common barriers (n = 2) include time constraints, having no symptoms, and the cost of screening. Age and advice from healthcare workers were the most common facilitators of CCS (n = 3), followed by health center characteristics (manpower, operations, and location), and support from friends or family members (n = 2).

Brunei (n = 1)
Based on a population health survey among adults aged 18 to 69 years old, 56.5% of female participants had a history of having a pap smear [100]. Barriers to CCS include older age, employment type, and breast cancer screening attendance [100]. Facilitators to CCS include being married, the presence of comorbidities or family members with comorbidities, diet, and alcohol intake [100].

Cambodia (n = 1)
Among women aged 20 to 69 in a rural district, only 7.0% have ever received a pap smear [101]. Only facilitators were reported in this cross-sectional study, where younger women, and those with good awareness towards screening expressed greater willingness to CCS [101].
Of the seven studies reporting barriers to CCS in Indonesia, four studies reported facilitators in the categories of knowledge as well as perception, attitude, and belief. No studies reported barriers related to demographics or socio-economic status. Embarrassment [74,81], knowledge deficits in CCS [81,84], having no symptoms [74,81], and fear of result [76,81], were among the top barriers in Indonesia. Two studies described the lack of knowledge of cervical cancer as a barrier to CCS, which was only reported in Indonesia [74,81].
Facilitators were more commonly described in the categories of perception, attitude, and beliefs (n = 7) as well as motivation and perception (n = 5) among 13 studies from Indonesia. There were no facilitators in the classification of psychological or emotional factors, and healthcare utilization. Intentions to screening was among the top facilitators of CCS [72,78,80], which was reported more commonly in Indonesia compared to other SEA countries. In addition, support from family or friends was another crucial facilitator of CCS based on three publications [71,74,81].

Laos (n = 3)
All three quantitative studies from Laos described pap smears as the screening modality of interest, two of which were published after 2010 [103,104]. Among working women, a higher prevalence of ever receiving a pap smear was reported (46.3%) [104], compared to village residents and women with HIV (3.9% to 4.5%) [102,103].
All three studies reported barriers in the category of psychological or emotional factors, knowledge, risk perception, financial access, and the health system. No studies reported barriers in the category of socio-economic status. Barriers reported by at least two studies include embarrassment [102][103][104], fear of pain [102][103][104], fear of results [102,103], poor awareness [103,104], poor perceived susceptibility [102,103], being not at risk for cancer [103,104], and having no symptoms [103,104]. Other barriers include concerns with screening cost [102][103][104], an inaccessible screening location [102,103], and the lack of CCS advice from a healthcare worker [103,104]. Only one study described a knowledge-related facilitator, where higher scores for knowledge of cervical cancer and prevention were reported among women who received CCS in the past [104].

Malaysia (n = 31)
Nineteen studies were published from 2011, five of which were qualitative studies. The take up of pap smear in different female populations varied largely, from 6.0% among university students [18], to 79.5% among patients from an obstetrics and gynecology clinic [47]. Similarly, screening in the past three years varied largely from 3.8% among African immigrants to Malaysia [22], to 42.8% among university staff [38].

Myanmar (n = 1)
A total of 666 migrant women were surveyed in a study, where 19.1% had CCS in the past three years [105]. Screening in the past three years was more likely among older women, those with a family history of cancer, had expressed willingness to pay for screening, received encouragement from nurses, had low perceived barriers, and had good disease and screening knowledge [105].
Of the 12 studies reporting facilitators in Singapore, five reported facilitators within the category of perception, attitude, and belief, while four described facilitators in the categories of knowledge, demographics, and healthcare utilization. Top facilitating factors were related to age [89,92,99], support from family and friends [88,89,92], good awareness of screening [89,92,96], and high perceived benefit [90,92,99]. Other top facilitators include healthcare worker advice for screening [89,92,96] and health center characteristics such as a convenient screening location [87,93,96] and the availability of female health workers or nurses for the conduct of screening [87,96].
3.5.9. Vietnam (n = 2) A qualitative and a mixed methods study with a total of 216 participants revealed a low prevalence of prior pap smear or VIA ranging from 3.1% to 7.1% [106,107]. Barriers to CCS were related to religious beliefs, low risk perception, and the lack of healthcare worker advice [106]. Both studies reported poor awareness as a barrier to screening [106,107], while the beliefs of health workers that CCS is only for married women was reported in one study [107]. Facilitators to CCS include spousal support, low cost of screening, and having healthcare workers' advice for CCS [106].

Discussion
To our knowledge, this is the first systematic review to focus on barriers to and facilitators of CCS among women in SEA, a region with high disease incidence yet poor screening uptake. Over 60 barriers from seven countries and over 70 barriers from nine countries were identified and categorized into 11 broad categories. We presented the findings at the country level to provide insights on how screening uptake can be improved in each country. We also compared the top barriers and facilitators between countries, to provide guidance for countries that have limited information on factors affecting CCS. A majority of the studies in this review were published within the past 10 years, which highlights the growing interest and challenges faced in the area of cervical cancer screening within SEA. A broad search strategy was employed in this study to maximize findings by including both quantitative and qualitative studies without any date restrictions. This allowed for the study of a broader perspective from patients, family members, healthcare providers, and health officials, which provides valuable insight to guide the design of public health programs.
The barriers and facilitators identified from this study are related to demographics, socio-economic status, social support, knowledge, attitudes, perceptions, financial access, health system, and psychological or emotional factors. We found that the top barrier category to CCS is psychological or emotional factors (n = 44), namely embarrassment and fear. This is followed by knowledge (n = 38), which includes the lack of knowledge and awareness to cervical cancer and CCS. The top facilitator categories are predominantly factors related to demographics (n = 33), as well as perception, attitudes, and beliefs to screening (n = 29). These are consistent with prior research in lower-middle income countries [108][109][110], and interestingly in developed countries as well, such as the United States [111] and Australia [112]. Our findings also support a previously demonstrated relationship between higher education status and higher CCS uptake [7]. Similarly, psychosocial and contextual factors described in prior systematic literature reviews [9,10] were also reported by women in SEA. These include factors associated with the health system, cost, time constraints, screening attitudes, knowledge, awareness, emotional factors, social support, and experiences with healthcare professionals. However, our findings differed from a review among high cervical cancer incidence countries where the top barriers to CCS were fatalism, and negative attitudes and beliefs towards non-traditional healthcare [11]. A possible reason is that a majority of the studies included in that review are from Africa, where traditional healers are likely sought prior to or in conjunction with medical care [113].
Barriers common to SEA countries, reported by five to six countries, include poor awareness and knowledge of screening, poor perceived susceptibility to cervical cancer, having no symptoms, and factors related to health center characteristics. Facilitators common across countries include the influence of age, receiving advice from healthcare workers, and good awareness of screening. These common factors identified can also provide guidance for countries with limited insights into barriers and facilitators to CCS, such as the Philippines, Timor-Leste, Cambodia, Myanmar, Vietnam, and Laos. Several factors were also unique in certain countries, which reported certain barriers and facilitators more frequently than other countries. For example, religion and poor impression of the health system were more frequently reported barriers in Thailand while occupation type, advice from employers, and receiving CCS as part of a structured health program were more frequently reported facilitators. In Malaysia, unique barriers include the lack of support from husband, family members, and friends, while unique facilitators include the knowledge of screening and the use of contraceptives. Reasons for these differences between countries could be driven by the social, cultural, religious, and health system differences of SEA countries [114], as well as researchers' interests in specific factors affecting CCS in the country. Hence, existing CCS programs should consider addressing the country-specific barriers and facilitators in the design of interventions to increase screening uptake.
Broadly, our findings suggest that patient education-based interventions are key to increasing CCS uptake in SEA, as key barriers to CCS such as fear, embarrassment, and the lack of knowledge can be addressed. Through the use of community health workers, brochures, phone counselling, and multimedia, educational interventions alone has been found to increase the odds of CCS uptake by more than 2 times [115], compared to routine care. Equally important, facilitators of CCS should be considered in the design of such interventions to increase CCS uptake, as barriers and facilitators are often two sides of the same coin. For example, knowledge of screening is one of the 29 factors that was described both as a barrier and facilitator across studies in SEA. Improving knowledge to screening among women facilitates CCS uptake while the lack of it represents a barrier. While these factors may represent key targets for intervention design, their differential impact across various contexts have been carefully considered [116]. Furthermore, the experience of different facilitators may have a greater influence on CCS uptake in a setting where barriers are commonly experienced by women. In a UK study, women with up-to-date CCS prioritized the following facilitators of CCS compared to those who had overdue or never had CCS: (1) Perceived benefits of CCS and (2) perceived self-responsibility over one's health [117]. On the other hand, the ranking of common barriers, such as fear and embarrassment did not differ by participants' screening history. The interplay of barriers and facilitators to CCS warrants further research, and the findings can be harnessed to guide interventions to increase CCS uptake. Therefore, we have presented barriers to CCS alongside its facilitators at the country level in this study.
The current systemic literature review has a few limitations. Firstly, the availability of evidence varies in SEA countries. A majority of the studies identified in the current review are from upper-middle income countries according to the World Bank criteria (Indonesia, Malaysia, and Thailand) [118], and fewer are published from lower-middle income countries (Myanmar, Cambodia, Vietnam, and Laos). In addition, there was no study from the Philippines and Timor-Leste. Although the common themes identified across SEA countries can provide insights into barriers to and facilitators of CCS in lowermiddle income countries in the region, we do think that country-specific studies are still necessary, owing to the cultural differences between countries. However, technical expertise may be lacking in some countries, which highlights the need for support from foundations or non-governmental organizations with interests in women's health. Secondly, we have applied an English language restriction in this review, while relevant articles may have been published in local languages. However, we assess its impact to be low as few studies (n = 3) were not published in English. Thirdly, the top barriers and facilitators identified in this review was based on publication numbers, which are dependent on previous researchers' study interest, as well as questionnaire or interview design, where selected factors may be explored more frequently. Nevertheless, this remains a common methodology employed to assess the importance of factors identified in barriers and facilitator reviews, especially when no acceptable standard practice guideline is available at present [116]. Lastly, the heterogeneity among studies limits us from assessing the effect size of each barrier or facilitator on CCS uptake. Such heterogenicity is anticipated and necessary, which highlights the need for culture-specific studies and interventions to address the diverse cultural contexts in SEA countries.

Conclusions
A significant number of barriers affect the uptake of cervical cancer screening. Coupled with a lack of resources and possibly low prioritization of cervical cancer, challenges to address these barriers remain. This is perhaps why women in SEA continue to face a high risk of cervical cancer mortality and morbidity while significant progress has been made in the developed world. This review of studies published in the SEA region from 1994 to 2020 identified that psychological-, emotional-, and knowledge-related factors remain a significant concern among women in SEA. Facilitating factors include receiving advice from healthcare workers for CCS, and factors associated to patient demographics. Future studies can explore the interplay of the barriers and facilitators on CCS and generate more insights into low-middle income countries in the region. Nevertheless, findings from this review may inform health policy makers in developing effective cervical cancer screening programs in SEA countries.

Supplementary Materials:
The following are available online at https://www.mdpi.com/article/10 .3390/ijerph18094586/s1, Table S1: Search strategy in each database. Table S2: Quality assessment of included studies using the Mixed Methods Appraisal Tool. Table S3: Barriers to cervical cancer screening in Southeast Asia. Table S4: Facilitators of cervical cancer screening in Southeast Asia. Figure S1: Factors described as barriers to and facilitators of cervical cancer screening in Southeast Asia, according to country and publication numbers.

Data Availability Statement:
No new data were created or analyzed in this study. Data sharing is not applicable to this article.