Barriers and Facilitators for Cervical Cancer Screening Among Young Women: A Systematic Review

Though an international We conducted a systematic review following PRISMA guidelines of four databases: Medline-OVID, EMBASE, CINAHL, and ClinicalTrials.Gov. Databases were examined from inception until the date of our literature searches (12/03/2020). We only examined original, peer-reviewed literature. Articles were excluded if they did not specically discuss cervical cancer screening, were not specic to young women, or did not report outcomes or evaluation. All screening, extraction, and synthesis was completed in duplicate with two independent reviewers. Outcomes were summarized descriptively. Risk of bias for individual studies was graded using an adapted rating scale based on the Risk of Bias Instrument for Cross-Sectional Surveys of Attitudes and Practices. Of the 2177 database we included 36 studies that met inclusion criteria. Our systematic review found that there are three large categories of barriers for young women: lack of knowledge/awareness, negative perceptions of the test, and practical barriers to testing. Facilitators included stronger relationships with healthcare providers, social norms, support from family, and self-ecacy.

The age cut-off of 35 years was determined based on previous literature regarding young women and cervical cancer screening. 8,12 We only examined original, peer-reviewed literature. Databases were examined from inception until the date of our literature searches (12/03/2020). Published conference posters, papers, and abstracts were eligible for inclusion. Articles were excluded if they did not speci cally discuss cervical cancer screening, were not speci c to young women, or did not report outcomes or evaluation. Eligibility criteria are outlined in Table 2.

Study Selection and Extraction
All steps of the systematic review were performed in duplicate. Study selection was completed by two independent, parallel reviewers (AK, SL) for both title and abstract screening as well as full-text screening. Data extraction was performed by two investigators (AK, SL), with a third (XL) resolving discrepancies. Outcomes were summarized descriptively. Risk of bias for individual studies was graded using an adapted rating scale based on the Risk of Bias Instrument for Cross-Sectional Surveys of Attitudes and Practices. 19

Search Yield
Results of the study screening process are available in the PRISMA diagram in Figure 1. Of the 2177 original database citations, 1563 records remained after duplicates were removed. After title and abstract screening, 226 were eligible for full-text evaluation. After a handsearch of relevant journals and citations, no additional studies were added. Of the 226 full-text articles, a total of 36 were included in the systematic review.
Inter-rater agreement for study screening for titles and abstracts was 94.54% with a kappa of 0.79. Inter-rater agreement for full-text screening was 96.2% with a kappa of 0.84, indicating substantial agreement.
The included study designs were largely qualitative and observational. The majority (25/36, 69.4%) included either surveys or questionnaires, with the remainder including either focus groups (7/36, 19.4%) or interviews (2/36, 5.6%). All studies were graded as medium risk for bias using the Risk of Bias Instrument for Cross-Sectional Surveys of Attitudes and Practices.
The 36 studies included a total of 14362 participants, with an average sample size of 410.3 (SD 662.7) participants per study. Around half (17/36, 47.2%) of studies speci cally targeted students. The average age of participants across all studies was 22.4 years (SD 4.5).
Details of the included studies are provided in Table 3.

Analysis of Notable Barriers
There were numerous barriers cited by the young women and adolescents regarding cervical cancer screening. The barriers can be grouped into three large groups: lack of knowledge/awareness, negative perceptions of testing, and practical barriers. Three studies [20][21][22] noted lack of physician recommendation, while one noted low overall health literacy of participants. 23 Misinformation included beliefs that young women were not susceptible in 4/36 studies, 20,24-26 that screening was not necessary if not currently experiencing symptoms, 27 and that the Pap test was not effective/reliable for screening cervical cancer. 28,29 Other misconceptions included that a male partner's circumcision prevented their need for cervical cancer screening. 30 In four studies, there was a fear that pelvic exams could "take one's virginity," reported in Ghana, Malaysia, and the United States. 21,23,24,31 ii) Negative Perceptions of Testing A large number of young women had fears and anxieties regarding the screening experience. Ten studies cited a fear of pain/discomfort during Pap smears, with 13/36 studies noting embarrassment of the intimate examination. Three studies noted the invasiveness of the procedure being of particular concern. 32-34 Male gender of physicians was also noted to impede motivation for screening in two studies. 32,35 Stigma around cervical cancer was noted in 4 studies, 23,30,33,36 with two of the studies reporting stigma around the general act of visiting a gynecologist's o ce. 23,33 Con dentiality was a concern noted in three studies, 37-39 with two speci cally noting privacy from parents. 37,39 Two studies discussed fear of side effects or complications from screening. 36,40 Five studies discussed fear regarding potential diagnosis of cancer as a barrier to screening. 34,38,39,41,42 iii) Practical Barriers to Testing There were a number of logistical barriers noted to accessing cervical cancer screening.
Six studies discussed low accessibility to services. 22,23,26,32,37,41 Participants reported di culties in nding a consistent healthcare provider, especially after moving away for work or school. 26,32 Di culties were also noted in rural areas with only a single provider 24 or locations with reduced access to female physicians. 32 Transportation was noted as a barrier in two studies. 39,43 Cost of screening services and nancial constraints were noted as a barrier in six studies, 20,21,24,[37][38][39] with two studies located in lower income countries (Ghana, Malaysia) and the remainder in the United States.
Time constraints were cited in three studies. 20,24,26 One study noted that participants preferred to schedule their appointments according to their menstrual cycle, which posed further limitations. 26

Analysis of Notable Facilitators
Many studies discussed facilitators and interventions that encouraged young women to undergo cervical cancer screening. Increased knowledge and awareness were noted in twelve studies. 24,26,28,30,33,34,36,39,42,[44][45][46] Speci c points of knowledge included severity of disease, 24,30 as well as the understanding that the test could allow successful prevention and treatment of cancer. 28 High self-e cacy and perceived control/empowerment about health was a facilitator in three studies. 43,47,48 Trusting and longitudinal relationships with their healthcare providers were noted as facilitators in four studies, 25,32,39,42 as was choice of healthcare provider speci cally 25 or testing by a female physician. 32 Hobbs et al 39 speci cally noted that physicians who were able to communicate well and put patients at ease acted as a facilitator. Alternative methods of screening such as self-sampling were noted as a facilitator of cervical cancer screening to avoid perceived invasiveness. 34,49 Social norms and public perceptions, including if friends and family members received testing, was noted as a facilitator. 20,29,33,37,46,48 A diagnosis of cervical cancer in the family was noted as a motivation for undergoing screening, 33 as well as support or encouragement from one's mother speci cally. 37 Media coverage was noted to encourage participation in cervical cancer screening, particularly if involving celebrities or public gures. 26,34 Facilitators to improve the logistical barriers of cervical cancer were analyzed. Five studies noted either telephone or written reminders would be helpful for patients. 25 Our study is the rst systematic review of barriers and facilitators to cervical cancer screening speci cally for young women and adolescents under the age of 35. While there have been calls to action regarding this topic, it has been di cult to characterize the breadth of young women's perspectives regarding screening. Our 36 included studies had a diverse spread of country locations across low-, middleand high-income countries in addition to a range of study populations. Barriers encompassed three groups: lack of knowledge/awareness, negative perceptions of the test, and practical barriers to testing. Facilitators included stronger relationships with healthcare providers, social norms, support from family, and self-e cacy.
Our results support the current literature base regarding the uptake of cervical cancer screening in young women. Young women face unique barriers and facilitators in comparison to older groups, necessitating age-speci c interventions. Our studies highlighted age-speci c barriers such as concern about privacy from parents, transportation di culties, and continuity of care after moving away for school. In addition, as this is typically the rst invasive procedure that young women undergo, there were concerns about pain, discomfort, and the intimacy of the pelvic exam. The young women who participated in these studies had helpful suggestions regarding age-speci c interventions, such as emailed reminders in comparison to written reminders, or screening provided on college campuses. Our literature also aligns with the greater research base regarding young people and low preventative service use in general, as many young people do not have a consistent family physician. 50,51 When comparing results internationally, we noticed that many themes were universally represented across income levels. There were accessibility concerns, cost concerns, and knowledge gaps in both lower and higher income countries. However, it is important to note that screening rates differ across the globe, and even within the same country for lower income and minority populations. As nancial constraints were cited as a frequent barrier in our included studies, it is not surprising that women from lower socioeconomic backgrounds have lower screening rates. 52,53 In addition, women from minority populations may have more strained relationships with the health system due to discrimination, lack of cultural competence, and the historic failure of medical systems to be equitable towards minority groups. 54,55 This is particularly relevant to cervical screening, as the patient's individual relationship with the health system was noted as an important barrier or facilitator towards screening. To increase cervical screening rates, it is important that we improve health system interactions overall to be more equitable.
Additionally, we noted that cultural barriers were discussed in several studies, including sex-negative beliefs. 23,30,34,36 Several studies highlighted a fear of hymen breakage with the pelvic exam, which has the societal stigma against virginity loss. 21,23,24,31 This concept was not only studied in Asia and Africa, but also included two studies from the United States. 23,31 It is important to educate about the concept of virginity as a social construct and improve sexual education for girls. In higher-income countries, language barriers, health literacy, and cultural beliefs were also noted as barriers among recent immigrants. Recent literature has shown that the "healthy immigrant effect" tends to taper off after several decades in a new country, with immigrants at higher risk of poor health outcomes and underuse of health services. 56,57 Speci c to cervical cancer, immigrant and minority populations in developed countries are at higher risk, often due to low screening rates. 58,59 Thus, interventions that target cervical screening uptake should have an intersectional approach in addressing these issues, rather than a "one size ts all" approach.

Strengths and Limitations
Strengths of our review include our systematic search of four databases using broad search criteria to maximize ndings. Studies were not excluded by basis of date of publication, country of origin, or language of origin. To capture the full breadth of explored research, conference abstracts were included. Our two parallel reviewers had high inter-rater agreement. We also included age ranges up to 35 years, based on what has been completed in previous literature. Limitations include that this review included qualitative studies that may have been limited by selection and publication bias, particularly for lower-income countries that may not be well-represented in academic research. In addition, cervical cancer screening guidelines (e.g. age to start screening) may differ depending on country, which may limit generalizability of results. Survey and interview results may also be compromised by reporting bias, if study participants are potentially embarrassed to discuss barriers or facilitators. More rigorous and systematic research with an equity-focused lens is recommended to generalize results to different populations and obtain higher quality information.

Next Steps and Implications for Care
Further research is required to characterize which interventions are the most effective for different age groups, including a diverse range of ethnicities, sexual orientations, educational backgrounds, and income levels. Moreover, we were surprised that none of the studies speci cally targetted the beliefs of non-heterosexual or non-cisnormative participants, as this has been documented as a growing public health concern and source of misinformation. [62][63][64][65] Studies regarding transgender men were eligible for study inclusion, but yielded no search results based on our protocol. Further speci c investigation is required to understand this topic, from both the perspective of the patient and the physician.
Our results were encouraging regarding potential solutions for improving cervical cancer screening uptake. While some barriers such as fear of cancer diagnosis or longstanding cultural beliefs are di cult to address, other barriers offer feasible solutions. Younger women may have less control in their lives regarding transportation and scheduling, particularly when coordinating with parents, babysitting siblings, or school schedules. It was remarkable how many small changes, such as written reminders, pamphlets, or linking screening with other appointments, were noted to act as facilitators. In addition, multiple misconceptions about cervical cancer screening still persist, such as the belief that screening is only required if a patient is experiencing symptoms. Our studies suggested the effectiveness of awareness campaigns that are speci cally aimed at younger people. Campaigns targeting the parents of younger girls, particularly mothers, may also be important as studies noted that parental support was a facilitator for screening.
Through addressing the above barriers and facilitators, health systems worldwide can hopefully address the much-touted goal of zero preventable deaths from cervical cancer. Young women who undergo screening are more likely to continue the practice as a lifelong habit as well as later recommend the practice to their children and peers. [8][9][10][11] They are also more likely to espouse positive beliefs about the health system, sex-positive beliefs, and regain empowerment regarding their health. 60,61 As such, every young woman who is screened offers a chance of strengthening a community around women's health.

Conclusion
Our comprehensive systematic review found that there are three large categories of barriers for young women: lack of knowledge/awareness, negative perceptions of the test, and practical barriers to testing. Facilitators included stronger relationships with healthcare providers, social norms, support from family, and self-e cacy. Health systems worldwide should address the above barriers and facilitators to increase cervical cancer screening rates in young women.

Declarations
Ethics approval and consent to participate: Not applicable Consent for publication: Not applicable Availability of data and materials: The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.  (youth* or adolescen* or (young adj2 (adult* or person* or individual* or people* or population* or wom#n)) or youngster* or college* or university*).ti,ab. or adolescent/ or young adult/ 10 (barrier* OR facilitator* OR perception* OR perspective* OR utilization* OR view*).ti,ab.  PRISMA Diagram

Supplementary Files
This is a list of supplementary les associated with this preprint. Click to download. PRISMAChecklistcervicalcancer2020.doc