Trends and Determinants in Uptake of Cervical Cancer Screening in Spain: An Analysis of National Surveys from 2017 and 2020

Simple Summary Cervical cancer is the fourth leading cause of death and morbidity in women worldwide. Although screening is a successful technique for lowering these rates, there are still great differences in screening adherence in Spain. The aims of this study were to examine the evolution of cytology screening adherence from 2017 and 2020 and to identify the factors associated with uptake among women in Spain. We found that 73.18% of women had received a cytology test during the previous three years. From 2017 and 2020, there was an increase in cytology screening participation among women aged 45–65 years. Foreigners were less likely to have a cytology test. The characteristics associated with cervical cancer screening that we discovered have significant value for public health initiatives, as they will assist health professionals in identifying women who are less likely to undergo screening and encouraging these women to do so. Abstract Cervical cancer rates have declined in industrialized nations as a result of cytology screening programs. However, there are still sizeable differences in screening adherence in Spain. This study aimed to identify the prevalence of cervical cancer screening among women in Spain, to analyze trends in that prevalence from 2017 and 2020 and to identify socio-demographic, health, and lifestyle factors related with adherence to this screening test. We conducted a cross-sectional study of 13,619 women aged 25–65 who participated in the 2017 Spanish National Health Survey and the 2020 European Health Survey for Spain. We used logistic regression to examine the relationship between socio-demographic, health and lifestyle factors and cervical cancer adherence. The prevalence of adherence was 73.18%. Additionally, there was a significant decrease in cervical cancer screening uptake from 2017 and 2020 among women aged 25–44 years (2017: 77.80%, 2020: 75.20%, p = 0.02), but an increase in the age group of 45–65 years (2017: 68.93%, 2020: 72.39%, p < 0.01) and in foreigners (2017: 64.29%, 2020: 72.29%, p < 0.01). Screening for cervical cancer is related with age, educational level, social class, insurance status, visits to the family doctor, alcohol consumption and free time physical exercise.


Introduction
Cervical cancer is probably the most thoroughly studied and preventable human cancer [1]. However, it remains the fourth most common cancer and the fourth leading cause of cancer mortality in women, with an estimated 604,000 new cases and 342,000 deaths globally in 2020 [2]. In 2020, low-and middle-income countries accounted for over 90% of new cases and deaths worldwide [2]. Furthermore, while the incidence of cervical cancer has declined over time in Western Europe, particularly in Spain [3], which has one of the vical cancer have never had any cytology testing [19], are what prompted us to conduct the current study, which aimed to identify the prevalence of cervical cancer screening among women in Spain, to analyze trends in that prevalence from 2017 and 2020 and to identify socio-demographic, health, and lifestyle factors related with adherence to this screening test.

Materials and Methods
To conduct this cross-sectional study, we used secondary data from the 2017 Spanish National Health Survey (SNHS) [20] and the 2020 European Health Interview Survey for Spain (EHIS) [21]. Both surveys were conducted from October 2016-October 2017 and July 2019-July 2020, respectively, by the National Statistics Institute under the supervision of the Spanish Ministry of Health and Social Affairs. These surveys were carried out by applying home-based personal interviews on a countrywide, representative sample of non-institutionalized subjects aged 15 years and older who had their main family residence in Spain. The team who administered the survey had previously been taught fundamental communication skills, associated processes, and in particular questionnaire training. Before taking the surveys, all the participants completed informed consent forms. More information on the methodology of SNHS 2017 and EHIS 2020 is available elsewhere [22,23].
The following samples of women aged 25-65 were chosen based on the screening guideline age groups [16]: 7695 women in SNHS 2017 and 6914 in EHIS 2020. Despite having similar characteristics to the other women, 990 participants (7.13%) were eventually discarded from the sample because they were unwilling to complete the questionnaires (SNHS 2017: n = 441; EHIS 2020: n = 549).
Our study includes the self-reported responses from these surveys. The variables we used were based on many of the items contained in the questionnaires, which were the same in all the surveys. The dependent variable was cervical cancer screening uptake, which was measured by asking "Have you ever had a cytology test?" Those who answered yes were then asked, "When was the last time you had a cytology test?". Following the classification of the women who followed the recommended screening period [16], those who admitted to having their most current cytology within the previous three years were referred to as "uptakers". The other women were referred to as "non-uptakers" (Figure 1).
As independent variables, we examined socio-demographic, health, and lifestyle factors. Age group (25-44, 45-65 years), educational level (without studies, primary, secondary, university), marital status (single, married, widowed, separated or divorced), social class (upper, middle, lower) [24], place of residence (rural/urban) [25] and nationality (Spanish/foreigner) were socio-demographic characteristics. In terms of health, their self-assessed state of health (very good, good, average, bad, very bad), insurance status (public/private) and visits to the family doctor in the preceding four weeks (yes/no) were all considered. The presence of physician-diagnosed mental illnesses, such as chronic anxiety or chronic depression, as well as other psychiatric disorders, was measured by self-reporting. Any woman who was diagnosed with one or more of these three illnesses was termed as "suffering from mental condition". Finally, body mass index (underweight, normal weight, overweight, obesity) [26], tobacco habit (yes, no), alcohol consumption in the previous year (yes, no) and free time physical exercise (yes, no) were used to measure lifestyle behaviors.
The qualitative variables were reported in terms of frequencies and percentages, while the quantitative variables were expressed in the form of mean and standard deviation (SD). To draw comparisons, the Chi-squared test was applied (from 2017 to 2020, Chi-squared trend analysis was employed widely to discover significant trends in cytology adherence). We also carried out a multivariable analysis to identify which characteristics were independent predictors of cervical cancer screening adherence, and we used the crude and adjusted odds ratio (OR), with their respective 95% confidence intervals, to assess the strength of association. The Hosmer-Lemeshow test was used to evaluate the quality of fit, and to measure the goodness of fit, we examined the adjusted coefficient of determination (R 2 ), the F statistic and the normality of the residues. The multivariate model contained only covariates which had a possible association (p ≤ 0.15) with the dependent variable, and non-significant variables were discarded using backward selection based on the likelihood of the Wald statistic. The level of statistical significance was set at α = 0.05. SPSS 25.0 software, licensed to the University of Córdoba (Spain), was used to carried out the statistical analysis. The research data are included in the Supplementary File S1. As independent variables, we examined socio-demographic, healt tors. Age group (25-44, 45-65 years), educational level (without studie ary, university), marital status (single, married, widowed, separated o class (upper, middle, lower) [24], place of residence (rural/urban) [2 (Spanish/foreigner) were socio-demographic characteristics. In terms o assessed state of health (very good, good, average, bad, very bad), insu

Results
We evaluated the data from 13,619 women residing in Spain aged 25 to 65 years old. Most of these women were between the ages of 45 and 65 (57.19%), belonged to the lower socioeconomic class (45.37%) and did free time physical exercise (63.93%) ( Figure 2). carried out the statistical analysis. The research data are included in the Supplementary File S1.

Results
We evaluated the data from 13,619 women residing in Spain aged 25 to 65 years old. Most of these women were between the ages of 45 and 65 (57.19%), belonged to the lower socioeconomic class (45.37%) and did free time physical exercise (63.93%) ( Figure 2).  Table 1 shows the rates of cervical cytology uptake based on socio-demographic factors, health-related characteristics, and lifestyle habits. A higher uptake rate for cervical cytology was found in the youngest age group, those who were married, with university studies, belonging to the upper social class, of Spanish nationality, without mental illness, with private health insurance, those who visited a general practitioner in the four weeks preceding survey completion, were of normal weight, had consumed alcohol in the previous year and did physical activity during leisure time.   Table 1 shows the rates of cervical cytology uptake based on socio-demographic factors, health-related characteristics, and lifestyle habits. A higher uptake rate for cervical cytology was found in the youngest age group, those who were married, with university studies, belonging to the upper social class, of Spanish nationality, without mental illness, with private health insurance, those who visited a general practitioner in the four weeks preceding survey completion, were of normal weight, had consumed alcohol in the previous year and did physical activity during leisure time. In the previous three years, 73.18% of women between 25 and 65 years had undergone cervical cytology ( Figure 3). There were no variations in cytology testing from 2017 to 2020 (2017: 72.87%, 2020: 73.54%, p = 0.38). From 2017 and 2020, we observed an increase in the prevalence of cytology test adherence in foreigners (2017: 64.29%, 2020: 72.29%, p < 0.01) ( Table 2).  There were no variations in cytology testing from 2017 to 2020 (2017: 72.87%, 2020: 73.54%, p = 0.38). From 2017 and 2020, we observed an increase in the prevalence of cytology test adherence in foreigners (2017: 64.29%, 2020: 72.29%, p < 0.01) ( Table 2).  Figure 4 illustrates the age-group distribution of cervical cytology screening adherence from 2017 and 2020. Women aged between 45 and 65 years old reported more frequently   Figure 4 illustrates the age-group distribution of cervical cytology screening adherence from 2017 and 2020. Women aged between 45 and 65 years old reported more frequently having undergone cytology screening in 2017 than in 2020 (2017: 68.93%, 2020: 72.39%, p < 0.01). However, adherence to cervical cytology decreased across the study years in women aged 25 to 44 (2017: 77.80%, 2020: 75.20%, p = 0.02).  Table 3 shows the crude and adjusted ORs allowing for the identification of determinants of cervical cytology test adherence in the study population. Positive predictors were:

Main Findings
The current study analyzed cervical cytology screening adherence in Spain from 2017 and 2020 and shows predictors of cervical cytology testing in a nationally representative sample of women aged 25 to 65. The study also describes the characteristics of women who did not undergo cytology testing.
In our study, 73.18% of the women surveyed reported undertaking a cervical cytology in the previous three years. This finding is very similar to the cytology uptake value previously reported in Spanish women [27] and may be due to the growing efforts by the Spanish Health System to raise awareness of the benefits of screening for cervical cancer [28]. Moreover, that adherence meets one of the World Health Organization's stated objectives for 2030 for nations to target the elimination of cervical cancer: 70% of women screened by the age of 35, and again by the age of 45 [29]. Additionally, testing rates vary widely across Europe. The current study's cervical cytology screening uptake rate lies midway between Northern European nations (ranging from 67% to 94%) and Eastern European countries, which have the lowest prevalence of cytology adherence (10.3%) [30,31]. Nevertheless, in response to the COVID-19 pandemic, screening activities in Spain were reasonably postponed, the priority of periodic cervical cancer screening decreased, and Pap smears were significantly than in March 2019, all of which could have a negative impact on the adherence to cytology screening.
We also looked into potential variables linked to cervical cancer screening uptake, one of the most important of which was age. Our findings revealed that being between the ages of 25 and 44 was related with increased uptake. This is consistent with other findings [32,33], and may be related partly to reproductive years. Younger women may have more frequent gynecologic requirements due to family planning, which may necessitate more frequent examinations and testing, and physicians may be more actively recommending this age group to screen more regularly [34]. Nevertheless, when analyzing the changes from 2017 and 2020, the prevalence of cervical cancer screening adherence differed by age group of women: we observed a reduction in cytology screening uptake among women aged 25-44 and the opposite among those aged 45-65. The decline in screening adherence among younger women over time is especially concerning because women who are screened from an early age receive the most benefit from cervical cancer screening [35]. Here, there is evidence that HPV self-sampling has the potential to increase access to and adoption of screening globally [36], and in fact, self-sampling is now being tested in Spain [37]. Moreover, a number of education techniques, such as phone calls, mailings or group discussion, have been found to be highly successful in increasing cervical cancer compliance [38].
Lower cervical cancer screening rates are linked to a variety of socioeconomic conditions [39]. In general, women with a high level of education and those belonging to higher social status are more likely to undergo cervical cytology [5,[40][41][42], which is consistent with the findings from the current study. The link between educational attainment and access to information about cancer screening or the ability to make informed decisions could explain the association between educational level and cervical cancer screening adherence [43], whereas social class is related to the accessibility of cervical cancer screening [44]. These results should be interpreted in the light of the European Union's problem of overscreening for cervical cancer, which is notably prevalent among women with better socioeconomic level [45].
Across nationality groups, and as previously documented in other research [46,47], our findings demonstrated reduced cervical screening adherence among immigrant women. This is an important public health issue, and a wide range of sociodemographic and psychological factors, such as language difficulties, high mobility, difficult working conditions, and low risk perception, can all contribute to reduced immigrant screening uptake [48][49][50][51]. Surprisingly, our analysis found an increasing trend in the screening of immigrant women from 2017 to 2020. Spain saw an increase in its immigrant population from 2017 and 2020, with the majority coming from South America (2017: 30.64% and 2020: 34.97%) and Morocco (2017: 8.56% and 2020: 10.66%) [52]. Due to a concurrent expansion in population-based cervical screening programs in the different autonomous communities of Spain in those research years, immigration may have played a role in the observed increase in cervical cancer screening uptake over time [18]. Additionally, immigrant-specific cervical cancer screening interventions have been implemented in recent years to motivate this population to participate in screening programs, including ongoing dialogues with the family and community support, removing the social stigma of cervical cancer screening, improving women's awareness and ability to navigate the health care system (e.g., by translating screening messages into more familiar languages) or providing transportation [18]. We were unable to shed more light on the characteristics of lower adherent migrants due to a lack of data on their migration (time since migration or place of birth). Since there are few studies on the factors which promote and impede participation in cervical cancer screening among migrant women in Spain, further work is needed in this area.
Health insurance coverage is a significant predictor of participation in cancer screening [53]. According to our findings, women with supplementary private health insurance reported more frequently that they had had a screening in the last three years. This extra insurance provides access to specialized and preventative health care services with shorter waiting lists than public services, which contributes to increased uptake [54]. Furthermore, it is possible that having additional private insurance is related to other factors that may influence screening uptake, such as belonging to a privileged social class, the value placed on health or the insured person's knowledge of the health system [55], all of which increase the expected value of a screening test. Although the results in our study linking having supplementary insurance and higher compliance with cervical cancer screening are supported by the literature [56], some studies showed no such link [42,57]. It is particularly interesting to note that earlier studies have also shown that women with private insurance are more likely to report that they have not undergone screening [33,58]. This disparity might be explained by the fact that women with private insurance do not have a referral from a health care professional.
As previously described by other authors [42], frequent visits to the general practitioner positively impacted adherence to cervical cytology in the current research. As general practitioners provide health services that are closest to the community, they are respected, trusted members of the local community and may play an important role in health communication, such as mobilizing people to take part in screening programs [59].
In terms of lifestyle habits, women residing in Spain were shown to be more likely to undergo screening for cervical cancer if they consumed alcohol and engaged in physical activity during their free time. In Spain, moderate alcohol use is common among women with a high socioeconomic status, which is linked to greater utilization of cancer screening [27]. Although our results are in keeping with earlier research [35,60], data on the effect of alcohol use on cervical cancer screening adherence are conflicting. Some authors found no association [61,62], while others discovered a negative association [27]. According to these findings, further studies are needed to clarify the association between alcohol use and screening participation. Regarding physical activity, studies conducted in Lithuania and Spain found a beneficial effect on screening uptake [27,35]. It was expected that women who engaged in healthy activities would be more health conscious than those who engaged in unhealthy behaviors, and hence more likely to participate in cancer screening [63]. It is noteworthy that contradictory findings on this association have been reported, such as high rates of screening uptake among women who do little physical activity [64], implying that primary prevention programs should target all the populations, including those with healthy habits, rather than just those who lead more unhealthy lifestyles.

Strengths and Limitations
One of the major strengths of this study is the use of a large, nationally representative sample of women, which contributes to the generalizability of the findings. Nevertheless, there are also a number of study limitations. First, since this study has a cross-sectional design, the causality of associations cannot be determined. The second limitation is the information and social desirability bias, which may lead to an overestimation of cervical cancer screening adherence. Finally, because of the varied sources of uptake data, as well as the coexistence of different types of screening programs in different countries and their target populations, comparisons should be made with caution.

Implications for Research and Practice
The World Health Organization strategy for cervical cancer elimination suggests that each country should meet the 90-70-90 targets by 2030 (coverage of 90% of girls vaccinated, 70% of women screened, and treatment of 90% of women identified with cervical disease). Nevertheless, obtaining and maintaining the second target would be one of the most significant issues for many low-and middle-income countries [65]. Findings of our study may be useful in achieving that target recognizing and addressing the factors that are likely to influence women's disposition towards cervical cancer screening in order to explore focused interventions as effective ways to promote cervical cancer screening adherence. In high-income countries where some of these targets have been met, previous studies have shown that improvements in test performance and screening coverage have a greater effect on elimination timing than increases in vaccination coverage [66,67]. The results of the current study revealed population categories with low screening adherence that may be appropriate target groups for intervention to encourage screening behaviors for detecting cervical cancer in these countries.
On the other hand, health providers must be aware of the sectors of the population at high risk of non-participation and urge screening among these women. Moreover, communication skills, as well as the ability to gather information, are required to raise women's awareness of the etiology of cervical cancer, HPV infection, preventative strategies, and early detection. It would also be desirable to analyze the influence of the HPV vaccination on uptake of cervical cancer screening programs, as well as the efficiency of the vaccine in decreasing cervical cancer incidence and mortality, when further years of follow-up data from the cohort of immunized Spanish women become available.

Conclusions
In Spain, the adherence rate for cervical cancer screening is 73.18%. Despite the fact that adherence has increased in recent years among women aged 45-65 and foreigners, discrepancies based on many socio-demographic, health, and lifestyle variables remain. Age between 25 and 44, higher educational level, higher social status, private health insurance, frequent visits to the general practitioner, alcohol use, and physical activity are all positive predictors of cervical screening uptake, but immigration is a negative predictor.
Funding: This research received no external funding.
Institutional Review Board Statement: Ethical review and approval were waived for this study, due to according with Spanish legislation, when secondary data are used, there is no need for approval from an Ethics Committee.
Informed Consent Statement: Informed consent was obtained from all subjects involved in the study.

Data Availability Statement:
The data presented in this study are available as Supplementary Material (File S1: Research data).