Prevalence and determinants in cytology testing for cervical cancer screening in Spain (2006–14)

Prevalence and determinants in cytology testing for cervical cancer screening in Spain (2006–14) Abstract Background Cervical cancer has decreased in developed countries thanks to cytology screening programmes. The aims of this study were To analyse the frequency and evolution of performing cytology tests and to determine the variables that influence their use. Methods Cross-sectional study of non-institutionalized women who participated in the national health survey (2006, 2011/12) and the European Health Survey in Spain (2009, 2014). Study variables: cytology-testing, time since last cytology-test, reason for performing the test, age, nationality, marital status, social status, education level and place of residence. Results The study evaluated 53 628 women in Spain over 15 years old, with a mean age of 52.68 (SD ± 19.12). About 94.1% were Spanish, 49.2% were married and 77.2% lived with a partner. In 2014, 72% had a cytology test, a number that increased significantly. Women aged 25–65 were 5.13 times more likely to undergo a cytology test than those aged 15–24 years old (odds ratio (OR): 5.13; P < 0.001); women with university educations were 9.23 times more likely to undergo a cytology test than those without university educations (P > 0.001); those of social classes I and II (high) were 1.2 more likely to undergo a cytology test than those of low social class (P = 0.026); and Spanish women were 1.74 times more likely to undergo a cytology test than foreigners living in Spain (P < 0.001). Conclusion Frequency of cytology testing has increased in the last few years. Screening for cervical cancer is associated with higher social status, education level, age, and not being foreign. Introduction Cervical cancer has a high incidence worldwide, being the third most frequent type of cancer in women and the second cause of cancer-related mortality in women.1,2 In 2012, approximately 527 600 cases were diagnosed worldwide. The incidence varies between countries, with developing countries having the highest incidence (444 500 deaths). The worldwide mortality due to cervical cancer is 265 700 deaths and is also higher in developing countries (230 200 deaths).2,3 In USA, it was estimated that in 2016, 12 990 cases would be diagnosed, with 4120 deaths from cervical cancer.1 In Western European countries, the incidence has been decreasing,4,5 especially in Spain, which has the lowest occurrence of cervical cancer.5,6 However, the incidence has increased in the countries of Eastern Europe.5–7 Generally, in developed countries, although the incidence of cervical cancer in older women (> 55 years) has declined, there has been an increase in younger women aged 30–35 years.4,8,9 These differences in the incidence of cervical cancer among different countries (developed and developing) can be explained by the inequality of health systems’ capacities to establish programmes for the early detection of cancerous lesions and human papillomavirus (HPV) infection.2,9 Cervical cancer is associated with HPV infection.10 The prevalence of HPV infection also differs among countries, varying from 9 to 21% in Africa, Latin America and Southeast Asia to approximately 5% in the United States.11 In Spain, in recent years, the prevalence of HPV infection has increased to 14.3%, of which 28.8% are women between 18 and 25 years old.12 This increase in recent years may be due to changes in the sexual behaviour of young women (i.e. sexual initiation at earlier ages and greater numbers of sexual partners).13 Screening programmes have been in place in Europe since the 1980 s, Norway, Finland and the Netherlands were the first ones.14 In the different countries where population-based screening programmes have been established (the Netherlands,15 Italy,16 Denmark,4 Norway14 and Sweden14), the mortality due to cervical cancer has been reduced. As mentioned previously, Spain is among the countries with the lowest rates of cervical cancer,5 which is the reason because population-based screening programmes have not been scheduled.17 The cervical cancer screening programmes are opportunistic (on demand), although specific screening and follow-up guidelines for low- and high-risk women are followed.17 Given that the screening programmes are opportunistic and given the change in the patterns of sexual behaviour in Spanish women (which may be the cause of the increasing incidence of HPV infections), it is of interest to know the frequency of cervical cytology testing and to assess the sociodemographic profiles that may influence adherence to early detection behaviours. The study aims are: (i)to analyse the frequency of cervical cytology testing in women in Spain and to evaluate the evolution in the period from 2006 to 2014; (ii) to describe the sociodemographic profile of the women who are tested; and (iii) to determine the variables that influence having cytology tests performed. Methods This is a descriptive cross-sectional study. A total of 53 628 women aged 15 years and older residing in Spain were selected from the two main sources of data: the National Health Survey (NHS) 200618 and 201119 in Spain and the European Health Survey of Spain (EHSS) for the years 200920 and 2014.21 These surveys were conducted by the Instituto Nacional de Estadística (National Institute of Statistics; NIS) in collaboration with the Ministerio de Sanidad, Servicios Sociales, e Igualdad (Spanish Ministry of Health, Social Services, and Equality). Both surveys had a cross-sectional and population-based design, with stratified three-point representative sampling, and were conducted at the national level, focusing on the non-institutionalized population residing in Spain, through an interview. The sampling procedure was multi-stage and stratified by clusters, with the selection of primary sampling units (municipalities) and secondary units (sections) in a proportional random fashion and the last units (individuals) by random routes and sex and age quotas. The data are available to any researcher on the NIS website in the form of an anonymous microdata file. For the current study, all the records corresponding to women were selected: NHS 200618 (17 833); EHSS 200919 (12 143); NHS 2011/1220 (11 358) and the EHSS 201421 (12 294); therefore, no authorizations for its use are required. The microdata files18–21 were downloaded and processed in a single database. The dependent variables of the study were (i) cytology test performed; (ii) frequency of performing the test (less than 3 years, between 3 and 5 years, more than 5 years); and (iii) reason for performing the test (‘for some problem, symptom, or illness’; ‘on the advice of your primary care physician or specialist’; ‘because you received a letter or phone call or was asked at your health centre if you wanted to be tested’; and ‘other’). Sociodemographic variables included age, nationality, education level, social status, job, marital status, current cohabitation and residency. Social class was stratified into three levels: high class (level I: directors and managers of companies with 10 or more employees and professionals with university degrees; level II: directors of companies with less than 10 employees and professionals with college diplomas); medium class (level III: intermediate occupations; level IV: workers in qualified technical occupations); and low class (level V: primary sector workers, level VI: unskilled workers).18–21 For the data analysis, we used IBM SPSS version 22.0 (IBM Corp., Armonk, NY, USA), a statistical program licensed for use from the Universidad de Castilla la Mancha (University of Castilla la Mancha). In the descriptive analysis of the qualitative variables, counts (n) and percentages (%) were used, and for the quantitative variables, means (m) and standard deviations (SD) were used. A χ2 test was used for the comparison of categorical variables. A multiple logistic regression was performed to determine the influence of the variables in having a cytology test performed. The ORs were calculated with their confidence intervals. A level of significance was set at P = 0.05 for all tests and comparisons. Results The records of 53 628 women residing in Spain over 15 years of age were analysed, resulting in a mean age of 52.68 (SD ± 19.12). A total of 94.1% of the women were Spanish, 49.2% were married and 77.2% lived with a partner. Table 1 shows the sociodemographic variables with respect to the survey years (table 1). Table 1 Women’ Sociodemographic characteristics, older than 15 years, in Spain (2006–2014)   2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)    Nationality  0.109      Spanish  Not registered  11 411 (94.0%)  10 662 (93.9%)  11 614 (94.5%)        Foreign    732 (6.0%)  696 (6.1%)  680 (5.5%)  Age        15–24 years  1120 (6.2%)  813 (6.7%)  814 (7.2%)  834 (6.8%)        25–65 years  11 904 (66.8%)  7842 (64.6%)  7022 (61.8%)  7766 (63.2%)  <0.001      >65 years  4809 (27.0%)  3488 (28.7%)  3522 (31.0%)  3694 (30%)    Civil status  <0.001  Single    2811 (23.2%)  2754 (24.2%)  2830 (23%)    Married  Not registered  6069 (50%)  5506 (48.5%)  6049 (49.2%)  Widower    2398 (19.7%)  2287 (20.1%)  2429 (19.8%)  Separated    372 (3.1%)  298 (2.6%)  315 (2.6%)  Divorced    488 (4%)  500 (4.5%)  655 (5.3%)  Do not know/answer    5 (0.0%)  13 (0.1%)  16 (0.1%)  Cohabitation        Yes    6581 (54.2%)    6090 (49.5%)        No  Not registered  5552 (45.7%)  Not registered  6123 (51.5%)  <0.001  Level study  <0.001  No studies    2485 (20.5%)    4788 (38.9%)    Primaries  Not registered  4746 (39.3%)  Not registered  3511 (28.6%)  High school/FP    2828 (23.3%)    1584 (12.9%)  University    1064 (16.9%)    2.411 (19.6%)  Level Social  <0.001      Classes I–II  3231 (18.6%)    1938 (18.0%)  2310 (19.5%)        Classes III–IV  9055 (52.3%)  Not registered  3499 (32.6%)  3901 (32.9%)      Classes V–VI  5039 (29.1%)    5307 (49.4%)  5658 (47.6%)    2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)    Nationality  0.109      Spanish  Not registered  11 411 (94.0%)  10 662 (93.9%)  11 614 (94.5%)        Foreign    732 (6.0%)  696 (6.1%)  680 (5.5%)  Age        15–24 years  1120 (6.2%)  813 (6.7%)  814 (7.2%)  834 (6.8%)        25–65 years  11 904 (66.8%)  7842 (64.6%)  7022 (61.8%)  7766 (63.2%)  <0.001      >65 years  4809 (27.0%)  3488 (28.7%)  3522 (31.0%)  3694 (30%)    Civil status  <0.001  Single    2811 (23.2%)  2754 (24.2%)  2830 (23%)    Married  Not registered  6069 (50%)  5506 (48.5%)  6049 (49.2%)  Widower    2398 (19.7%)  2287 (20.1%)  2429 (19.8%)  Separated    372 (3.1%)  298 (2.6%)  315 (2.6%)  Divorced    488 (4%)  500 (4.5%)  655 (5.3%)  Do not know/answer    5 (0.0%)  13 (0.1%)  16 (0.1%)  Cohabitation        Yes    6581 (54.2%)    6090 (49.5%)        No  Not registered  5552 (45.7%)  Not registered  6123 (51.5%)  <0.001  Level study  <0.001  No studies    2485 (20.5%)    4788 (38.9%)    Primaries  Not registered  4746 (39.3%)  Not registered  3511 (28.6%)  High school/FP    2828 (23.3%)    1584 (12.9%)  University    1064 (16.9%)    2.411 (19.6%)  Level Social  <0.001      Classes I–II  3231 (18.6%)    1938 (18.0%)  2310 (19.5%)        Classes III–IV  9055 (52.3%)  Not registered  3499 (32.6%)  3901 (32.9%)      Classes V–VI  5039 (29.1%)    5307 (49.4%)  5658 (47.6%)  Notes: N: count; P: significance of the χ2 test; PF: professional formation. Table 1 Women’ Sociodemographic characteristics, older than 15 years, in Spain (2006–2014)   2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)    Nationality  0.109      Spanish  Not registered  11 411 (94.0%)  10 662 (93.9%)  11 614 (94.5%)        Foreign    732 (6.0%)  696 (6.1%)  680 (5.5%)  Age        15–24 years  1120 (6.2%)  813 (6.7%)  814 (7.2%)  834 (6.8%)        25–65 years  11 904 (66.8%)  7842 (64.6%)  7022 (61.8%)  7766 (63.2%)  <0.001      >65 years  4809 (27.0%)  3488 (28.7%)  3522 (31.0%)  3694 (30%)    Civil status  <0.001  Single    2811 (23.2%)  2754 (24.2%)  2830 (23%)    Married  Not registered  6069 (50%)  5506 (48.5%)  6049 (49.2%)  Widower    2398 (19.7%)  2287 (20.1%)  2429 (19.8%)  Separated    372 (3.1%)  298 (2.6%)  315 (2.6%)  Divorced    488 (4%)  500 (4.5%)  655 (5.3%)  Do not know/answer    5 (0.0%)  13 (0.1%)  16 (0.1%)  Cohabitation        Yes    6581 (54.2%)    6090 (49.5%)        No  Not registered  5552 (45.7%)  Not registered  6123 (51.5%)  <0.001  Level study  <0.001  No studies    2485 (20.5%)    4788 (38.9%)    Primaries  Not registered  4746 (39.3%)  Not registered  3511 (28.6%)  High school/FP    2828 (23.3%)    1584 (12.9%)  University    1064 (16.9%)    2.411 (19.6%)  Level Social  <0.001      Classes I–II  3231 (18.6%)    1938 (18.0%)  2310 (19.5%)        Classes III–IV  9055 (52.3%)  Not registered  3499 (32.6%)  3901 (32.9%)      Classes V–VI  5039 (29.1%)    5307 (49.4%)  5658 (47.6%)    2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)    Nationality  0.109      Spanish  Not registered  11 411 (94.0%)  10 662 (93.9%)  11 614 (94.5%)        Foreign    732 (6.0%)  696 (6.1%)  680 (5.5%)  Age        15–24 years  1120 (6.2%)  813 (6.7%)  814 (7.2%)  834 (6.8%)        25–65 years  11 904 (66.8%)  7842 (64.6%)  7022 (61.8%)  7766 (63.2%)  <0.001      >65 years  4809 (27.0%)  3488 (28.7%)  3522 (31.0%)  3694 (30%)    Civil status  <0.001  Single    2811 (23.2%)  2754 (24.2%)  2830 (23%)    Married  Not registered  6069 (50%)  5506 (48.5%)  6049 (49.2%)  Widower    2398 (19.7%)  2287 (20.1%)  2429 (19.8%)  Separated    372 (3.1%)  298 (2.6%)  315 (2.6%)  Divorced    488 (4%)  500 (4.5%)  655 (5.3%)  Do not know/answer    5 (0.0%)  13 (0.1%)  16 (0.1%)  Cohabitation        Yes    6581 (54.2%)    6090 (49.5%)        No  Not registered  5552 (45.7%)  Not registered  6123 (51.5%)  <0.001  Level study  <0.001  No studies    2485 (20.5%)    4788 (38.9%)    Primaries  Not registered  4746 (39.3%)  Not registered  3511 (28.6%)  High school/FP    2828 (23.3%)    1584 (12.9%)  University    1064 (16.9%)    2.411 (19.6%)  Level Social  <0.001      Classes I–II  3231 (18.6%)    1938 (18.0%)  2310 (19.5%)        Classes III–IV  9055 (52.3%)  Not registered  3499 (32.6%)  3901 (32.9%)      Classes V–VI  5039 (29.1%)    5307 (49.4%)  5658 (47.6%)  Notes: N: count; P: significance of the χ2 test; PF: professional formation. Table 2 shows the cytology tests conducted in different years. There was a significant increase in cytology testing in 2014 with respect to the other years. In addition, in 2012 and 2014, the reasons for testing changed, increasing due to the receipt of a letter advising testing and due to symptomatology (table 2). Table 2 Cytology testing analysed in the period 2006–2014 in Spain   2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)  Have you ever had a cytology test?  < 0.001      Yes  11815 (66.3%)  8624 (71.0%)  7953 (70.0%)  9005 (73.2%)      No  5, 882 (33.0%)  3, 324 (27.4%)  3, 139 (27.6%)  3, 114 (25.3%)  Do not know/answer  136 (0.8%)  195 (1.6%)  266 (2.4%)  175 (1.5%)  Reason for cytology test  < 0.001      For some problem, symptom or illness  849 (7.2%)  462 (5.4%)  952 (12.0%)  937 (10.5%)      On the advice of your AP doctor or specialist, although you had no problem  9326 (78.9%)  6287 (72.9%)  4461 (56.1%)  5754 (63.9%)      Because you received a letter, someone called you, or you were asked at your health centre if you wanted to do this test  569 (4.8%)  950 (11.0%)  1426 (17.9%)  1346 (14.9%)      Other reasons  990 (8.4%)  890 (10.3%)  1093 (13.7%)  954 (10.6%)      Do not know/answer  81 (0.7%)  35 (0.4%)  24 (0.4%)  14 (0.1%)  Testing frequency  <0.001      3 years or less  8425 (71.3%)  6085 (70.6%)  5911 (74.3%)  6528 (72.5%)      Between >3 and 5 years  439 (3.7%)  1064 (12.3%)  795 (10%)  797 (8.9%)      More than 5 years  2742 (23.2%)  1430 (16.6%)  1201 (15.1%)  1637 (18.2%)      Do not know/answer  209 (1.8%)  45 (0.5%)  46 (0.6%)  43 (0.5%)    2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)  Have you ever had a cytology test?  < 0.001      Yes  11815 (66.3%)  8624 (71.0%)  7953 (70.0%)  9005 (73.2%)      No  5, 882 (33.0%)  3, 324 (27.4%)  3, 139 (27.6%)  3, 114 (25.3%)  Do not know/answer  136 (0.8%)  195 (1.6%)  266 (2.4%)  175 (1.5%)  Reason for cytology test  < 0.001      For some problem, symptom or illness  849 (7.2%)  462 (5.4%)  952 (12.0%)  937 (10.5%)      On the advice of your AP doctor or specialist, although you had no problem  9326 (78.9%)  6287 (72.9%)  4461 (56.1%)  5754 (63.9%)      Because you received a letter, someone called you, or you were asked at your health centre if you wanted to do this test  569 (4.8%)  950 (11.0%)  1426 (17.9%)  1346 (14.9%)      Other reasons  990 (8.4%)  890 (10.3%)  1093 (13.7%)  954 (10.6%)      Do not know/answer  81 (0.7%)  35 (0.4%)  24 (0.4%)  14 (0.1%)  Testing frequency  <0.001      3 years or less  8425 (71.3%)  6085 (70.6%)  5911 (74.3%)  6528 (72.5%)      Between >3 and 5 years  439 (3.7%)  1064 (12.3%)  795 (10%)  797 (8.9%)      More than 5 years  2742 (23.2%)  1430 (16.6%)  1201 (15.1%)  1637 (18.2%)      Do not know/answer  209 (1.8%)  45 (0.5%)  46 (0.6%)  43 (0.5%)  Note: N: count; P: significance of the χ2 test; AP: primary care. Table 2 Cytology testing analysed in the period 2006–2014 in Spain   2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)  Have you ever had a cytology test?  < 0.001      Yes  11815 (66.3%)  8624 (71.0%)  7953 (70.0%)  9005 (73.2%)      No  5, 882 (33.0%)  3, 324 (27.4%)  3, 139 (27.6%)  3, 114 (25.3%)  Do not know/answer  136 (0.8%)  195 (1.6%)  266 (2.4%)  175 (1.5%)  Reason for cytology test  < 0.001      For some problem, symptom or illness  849 (7.2%)  462 (5.4%)  952 (12.0%)  937 (10.5%)      On the advice of your AP doctor or specialist, although you had no problem  9326 (78.9%)  6287 (72.9%)  4461 (56.1%)  5754 (63.9%)      Because you received a letter, someone called you, or you were asked at your health centre if you wanted to do this test  569 (4.8%)  950 (11.0%)  1426 (17.9%)  1346 (14.9%)      Other reasons  990 (8.4%)  890 (10.3%)  1093 (13.7%)  954 (10.6%)      Do not know/answer  81 (0.7%)  35 (0.4%)  24 (0.4%)  14 (0.1%)  Testing frequency  <0.001      3 years or less  8425 (71.3%)  6085 (70.6%)  5911 (74.3%)  6528 (72.5%)      Between >3 and 5 years  439 (3.7%)  1064 (12.3%)  795 (10%)  797 (8.9%)      More than 5 years  2742 (23.2%)  1430 (16.6%)  1201 (15.1%)  1637 (18.2%)      Do not know/answer  209 (1.8%)  45 (0.5%)  46 (0.6%)  43 (0.5%)    2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)  Have you ever had a cytology test?  < 0.001      Yes  11815 (66.3%)  8624 (71.0%)  7953 (70.0%)  9005 (73.2%)      No  5, 882 (33.0%)  3, 324 (27.4%)  3, 139 (27.6%)  3, 114 (25.3%)  Do not know/answer  136 (0.8%)  195 (1.6%)  266 (2.4%)  175 (1.5%)  Reason for cytology test  < 0.001      For some problem, symptom or illness  849 (7.2%)  462 (5.4%)  952 (12.0%)  937 (10.5%)      On the advice of your AP doctor or specialist, although you had no problem  9326 (78.9%)  6287 (72.9%)  4461 (56.1%)  5754 (63.9%)      Because you received a letter, someone called you, or you were asked at your health centre if you wanted to do this test  569 (4.8%)  950 (11.0%)  1426 (17.9%)  1346 (14.9%)      Other reasons  990 (8.4%)  890 (10.3%)  1093 (13.7%)  954 (10.6%)      Do not know/answer  81 (0.7%)  35 (0.4%)  24 (0.4%)  14 (0.1%)  Testing frequency  <0.001      3 years or less  8425 (71.3%)  6085 (70.6%)  5911 (74.3%)  6528 (72.5%)      Between >3 and 5 years  439 (3.7%)  1064 (12.3%)  795 (10%)  797 (8.9%)      More than 5 years  2742 (23.2%)  1430 (16.6%)  1201 (15.1%)  1637 (18.2%)      Do not know/answer  209 (1.8%)  45 (0.5%)  46 (0.6%)  43 (0.5%)  Note: N: count; P: significance of the χ2 test; AP: primary care. There were differences in cytology testing according to the health service of the autonomous community to which the women belonged, with Catalonia and Madrid being the communities with the highest percentage and Ceuta and Melilla having the lowest (P < 0.001). Navarra was the community which there was a higher participation in cytology testing for the reason of receipt a letter; but this reason was not the principal one to participate in cytology testing. However, in spite of receipt a letter, Navarra had not higher prevalence in cytology testing. In general, in Spain, the principal reason of cytology testing was the advice of primary care physician or specialist (table 2). Table 3 shows the sociodemographic variables associated with cytology testing. Women of lower class, of foreign origin and/or with less education had significantly fewer cytology tests, while women with university educations had significantly more tests. Table 3 Women’ Sociodemographic characteristics related with cytology testing in Spain (2006–2014)   Yes  No  P  N (%)  N (%)  Nationality      <0.001  Spanish  24 179 (94.5%)  8914 (93.1%)  Foreign  1403 (5.5%)  663 (6.9%)  Age      15–24 years old  12 285 (3.4%)  2270 (14.7%)  De 25–65 years old  28 603(76.5%)  5160 (33.4%)  <0.001  >65 years old  7509 (20.1%)  8029 (51.9%)  Civil status      <0.001  Single  5160 (20.2%)  3153 (32.9%)  Married  14 474 (56.6%)  2941 (30.7%)  Widower  3641 (14.2%)  3151 (32.9%)  Separated  800 (3.1%)  179 (1.9%)  Divorcer  1487 (5.8%)  146 (1.5%)  Did not know/answer  20 (0.1%)  7 (0.1%)  Cohabitation      <0.001  Yes  10 573 (60%)  1979 (30.7%)  No  6976 (39.6%)  4449 (69.1%)  Level of studies      <0.001  No studies  3837 (21.8%)  3182 (49.4%)  Primary studies  6147(34.9%)  2044(31.8%)  High School or FP  3702 (21%)  696 (10.8%)  University studies  3940 (22.4%)  514 (8%)  Social Class      <0.001  Classes I and II  6140 (21.9%)  1274 (11.2%)  Classes III and IV  11 745 (41.9%)  4570 (40%)  Classes V and VI  10 140 (36.2%)  5568 (48.8%)    Yes  No  P  N (%)  N (%)  Nationality      <0.001  Spanish  24 179 (94.5%)  8914 (93.1%)  Foreign  1403 (5.5%)  663 (6.9%)  Age      15–24 years old  12 285 (3.4%)  2270 (14.7%)  De 25–65 years old  28 603(76.5%)  5160 (33.4%)  <0.001  >65 years old  7509 (20.1%)  8029 (51.9%)  Civil status      <0.001  Single  5160 (20.2%)  3153 (32.9%)  Married  14 474 (56.6%)  2941 (30.7%)  Widower  3641 (14.2%)  3151 (32.9%)  Separated  800 (3.1%)  179 (1.9%)  Divorcer  1487 (5.8%)  146 (1.5%)  Did not know/answer  20 (0.1%)  7 (0.1%)  Cohabitation      <0.001  Yes  10 573 (60%)  1979 (30.7%)  No  6976 (39.6%)  4449 (69.1%)  Level of studies      <0.001  No studies  3837 (21.8%)  3182 (49.4%)  Primary studies  6147(34.9%)  2044(31.8%)  High School or FP  3702 (21%)  696 (10.8%)  University studies  3940 (22.4%)  514 (8%)  Social Class      <0.001  Classes I and II  6140 (21.9%)  1274 (11.2%)  Classes III and IV  11 745 (41.9%)  4570 (40%)  Classes V and VI  10 140 (36.2%)  5568 (48.8%)  Note: N: count; P: significance of the χ2 test. Table 3 Women’ Sociodemographic characteristics related with cytology testing in Spain (2006–2014)   Yes  No  P  N (%)  N (%)  Nationality      <0.001  Spanish  24 179 (94.5%)  8914 (93.1%)  Foreign  1403 (5.5%)  663 (6.9%)  Age      15–24 years old  12 285 (3.4%)  2270 (14.7%)  De 25–65 years old  28 603(76.5%)  5160 (33.4%)  <0.001  >65 years old  7509 (20.1%)  8029 (51.9%)  Civil status      <0.001  Single  5160 (20.2%)  3153 (32.9%)  Married  14 474 (56.6%)  2941 (30.7%)  Widower  3641 (14.2%)  3151 (32.9%)  Separated  800 (3.1%)  179 (1.9%)  Divorcer  1487 (5.8%)  146 (1.5%)  Did not know/answer  20 (0.1%)  7 (0.1%)  Cohabitation      <0.001  Yes  10 573 (60%)  1979 (30.7%)  No  6976 (39.6%)  4449 (69.1%)  Level of studies      <0.001  No studies  3837 (21.8%)  3182 (49.4%)  Primary studies  6147(34.9%)  2044(31.8%)  High School or FP  3702 (21%)  696 (10.8%)  University studies  3940 (22.4%)  514 (8%)  Social Class      <0.001  Classes I and II  6140 (21.9%)  1274 (11.2%)  Classes III and IV  11 745 (41.9%)  4570 (40%)  Classes V and VI  10 140 (36.2%)  5568 (48.8%)    Yes  No  P  N (%)  N (%)  Nationality      <0.001  Spanish  24 179 (94.5%)  8914 (93.1%)  Foreign  1403 (5.5%)  663 (6.9%)  Age      15–24 years old  12 285 (3.4%)  2270 (14.7%)  De 25–65 years old  28 603(76.5%)  5160 (33.4%)  <0.001  >65 years old  7509 (20.1%)  8029 (51.9%)  Civil status      <0.001  Single  5160 (20.2%)  3153 (32.9%)  Married  14 474 (56.6%)  2941 (30.7%)  Widower  3641 (14.2%)  3151 (32.9%)  Separated  800 (3.1%)  179 (1.9%)  Divorcer  1487 (5.8%)  146 (1.5%)  Did not know/answer  20 (0.1%)  7 (0.1%)  Cohabitation      <0.001  Yes  10 573 (60%)  1979 (30.7%)  No  6976 (39.6%)  4449 (69.1%)  Level of studies      <0.001  No studies  3837 (21.8%)  3182 (49.4%)  Primary studies  6147(34.9%)  2044(31.8%)  High School or FP  3702 (21%)  696 (10.8%)  University studies  3940 (22.4%)  514 (8%)  Social Class      <0.001  Classes I and II  6140 (21.9%)  1274 (11.2%)  Classes III and IV  11 745 (41.9%)  4570 (40%)  Classes V and VI  10 140 (36.2%)  5568 (48.8%)  Note: N: count; P: significance of the χ2 test. Figure 1 shows the women of total sample who received cytology testing less than 3 years ago, analysed by age group and year of survey. In the year 2014, there was an increase in the percentage of women aged 25–65 years old who had undergone cytology testing in the last 3 years. Figure 1 View largeDownload slide Evolution by age of women who received cytology testing less than three years ago Figure 1 View largeDownload slide Evolution by age of women who received cytology testing less than three years ago Through logistic regression (table 4), we studied the variables related to obtaining cytology tests. Women aged 25–65 years old were 5.13 times more likely to have a cytology test than women aged 15–24 years old (OR: 5.13; P < 0.001). The level of academic studies attained also influenced the cytology testing. University-educated women were 9.23 times more likely than those without education to receive cytology testing (P < 0.001), and women with baccalaureate degrees or vocational training were 8.2 times more likely than those without educations to receive cytology testing. Women of social classes I and II (high) were 1.2 times more likely to have a cytology test (P = 0.026) than those of low social class (V and VI). Women of Spanish origin were 1.74 times more likely to have a cytology test than those who, although residing in Spain, were of foreign origin (P < 0.001). Table 4 Variables associated with cytology in women residing in Spain (2006–2014) Variables  OR (CI 95%)  P  Age      From 15 to 24 years old  Reference        From 25 to 64 years old  5.13 (4.53–5.81)  <0.001      ≥ 65 years  3.03 (2.64–3.47)  <0.001  Level of studies      No studies  Reference        Primary or secondary  3.52 (3.12–3.98)  <0.001      Bachelor's or vocational training  8.2 (6.78–9.92)  <0.001      University students  9.23 (7.67–11.1)  <0.001  Social class      Classes I and II (High)  1.2 (1.02–1.41)  0.026      Classes III and IV (Average)  0.92 (0.79–1.08)  0.305      Classes V and VI (Low)  Reference    Spanish nationality      No  Reference        Yes  1.74 (1.43–2.12)  <0.001  Variables  OR (CI 95%)  P  Age      From 15 to 24 years old  Reference        From 25 to 64 years old  5.13 (4.53–5.81)  <0.001      ≥ 65 years  3.03 (2.64–3.47)  <0.001  Level of studies      No studies  Reference        Primary or secondary  3.52 (3.12–3.98)  <0.001      Bachelor's or vocational training  8.2 (6.78–9.92)  <0.001      University students  9.23 (7.67–11.1)  <0.001  Social class      Classes I and II (High)  1.2 (1.02–1.41)  0.026      Classes III and IV (Average)  0.92 (0.79–1.08)  0.305      Classes V and VI (Low)  Reference    Spanish nationality      No  Reference        Yes  1.74 (1.43–2.12)  <0.001  Note: Nagelkerke’s R2: 0.224; OR: odds ratio; CI 95%: 95% confidence interval. Table 4 Variables associated with cytology in women residing in Spain (2006–2014) Variables  OR (CI 95%)  P  Age      From 15 to 24 years old  Reference        From 25 to 64 years old  5.13 (4.53–5.81)  <0.001      ≥ 65 years  3.03 (2.64–3.47)  <0.001  Level of studies      No studies  Reference        Primary or secondary  3.52 (3.12–3.98)  <0.001      Bachelor's or vocational training  8.2 (6.78–9.92)  <0.001      University students  9.23 (7.67–11.1)  <0.001  Social class      Classes I and II (High)  1.2 (1.02–1.41)  0.026      Classes III and IV (Average)  0.92 (0.79–1.08)  0.305      Classes V and VI (Low)  Reference    Spanish nationality      No  Reference        Yes  1.74 (1.43–2.12)  <0.001  Variables  OR (CI 95%)  P  Age      From 15 to 24 years old  Reference        From 25 to 64 years old  5.13 (4.53–5.81)  <0.001      ≥ 65 years  3.03 (2.64–3.47)  <0.001  Level of studies      No studies  Reference        Primary or secondary  3.52 (3.12–3.98)  <0.001      Bachelor's or vocational training  8.2 (6.78–9.92)  <0.001      University students  9.23 (7.67–11.1)  <0.001  Social class      Classes I and II (High)  1.2 (1.02–1.41)  0.026      Classes III and IV (Average)  0.92 (0.79–1.08)  0.305      Classes V and VI (Low)  Reference    Spanish nationality      No  Reference        Yes  1.74 (1.43–2.12)  <0.001  Note: Nagelkerke’s R2: 0.224; OR: odds ratio; CI 95%: 95% confidence interval. Discussion To our knowledge, the present study is the first performed in Spain, at a national level, to assess the frequency and sociodemographic variables that influence cytology testing and their evolution over time. This study also outlines the profile of a woman who does not participate in cytology testing. The data analysis showed that the frequency of cytology testing had increased. In 2014, more than 52% of women surveyed had undergone cytology testing in the previous three years. This increase could be due to since 2007, The Spanish Health System has included the free HPV vaccine among adolescent girls (ages 11–14). In addition, since then it has increased the information about the importance in the prevention and etiology of cervical cancer: both the HPV vaccine and the early detection of cervical cancer.17,22 Although coverage increased from 2006 to 2014 (from 66.3% to 73.2%), some Spanish studies have shown that 60% of women diagnosed with cervical cancer had not previously had any cytology testing.23 The widespread and equitable implementation of effective interventions, including HPV vaccination and cervical cancer screening, could substantially reduce the incidence of cancer among women in both developed and developing countries.24 Pap smears and HPV tests are performed for cervical cancer screening. Since the 1960 s, screening programmes15,16,25 have been conducted in Europe and the United States of America, which may be opportunistic or population based. In Spain, given that the incidence of cervical cancer is not very high,5 the health system policy recommends screening opportunistically,17 with the objective of 70% of women youngest 30 years having cytology tests every 3 years and women 30–65 years having HPV tests every 5 years.17 From the records studied, 72% of the women had a cytology test, although opportunistic screening did not appear to reach the entire population, creating inequalities in its administration. Of the data analysed, the women that were tested less often included women of foreign origin and those living in Ceuta and Melilla (Spanish cities located in North Africa). These findings are in line with other studies in which women belonging to ethnic minorities are less likely to engage in prevention campaigns, including mammograms and cervical cytology tests.26,27 This difference may be due to poor access to health systems, lower socioeconomic levels, not understanding the language, and cultural differences, among other factors.8,25,28–30 The profile of women who underwent the least amount of cytology tests in Spain, despite the fact that the health system is public, consisted of young women with a low level of education and low income and/or those who were foreign.25,30,31 Other studies have suggested that increasing health knowledge in these groups could improve adherence to testing.32 The latest recommendations of the European practice guidelines recommend cytology testing every 3 years for women from 25 to 29 years old, co-testing every 5 years from 30 years of age to 65 years, and concluding screening at age 65 if previous screenings were negative. In the study being presented, a reduction in cytology testing was observed in women over 65 years old, a fact that coincides with the latest European recommendations.17,33,34 In the Netherlands,15 the screening system is based on population coverage by inviting women to participate. In a study comparing the Netherlands screening programme with the USA opportunistic programme,15 it was possible to see that the percentage of adherence to cervical cancer screening increased in the Netherlands, avoided an increase in cytology testing in the same person; the coverage of minority groups was facilitated and reduced the cost of performing unnecessary cytology tests; achieving the same detection rates of cervical cancer.15 Opportunistic screening reduces coverage, increases inequality, and decreases effectiveness and efficiency, resulting in a higher cost.15,17 In addition to follow health policies, health professionals should try to improve the adherence of people who do not participate in screening activities. Several studies have shown that sending a letter to such people can improve adherence.22,35–37 Currently, in addition to the reminder letter, studies are being conducted to encourage participation in screening, including sending swabs for self-sampling at home. Data are contradictory in this regard. In Australia, cytology testing improved for both the self-sampling group and the group that was sent a reminder letter, being higher in the first group.38 In Switzerland, these differences between self-sampling and getting a reminder letter were not observed, although coverage did increase.36 In Finland, cytology testing increased for both the reminder and self-sampling groups.39 It is very important that health professionals know how to recognize the variables that influence adherence to cytology testing. Therefore, communication skills are necessary, along with the capacity to capture information to increase women’s knowledge regarding the aetiology of cervical cancer, HPV infection, prevention measures and early diagnosis.40,41 Strength and limitations These results were obtained from the analysis of the records of the NHS and EHSS surveys, which did not allow the type of cytology test to be distinguished (i.e. pap smear or HPV test) because that question was not included in the questionnaires. In addition, the analysed data are self-reported information. The conclusions of the study refer exclusively to the scope described. On the other hand, the study has strength because, to our knowledge, it is one of the few with such a large sample size (53 628 women) that is updated and representative at the national level, which allows comparisons with similar environments in other Western societies. Conclusion The incidence of cytology testing in Spain is greater than 70%, and its frequency has increased in the past few years. Since 2007, the Spanish Health System has included the free HPV vaccine among adolescent girls (ages 11–15), increasing the information about prevention of cervical cancer. The cervical cancer screening programme in Spain is opportunistic, which increases access inequality. There are differences in the prevalence of cytology testing according to different health services and in different socioeconomic strata. The profile of women who obtain less cytology testing includes those of low socioeconomic status, those who lack education and those who are younger and/or foreign or ethnic minorities. Funding This study was conducted using the research group's own resources. Conflicts of interest: None declared. Key points This study clarifies the variables associated with adhesion to undergoing cytology tests for cervical cancer screening (women with lower educational level, low socioeconomic status, and younger) There are differences in the prevalence of cytology testing according to different health services and in different socioeconomic strata. This study shows the prevalence rates of women who participated in cytology testing from 2006 to 2014 in Spanish population. References 1 Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin  2016; 66: 7– 30. Google Scholar CrossRef Search ADS PubMed  2 Torre LA, Bray F, Siegel RL, et al.   Global cancer statistics, 2012. CA Cancer J Clin  2015; 65: 87– 108. Google Scholar CrossRef Search ADS PubMed  3 Ferlay J, Soerjomataram I, Dikshit R, et al.   Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer  2015; 136: E359– 86. 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Google Scholar CrossRef Search ADS PubMed  12 Castellsagué X, Iftner T, Roura E, et al.   Prevalence and genotype distribution of human papillomavirus infection of the cervix in Spain: the CLEOPATRE study. J Med Virol  2012; 84: 947– 56. Google Scholar CrossRef Search ADS PubMed  13 De Sanjose S, Cortes X, Mendez C, et al.   Age at sexual initiation and number of sexual partners in the female Spanish population Results from the AFRODITA survey. Eur J Obs Gyn Reprod Biol  2008; 140: 234– 40. Google Scholar CrossRef Search ADS   14 Vaccarella S, Franceschi S, Engholm G, et al.   50 years of screening in the Nordic countries: quantifying the effects on cervical cancer incidence. B J Cancer  2014; 111: 965. Google Scholar CrossRef Search ADS   15 Habbema D, De K, Inge M, Brown Martin L. Cervical cancer screening in the United States and the Netherlands: a tale of two countries. Milbank Q  2012; 90: 5– 37. Google Scholar CrossRef Search ADS PubMed  16 Serraino D, Gini A, Taborelli M, et al.   Changes in cervical cancer incidence following the introduction of organized screening in Italy. Prev Med  2015; 75: 56– 63. Google Scholar CrossRef Search ADS PubMed  17 Torné Bladé A, del Pino Saladrigues M, Gimferrer MC, et al.   Guía de cribado del cáncer de cuello de útero en España, 2014. Rev Esp Patol  2014; 47: 1– 43. 18 Ministerio de Sanidad Servicios Sociales e Igualdad. Encuesta Nacional de Salud ENS 2006: Ministerio de Sanidad y Consumo 2006. Available at: www.msssi.gob.es (17 July 2017, date last accessed). 19 Ministerio de Sanidad Servicios Sociales e Igualdad. Instituto Nacional de Estadística. Encuesta Europea de Salud en España EESE 2009 Madrid 2010. Available at: www.ine.es (17 July 2017, date last accessed). 20 Ministerio de Sanidad Servicios Sociales e Igualdad. Instituto Nacional de Estadística. Encuesta Nacional de Salud España ENSE 2011/12 Madrid 2013. Available at: www.ine.es (17 July 2017, date last accessed). 21 Ministerio de Sanidad Servicios Sociales e Igualdad. Instituto Nacional de Estadística. Encuesta Europea de Salud en España EESE 2014 2015. Available at: www.ine.es (17 July 2017, date last accessed). 22 Bosch FX, de Sanjosé S, Miralles C, Castellsagué X. La prevalencia y cáncer cervical en España: nuevas opciones para el siglo XXI. Folia Clin Obstect Ginecol  2010; 81: 6– 24. 23 Castillo M, Astudillo A, Clavero O, et al.   Poor cervical cancer screening attendance and false negatives. a call for organized screening. PLoS one  2016; 11: e0161403. Google Scholar CrossRef Search ADS PubMed  24 Torre L, Islami F, Siegel R, et al.   Global cancer in women: burden and Trends. Epidemiol Biomarkers Prev  2017; 26: 444– 57. Google Scholar CrossRef Search ADS   25 Roland KB, Benard V, Soman A, et al.   Cervical cancer screening among young adult women in the United States. Epidemiol Biomarkers Prev  2013; 22: 580– 8. 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PLoS one  2017; 12: e0170371. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2018. Published by Oxford University Press on behalf of the European Public Health Association. All rights reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices) http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png The European Journal of Public Health Oxford University Press

Prevalence and determinants in cytology testing for cervical cancer screening in Spain (2006–14)

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Oxford University Press
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© The Author(s) 2018. Published by Oxford University Press on behalf of the European Public Health Association. All rights reserved.
ISSN
1101-1262
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1464-360X
D.O.I.
10.1093/eurpub/cky015
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Abstract

Abstract Background Cervical cancer has decreased in developed countries thanks to cytology screening programmes. The aims of this study were To analyse the frequency and evolution of performing cytology tests and to determine the variables that influence their use. Methods Cross-sectional study of non-institutionalized women who participated in the national health survey (2006, 2011/12) and the European Health Survey in Spain (2009, 2014). Study variables: cytology-testing, time since last cytology-test, reason for performing the test, age, nationality, marital status, social status, education level and place of residence. Results The study evaluated 53 628 women in Spain over 15 years old, with a mean age of 52.68 (SD ± 19.12). About 94.1% were Spanish, 49.2% were married and 77.2% lived with a partner. In 2014, 72% had a cytology test, a number that increased significantly. Women aged 25–65 were 5.13 times more likely to undergo a cytology test than those aged 15–24 years old (odds ratio (OR): 5.13; P < 0.001); women with university educations were 9.23 times more likely to undergo a cytology test than those without university educations (P > 0.001); those of social classes I and II (high) were 1.2 more likely to undergo a cytology test than those of low social class (P = 0.026); and Spanish women were 1.74 times more likely to undergo a cytology test than foreigners living in Spain (P < 0.001). Conclusion Frequency of cytology testing has increased in the last few years. Screening for cervical cancer is associated with higher social status, education level, age, and not being foreign. Introduction Cervical cancer has a high incidence worldwide, being the third most frequent type of cancer in women and the second cause of cancer-related mortality in women.1,2 In 2012, approximately 527 600 cases were diagnosed worldwide. The incidence varies between countries, with developing countries having the highest incidence (444 500 deaths). The worldwide mortality due to cervical cancer is 265 700 deaths and is also higher in developing countries (230 200 deaths).2,3 In USA, it was estimated that in 2016, 12 990 cases would be diagnosed, with 4120 deaths from cervical cancer.1 In Western European countries, the incidence has been decreasing,4,5 especially in Spain, which has the lowest occurrence of cervical cancer.5,6 However, the incidence has increased in the countries of Eastern Europe.5–7 Generally, in developed countries, although the incidence of cervical cancer in older women (> 55 years) has declined, there has been an increase in younger women aged 30–35 years.4,8,9 These differences in the incidence of cervical cancer among different countries (developed and developing) can be explained by the inequality of health systems’ capacities to establish programmes for the early detection of cancerous lesions and human papillomavirus (HPV) infection.2,9 Cervical cancer is associated with HPV infection.10 The prevalence of HPV infection also differs among countries, varying from 9 to 21% in Africa, Latin America and Southeast Asia to approximately 5% in the United States.11 In Spain, in recent years, the prevalence of HPV infection has increased to 14.3%, of which 28.8% are women between 18 and 25 years old.12 This increase in recent years may be due to changes in the sexual behaviour of young women (i.e. sexual initiation at earlier ages and greater numbers of sexual partners).13 Screening programmes have been in place in Europe since the 1980 s, Norway, Finland and the Netherlands were the first ones.14 In the different countries where population-based screening programmes have been established (the Netherlands,15 Italy,16 Denmark,4 Norway14 and Sweden14), the mortality due to cervical cancer has been reduced. As mentioned previously, Spain is among the countries with the lowest rates of cervical cancer,5 which is the reason because population-based screening programmes have not been scheduled.17 The cervical cancer screening programmes are opportunistic (on demand), although specific screening and follow-up guidelines for low- and high-risk women are followed.17 Given that the screening programmes are opportunistic and given the change in the patterns of sexual behaviour in Spanish women (which may be the cause of the increasing incidence of HPV infections), it is of interest to know the frequency of cervical cytology testing and to assess the sociodemographic profiles that may influence adherence to early detection behaviours. The study aims are: (i)to analyse the frequency of cervical cytology testing in women in Spain and to evaluate the evolution in the period from 2006 to 2014; (ii) to describe the sociodemographic profile of the women who are tested; and (iii) to determine the variables that influence having cytology tests performed. Methods This is a descriptive cross-sectional study. A total of 53 628 women aged 15 years and older residing in Spain were selected from the two main sources of data: the National Health Survey (NHS) 200618 and 201119 in Spain and the European Health Survey of Spain (EHSS) for the years 200920 and 2014.21 These surveys were conducted by the Instituto Nacional de Estadística (National Institute of Statistics; NIS) in collaboration with the Ministerio de Sanidad, Servicios Sociales, e Igualdad (Spanish Ministry of Health, Social Services, and Equality). Both surveys had a cross-sectional and population-based design, with stratified three-point representative sampling, and were conducted at the national level, focusing on the non-institutionalized population residing in Spain, through an interview. The sampling procedure was multi-stage and stratified by clusters, with the selection of primary sampling units (municipalities) and secondary units (sections) in a proportional random fashion and the last units (individuals) by random routes and sex and age quotas. The data are available to any researcher on the NIS website in the form of an anonymous microdata file. For the current study, all the records corresponding to women were selected: NHS 200618 (17 833); EHSS 200919 (12 143); NHS 2011/1220 (11 358) and the EHSS 201421 (12 294); therefore, no authorizations for its use are required. The microdata files18–21 were downloaded and processed in a single database. The dependent variables of the study were (i) cytology test performed; (ii) frequency of performing the test (less than 3 years, between 3 and 5 years, more than 5 years); and (iii) reason for performing the test (‘for some problem, symptom, or illness’; ‘on the advice of your primary care physician or specialist’; ‘because you received a letter or phone call or was asked at your health centre if you wanted to be tested’; and ‘other’). Sociodemographic variables included age, nationality, education level, social status, job, marital status, current cohabitation and residency. Social class was stratified into three levels: high class (level I: directors and managers of companies with 10 or more employees and professionals with university degrees; level II: directors of companies with less than 10 employees and professionals with college diplomas); medium class (level III: intermediate occupations; level IV: workers in qualified technical occupations); and low class (level V: primary sector workers, level VI: unskilled workers).18–21 For the data analysis, we used IBM SPSS version 22.0 (IBM Corp., Armonk, NY, USA), a statistical program licensed for use from the Universidad de Castilla la Mancha (University of Castilla la Mancha). In the descriptive analysis of the qualitative variables, counts (n) and percentages (%) were used, and for the quantitative variables, means (m) and standard deviations (SD) were used. A χ2 test was used for the comparison of categorical variables. A multiple logistic regression was performed to determine the influence of the variables in having a cytology test performed. The ORs were calculated with their confidence intervals. A level of significance was set at P = 0.05 for all tests and comparisons. Results The records of 53 628 women residing in Spain over 15 years of age were analysed, resulting in a mean age of 52.68 (SD ± 19.12). A total of 94.1% of the women were Spanish, 49.2% were married and 77.2% lived with a partner. Table 1 shows the sociodemographic variables with respect to the survey years (table 1). Table 1 Women’ Sociodemographic characteristics, older than 15 years, in Spain (2006–2014)   2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)    Nationality  0.109      Spanish  Not registered  11 411 (94.0%)  10 662 (93.9%)  11 614 (94.5%)        Foreign    732 (6.0%)  696 (6.1%)  680 (5.5%)  Age        15–24 years  1120 (6.2%)  813 (6.7%)  814 (7.2%)  834 (6.8%)        25–65 years  11 904 (66.8%)  7842 (64.6%)  7022 (61.8%)  7766 (63.2%)  <0.001      >65 years  4809 (27.0%)  3488 (28.7%)  3522 (31.0%)  3694 (30%)    Civil status  <0.001  Single    2811 (23.2%)  2754 (24.2%)  2830 (23%)    Married  Not registered  6069 (50%)  5506 (48.5%)  6049 (49.2%)  Widower    2398 (19.7%)  2287 (20.1%)  2429 (19.8%)  Separated    372 (3.1%)  298 (2.6%)  315 (2.6%)  Divorced    488 (4%)  500 (4.5%)  655 (5.3%)  Do not know/answer    5 (0.0%)  13 (0.1%)  16 (0.1%)  Cohabitation        Yes    6581 (54.2%)    6090 (49.5%)        No  Not registered  5552 (45.7%)  Not registered  6123 (51.5%)  <0.001  Level study  <0.001  No studies    2485 (20.5%)    4788 (38.9%)    Primaries  Not registered  4746 (39.3%)  Not registered  3511 (28.6%)  High school/FP    2828 (23.3%)    1584 (12.9%)  University    1064 (16.9%)    2.411 (19.6%)  Level Social  <0.001      Classes I–II  3231 (18.6%)    1938 (18.0%)  2310 (19.5%)        Classes III–IV  9055 (52.3%)  Not registered  3499 (32.6%)  3901 (32.9%)      Classes V–VI  5039 (29.1%)    5307 (49.4%)  5658 (47.6%)    2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)    Nationality  0.109      Spanish  Not registered  11 411 (94.0%)  10 662 (93.9%)  11 614 (94.5%)        Foreign    732 (6.0%)  696 (6.1%)  680 (5.5%)  Age        15–24 years  1120 (6.2%)  813 (6.7%)  814 (7.2%)  834 (6.8%)        25–65 years  11 904 (66.8%)  7842 (64.6%)  7022 (61.8%)  7766 (63.2%)  <0.001      >65 years  4809 (27.0%)  3488 (28.7%)  3522 (31.0%)  3694 (30%)    Civil status  <0.001  Single    2811 (23.2%)  2754 (24.2%)  2830 (23%)    Married  Not registered  6069 (50%)  5506 (48.5%)  6049 (49.2%)  Widower    2398 (19.7%)  2287 (20.1%)  2429 (19.8%)  Separated    372 (3.1%)  298 (2.6%)  315 (2.6%)  Divorced    488 (4%)  500 (4.5%)  655 (5.3%)  Do not know/answer    5 (0.0%)  13 (0.1%)  16 (0.1%)  Cohabitation        Yes    6581 (54.2%)    6090 (49.5%)        No  Not registered  5552 (45.7%)  Not registered  6123 (51.5%)  <0.001  Level study  <0.001  No studies    2485 (20.5%)    4788 (38.9%)    Primaries  Not registered  4746 (39.3%)  Not registered  3511 (28.6%)  High school/FP    2828 (23.3%)    1584 (12.9%)  University    1064 (16.9%)    2.411 (19.6%)  Level Social  <0.001      Classes I–II  3231 (18.6%)    1938 (18.0%)  2310 (19.5%)        Classes III–IV  9055 (52.3%)  Not registered  3499 (32.6%)  3901 (32.9%)      Classes V–VI  5039 (29.1%)    5307 (49.4%)  5658 (47.6%)  Notes: N: count; P: significance of the χ2 test; PF: professional formation. Table 1 Women’ Sociodemographic characteristics, older than 15 years, in Spain (2006–2014)   2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)    Nationality  0.109      Spanish  Not registered  11 411 (94.0%)  10 662 (93.9%)  11 614 (94.5%)        Foreign    732 (6.0%)  696 (6.1%)  680 (5.5%)  Age        15–24 years  1120 (6.2%)  813 (6.7%)  814 (7.2%)  834 (6.8%)        25–65 years  11 904 (66.8%)  7842 (64.6%)  7022 (61.8%)  7766 (63.2%)  <0.001      >65 years  4809 (27.0%)  3488 (28.7%)  3522 (31.0%)  3694 (30%)    Civil status  <0.001  Single    2811 (23.2%)  2754 (24.2%)  2830 (23%)    Married  Not registered  6069 (50%)  5506 (48.5%)  6049 (49.2%)  Widower    2398 (19.7%)  2287 (20.1%)  2429 (19.8%)  Separated    372 (3.1%)  298 (2.6%)  315 (2.6%)  Divorced    488 (4%)  500 (4.5%)  655 (5.3%)  Do not know/answer    5 (0.0%)  13 (0.1%)  16 (0.1%)  Cohabitation        Yes    6581 (54.2%)    6090 (49.5%)        No  Not registered  5552 (45.7%)  Not registered  6123 (51.5%)  <0.001  Level study  <0.001  No studies    2485 (20.5%)    4788 (38.9%)    Primaries  Not registered  4746 (39.3%)  Not registered  3511 (28.6%)  High school/FP    2828 (23.3%)    1584 (12.9%)  University    1064 (16.9%)    2.411 (19.6%)  Level Social  <0.001      Classes I–II  3231 (18.6%)    1938 (18.0%)  2310 (19.5%)        Classes III–IV  9055 (52.3%)  Not registered  3499 (32.6%)  3901 (32.9%)      Classes V–VI  5039 (29.1%)    5307 (49.4%)  5658 (47.6%)    2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)    Nationality  0.109      Spanish  Not registered  11 411 (94.0%)  10 662 (93.9%)  11 614 (94.5%)        Foreign    732 (6.0%)  696 (6.1%)  680 (5.5%)  Age        15–24 years  1120 (6.2%)  813 (6.7%)  814 (7.2%)  834 (6.8%)        25–65 years  11 904 (66.8%)  7842 (64.6%)  7022 (61.8%)  7766 (63.2%)  <0.001      >65 years  4809 (27.0%)  3488 (28.7%)  3522 (31.0%)  3694 (30%)    Civil status  <0.001  Single    2811 (23.2%)  2754 (24.2%)  2830 (23%)    Married  Not registered  6069 (50%)  5506 (48.5%)  6049 (49.2%)  Widower    2398 (19.7%)  2287 (20.1%)  2429 (19.8%)  Separated    372 (3.1%)  298 (2.6%)  315 (2.6%)  Divorced    488 (4%)  500 (4.5%)  655 (5.3%)  Do not know/answer    5 (0.0%)  13 (0.1%)  16 (0.1%)  Cohabitation        Yes    6581 (54.2%)    6090 (49.5%)        No  Not registered  5552 (45.7%)  Not registered  6123 (51.5%)  <0.001  Level study  <0.001  No studies    2485 (20.5%)    4788 (38.9%)    Primaries  Not registered  4746 (39.3%)  Not registered  3511 (28.6%)  High school/FP    2828 (23.3%)    1584 (12.9%)  University    1064 (16.9%)    2.411 (19.6%)  Level Social  <0.001      Classes I–II  3231 (18.6%)    1938 (18.0%)  2310 (19.5%)        Classes III–IV  9055 (52.3%)  Not registered  3499 (32.6%)  3901 (32.9%)      Classes V–VI  5039 (29.1%)    5307 (49.4%)  5658 (47.6%)  Notes: N: count; P: significance of the χ2 test; PF: professional formation. Table 2 shows the cytology tests conducted in different years. There was a significant increase in cytology testing in 2014 with respect to the other years. In addition, in 2012 and 2014, the reasons for testing changed, increasing due to the receipt of a letter advising testing and due to symptomatology (table 2). Table 2 Cytology testing analysed in the period 2006–2014 in Spain   2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)  Have you ever had a cytology test?  < 0.001      Yes  11815 (66.3%)  8624 (71.0%)  7953 (70.0%)  9005 (73.2%)      No  5, 882 (33.0%)  3, 324 (27.4%)  3, 139 (27.6%)  3, 114 (25.3%)  Do not know/answer  136 (0.8%)  195 (1.6%)  266 (2.4%)  175 (1.5%)  Reason for cytology test  < 0.001      For some problem, symptom or illness  849 (7.2%)  462 (5.4%)  952 (12.0%)  937 (10.5%)      On the advice of your AP doctor or specialist, although you had no problem  9326 (78.9%)  6287 (72.9%)  4461 (56.1%)  5754 (63.9%)      Because you received a letter, someone called you, or you were asked at your health centre if you wanted to do this test  569 (4.8%)  950 (11.0%)  1426 (17.9%)  1346 (14.9%)      Other reasons  990 (8.4%)  890 (10.3%)  1093 (13.7%)  954 (10.6%)      Do not know/answer  81 (0.7%)  35 (0.4%)  24 (0.4%)  14 (0.1%)  Testing frequency  <0.001      3 years or less  8425 (71.3%)  6085 (70.6%)  5911 (74.3%)  6528 (72.5%)      Between >3 and 5 years  439 (3.7%)  1064 (12.3%)  795 (10%)  797 (8.9%)      More than 5 years  2742 (23.2%)  1430 (16.6%)  1201 (15.1%)  1637 (18.2%)      Do not know/answer  209 (1.8%)  45 (0.5%)  46 (0.6%)  43 (0.5%)    2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)  Have you ever had a cytology test?  < 0.001      Yes  11815 (66.3%)  8624 (71.0%)  7953 (70.0%)  9005 (73.2%)      No  5, 882 (33.0%)  3, 324 (27.4%)  3, 139 (27.6%)  3, 114 (25.3%)  Do not know/answer  136 (0.8%)  195 (1.6%)  266 (2.4%)  175 (1.5%)  Reason for cytology test  < 0.001      For some problem, symptom or illness  849 (7.2%)  462 (5.4%)  952 (12.0%)  937 (10.5%)      On the advice of your AP doctor or specialist, although you had no problem  9326 (78.9%)  6287 (72.9%)  4461 (56.1%)  5754 (63.9%)      Because you received a letter, someone called you, or you were asked at your health centre if you wanted to do this test  569 (4.8%)  950 (11.0%)  1426 (17.9%)  1346 (14.9%)      Other reasons  990 (8.4%)  890 (10.3%)  1093 (13.7%)  954 (10.6%)      Do not know/answer  81 (0.7%)  35 (0.4%)  24 (0.4%)  14 (0.1%)  Testing frequency  <0.001      3 years or less  8425 (71.3%)  6085 (70.6%)  5911 (74.3%)  6528 (72.5%)      Between >3 and 5 years  439 (3.7%)  1064 (12.3%)  795 (10%)  797 (8.9%)      More than 5 years  2742 (23.2%)  1430 (16.6%)  1201 (15.1%)  1637 (18.2%)      Do not know/answer  209 (1.8%)  45 (0.5%)  46 (0.6%)  43 (0.5%)  Note: N: count; P: significance of the χ2 test; AP: primary care. Table 2 Cytology testing analysed in the period 2006–2014 in Spain   2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)  Have you ever had a cytology test?  < 0.001      Yes  11815 (66.3%)  8624 (71.0%)  7953 (70.0%)  9005 (73.2%)      No  5, 882 (33.0%)  3, 324 (27.4%)  3, 139 (27.6%)  3, 114 (25.3%)  Do not know/answer  136 (0.8%)  195 (1.6%)  266 (2.4%)  175 (1.5%)  Reason for cytology test  < 0.001      For some problem, symptom or illness  849 (7.2%)  462 (5.4%)  952 (12.0%)  937 (10.5%)      On the advice of your AP doctor or specialist, although you had no problem  9326 (78.9%)  6287 (72.9%)  4461 (56.1%)  5754 (63.9%)      Because you received a letter, someone called you, or you were asked at your health centre if you wanted to do this test  569 (4.8%)  950 (11.0%)  1426 (17.9%)  1346 (14.9%)      Other reasons  990 (8.4%)  890 (10.3%)  1093 (13.7%)  954 (10.6%)      Do not know/answer  81 (0.7%)  35 (0.4%)  24 (0.4%)  14 (0.1%)  Testing frequency  <0.001      3 years or less  8425 (71.3%)  6085 (70.6%)  5911 (74.3%)  6528 (72.5%)      Between >3 and 5 years  439 (3.7%)  1064 (12.3%)  795 (10%)  797 (8.9%)      More than 5 years  2742 (23.2%)  1430 (16.6%)  1201 (15.1%)  1637 (18.2%)      Do not know/answer  209 (1.8%)  45 (0.5%)  46 (0.6%)  43 (0.5%)    2006  2009  2011  2014  P  N (%)  N (%)  N (%)  N (%)  Have you ever had a cytology test?  < 0.001      Yes  11815 (66.3%)  8624 (71.0%)  7953 (70.0%)  9005 (73.2%)      No  5, 882 (33.0%)  3, 324 (27.4%)  3, 139 (27.6%)  3, 114 (25.3%)  Do not know/answer  136 (0.8%)  195 (1.6%)  266 (2.4%)  175 (1.5%)  Reason for cytology test  < 0.001      For some problem, symptom or illness  849 (7.2%)  462 (5.4%)  952 (12.0%)  937 (10.5%)      On the advice of your AP doctor or specialist, although you had no problem  9326 (78.9%)  6287 (72.9%)  4461 (56.1%)  5754 (63.9%)      Because you received a letter, someone called you, or you were asked at your health centre if you wanted to do this test  569 (4.8%)  950 (11.0%)  1426 (17.9%)  1346 (14.9%)      Other reasons  990 (8.4%)  890 (10.3%)  1093 (13.7%)  954 (10.6%)      Do not know/answer  81 (0.7%)  35 (0.4%)  24 (0.4%)  14 (0.1%)  Testing frequency  <0.001      3 years or less  8425 (71.3%)  6085 (70.6%)  5911 (74.3%)  6528 (72.5%)      Between >3 and 5 years  439 (3.7%)  1064 (12.3%)  795 (10%)  797 (8.9%)      More than 5 years  2742 (23.2%)  1430 (16.6%)  1201 (15.1%)  1637 (18.2%)      Do not know/answer  209 (1.8%)  45 (0.5%)  46 (0.6%)  43 (0.5%)  Note: N: count; P: significance of the χ2 test; AP: primary care. There were differences in cytology testing according to the health service of the autonomous community to which the women belonged, with Catalonia and Madrid being the communities with the highest percentage and Ceuta and Melilla having the lowest (P < 0.001). Navarra was the community which there was a higher participation in cytology testing for the reason of receipt a letter; but this reason was not the principal one to participate in cytology testing. However, in spite of receipt a letter, Navarra had not higher prevalence in cytology testing. In general, in Spain, the principal reason of cytology testing was the advice of primary care physician or specialist (table 2). Table 3 shows the sociodemographic variables associated with cytology testing. Women of lower class, of foreign origin and/or with less education had significantly fewer cytology tests, while women with university educations had significantly more tests. Table 3 Women’ Sociodemographic characteristics related with cytology testing in Spain (2006–2014)   Yes  No  P  N (%)  N (%)  Nationality      <0.001  Spanish  24 179 (94.5%)  8914 (93.1%)  Foreign  1403 (5.5%)  663 (6.9%)  Age      15–24 years old  12 285 (3.4%)  2270 (14.7%)  De 25–65 years old  28 603(76.5%)  5160 (33.4%)  <0.001  >65 years old  7509 (20.1%)  8029 (51.9%)  Civil status      <0.001  Single  5160 (20.2%)  3153 (32.9%)  Married  14 474 (56.6%)  2941 (30.7%)  Widower  3641 (14.2%)  3151 (32.9%)  Separated  800 (3.1%)  179 (1.9%)  Divorcer  1487 (5.8%)  146 (1.5%)  Did not know/answer  20 (0.1%)  7 (0.1%)  Cohabitation      <0.001  Yes  10 573 (60%)  1979 (30.7%)  No  6976 (39.6%)  4449 (69.1%)  Level of studies      <0.001  No studies  3837 (21.8%)  3182 (49.4%)  Primary studies  6147(34.9%)  2044(31.8%)  High School or FP  3702 (21%)  696 (10.8%)  University studies  3940 (22.4%)  514 (8%)  Social Class      <0.001  Classes I and II  6140 (21.9%)  1274 (11.2%)  Classes III and IV  11 745 (41.9%)  4570 (40%)  Classes V and VI  10 140 (36.2%)  5568 (48.8%)    Yes  No  P  N (%)  N (%)  Nationality      <0.001  Spanish  24 179 (94.5%)  8914 (93.1%)  Foreign  1403 (5.5%)  663 (6.9%)  Age      15–24 years old  12 285 (3.4%)  2270 (14.7%)  De 25–65 years old  28 603(76.5%)  5160 (33.4%)  <0.001  >65 years old  7509 (20.1%)  8029 (51.9%)  Civil status      <0.001  Single  5160 (20.2%)  3153 (32.9%)  Married  14 474 (56.6%)  2941 (30.7%)  Widower  3641 (14.2%)  3151 (32.9%)  Separated  800 (3.1%)  179 (1.9%)  Divorcer  1487 (5.8%)  146 (1.5%)  Did not know/answer  20 (0.1%)  7 (0.1%)  Cohabitation      <0.001  Yes  10 573 (60%)  1979 (30.7%)  No  6976 (39.6%)  4449 (69.1%)  Level of studies      <0.001  No studies  3837 (21.8%)  3182 (49.4%)  Primary studies  6147(34.9%)  2044(31.8%)  High School or FP  3702 (21%)  696 (10.8%)  University studies  3940 (22.4%)  514 (8%)  Social Class      <0.001  Classes I and II  6140 (21.9%)  1274 (11.2%)  Classes III and IV  11 745 (41.9%)  4570 (40%)  Classes V and VI  10 140 (36.2%)  5568 (48.8%)  Note: N: count; P: significance of the χ2 test. Table 3 Women’ Sociodemographic characteristics related with cytology testing in Spain (2006–2014)   Yes  No  P  N (%)  N (%)  Nationality      <0.001  Spanish  24 179 (94.5%)  8914 (93.1%)  Foreign  1403 (5.5%)  663 (6.9%)  Age      15–24 years old  12 285 (3.4%)  2270 (14.7%)  De 25–65 years old  28 603(76.5%)  5160 (33.4%)  <0.001  >65 years old  7509 (20.1%)  8029 (51.9%)  Civil status      <0.001  Single  5160 (20.2%)  3153 (32.9%)  Married  14 474 (56.6%)  2941 (30.7%)  Widower  3641 (14.2%)  3151 (32.9%)  Separated  800 (3.1%)  179 (1.9%)  Divorcer  1487 (5.8%)  146 (1.5%)  Did not know/answer  20 (0.1%)  7 (0.1%)  Cohabitation      <0.001  Yes  10 573 (60%)  1979 (30.7%)  No  6976 (39.6%)  4449 (69.1%)  Level of studies      <0.001  No studies  3837 (21.8%)  3182 (49.4%)  Primary studies  6147(34.9%)  2044(31.8%)  High School or FP  3702 (21%)  696 (10.8%)  University studies  3940 (22.4%)  514 (8%)  Social Class      <0.001  Classes I and II  6140 (21.9%)  1274 (11.2%)  Classes III and IV  11 745 (41.9%)  4570 (40%)  Classes V and VI  10 140 (36.2%)  5568 (48.8%)    Yes  No  P  N (%)  N (%)  Nationality      <0.001  Spanish  24 179 (94.5%)  8914 (93.1%)  Foreign  1403 (5.5%)  663 (6.9%)  Age      15–24 years old  12 285 (3.4%)  2270 (14.7%)  De 25–65 years old  28 603(76.5%)  5160 (33.4%)  <0.001  >65 years old  7509 (20.1%)  8029 (51.9%)  Civil status      <0.001  Single  5160 (20.2%)  3153 (32.9%)  Married  14 474 (56.6%)  2941 (30.7%)  Widower  3641 (14.2%)  3151 (32.9%)  Separated  800 (3.1%)  179 (1.9%)  Divorcer  1487 (5.8%)  146 (1.5%)  Did not know/answer  20 (0.1%)  7 (0.1%)  Cohabitation      <0.001  Yes  10 573 (60%)  1979 (30.7%)  No  6976 (39.6%)  4449 (69.1%)  Level of studies      <0.001  No studies  3837 (21.8%)  3182 (49.4%)  Primary studies  6147(34.9%)  2044(31.8%)  High School or FP  3702 (21%)  696 (10.8%)  University studies  3940 (22.4%)  514 (8%)  Social Class      <0.001  Classes I and II  6140 (21.9%)  1274 (11.2%)  Classes III and IV  11 745 (41.9%)  4570 (40%)  Classes V and VI  10 140 (36.2%)  5568 (48.8%)  Note: N: count; P: significance of the χ2 test. Figure 1 shows the women of total sample who received cytology testing less than 3 years ago, analysed by age group and year of survey. In the year 2014, there was an increase in the percentage of women aged 25–65 years old who had undergone cytology testing in the last 3 years. Figure 1 View largeDownload slide Evolution by age of women who received cytology testing less than three years ago Figure 1 View largeDownload slide Evolution by age of women who received cytology testing less than three years ago Through logistic regression (table 4), we studied the variables related to obtaining cytology tests. Women aged 25–65 years old were 5.13 times more likely to have a cytology test than women aged 15–24 years old (OR: 5.13; P < 0.001). The level of academic studies attained also influenced the cytology testing. University-educated women were 9.23 times more likely than those without education to receive cytology testing (P < 0.001), and women with baccalaureate degrees or vocational training were 8.2 times more likely than those without educations to receive cytology testing. Women of social classes I and II (high) were 1.2 times more likely to have a cytology test (P = 0.026) than those of low social class (V and VI). Women of Spanish origin were 1.74 times more likely to have a cytology test than those who, although residing in Spain, were of foreign origin (P < 0.001). Table 4 Variables associated with cytology in women residing in Spain (2006–2014) Variables  OR (CI 95%)  P  Age      From 15 to 24 years old  Reference        From 25 to 64 years old  5.13 (4.53–5.81)  <0.001      ≥ 65 years  3.03 (2.64–3.47)  <0.001  Level of studies      No studies  Reference        Primary or secondary  3.52 (3.12–3.98)  <0.001      Bachelor's or vocational training  8.2 (6.78–9.92)  <0.001      University students  9.23 (7.67–11.1)  <0.001  Social class      Classes I and II (High)  1.2 (1.02–1.41)  0.026      Classes III and IV (Average)  0.92 (0.79–1.08)  0.305      Classes V and VI (Low)  Reference    Spanish nationality      No  Reference        Yes  1.74 (1.43–2.12)  <0.001  Variables  OR (CI 95%)  P  Age      From 15 to 24 years old  Reference        From 25 to 64 years old  5.13 (4.53–5.81)  <0.001      ≥ 65 years  3.03 (2.64–3.47)  <0.001  Level of studies      No studies  Reference        Primary or secondary  3.52 (3.12–3.98)  <0.001      Bachelor's or vocational training  8.2 (6.78–9.92)  <0.001      University students  9.23 (7.67–11.1)  <0.001  Social class      Classes I and II (High)  1.2 (1.02–1.41)  0.026      Classes III and IV (Average)  0.92 (0.79–1.08)  0.305      Classes V and VI (Low)  Reference    Spanish nationality      No  Reference        Yes  1.74 (1.43–2.12)  <0.001  Note: Nagelkerke’s R2: 0.224; OR: odds ratio; CI 95%: 95% confidence interval. Table 4 Variables associated with cytology in women residing in Spain (2006–2014) Variables  OR (CI 95%)  P  Age      From 15 to 24 years old  Reference        From 25 to 64 years old  5.13 (4.53–5.81)  <0.001      ≥ 65 years  3.03 (2.64–3.47)  <0.001  Level of studies      No studies  Reference        Primary or secondary  3.52 (3.12–3.98)  <0.001      Bachelor's or vocational training  8.2 (6.78–9.92)  <0.001      University students  9.23 (7.67–11.1)  <0.001  Social class      Classes I and II (High)  1.2 (1.02–1.41)  0.026      Classes III and IV (Average)  0.92 (0.79–1.08)  0.305      Classes V and VI (Low)  Reference    Spanish nationality      No  Reference        Yes  1.74 (1.43–2.12)  <0.001  Variables  OR (CI 95%)  P  Age      From 15 to 24 years old  Reference        From 25 to 64 years old  5.13 (4.53–5.81)  <0.001      ≥ 65 years  3.03 (2.64–3.47)  <0.001  Level of studies      No studies  Reference        Primary or secondary  3.52 (3.12–3.98)  <0.001      Bachelor's or vocational training  8.2 (6.78–9.92)  <0.001      University students  9.23 (7.67–11.1)  <0.001  Social class      Classes I and II (High)  1.2 (1.02–1.41)  0.026      Classes III and IV (Average)  0.92 (0.79–1.08)  0.305      Classes V and VI (Low)  Reference    Spanish nationality      No  Reference        Yes  1.74 (1.43–2.12)  <0.001  Note: Nagelkerke’s R2: 0.224; OR: odds ratio; CI 95%: 95% confidence interval. Discussion To our knowledge, the present study is the first performed in Spain, at a national level, to assess the frequency and sociodemographic variables that influence cytology testing and their evolution over time. This study also outlines the profile of a woman who does not participate in cytology testing. The data analysis showed that the frequency of cytology testing had increased. In 2014, more than 52% of women surveyed had undergone cytology testing in the previous three years. This increase could be due to since 2007, The Spanish Health System has included the free HPV vaccine among adolescent girls (ages 11–14). In addition, since then it has increased the information about the importance in the prevention and etiology of cervical cancer: both the HPV vaccine and the early detection of cervical cancer.17,22 Although coverage increased from 2006 to 2014 (from 66.3% to 73.2%), some Spanish studies have shown that 60% of women diagnosed with cervical cancer had not previously had any cytology testing.23 The widespread and equitable implementation of effective interventions, including HPV vaccination and cervical cancer screening, could substantially reduce the incidence of cancer among women in both developed and developing countries.24 Pap smears and HPV tests are performed for cervical cancer screening. Since the 1960 s, screening programmes15,16,25 have been conducted in Europe and the United States of America, which may be opportunistic or population based. In Spain, given that the incidence of cervical cancer is not very high,5 the health system policy recommends screening opportunistically,17 with the objective of 70% of women youngest 30 years having cytology tests every 3 years and women 30–65 years having HPV tests every 5 years.17 From the records studied, 72% of the women had a cytology test, although opportunistic screening did not appear to reach the entire population, creating inequalities in its administration. Of the data analysed, the women that were tested less often included women of foreign origin and those living in Ceuta and Melilla (Spanish cities located in North Africa). These findings are in line with other studies in which women belonging to ethnic minorities are less likely to engage in prevention campaigns, including mammograms and cervical cytology tests.26,27 This difference may be due to poor access to health systems, lower socioeconomic levels, not understanding the language, and cultural differences, among other factors.8,25,28–30 The profile of women who underwent the least amount of cytology tests in Spain, despite the fact that the health system is public, consisted of young women with a low level of education and low income and/or those who were foreign.25,30,31 Other studies have suggested that increasing health knowledge in these groups could improve adherence to testing.32 The latest recommendations of the European practice guidelines recommend cytology testing every 3 years for women from 25 to 29 years old, co-testing every 5 years from 30 years of age to 65 years, and concluding screening at age 65 if previous screenings were negative. In the study being presented, a reduction in cytology testing was observed in women over 65 years old, a fact that coincides with the latest European recommendations.17,33,34 In the Netherlands,15 the screening system is based on population coverage by inviting women to participate. In a study comparing the Netherlands screening programme with the USA opportunistic programme,15 it was possible to see that the percentage of adherence to cervical cancer screening increased in the Netherlands, avoided an increase in cytology testing in the same person; the coverage of minority groups was facilitated and reduced the cost of performing unnecessary cytology tests; achieving the same detection rates of cervical cancer.15 Opportunistic screening reduces coverage, increases inequality, and decreases effectiveness and efficiency, resulting in a higher cost.15,17 In addition to follow health policies, health professionals should try to improve the adherence of people who do not participate in screening activities. Several studies have shown that sending a letter to such people can improve adherence.22,35–37 Currently, in addition to the reminder letter, studies are being conducted to encourage participation in screening, including sending swabs for self-sampling at home. Data are contradictory in this regard. In Australia, cytology testing improved for both the self-sampling group and the group that was sent a reminder letter, being higher in the first group.38 In Switzerland, these differences between self-sampling and getting a reminder letter were not observed, although coverage did increase.36 In Finland, cytology testing increased for both the reminder and self-sampling groups.39 It is very important that health professionals know how to recognize the variables that influence adherence to cytology testing. Therefore, communication skills are necessary, along with the capacity to capture information to increase women’s knowledge regarding the aetiology of cervical cancer, HPV infection, prevention measures and early diagnosis.40,41 Strength and limitations These results were obtained from the analysis of the records of the NHS and EHSS surveys, which did not allow the type of cytology test to be distinguished (i.e. pap smear or HPV test) because that question was not included in the questionnaires. In addition, the analysed data are self-reported information. The conclusions of the study refer exclusively to the scope described. On the other hand, the study has strength because, to our knowledge, it is one of the few with such a large sample size (53 628 women) that is updated and representative at the national level, which allows comparisons with similar environments in other Western societies. Conclusion The incidence of cytology testing in Spain is greater than 70%, and its frequency has increased in the past few years. Since 2007, the Spanish Health System has included the free HPV vaccine among adolescent girls (ages 11–15), increasing the information about prevention of cervical cancer. The cervical cancer screening programme in Spain is opportunistic, which increases access inequality. There are differences in the prevalence of cytology testing according to different health services and in different socioeconomic strata. The profile of women who obtain less cytology testing includes those of low socioeconomic status, those who lack education and those who are younger and/or foreign or ethnic minorities. Funding This study was conducted using the research group's own resources. Conflicts of interest: None declared. Key points This study clarifies the variables associated with adhesion to undergoing cytology tests for cervical cancer screening (women with lower educational level, low socioeconomic status, and younger) There are differences in the prevalence of cytology testing according to different health services and in different socioeconomic strata. This study shows the prevalence rates of women who participated in cytology testing from 2006 to 2014 in Spanish population. References 1 Siegel RL, Miller KD, Jemal A. Cancer statistics, 2016. CA Cancer J Clin  2016; 66: 7– 30. Google Scholar CrossRef Search ADS PubMed  2 Torre LA, Bray F, Siegel RL, et al.   Global cancer statistics, 2012. CA Cancer J Clin  2015; 65: 87– 108. Google Scholar CrossRef Search ADS PubMed  3 Ferlay J, Soerjomataram I, Dikshit R, et al.   Cancer incidence and mortality worldwide: sources, methods and major patterns in GLOBOCAN 2012. Int J Cancer  2015; 136: E359– 86. 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PLoS one  2017; 12: e0170371. Google Scholar CrossRef Search ADS PubMed  © The Author(s) 2018. Published by Oxford University Press on behalf of the European Public Health Association. All rights reserved. This article is published and distributed under the terms of the Oxford University Press, Standard Journals Publication Model (https://academic.oup.com/journals/pages/about_us/legal/notices)

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The European Journal of Public HealthOxford University Press

Published: Feb 12, 2018

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