Setting
Screening policies vary between countries [
11] but European guidelines recommend that organized cervical cancer screening programs include women before they reach age 35 years and continue at least until they reach 64 years. Depending on disease burden and resources, screening could begin earlier and/or end later than recommended. The recommended screening interval is 3–5 years, and the recommended screening method is a sample of cellular material from the uterine cervix (cervical cytology). In Denmark, cervical cancer screening was introduced locally in 1962 and non-systematically implemented in the rest of the country until reaching nationwide coverage in late 1990s. All Danish women between 23 and 49 are now offered cervical cancer screening three years after their last screening test or last invitation; women between 50 and 64 years five years after the last screening test or last invitation [
6,
12]. Danish women also have the possibility to be tested opportunistically by a general practitioner or a gynecologist. All screening procedures and treatment in hospitals, e.g. hysterectomy, is free of charge in Denmark.
Study population
Inclusion criterion was women being in the NCCSP target population on 12 January 2012. Women, who had been in the screening population for less than one entire screening round, corresponding to women <26 years on 12 January 2012, were excluded. Furthermore, as women aged 50–54 years, are in a transition period between invitations every third and every fifth year, these women were also excluded. Thus, the study population included women born from January 12, 1947, to January 12, 1957 and from January 12, 1963 to January 12, 1986.
Data
The study population was identified from the Danish Civil Registration System, which is updated daily and holds information such as age and gender for all Danish residents [
13].
Data on hysterectomized women in the study population were retrieved from the Danish National Patient Registry (NPR), which includes data on hospital contacts since 1977. Only total hysterectomy was included in this study; women with a supracervical hysterectomy were not considered as they should remain in the screening program. From 1977 to 1994, diagnoses and procedures in the NPR were classified according to the International Classification of Diseases (ICD) 8 and afterwards according to ICD10 [
14]. The following procedure codes were used to identify women with total hysterectomy: 61,020, 61,040, 61,050, 61,100, 61,780, 62,300, 72,230, 72,240, and 72,650 (ICD8) and KLCD00, KLCD01, KLCD04, KLCD10, KLCD11, KLCD30, KLCD31, KLCD40, KLDC13, KLDC20, KLDC23, KLCD96, KLCD97, KLEF00B, KLEF13, and KMCA33 (ICD10).
From the Danish National Pathology Registry [
15], dates of cervical cytology were retrieved for all women between July 12, 2006, and January 12, 2012. For each woman, only the most recent cervical cytology in the study period was included. Thus, women ages 26–49 years were included with their most recently performed cervical cytology during the period July 12, 2008, to January 12, 2012, and women between 55 and 64 years were included with their most recent cervical cytology between July 12, 2006, and January 12, 2012.
From Statistics Denmark [
16], data on sociodemographic characteristics of the study population by the end of 2012 were obtained. Several variables were included: Educational level was defined as low (≤10 years), middle (11–15 years) and high (>15 years). Occupation was classified as 1) employed, 2) self-employed or chief executive, 3) unemployed or receiving supplementary benefits other than social welfare, 4) retired, 5) social welfare recipient and 6) other. Marital status was categorized as married/cohabiting and single. Ethnicity was categorized as Danish, immigrant and descendant (a person born to an immigrant or to a parent with foreign citizenship). Annual disposable income (income deducted taxes, interest charges) was used as an income measure. Based on tertiles and rounded off to the nearest 100 Euros, disposable annual income was categorized as low (<22,300 Euros), middle (22,300–31,500 Euros) and high (≥31,500 Euros). We linked data using the civil registration number, assigned to all Danish residents [
14].
Analyses
Coverage is defined as the proportion of women in the target population tested at least once within the recommended screening interval. The target population is defined as all women in the age group comprised by the screening program. Thus, women were defined as covered by the NCCSP if they were registered in the Danish National Pathology Registry with at least one cervical cytology within the last 3.5 years (ages 26–49 years) or 5.5 years (ages 55–64 years), allowing for a 6-month delay for cervical cytology. Coverage of the screening program was calculated as follows:
$$ Coverage=\frac{women\ with\ cervical\ cytology\ in\ \Delta t}{women\ in\ t arget\ population\ at\ t he\ end\ of\ \Delta t} $$
Where Δt is the screening interval from July 12, 2008, to January 12, 2012, for women between 26 and 49 years and from July 12, 2006, to January 12, 2012, for women between 55 and 64 years.
The recalculated coverage excluded women from the target population who had undergone total hysterectomy.
To test the differences between the total coverage and the recalculated coverage in two independent samples, a two-sample z-test of the difference between the proportion of covered hysterectomized women and the proportion of covered non-hysterectomised women were carried at each age. The threshold of significance was adjusted for the total of 34 tests (24 for ages 26–49; 10 for ages 55–64) using the Bonferroni method. Likewise, confidence intervals at each age were determined with this method of correction for multiple comparisons. Sensitivity analyses were conducted excluding immigrants and immigrants and descendants to qualify if there may be missing data on hysterectomy among women with other origin than Danish.
A logistic regression model was used to analyze the association between having had a total hysterectomy and sociodemographic factors in the two age groups: 26–49 years (3-year screening interval) and 55–64 years (5-year screening interval). These analyses were also performed adjusting for age as a continuous variable within each age group and the categorical variables ethnicity, marital status, education, occupation and disposable income. Results are presented as odds ratios (ORs) with 95% confidence intervals (CIs). Statistical analyses were conducted using STATA version 12 (STATA Copr., College Station, Tex, USA).