Socioeconomic disparity in cervical cancer screening among Korean women: 1998–2010

Background Cervical cancer is the sixth most common cause of cancer among Korean women and is one of the most preventable cancers in the world. This study aimed to investigate the change in cervical cancer screening rates, the level of socioeconomic disparities in cervical cancer screening participation, and whether there was a reduction in these disparities between 1998 and 2010. Methods Using the Korean Health and Nutrition Examination Survey, women 30 years or older without a history of cervical cancer and who completed a health questionnaire, physical examination, and nutritional survey were included (n = 17,105). Information about participation in cervical cancer screening was collected using a self-administered questionnaire. Multiple logistic regression analysis was performed to investigate the relationship between cervical cancer screening participation and the socioeconomic status of the women. Results The cervical cancer screening rate increased from 40.5% in 1998 to 52.5% in 2010. Socioeconomic disparities influenced participation, and women with lower educational levels and lower household income were less likely to be screened. Compared with the lowest educational level, the adjusted odds ratios (ORs) for screening in women with the highest educational level were 1.56 (95% confidence interval (CI): 1.05–2.30) in 1998, and 1.44 (95% CI: 1.12–1.87) in 2010. Compared with women with the lowest household income level, the adjusted ORs for screening in women with the highest household income level were 1.80 (95% CI: 1.22–2.68), 2.82 (95% CI: 2.01–3.96), and 1.45 (95% CI: 1.08–1.94) in 2001, 2005, and 2010, respectively. Conclusion Although population-wide progress has been made in participation in cervical cancer screening over the 12-year period, socioeconomic status remained an important factor in reducing compliance with cancer screening.


Background
Cervical cancer is one of the most preventable cancers in the world but it is the eighth leading cause of cancerrelated deaths in Korea [1,2]. Regular Papanicolaou (Pap) tests are an excellent diagnostic tool for detecting not only cancerous, but also precancerous cells, both of which can be removed [3][4][5]. Previous observational studies have consistently shown dramatic reductions in the cervical cancer mortality rate after the implementation of population-based screening programs [6,7].
Since its introduction in the 1940s, the Pap smear has been associated with sharp declines in cervical cancer incidence and mortality [8,9]. In Korea, the age-adjusted incidence of cervical cancer dropped from 18.6 (per 100,000) in 1999 to 12.0 in 2009, and its mortality declined from6.2 per 100,000 in 1995 to 3.8 per 100,000 in 2009 [1,10].
In Korea, there are currently three main cancer screening programs [10], namely the National Cancer Screening Program (NCSP), the Korea National Health Insurance (NHI) program, and screening services voluntarily provided by independent medical facilities. In 1999, the Korean government created the NCSP and established a 10-year plan for cancer control [11]. The NCSP provided free cancer screening services for stomach, breast, and cervical cancers to medical aid recipients between 1999 and 2001 [12]. In 2002, coverage of free cancer screening was expanded to NHI beneficiaries within the lowest 20% income bracket, and in 2003, those within the lowest 30% income bracket were included in the target population. From 2005, the NCSP expanded coverage of free screening for stomach, breast, cervical, liver and colorectal cancer to Medical Aid recipients, and the NHI included beneficiaries who were within the lower 50% of income earners [13].
Despite these public health efforts, the rate of cervical cancer screening may not be uniform across groups with different socioeconomic status. Previous studies suggested that socioeconomic disparities existed in cancer screening rates [14,15], and, in particular, global evidence suggested that the cervical cancer screening rate was influenced by socioeconomic factors as well as demographic factors such as race [16][17][18][19][20][21]. Studies in the United States and Korea also showed that socioeconomic disparities continued in cervical cancer screening participation, though there has been an improvement in overall screening rate [14,22].
Although the above-mentioned studies are informative in identifying important factors influencing cervical cancer screening, they are either cross-sectional studies or not nationally representative, or their study periods were in the late 1990s or the early 2000s. To achieve timely and challenging objectives in public health, such as improvement in cancer screening rates with a reduction in socioeconomic disparities, it is necessary to monitor the long-term trend. Therefore, the objective of this study was to investigate the changes in cervical cancer screening rate over the 12-year period from 1998 to 2010 in a nationally representative sample of Korean women, and to examine whether socioeconomic disparities in cervical cancer screening rates have been reduced over this period.

Data source and subjects
This study used data from the 1998-2010 Korea National Health and Nutrition Examination Survey (KNHANES). The KNHANES is a nationally-representative study managed by the Korean Ministry of Health and Welfare. Participants were enrolled from the household registry using a stratified multistage probability design. The KNHANES consists of four parts: a health interview survey, a health behavior survey, a physical examination, and a nutritional survey. Trained interviewers conducted all surveys and trained healthcare professionals conducted all physical examinations. All participants provided informed consent before participation in the KNHANES.
There were 211,116 women aged 30 years or older who completely answered the health behavior survey between 1998 and 2010. Women who did not provide information about cervical cancer screening or nutrition or who did not have an additional physical examination were excluded from the study. Finally, a total of 17,105 women

Independent variables and outcome variables
From 1998 to 2001, participants were asked, "Have you ever been screened for cervical cancer?" and answers were recorded as either yes or no. From 2005 to 2010, participants were asked, "When was the last time you were screened for cervical cancer?" and answers were recorded as either never, less than 1 year ago, 1-2 years ago, or more than 2 years ago. According to the Korean NCSP guidelines, women 30 years of age and older should receive a Pap smear test every 2 years. In the present study, the outcome variable was whether participants adhered to the Korean NCSP guidelines. We defined participants as not adhering to the NCSP guidelines if they reported never being screened for cervical cancer or were examined more than 2 years prior to completing the questionnaire.
Based on a literature review, we chose several variables as possible factors related to screening participation. Thus, our primary variables of interest were socioeconomic factors, including education, household income, and occupation. Other variables included in the study were age, marital status, health insurance type, health status (limitation in general activities and perceived health status), and health behavior (smoking and obesity). Educational status was divided into three groups: none or elementary school, middle school to high school, and university or higher. Household income, provided by the KNHANES, was calculated by dividing the monthly household income by the square root of the household size, and grouped into four household income quartiles. Occupation was categorized as "white collar (manager, professional level, office workers, service workers, sales)", "blue collar (agriculture, fishery, technicians, mechanics, assemblers, simple labor)", and "others (student, housewife, unemployed)". Marital status was "married" vs. "not married". Health insurance type was categorized as national health insurance for the self-employed, national health insurance for those not self-employed, and being in receipt of Medical Aid. Health status and health behavioral factors included limitation in general activities (yes, no), perceived health status (good or regular vs. bad), smoking (non, ex or current), and body mass index (BMI), categorized as < 18.5, 18.5-< 23, 23-< 25, and ≥ 25 kg/m 2 according to the guidelines provided by the World Health Organization West Pacific Region (2000).

Statistical analysis
The KNHANES was based on a complex sample design. Therefore, all statistical analyses were performed using the survey procedure of SAS version 9.2 (SAS Inc., Cary, NC, USA), specifically designed to analyze such sample survey results. In the survey procedure, information pertaining to complex sample designs such as stratification, clustering, and unequal weighting is combined to analyze the parameters. We used descriptive statistics for the characteristics of the subjects, and reported the number and percentage for each variable. The participation rates in cervical screening were calculated according to all variables. The odds ratios (ORs) and 95% confidence intervals (CIs) were calculated to measure the strength of the association between the measured variables and screening participation. We regarded a p-value of less than 0.05 as statistically significant.

Baseline characteristics and participation in cervical cancer screening
The characteristics of the study population and participation rate in cervical cancer screening from 1998 to 2010 are summarized in Table 1. In this study, the majority of women were married, and enrolled in the NHI program. Most women reported no limitation in their daily activities and were non-smokers. The cervical cancer participation rates increased from 40.5% in 1998 to 52.5% in 2010.
Women with the lowest educational status had a participation rate of 26.1% in 1998 and 43.6% in 2010. However, women with the highest educational status reported a higher participation rate of 54.4% in 1998 and 59.5% in 2010. Women in the lowest household income group had a participation rate of 24.8% in 1998 and 40.7% in 2010. Women in the highest household income group had a participation rate of 47.0% in 1998 and 60.6% in 2010. Figure 1 indicates that the gaps between the highest and lowest educational status and income groups narrowed during the 12 years in Korea. Among the other variables, age was a statistically significant factor which was inversely related to cervical cancer screening during 1998-2010, suggesting that older women were less likely to participate in screening. Although marital status, health insurance type, and smoking status were statistically significant factors in one or two study years, their significance was either not as strong as socioeconomic status or somewhat inconsistent.

Discussion
The objective of this study was to examine the change in rates of participation in cervical cancer screening among Korean women from 1998 to 2010, and to test whether socioeconomic disparities in cervical cancer screening decreased, stayed the same, or worsened. We observed that the participation rate of Korean women 30 years or older in cervical cancer screening was 40.5% in 1998,  2010). Importantly, the participation rates of women in the lowest education and income groups markedly improved over the years, and the gaps with the highest education and income groups were reduced. The results of our study suggest important policy implications for policymakers to improve participation rates and to further reduce the difference in rates according to socioeconomic status. Previous studies have found educational level to be a significant predictor of cervical cancer screening participation [23,24], and educational level has a huge effect on knowledge of the advantages of participation in cervical cancer screening after controlling for other covariates [25,26]. The results of our study are consistent with previous studies in showing that educational level was significantly associated with participation in cervical cancer screening among Korean women, and, more importantly, that the association lasted over a decade. It is worth noting that two previous studies found that disparities in cancer screening by household income were improved, but there was no improvement for disparities in cancer screening by education level among Korean women [27,28].
Previous studies also found that household income was a significant predictor of cervical cancer screening participation [28,29]. It was suggested that to improve cancer screening participation rates in lower income individuals, a primary health care intervention such as an organized program of cervical screening that focuses on deprived groups is needed [30]. Therefore, it is important to keep monitoring how public health policies impact on participation rates over time, such as that which expanded the scope of free cervical cancer examinations to women in the lower 50% income bracket of households [13].
Our study has several limitations. First, although this study examined data in a 12-year study period, it was based on pooled cross-sectional data, from which we cannot detect a causal relationship. Second, the KNHANES is based on self-reported responses to participation in cervical cancer screening, which may raise acquiescence bias or recall bias. To minimize recall bias in collecting the data, the KNHANES was conducted by educated and trained interviewers. However, we acknowledge that the survey was unable to perform a cross-check with medical records. Therefore, recall and acquiescence (social desirability) bias can remain, and may result in misclassification. Although misclassification can be either random or nonrandom, we believe that, in a large nationwide survey such as KNHANES, it was random. Therefore, potential recall bias may lead to an association toward null, and an underestimate of the true association. A previous study also pointed out a similar possibility of underestimation of the actual participation rate [31][32][33]. Finally, other factors that may be significant determinants of cervical cancer screening participation were not included in the current study. For example, there was no control for family history of cervical cancer, age at first sexual intercourse, and knowledge and attitudes about cervical cancer risk factors and benefits of the Pap test.

Conclusion
In conclusion, in the analysis of nationally representative data over a decade, we found that there was an increase in participation in cervical cancer screening programs by Korean women from 40.5% in 1998 to 52.5% in 2010, though the rate remained lower than in other developed countries. We also observed that despite the overall increase in screening rates, socioeconomic disparities continued to exist. Although screening rates in women with the lowest educational levels and household incomes improved over the period, they remained lower than in women of the highest education and income groups. These results demonstrate the need for more aggressive interventions and policies to improve participation in cervical cancer screening especially for those at a lower income and education level. Analyses of cervical cancer screening rates by measures of household income, educational level, and other factors over the long term may help policy-makers to better direct their resources to those of greatest need. Ensuring that free cervical cancer screening programs or other public health programs remain available for women in the lower income groups can lead us closer to national screening goals, yet policies or campaigns still need to address disparities in cervical cancer screening according to educational level.