Differences and trends in gastric, breast, and cervical cancer screening rates between rural and urban areas in 2007-2012 among the Korean population

Abstract

Purpose

This study aimed at examining the ever and recommended screening inequalities of cancers (gastric, breast, and cervical) in rural and urban areas including socio-economic disparities, from 2007 to 2012 amongst Koreans.

Methodology

This cross-sectional population-based study used data from the Korean National Health and Nutrition Examination Survey (KNHANES) of 2007–2012. It included people with no previous cancer diagnosis for gastric, breast, and cervical cancers. Annual Percent Change (APC) was calculated at 95% confidence interval using STATA version 13.0 and MS Excel.

Results

In the ever cancer screening group, the screening rates and trends had an increased in both urban and rural areas: APC values were 4.6% (95% CI, 1.6 to 7.8) and 5.6% (95% CI, 2.7 to 8.6) for gastric cancers, 3.6% (95% CI, 1.5 to 5.6) and 3.6% (95% CI, -0.3 to 7.7) for breast cancers, and 0.3% (95% CI, -0.4 to 1.2) and 0.7% (95% CI, -1.0 to 1.4) for cervical cancers in urban and rural areas, respectively.

Conclusion

Cancer screening rates for gastric and breast cancers showed significant increase from 2007–2012 in both areas. More effort should be implemented and focused on the improvement of cervical cancer screening rates which showed significant lower cancer screening rates compared to the other cancers in both areas.

Introduction

Cancer with varying meanings, is known to be a group of illnesses where cells undergo rapid multiplication and becomes destructive as it develops with distinctive features to attack the immune system [1]. It is one of the chronic diseases causing enormous burden to the society leading to public health problems worldwide. As of GLOBOCAN 2018, cancer incidence and mortality have continuously been rising with an estimated 18.1 million deaths recorded in 2018 [2].

Cancer screening remains important at early stages before it gets complicated with increased chances of better treatment through early diagnosis [3]. Research on cancer screening with respect to urbanity had shown lower screening rates due to unequitable distribution of screening facilities and limited health providers, leading to low screening rates in rural areas compared to urban areas [4, 5]. Urbanity in cancer screening remains a debatable idea even though urban and rural areas have discrepancies depending on socio economic settings, including population size, per capita income, and number of habitants per square kilometer [6, 7].

Korea is also involved as cancer has been a leading cause of death with an incidence estimated at 98.2% as of 2015 [8]. The National Cancer Screening Program (NCSP) in Korea was created to initiate a comprehensive 10-year cancer control plan geared towards building a framework to combat cancer by reducing cancer burden. Screening was done using specific guidelines including a mammography test done every two years for women aged 40 years and above for breast cancer, a Pap smear test done every two years for women aged 30years and above for cervical cancer, a gastro-endoscopy or upper gastrointestinal series every two years for men and women aged 40 years and above for gastric cancer (Supplementary Table 1).

To the understanding of the authors, so far, no study has been done in Korea focused on the same objective to examine the differences in the trends and the evaluation of socioeconomic disparity in cancer screening of gastric, breast and cervical cancers the ever and recommended screening rates between rural and urban areas from 2007–2012 among Koreans. This study is aimed at assessing the discrepancies in cancer screening rates with respect to urbanity and socio-economic status in the Korean population.

Materials And Methods

This study was a cross-sectional, population-based study and the primary source of data was from the Korean National Health and Nutrition Examination Survey (KNHANES) from 2007–2012. KNHANES 2007–2012 study years were chosen because during this period the questionnaire system of data collection was used for cancer screening and information about the last time participants had screening was also included in the questionnaire. The target population of KNHANES comprises noninstitutionalized Korean citizens residing in Korea and the sampling plan followed by a multistage clustered probability design. Independent variables included were urban and rural areas classified according to the Korean Local Government Act. Korea consists of metropolitan cities, provinces and nonmetropolitan cities divided into districts, and provinces divided into cities and counties. The cities and districts include multiple “dong” and counties including multiple “eup” and “myeon” hence in this study we classified dong as urban areas and eup and myeon as rural areas respectively as independent variables.

This study included men and women of ages ≥ 40 years, women of ages ≥ 40 years and women of ages ≥ 30 for gastric, breast and cervical cancers respectively with no previous cancer diagnosis in all three cancers living in rural or urban areas according to the target population of NCSP (Supplementary Table 1). Amongst a total of 4,594 participants in 2007 gastric cancer having 1,984 participants, 1,126 for breast cancer and 1,490 for cervical cancer were involved in the final analysis after exclusion of participants with previous cancer history, lower age group, missing values in cancer screening and inspection methods. The same method was followed for the 2008, 2009 and 2010 years.

In this study, we considered dependent variables based on previous studies on cancer screening rates in rural and urban areas [9–11]. Socio-demographic variables involved in this study were age, education, income, and medical insurance. Medical insurance includes the National Health Insurance (NHI) which is compulsory to all Koreans residents and the Medical Aid Program put in place by the government to secure the minimum living standards to low income-households [12].

The general characteristics of study participants and cancer screening rate were calculated using summary statistics and weighted frequencies and percentages of screening rates, with 95% confidence intervals, were calculated for the three different cancers in rural and urban areas using chi-squared tests. We adjusted for age after dividing the number of ever cancer screened participants by the total number of screened and unscreened population in each age category as a percentage and multiplied by age-specific weights using the Korea 2000 mid-year as standard population within each age category. The weighted rates were later summed up to give the age-adjusted screening rates in urban and rural areas.

Trends in cancer screening rates were calculated using the Annual Percentage Change (APC) as an estimator in the Korean population from 2007 to 2012 in urban and rural areas. Changes in annual screening rates with 95% confident intervals in rural and urban areas were calculated after adjusting for age using the Korea 2000 mid-year as standard population.

Annual percent change as an estimator

Denote the observed screening rate at time t_i as r_i with the associated random variable R_i, and denote the corresponding expected rate as y_i= E(R_i/t_i), where n observed ordered time points are a = t₁ < t₂……<t_n = b. Assume that t_i represents years and is equally distributed over [a,b] with t_j+1 = t_j + 1. Also assume that log (γ_i) is linear over the entire time interval [a,b], that is log (γ_i) = β_o + βt_i for I = 1……n. Then the annual rate of change is γ_j+1/γ_j = exp(β). (γ-_j -γ- _j)/γ-_{j =}exp(β)-1 and the conventional APC is APC = [exp(β)-1] [13].

Socio-economic characteristics including age range, income status, education levels and residential areas on recommended and ever screening rates from 2007–2009 and 2010–2012 were analyzed using the multivariable logistic regression. This was done to verify which socio-economic factors are more liable to influence screening in urban and rural areas. A p-value of < 0.05 was considered significant for all analysis. All analyses were conducted using STATA software version 12.0.

Results

Table 1 shows the distribution of study participants according to socio-economic status. There were significant differences between the different socio demographic factors in participants in urban areas compared to those in rural areas with significant p-values of <0.001 even though there was no statistical significance in male and female participants with insurance status in some years.

Table 2 shows age-standardized ever screening rate and annual percent changes of gastric, breast and cervical cancer from 2007 to 2012. Cancer screening rates in gastric and breast cancers had increased during the study years, but cervical cancer did not show any significant increase in screening trends. The screening trends had increased by 4.6%, 3.6%, and 0.3% in urban areas and 5.6%, 3.6%, and 0.7% in rural areas in gastric, breast, and cervical cancers, respectively.

In gastric cancer, after adjusting for age, income and educational levels, there was no significant differences between urban and rural areas. However, during 2007-2009, rural areas showed a 10% higher recommended screening rate with respect to urban areas (Table 3).

However, the significant differences between urban and rural areas were not observed during the 2010-2012 study years. In breast cancer, even though other socio-economic status was affected by screening during 2007-2009, rural areas showed about 1.2 folds higher for the ever and recommended screening rates during 2007-2012 with respect to urban areas. However, rural areas had a lower recommended screening during 2010-2012 even though the screening rate was not statistically significant as compared to urban areas (Table 4). After adjusting for socio-demographic factors including age, education, and income status, there was a 20% lower recommended cervical cancer screening in 2007-2009 in rural areas, compared to urban areas, and the differences were exaggerated from 2010-2012 (Table 5).

Discussion

Recommended and the ever-screening rates for gastric, breast and cervical cancers had increased during 2007–2012 in both rural and urban areas. There was no significant increase in cervical cancer screening rates which might have been due to women believes and reactions towards male gynecologist. Studies in Greece and Korea on women’s attitude about cervical screening showed a significant number of women preferring female physicians as to male physicians [14, 15]. In Korea, lower cervical cancer screening has also been observed in some recent studies done in 2017 using data from KHNANES with similar results [16] suggesting that this was associated with lack of medical equipment leading to reduced cancer screening rates. In 2009, one study done in Korea on status of Korean women to receive cervical cancer screening showed similar lower screening rates among old women and emphasized this is because they believe menopause frees them from diseases related to sexual organs [17]. This study shows lower screening rate of cervical cancer in participants ages ≥ 50 years. A research done in Asia [18] evocated that lower cervical cancer screening rates is due to several barriers including knowledge about cervical cancer screening, emotional barriers including fear and social stigma, including rural availability of appropriate equipment example appropriate chair for sample collection and specialist for cervical cancer screening. Screening rates for gastric and breast cancers increased during 2007–2012 but there was no consistent trend by urban and rural areas. Cervical cancer screening had not increased that much as compared to other cancers in rural and urban areas, but annual percent change had shown increasing trends in both urban and rural areas from 2007–2012 certainly due to the implementation of the NCSP.

Inequality in screening between rural and urban areas has been a debatable topic and a cause for concern to many researchers due to differences in socio-economic settings. The uneven distribution of medical facilities contributes to screening discrepancies in various geographical regions. Being the main aim of this study, the results proved otherwise in the Korean population showing that urban and rural areas does not observe inequality in screening rates especially in gastric and breast cancers certainly due to the implementation of nationwide screening program non the less cervical cancer had showed increased screening inequality. Studies done abroad with similar objective showed lower cancers screening rates in rural areas compared to urban areas due to socio economic disparity [19, 20], a study done also in USA showed no discrepancy in urban rural screening rates and the older age groups showed lower screening rates [9] in accordance with this study but the results cannot be compared with the results of this study since Korea has NCSP.

This study showed socio-economic disparity in ever and recommended screening rates in both rural and urban areas. The older age groups had shown significantly lower screening rates in both rural and urban areas in all three cancers, compared to lower age groups. his was contradictory to one study done in Australia on the disparities in breast cancer stages at diagnosis in urban and rural adult women even though in this study rural women were more likely to be diagnosed at advanced stages of breast cancer compared to participants from urban areas [21]. Education and income status were directly proportional to screening rates in all three cancers in this study from 2007–2012. Income status was not left out in this study however the increase cancer screening rates in high income earners in both rural and urban areas was in conformity with some previous studies done in Korea and abroad with recommended cancer screening programs showing income disparity in cancer screening even though in Korea there is a nationwide insurance coverage [22, 23] that was put in place since 1989. One study done in Croatia [24] also had similar results and proposed this can be due to reduced accessibility to screening and screening expenses, but this could not be applied to the case of Korea with NCSP implemented since 1999 there has been a sending of reminders to high-risk population, an increased access to screening programs, a reduction of personal expenses, and provider assessments and feedback [25]. Some previous studies done on cancer screening also experienced education and income disparity even though the screening test used in these studies was less expensive [22–24]. However, this was not very different from the Korean system with almost free cancer screening programs. Previous studies regarding reasons of nonattendance of cancer screening provided that the proportion of economic reasons has been decreased [26], suggesting that NCSP decreased economic barrier.

This study has several limitations. Being a population-based, cross- sectional study, it might have been limited by non-response bias. Secondly, the 2005 survey was eliminated in this study because the data set was very heterogeneous with more than 10 thousand missing values which might have affected the results. Thirdly, there was unequal distribution of the number of participants in rural and urban areas. Lastly the 1998 to 2006 survey years was not included in this study even though the year 2007 marks the beginning of a yearly cancer screening survey with the health interview, examination, and nutrition survey conducted by the Korean Center for Disease and Control. In 2007, there has been survey region widening with a sudden expansion of the number of regions from 200 (1998–2005) to 500 regions in 2007, with the health examination survey conducted from July to December. In addition to expansion of the cancer screening coverage, changes in survey scheme may also affect the rapid increment in 2007[14]. The changes and widening of KNHANES survey scheme were aimed at providing timely health statistics for monitoring changes in health risk factors and diseases and also in the development of public health policy programs [15].

Despite the limitations, this study also has some strengths, including the fact that this a nationwide, population-based study that has been conducted since 1998 is sufficiently representative to investigate the yearly changes in cancer screening rates in rural and urban areas from 2007–2012 in the Korean population.

In conclusion, this study has found out that cancer screening rates had increased in all three cancers in a steady manner from 2007–2012 in both rural and urban areas. There were not much significant discrepancies in cancer screening rates between rural and urban areas even though rural areas presented slightly lower screening rates compared to urban areas in cervical cancer screening. This may be due to unequitable distribution of screening facilities. Participants with low-income levels and those of the older age groups have shown significantly lower screening rates as compared to other socio-economic factors however the annual percent change was highest in these two groups showing that screening disparity with respect to socio economic status have gradually been improved in older age groups and people with lowest income levels during the study period. More effort should be implemented and focused on the improvement of cervical cancer screening rates which showed significant lower cancer screening rates compared to the other cancers in both areas.

Declarations

Funding: The authors declare no funds were received during the preparation of this manuscript.

Conflict of interest: The authors declare no conflict of interest.

Authors contributions: Designed the study and Data analysis: Kumban WC. Yunhwan L. Authored the paper: Kumban WC. Yunhwan L. Writing review.

Data availability: Data availability statement:  KNHANES 2019 available using the link below with consent. https://knhanes.kdca.go.kr/knhanes/sub03/sub03_02_05.do.

Ethical approval: The IRB of the institution confirms no ethical statement is required since it’s a longitudinal study using secondary data.

Consent to participate: All authors signed a consent to keep the privacy of the study participants with respect to the data guidelines.

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Tables

Table 1 is available in the Supplementary Files section.

Table 2: Age standardized ever screening rate and annual percent change of gastric, breast and cervical cancer from   2007-2012.

N% (screening rate in percentage), 95%CI (95% Confidence Interval), APC (Annual Percent Change),

Table 3: Multivariate logistic regression of ever and recommended gastric cancer screening rate with respect to urban and rural areas.

(OR=Odd Ratio), (95% CI= 95% Confidence Interval), (Ref=reference)

Table 4: Multivariate logistic regression of ever and recommended breast cancer screening rate with respect to urban and rural areas.

Table 5: Multivariate logistic regression of ever and recommended Cervical cancer screening rate with respect to urban and rural areas.