Cancer survivors are at a higher risk of primary cancer recurrence and development of second primary cancer. In both cases, early disease detection is crucial. This cross-sectional study assessed cancer screening participation rates according to cancer history.
Data were obtained from the 2010–2012 Korea National Health and Nutrition Examination Survey for 12,500 participants. Of these, 624 cancer survivors were enrolled in this study. Sampling weights were applied to maintain the representativeness of the Korean adult population.
Overall 2-year cancer screening rates prior to the survey in male and female cancer survivors were 59.9% and 73.7%, respectively, while opportunistic cancer screening rates were 33.5% and 52.1%, respectively. The odds ratios (95% confidence interval) of the overall cancer screening among the cancer survivors, compared to others, were 1.16 (0.79–1.72) in male and 1.78 (1.20–2.63) in female participants, after the adjustment for confounding variables. The odds ratios (95% confidence interval) for opportunistic cancer screening and National Cancer Screening Program among cancer survivors were 1.56 (1.07–2.27) and 0.80 (0.53–1.21) in males and 2.05 (1.46–2.88) and 0.66 (0.46–0.95) in females.
Female cancer survivors showed a higher rate of overall and opportunistic cancer screening than did the male cancer survivors. Further efforts are required to improve cancer screening among male cancer survivors.
In 1986, the National Coalition for Cancer Survivorship in the United States established the definition of a cancer survivor as any person diagnosed with cancer from the time of initial diagnosis until death [
Important concerns for cancer survivors are disease recurrence or metastasis of primary cancer, the development of second primary cancer, and treatment-related adverse effects. A previous study based on cancer registry data showed that cancer survivors faced a 1.1- to 1.6-fold higher risk of a second primary cancer than that of the general population [
The present study aimed to investigate whether a higher rate of cancer screening is evident in cancer survivors than in individuals without a history of cancer. Moreover, we examined the association between a history of cancer and participation in organized versus opportunistic cancer screening.
The 2010–2012 Korea National Health and Nutrition Examination Survey (KNHANES) was conducted as a population-based cross-sectional survey that is designed to assess the health-related behavior, health condition, and nutritional status of Koreans. All health examination components were conducted in a local hospital or at mobile examination centers that traveled to each survey location. The field operation team consisted of a doctor, nurse, radiological technician, interviewer, and dietitian, all of whom followed standardized protocols. The sampling units were households selected using a stratified, multistage, probability sampling design according to the geographic area, sex, and age group, based on household registries. Participants who agreed to participate in the study provided written informed consent [
This present study utilized the data from 25,534 individuals who participated in the 2010–2012 KNHANES. Individuals younger than 40 years (n=11,873) and nonresponders regarding cancer diagnosis (n=140) and cancer screening (n=1,021) were excluded from the study. Thus, the final study population consisted of 12,500 participants (5,369 males and 7,131 females), including 624 cancer survivors (229 male and 395 female survivors).
All participants provided written informed consent and were given the right to refuse to participate according to the National Health Enhancement Act. This study was approved by the Institutional Review Board of the Korea Centers for Disease Control and Prevention.
Body mass index (BMI) was calculated as the ratio of the individual’s weight in kilograms to his or her height in meters squared (kg/m2).
Health-related behaviors and lifestyle information were evaluated using a self-reported questionnaire administered during each survey period. Daily calorie intake was assessed using a 24-hour food recall method. Smoking status was classified as never smoker, former smoker, and current smoker. Participants who smoked cigarettes during the relevant survey period were defined as current smokers. “At-risk” drinking was screened using the Alcohol Use Disorders Identification Test (AUDIT), which consists of three domains: hazardous alcohol use, dependence symptoms, and harmful alcohol use. Participants who engaged in the vigorous-intensity physical activity at least 3 days a week and/or moderate-intensity physical activity or walking at least 5 days a week were part of the regular physical activity group. Participants with chronic diseases were those who answered “yes” to the question “Have you ever been clinically diagnosed with hypertension, dyslipidemia, diabetes, or cardiovascular/cerebrovascular disease?”
Participants were also asked to respond to open-ended questionnaires that included the following question: “What is your average monthly income including salary, property income, pension, government subsidies, and allowance?” Marital status was defined as married and not separated (currently married and living with his or her spouse), single (either not married, previously married but now separated, widowed, or divorced), or nonresponders (a participant who did not respond). Educational level was classified into four categories: elementary school or less, middle school, high school, and college or more. Occupational status was categorized into three groups: (1) manual worker; clerk; service or sales worker; skilled worker in agriculture, forestry, or fisheries; an operator or assembler of vehicles, boats, or planes or of equipment and other machinery; and factory workers; (2) office worker, manager, professional, and administrator; and (3) others, defined as unemployed, housekeepers, and students. Urban residents were defined as individuals who live in the metropolitan regions of cities. Insurance type was categorized as national health insurance (regionally insured and workplace insured) and public assistance (medical aid and essential livelihood protection).
Cancer survivors comprised those who answered “yes” to “Have you ever experienced any cancer or malignancy in your lifetime?” Those who answered “no” were assigned to the non-cancer group.
Participants were also asked the following question: “Have you undergone cancer screening any time within the last 2 years?” Participants who answered “yes” were further questioned about the type of cancer screening. Cancer screening was recategorized as opportunistic or via the National Cancer Screening Program (NCSP) according to the funding source of screening. Participants were included in both groups if they answered that they had received both tests. Opportunistic cancer screening was defined as cancer screening in which the examinee, his or her acquaintances including their family, or employer paid the cost for an examination performed in either the private healthcare sector, such as private general hospitals, clinics, and health checkup centers. The NCSP offers free cancer screening via the Korean National Health Insurance Corporation or at public health centers.
Data obtained from the 2010–2012 KNHANES were considered to represent the standard population. We applied sampling weights to each participant’s data to ensure that the dataset represented the entire Korean population without biased estimates. Continuous variables were presented as a means±standard error (SE), and categorical variables were described as weighted frequencies±SE.
General linear models and χ2 tests were used to compare the means of continuous variables and the frequencies of categorical variables according to cancer history by sex. Odds ratios (ORs) and corresponding 95% confidence intervals (95% CI) for cancer screening among cancer survivors were calculated using multivariate survey logistic regression analyses. The statistical analyses were performed using SAS statistical software ver. 9.4 (SAS Institute Inc., Cary, NC, USA). Differences were considered significant at values of P<0.05 [
The general characteristics of all study participants are shown in
To further examine the association between a cancer diagnosis and cancer screening type, logistic regression analyses were performed after stratifying overall cancer screening by opportunistic screening and NCSP screening (
The results of this cross-sectional study showed that female cancer survivors were more likely to undergo overall cancer screening than females without a history of cancer, after controlling for age and other confounding factors. However, this difference was not observed in male cancer survivors. Stratification of overall cancer screening by opportunistic and NCSP-based screening showed that both male and female cancer survivors were more likely to choose opportunistic cancer screening. For female cancer survivors, the OR for participating in the NCSP was relatively low.
Cancer is the leading cause of death in Korea [
Cancer survivors are at higher risk for not only recurrence of primary cancer but also a second primary malignancy and comorbidities such as cardiovascular diseases and diabetes. These susceptibilities are attributed to genetic factors, behavioral risk factors, and previous anticancer treatment, including chemotherapy and radiotherapy [
After analyzing the 2001, 2005, and 2007 KNHANES data, Cho et al. [
Because this study could not confirm the date of the screening test, it is possible that participants did not receive the NCSP because they received opportunistic screening.
Previous studies reported that barriers hindering participation in NCSPs include less trust in these programs and a lack of awareness of the existence and importance thereof [
Our study had several limitations. First, we could not confirm our conclusion that cancer survivors are more likely to undergo cancer screening because of the cross-sectional design of our study. Individuals concerned about their health tend to undergo more regular health checkups, introducing a risk of overdiagnosis of cancer. However, regardless of the association between cancer survivors and screening rates, all physicians should recommend routine screening for these patients based on practice guidelines. A second limitation was the potential misclassification of some participants, as cancer screening was self-reported using a questionnaire.
Additionally, some cancer survivors might have confused a periodic follow-up after anticancer treatment as active second primary cancer screening [
Despite these limitations, this study has several strengths. It examined the association between cancer history and cancer screening based on the nationally representative 2010–2012 KNHANES data. Sampling weights were applied to all analyses to ensure that the results were representative of the general Korean population. Additionally, overall cancer screening was stratified as either opportunistic cancer screening or NCSP-based screening, which allowed us to discriminate between users of the public versus private healthcare system.
In conclusion, this study showed that all cancer survivors exhibit higher rates of opportunistic cancer screening than non-cancer patients. Moreover, female, but not male, cancer survivors are more likely to participate in overall cancer screening, although female cancer survivors are less likely to participate in the NCSP. These results highlight the need for greater participation of male cancer survivors in cancer screening, for improvements in the NCSP, and for increased public awareness of the national screening program. Health authorities should develop cancer policies that ensure better distribution of their limited resources to those individuals and healthcare units most in need. Finally, access to adequate cancer screening by cancer survivors requires that healthcare professionals establish appropriate evidencebased and cost-effective guidelines.
No potential conflict of interest relevant to this article was reported.
The KNHANES was conducted by the Korea Ministry of Health and Welfare in 2010–2012. We thank all of those who attended the KNHANES and all of the participants in this survey.
Odds ratios for cancer screening of cancer survivors compared to individuals without a history of cancer. Adjusted for age, body mass index, daily calorie intake, household income, marital status, years of education, occupational status, residence area, insurance type, smoking, Alcohol Use Disorders Identification Test score, physical activity, and chronic diseases, including hypertension, dyslipidemia, diabetes, and cardiovascular/cerebrovascular diseases.
General characteristics of all study participants
Characteristic | Males | Females |
---|---|---|
Unweighted no. of participants | 5,369 | 7,131 |
Cancer survivors (%) | 3.2±0.3 | 5.1±0.3 |
Age (y) | 54.9±0.2 | 56.7±0.2 |
Body mass index (kg/m2) | 24.1±0.1 | 24.1±0.1 |
Daily calorie intake (kcal) | 2,353±19 | 1,646±12 |
Current smoker (%) | 41.5±0.9 | 5.1±0.4 |
AUDIT | 9.8±0.1 | 3.0±0.1 |
Regular physical activity (%) |
52.6±0.9 | 48.3±0.8 |
Chronic diseases (%) |
32.0±0.8 | 34.5±0.8 |
Household income (USD) |
459.2±17.8 | 398.9±14.1 |
Marital status (%) | ||
Married, not separated | 89.7±0.6 | 75.1±0.7 |
Single | 6.7±0.4 | 23.7±0.7 |
Nonresponder | 3.6±0.4 | 1.2±0.2 |
Educational level (%) | ||
Elementary school or less | 20.7±0.8 | 40.9±0.9 |
Middle school | 15.9±0.7 | 15.1±0.6 |
High school | 35.3±0.9 | 29.8±0.8 |
College or more | 28.1±1.0 | 14.2±0.7 |
Occupation (%) |
||
Office worker | 24.2±0.9 | 9.5±0.5 |
Manual worker | 55.5±1.0 | 40.9±0.9 |
Others | 20.4±0.7 | 49.6±0.8 |
Urban residence (%) |
44.3±1.3 | 45.2±1.2 |
Insurance type | ||
National health insurance subscriber (%) | 96.8±0.3 | 95.5±0.3 |
Public assistance (%) | 2.8±0.3 | 3.8±0.3 |
Cancer screening within 2 years (%) |
||
Overall | 56.6±0.9 | 60.8±0.8 |
Opportunistic | 30.4±0.9 | 39.2±0.8 |
NCSP | 27.0±0.8 | 30.2±0.8 |
Values are presented as mean or %±standard error.
AUDIT, Alcohol Use Disorders Identification Test; NCSP, National Cancer Screening Program.
Vigorous-intensity activity ≥3 days/wk and/or moderate-intensity activity including walking ≥5 days/wk.
Chronic diseases include hypertension, dyslipidemia, diabetes, and cardiovascular/cerebrovascular diseases.
1 USD=1,000 Korean won.
Occupation was classified as office workers (general managers, government administrators, professionals, and simple office workers), manual workers (clerk; service and sales workers; skilled agricultural, forestry, and fishery workers; persons who operate or assemble craft, equipment, or machines; and factory workers), and others (unemployed, housekeepers, and students).
Urban residents are defined as individuals who live within the metropolitan area of a city. Insurance type was categorized as beneficiaries of the national health insurance system (regionally insured and workplace insured) and public assistance (medical aid and essential livelihood protection).
Cancer screening was recategorized as opportunistic or NCSP according to the funding source of screening. Participants were included in both groups if they answered that they had received both tests. Opportunistic screening was defined as cancer screening which examinee, his or her acquaintances including their family, or employer paid the cost for an examination performed in either the private healthcare sector, such as private general hospital, clinics, and health checkup centers. The NCSP offers free cancer screening via the Korean National Health Insurance Corporation or at public health centers.
Characteristics of the participants according to cancer history
Characteristic | Males |
P-value |
Females |
P-value |
||
---|---|---|---|---|---|---|
Non-cancer controls | Cancer survivor | Non-cancer controls | Cancer survivor | |||
Unweighted no. of participants | 5,140 | 229 | 6,736 | 395 | ||
Age (y) | 54.6±0.2 | 63.2±1.0 | <0.001 | 56.6±0.2 | 59.2±0.7 | <0.001 |
Body mass index (kg/m2) | 24.1±0.1 | 22.8±0.2 | <0.001 | 24.1±0.1 | 24.0±0.2 | 0.725 |
Daily calorie intake (kcal) | 2,365±19 | 2,029±64 | <0.001 | 1,649±12 | 1,578±39 | 0.120 |
Current smoker (%) | 42.2±0.9 | 20.6±3.7 | <0.001 | 5.2±0.4 | 2.7±1.0 | 0.139 |
AUDIT | 9.9±0.1 | 6.9±0.7 | <0.001 | 3.1±0.1 | 1.95±0.22 | <0.001 |
Regular physical activity (%) |
52.6±0.9 | 55.0±4.5 | 0.606 | 48.4±0.9 | 46.4±3.1 | 0.536 |
Chronic diseases (%) |
31.8±0.8 | 37.4±4.0 | 0.145 | 34.1±0.8 | 41.8±3.0 | 0.010 |
Household income (USD) |
465.0±18.5 | 282.9±24.4 | <0.001 | 404.0±14.6 | 359.1±41.6 | 0.271 |
Marital status (%) | 0.461 | 0.010 | ||||
Married, not separated | 89.7±0.6 | 88.7±3.3 | 75.1±0.7 | 75.7±2.6 | ||
Single | 6.6±0.4 | 9.3±2.6 | 23.8±0.7 | 21.2±2.4 | ||
Nonresponder | 3.7±0.4 | 2.1±1.7 | 1.0±0.1 | 3.1±1.2 | ||
Educational level (%) | 0.001 | 0.143 | ||||
Elementary school or less | 20.3±0.8 | 34.0±4.0 | 40.9±1.0 | 41.0±2.9 | ||
Middle school | 15.9±0.7 | 15.2±3.0 | 15.0±0.6 | 17.5±2.1 | ||
High school | 35.6±0.9 | 26.1±3.8 | 29.7±0.8 | 31.8±3.1 | ||
College or more | 28.2±1.0 | 24.8±3.8 | 14.5±0.7 | 9.8±1.7 | ||
Occupation (%) |
<0.001 | <0.001 | ||||
Office worker | 24.5±0.9 | 14.0±3.2 | 9.7±0.5 | 5.7±1.6 | ||
Manual worker | 56.3±1.0 | 31.3±4.1 | 41.7±0.9 | 27.1±3.0 | ||
Others | 19.2±0.7 | 54.7±4.2 | 48.6±0.8 | 67.2±3.2 | ||
Urban residence (%) |
44.3±1.3 | 46.0±3.0 | 0.685 | 45.1±1.2 | 48.0±2.4 | 0.355 |
Insurance type | 0.256 | 0.080 | ||||
National health insurance subscribers (%) | 96.9±0.3 | 94.6±2.1 | 95.5±0.4 | 94.9±1.4 | ||
Public assistance (%) | 2.8±0.3 | 4.4±2.0 | 3.8±0.3 | 3.3±1.1 | ||
Cancer screening within 2 years (%) |
||||||
Overall | 56.5±0.9 | 59.9±4.1 | 0.437 | 65.4±0.8 | 73.7±3.1 | 0.006 |
Opportunistic | 30.3±0.9 | 33.5±3.9 | 0.410 | 38.6±0.8 | 52.1±3.1 | <0.001 |
NCSP | 27.0±0.8 | 28.1±3.4 | 0.749 | 30.5±0.8 | 24.4±2.6 | 0.033 |
Values are presented as mean or %±standard error.
AUDIT, Alcohol Use Disorders Identification Test; NCSP, National Cancer Screening Program.
P-values were obtained based on comparisons of the means (for the continuous variables) or frequencies (for the categorical variables) between cancer survivors and individuals without a history of cancer.
Vigorous-intensity activity ≥3 days/wk and/or moderate-intensity activity including walking ≥5 days/wk.
Chronic diseases include hypertension, dyslipidemia, diabetes, and cardiovascular/cerebrovascular diseases.
1 USD=1,000 Korean won.
Occupation was classified as office workers (general managers, government administrators, professionals, and simple office workers), manual workers (clerk; service and sales workers; skilled agricultural, forestry, and fishery workers; persons who operate or assemble craft, equipment, or machines; and factory workers), and others (unemployed, housekeepers, and students).
Urban residents are defined as individuals who live within the metropolitan area of a city. Insurance type was categorized as beneficiaries of the national health insurance system (regionally insured and workplace insured) and public assistance (medical aid and essential livelihood protection).
Cancer screening was recategorized as opportunistic or NCSP according to the funding source of screening. Participants were included in both groups if they answered that they had received both tests. Opportunistic screening was defined as cancer screening which examinee, his or her acquaintances including their family, or employer paid the cost for an examination performed in either the private healthcare sector, such as private general hospital, clinics, and health checkup centers. The NCSP offers free cancer screening via the Korean National Health Insurance Corporation or at public health centers.
Multivariate-adjusted odds ratios and 95% confidence intervals for cancer screening within 2 years among cancer survivors compared to individuals without a history of cancer (non-cancer)
Males |
Females |
|||
---|---|---|---|---|
Non-cancer controls | Cancer survivors | Non-cancer controls | Cancer survivors | |
Model 1 | 1 | 1.06 (0.74–1.52) | 1 | 1.62 (1.22–2.14) |
Model 2 | 1 | 1.18 (0.81–1.72) | 1 | 1.59 (1.19–2.13) |
Model 3 | 1 | 1.16 (0.79–1.72) | 1 | 1.78 (1.20–2.63) |
Values are presented as odds ratio (95% confidence interval). Model 1: adjusted for age; model 2: adjusted for age, body mass index, daily calorie intake, household income, marital status (married and not separated, single, nonresponders), educational level (elementary school or less, middle school, high school, college or more), occupational status (office worker, manual worker, others), residence area (urban or rural), and insurance type (national health insurance subscriber or public assistance); model 3: adjusted for smoking (never, former, current), Alcohol Use Disorders Identification Test score (continuous), physical activity (regular physical activity), and chronic diseases (hypertension, dyslipidemia, diabetes, cardiovascular/cerebrovascular disease), in addition to the factors in model 2.