Health Screening among HBV Carriers in the Korean National Health and Nutrition Examination Survey V (KNHANES V)

We aimed to investigate the differences in health screening, including medical checkups and cancer screening, between HBV carriers and non-carriers in the Republic of Korea. In the fifth Korean National Health and Nutrition Examination Survey (KNHANES V), conducted between 2010 and 2012, 17,865 persons who answered regarding their HBV-infection status, medical checkup history, liver cancer screening and general cancer screening within the past years were included in the final analysis. In total, 295 persons were HBV carriers. Logistic regression models were used to compare the health check-up rate between the HBV carriers and non-HBV carriers. The HBV carriers were more likely to have been screened for liver cancer [adjusted odds ratio (OR): 2.83, 95% confidence interval (95%CI): 1.90-4.21] or cancer [OR: 1.44, 95%CI: 1.04-1.99]. The HBV carriers showed a probability of receiving medical checkups that was identical to that of the non-carriers [OR: 0.99, 95%CI: 0.72-1.35]. The HBV carriers, who were at higher risk of developing chronic liver disease, were more likely to be screened for cancer, including liver cancer, than the non-HBV carriers; no difference in the rate of medical checkups was observed between the HBV carriers and non-HBV carriers.


Introduction
Hepatitis B virus (HBV) is a major cause of chronic liver diseases, including hepatocellular carcinoma (HCC).The prevalence of HCC in chronic hepatitis-B patients has been reported to be 2.7%, 11%, 25% and 35% at 5, 10, 15 and 20 years, respectively, after HBV infection, (Lee, 2005), and HBV is involved in approximately 70% of the HCC and 12% of occurrence of cholangiocarcinoma in the Korean population (Shin et al., 2011).With the introduction of a vaccination program in 1983, the prevalence of HBV carriers decreased from 8% in the 1980s to 3.7% in 2007 (Park et al., 2010;Yeo et al., 2013).Because of the health risk of HBV carriers, appropriate medical follow-ups should be conducted to prevent consequent HBV-related conditions (Sarkar et al., 2012;Song et al., 2013).According to the fourth Korean National Health and Nutrition Examination Survey (KNHANES IV), of 436 HBV-infected subjects, 27% were under regular liver cancer surveillance, and more than half of the HBV carriers had never received liver cancer screening (Park et al., 2012).Approximately 30% of the HBV carriers who participated in the cancerscreening program of the National Cancer Center in Korea were not aware of their infection status (Shin et al., 2009).
Individual, social, and economic factors determine health-related behaviors (Bae, 1993).This study used

Health Screening among HBV Carriers in the Korean National Health and Nutrition Examination Survey V (KNHANES V)
Hyung Eun Son1 , Sun Jae Jung2 , Aesun Shin3 * the KNHANES V (2010-2012) nationally representative survey to clarify the relationship between an awareness of HBV status and the use of medical care such as necessary medical services, medical screenings and cancer screenings.

Data source
The KNHANES survey is a nationally representative epidemiological study conducted in Korea.It is a study with multi-stage clustered-probability design, with a survey conducted in 20 households per primary sampling unit (PSU).In 2011, 192 PSUs were sampled from the 200,000 PSUs that are geographically defined throughout the country.The KNANES V survey includes annual surveys from 2010 to 2012 that consist of health interviews, physical examinations and nutrition surveys.The health interviews were conducted face-to-face by trained interviewers or self-administered in the mobile examination center (MEC).The physical examination and blood collection for the laboratory tests were conducted in the MEC (Kweon et al., 2014).

Definition of HBV carriers
Among the 25,534 persons who participated in the KNHANES V survey, 17,886 persons over 18 years of age answered the question, "Have you ever been told by doctors or health professionals that you have been infected with HBV?"Because the aim of the study was to assess the awareness of HBV infection and health check-ups, the individuals who answered "yes" to this question were assigned to the HBV carriers group, regardless of their laboratory test results for HBsAg.Similarly, the participants who were seropositive for HBsAg as well as those who were unaware of their infection status were included in the non-HBV carrier group.

Other measurements
The age of the respondents was categorized into 10year groups.The monthly household income was divided into quarters adjusted by age and gender.The AUDIT score was used to rate the level of alcohol consumption (Conigrave et al., 1995), and self-rated stress, a depressive mood, and health status were included in the analysis.The participants were asked for the family history of chronic diseases including hypertension, diabetes, ischemic stroke, ischemic heart disease, and dyslipidemia.The participants were questioned regarding their health examination history, which included medical checkups, cancer screening and liver-cancer screening, in the previous two years.Finally, 17,865 recipients were analyzed after excluding 21 persons who did not answer any of the questions regarding health checkups.

Statistical analysis
A chi-square test was performed to compare the HBV carriers and non-carriers.Logistic regression models were used to calculate the odds ratios (ORs) for health-service utilization by awareness of the HBV infection status after adjustment for related socio-demographic factors.The crude ORs were compared with the ORs adjusted for certain variables, and the factors that caused significant changes in the ORs (more than 0.2) were included as covariates in the model.Every process was conducted with weighted values.The analyses were performed using the software SAS, version 9.4, (SAS Institute Inc., Cary, NC, USA).

Ethics
In the KNHANES survey, written informed consent was provided by every participant.

Baseline characteristics of the participants
After excluding 21 persons who did not answer the questions regarding health checkups, 17,865 participants were included in the final analysis.Among them, 613 were HBsAg-positive by blood tests; 124 (18.4%) of the participants were aware of their infection, and 171 answered that they were infected with HBV.A total of 295 participants were regarded as HBV-carriers with awareness of their infection status.Among the 295 reported carriers, 167 were men (64.0%), and among the non-HBV carriers, 7,393 were men (49.0%).The mean age of the non-HBV carriers was younger than that of the HBV carriers (Table 1).A total of 82.5% of the HBV carriers were living with their spouses, as were 67.6% of the non-HBV carriers.There were higher rates of current smokers and ex-smokers among the HBV carriers relative to the non-HBV carriers.The HBV carriers were more likely to respond that their health status was "very bad".

Awareness of HBV status and the rate of health screening
Table 2 shows the association between awareness of the HBV carrier status and health checkup history.The self-reported HBV carriers were more likely to receive cancer screening, particularly for liver cancer (OR 2.81, 95%CI: 2.05-3.85)within the past two years.There was no difference in the rate for the general medical check-ups between the HBV carriers and non-carriers.

Attendance at general and liver cancer screenings and associated factors
Table 3 shows the association between demographic and lifestyle factors and attendance at general and liver cancer screenings.Among the study participants, those who were known to be HBV carriers tended to undergo general cancer screening and liver cancer screening more frequently [OR 1.44  Adjusted for age, gender, marital status, smoking status and self-rated health status, mutually.

Discussion
In this study, the awareness of HBV infection status was significantly related to the cancer-screening rate, including screening for liver cancer, with no association with medical checkups.In South Korea, the National Cancer Screening Program (NCSP) covers stomach, liver, colorectal, breast and cervical cancer, which makes the rate of general cancer screening higher than before.As a result of a 10-year plan for cancer control, the 5-year survival rate for liver cancer in Korea has improved from 13.2% in 199613.2% in -200013.2% in to 23.3% in 200313.2% in -200813.2% in (Yeo et al., 2013)).NCSP liver cancer screening in high risk groups including HBV carriers is done with alpha-feto protein level and ultrasonography, making the higher rate of liver cancer screening in self-reported HBV carriers.
Several studies have examined the epidemiological characteristics of HBV carriers and health screening related factors (Ayers et al., 2010;Kim et al., 2010;Tanaka et al., 2011;Yang et al., 2013), though few studies have examined the relationship between an awareness of HBV status and health screening.Because HBV carriers are at a higher risk for other chronic liver diseases including hepatocellular carcinoma (HCC) and liver cirrhosis (Lee, 2005;Lee et al., 2012), close medical follow-up of HBV carriers is very important.Liver cancer occurs in populations with a well-defined set of risk factors and has a protracted preclinical phase, meaning that timely identification of disease can lead to appropriate treatment at a more curable stage (Noh et al., 2012).Despite the importance of health screening in the early diagnosis of HBV and regular follow-up of high-risk patients, only 18% of the blood test-confirmed HBV carriers were aware of their status, and this low awareness level was consistent with a previous report from the fourth KNHANES survey (2007)(2008)(2009).
According to the previous studies, the likelihood of receiving medical checkups is affected by socioeconomic factors such as income, gender, health insurance, occupation and accompanying disability (Cho and Lee, 2011).Regarding cancer screening, similar, although different, factors are involved, such as gender, household income, previous cancer screening, health status, smoking status, physical activity and nutritional status (Kim et al., 2010).As a lot of factors affecting medical checkups and cancer screening, the factors considered in this study were adjusted with statistical ways.In this study, 60.2% of the HBV carriers had received medical checkups in the past two years, whereas 54.5% of the non-HBV carriers had.As carriers go to the clinic to check their HBV status through regular blood tests, they might not feel the need to seek medical check-ups other than liver screenings.Another potential explanation is that there is a misunderstanding of HBV hepatitis in the general population as well as a stigma against HBV carriers.In one survey in Japan, 17.1% of the participants answered that they worried regarding disease transmission, avoided contact with infected colleagues and had prejudiced opinions regarding infected colleagues (Eguchi and Wada, 2013).Misunderstandings and prejudices might lead HBV carriers to avoid necessary health screening (van der Veen et al., 2013).
Gender is significantly related to other socioeconomic factors that are significantly related to rates of liver-cancer screening [13].Another study showed that the rate of cancer screening differed according to the health-related responsibility, stress management and health-promoting behaviors (Lee, 2010).Individuals older than 60 might be more likely to be unemployed and could not receive cancer screening in the workplace, resulting in a slight decrease in the magnitude of increasing rate in cancer screening, including liver-cancer screening.In our study, persons who lived with a spouse were more likely to have had medical checkups and cancer screening than those who did not live with partners in marriage or were unmarried.This result agrees with the result of a study showing that married men receive more medical checkups (Yim et al., 2012).In this study, being married or living with a partner affected the higher rates of medical checkups and cancer screening in males and females.One study showed that the rate of medical checkups are affected by many factors, and there are some factors such as medical insurance, employment and physical barriers, not being considered in this study (Culica et al., 2002).
The limitation of the study is the low agreement rate between the self-reported and blood test results for HBV infection.The HBV carrier status was assessed by a questionnaire, regardless of the results of the laboratory test; however, 489 persons who answered that they were not infected with HBV showed positive in a surface HBV antigen in blood test.This low agreement was previously reported from the report using the KNHANES IV data (Park et al., 2013).A previous study reported that awareness of HBV or HCV infection was the determinant for liver cancer screening, and hepatitis carriers confirmed by blood test and unaware of their infection did not differ with non-carriers in the screening rate (Cho et al., 2010).In addition, as it is a cross-sectional study, this study doesn't show causality between awareness of HBV status and health screening.
In summary, HBV carriers who were aware of their carrier status were more likely to have been screened for cancer, including liver cancer; there was no difference in the rate of general medical checkups.Considering the consequences of chronic HBV infection, raising the awareness of carrier status should be emphasized.

Table 1 . General Characteristics of the Self-reported HBV Carriers and Non-HBV Carriers, the Korean National Health and Nutrition Survey V (2010-2012)
DOI:http://dx.doi.org/10.7314/APJCP.2015.16.9.3653Health Screening among HBV Carriers in the Korean National Health and Nutrition Examination Survey V

Table 2 . Relationship between Awareness of HBV Status and the Rate of Health Screening within the Past Two Years, the Korea National Health and Nutrition Survey V (2010-2012)
* adjusted mutually for age, gender, marital status, smoking status and self-rated health status