Literature DB >> 26712427

A Decade-old Change in the Screening Rate for Hepatocellular Carcinoma Among a Hepatitis B Virus-infected Population in Korea.

Hee Yeon Kim, Chang Wook Kim1, Jong Young Choi, Chung-Hwa Park, Chang Don Lee, Hyeon Woo Yim.   

Abstract

BACKGROUND: Evaluating a change in the screening rate for hepatocellular carcinoma (HCC) is critical for understanding screening implementation, and whether targeted population groups are receiving proper screening. This study examined recent nationwide changes in HCC screening use among hepatitis B virus (HBV)-infected populations after the introduction of the Korean National Cancer Screening Program and predictors of screening adherence.
METHODS: We analyzed 165 and 276 participants ≥40 years of age who were hepatitis B surface antigen-positive from 2001 (14,936 participants) to 2010-2011 (9159 participants) Korea National Health and Nutrition Examination Surveys, respectively. Demographic data, socioeconomic factors, and HCC screening use were collected by means of self-reported questionnaires.
RESULTS: The rate of HCC screening within the previous 2 years increased significantly from 17.5% in 2001 to 40.3% in 2010-2011 (P < 0.0001). The rate of HCC screening use increased from 2001 to 2010-2011 in all study populations. Subjects who had a higher income status and were aware of their infection were more likely to have undergone recent HCC screening.
CONCLUSIONS: This study showed a substantial increase in HCC screening in high-risk HBV-infected subjects from 2001 to 2010-2011. However, the HCC screening participation rate remained suboptimal despite the introduction of the nationwide screening program. Efforts should be made to identify high-risk individuals and increase attendance at HCC screening events among high-risk groups.

Entities:  

Mesh:

Year:  2016        PMID: 26712427      PMCID: PMC4797536          DOI: 10.4103/0366-6999.172551

Source DB:  PubMed          Journal:  Chin Med J (Engl)        ISSN: 0366-6999            Impact factor:   2.628


INTRODUCTION

Hepatocellular carcinoma (HCC) is the fifth and seventh most commonly diagnosed cancer in males and females, respectively, and the third leading cause of cancer mortality worldwide. The incidence and mortality rates for HCC are similar because most HCC patients are diagnosed at an advanced stage, highlighting the importance of early HCC detection in the application of potentially curable treatment options.[1] Hepatitis B virus (HBV) is the major risk factor for HCC[2] and early detection of HCC through surveillance of high-risk populations improves HCC mortality.[3] Therefore, national practice guidelines recommend regular HCC surveillance for high-risk HBV-infected persons.[45] In Korea, the Korean Association for the Study of the Liver and the National Cancer Center jointly developed guidelines for HCC screening in 2001 recommending that high-risk adults with HBV infection should undergo surveillance for HCC using ultrasonography and alpha-fetoprotein (AFP) every 6 months.[6] Based on this recommendation, the Korean government introduced nationwide HCC screening as a part of the organized National Cancer Screening Program (NCSP) for lower income levels in 2003. The NCSP provides a biannual ultrasonography and AFP test for males and females ≥40 years of age that were hepatitis B surface antigen (HBsAg)-positive, had hepatitis C infection, or liver cirrhosis. In the beginning, the NCSP supplied Medicaid recipients and National Health Insurance (NHI) beneficiaries in the lower 30% income bracket with free HCC screening services. In 2006, the NCSP provided participants in the lower 50% income bracket with HCC screening services free of charge.[7] In addition to these national HCC screening programs, ultrasonography and AFP testing are performed in outpatient clinics or private health promotion centers across Korea. Based on the advantages of early HCC detection, it is crucial to investigate the rate of adherence to HCC screening to understand how HCC surveillance tests are being implemented in high-risk groups in Korea. Previous studies have reported that the rate of adherence to HCC surveillance was low.[8910] Although a nationwide organized screening program has been provided in Korea since 2003, no study to date has investigated changes in adherence rates to HCC screening in practice. This study used data from the second and fifth Korea National Health and Nutrition Examination Surveys (KNHANES), which is a nationally representative, cross-sectional survey. We analyzed screening rates for HCC among the HBV-infected Korean population after the introduction of the nationwide HCC screening program and assessed factors related to HCC screening adherence.

METHODS

Study population

This study used the second KNHANES (KNHANES II) data collected during 2001 and fifth KNHANES (KNHANES V) data collected from 2010 to 2011. The KNHANES is a series of nationally representative, cross-sectional health and nutrition examination surveys conducted by the Korean Centers for Disease Control and Prevention since 1998. It uses a complex, stratified, multistage probability sample representative of the Korean population. The procedures for selecting the sample and conducting the interviews and examinations have been described elsewhere.[11] Consistent with current Korea NCSP recommendations, we restricted the analysis to adults ≥40 years of age at the time of the interview. There were 14,936 individuals who participated in KNHANES II and 9159 who participated in KNHANES V who met the age criteria; 3763 and 8145, respectively, of these participants, were tested for HBsAg. Of these, 176 and 285 participants in KNHANES II and V, respectively, were infected with HBV. Among these populations, we excluded participants who reported a personal history of HCC (n = 4 in KNHANES V) or did not answer questions on compliance to HCC screening tests (n = 11 and 5 in KNHANES II and V, respectively). In the final analysis, we included 165 and 276 participants ≥40 years of age who were HBsAg-positive from KNHANES II and V, respectively [Figure 1].
Figure 1

Flowchart of the study population selection. KNHANES: Korea National Health and Nutrition Examination Surveys.

Flowchart of the study population selection. KNHANES: Korea National Health and Nutrition Examination Surveys. All participants provided informed consent, and the protocol was approved by the Institutional Review Board of the Korea Centers for Disease Control.

Data collection

HBsAg was measured using enzyme-linked immunosorbent assays in KNHANES II (CODA; Bio-Rad, Hercules, CA, USA), and an electrochemiluminescence immunoassay (Modular E-170; Roche Diagnostics, Mannheim, Germany) in KNHANES V. All other parameters were determined from the self-reported questionnaires. The primary outcome variable was whether HCC screening had been conducted. In KNHANES II, participants were asked, “Have you had a screening test for HCC within the last 2 years?”; possible responses were “yes,” “no,” and “do not know.” In KNHANES V, participants were asked, “When was the last time you had HCC screening test?”; possible responses were “never,” “≤6 months ago,” “>6 months and ≤1 year ago,” “>1 year and ≤2 years ago,” “>2 years ago,” and “do not know.” To standardize the major outcome variable, participants who had undergone HCC screening test within the previous 2 years were considered to have undergone recent HCC screening. Participants were also asked, “Have you ever been diagnosed with HBV infection by a doctor or a health professional?” Subjects who answered positively to this question were defined as those who were self-aware of HBV infection. Data were also collected on demographic and socioeconomic factors (e.g., age, gender, urbanity, marital status, education, household income, health insurance, smoking, and alcohol consumption) relevant to HCC screening. Two categorical levels for education attainment were used based on the highest level of education achieved by the respondent: High school or higher, and less than high school. Household income was divided into four groups on the basis of monthly income quartile. With regard to health insurance, subjects were categorized into “NHI beneficiary” or “medical aid beneficiary.” Subjects were categorized into current smokers, past smokers, and nonsmokers. Three categorical groups for alcohol amount were used: Light drinking (<10 g/d for women, <20 g/d for men), moderate drinking (10–20 g/d for females, 20–40 g/d for males), and heavy drinking (≥20 g/d for females, ≥40 g/d for males).

Statistical analysis

Statistical analyses were performed using SAS software (version 9.3, SAS Institute, Cary, NC, USA), which incorporates sample weights and adjust the analyses for the complex sample design of the survey. The survey sample weights, which were calculated taking into consideration the sampling rate, response rate, and age/gender proportion of the reference population (2000 and 2005 National Census Registry, respectively), were used in all analyses to produce estimates representative of the noninstitutionalized civilian Korean population considering a complex, stratified, multistage probability sampling design. The prevalence and 95% confidence interval (CI) of HBV infection aged ≥40 years were estimated according to the baseline characteristics. The HCC screening rate within 2 years and 95% CI for each survey year were calculated using cross-tabulation. Differences in the proportion of participants who had HCC screening in each survey were analyzed using the Chi-square test (PROC SURVEYFREQ procedure). To identify risk factors for adherence to an HCC screening program, the crude and adjusted odds ratios (ORs) were calculated using logistic regression (PROC SURVEYLOGISTIC procedure). The covariates for the adjusted OR calculation were household income, smoking status, awareness of HBV infection, and survey year. These variables were obtained statistically significant variables by univariate logistic regression. A P < 0.05 was considered to indicate statistical significance.

RESULTS

Baseline characteristics of the participants ≥40 years of age with hepatitis B virus infection

There were 165 and 276 participants ≥40 years of age infected with HBV in 2001 and 2010–2011, respectively. The weighted seroprevalence of HBV infection was 4.3% in 2001, and 3.8% in 2010–2011. Table 1 shows the demographic characteristics of these participants. The baseline distribution of the study population was broadly similar between survey years, with the exception of educational attainment, household income, smoking status, and alcohol intake.
Table 1

Baseline characteristics of the participants ≥40 years of age with hepatitis B infection

VariablesKNHANES II (2001)KNHANES V (2010–2011)χ2P


% (95% CI)*Total number% (95% CI)*Total number
Overall4.3 (3.6–5.0)1653.8 (3.3–4.3)2761.310.253
Gender
 Male46.1 (38.1–54.2)7751.0 (43.4–58.6)1280.670.415
 Female53.9 (45.8–61.9)8849.0 (41.4–56.6)148
Age
 40–49 years48.9 (42.3–55.5)8238.7 (31.4–46.0)804.630.099
 50–59 years30.0 (23.6–36.3)4836.3 (29.4–43.2)95
 ≥60 years21.1 (14.7–27.4)3525.0 (19.7–30.2)101
Marital status
 Never married13.7 (8.8–18.5)239.9 (5.8–13.9)331.340.247
 Married or partnered86.3 (81.5–91.2)14290.1 (86.1–94.2)242
Education
 Less than high school56.9 (48.5–65.2)9443.3 (36.1–50.6)1375.380.020
 High school or higher43.1 (34.8–51.5)7056.7 (49.4–63.9)138
Household income
 1st quartile27.0 (20.3–33.7)4213.5 (9.3–17.7)5112.580.006
 2nd quartile23.7 (16.7–30.7)3930.4 (23.8–37.0)81
 3rd quartile22.6 (16.7–28.5)3522.9 (16.9–28.9)59
 4th quartile26.7 (20.0–33.4)4133.2 (26.5–39.9)83
Health insurance
 National health insurance97.4 (95.2–99.5)15897.7 (95.8–99.6)2690.010.915
 Medicaid2.6 (0.5–4.8)52.3 (0.4–4.2)7
Urbanity
 Urban72.9 (68.0–77.8)11775.9 (68.4–83.5)2050.920.338
 Rural27.1 (22.2–32.0)4824.1 (16.5–31.6)71
Smoking
 Nonsmoker59.3 (52.1–66.4)9852.3 (44.5–60.0)1569.100.011
 Past smoker10.6 (5.8–15.5)1823.1 (16.6–29.5)64
 Current smoker30.1 (23.0–37.2)4924.7 (18.1–31.3)55
Alcohol consumption
 No55.7 (46.9–64.6)9333.2 (26.3–40.0)10120.410.0001
 Light28.5 (21.9–35.2)4641.9 (34.9–49.0)120
 Moderate10.9 (5.2–16.5)1814.8 (9.0–20.6)33
 Heavy4.9 (2.2–7.6)810.1 (5.6–14.6)21
Awareness of hepatitis B infection
 No83.7 (77.8–89.5)13879.0 (73.0–85.0)2141.170.279
 Yes16.3 (10.5–22.2)2721.0 (15.0–27.0)62

*Based on weighted data. †Based on unweighted data. P values are derived from Rao-Scott Chi-square test (PROC SURVEYFREQ procedure). KNHANES: Korea National Health and Nutrition Examination Surveys; CI: Confidence interval.

Baseline characteristics of the participants ≥40 years of age with hepatitis B infection *Based on weighted data. †Based on unweighted data. P values are derived from Rao-Scott Chi-square test (PROC SURVEYFREQ procedure). KNHANES: Korea National Health and Nutrition Examination Surveys; CI: Confidence interval.

Rates of recent hepatocellular carcinoma screening tests within 2 years

Table 2 shows changes in rates of HCC screening use between 2001 and 2010–2011. The proportion of study participants with HBV infection reporting an HCC screening test within the previous 2 years increased significantly from 17.5% in 2001 to 40.3% in 2010–2011 (P < 0.0001). An increased rate of HCC screening tests from 2001 to 2010–2011 was also observed in the entire study population.
Table 2

Rate of recent hepatocellular carcinoma screening within 2 years

VariablesKNHANES II (2001)KNHANES V (2010–2011)χ2P

% (95% CI)*Total number% (95% CI)*Total number
Overall17.5 (12.0–22.9)2940.3 (33.2–47.4)10623.05<0.0001
Gender
 Male23.1 (14.5–31.7)1744.5 (33.7–55.3)538.920.003
 Female12.6 (5.1–20.1)1236.0 (26.5–45.4)5311.620.001
Age
 40–49 years24.1 (14.7–33.4)2040.1 (27.8–52.4)304.190.041
 50–59 years12.1 (2.3–22.0)643.0 (30.9–55.0)4210.990.001
 ≥60 years9.6 (0.0–21.0)336.8 (25.0–48.5)346.850.009
Marital status
 Never married23.2 (6.8–39.6)545.3 (24.1–66.5)132.690.101
 Married or partnered16.5 (10.9–22.2)2439.8 (32.4–47.3)9321.39<0.0001
Education
 Less than high school14.4 (7.5–21.3)1436.0 (25.6–46.5)4910.980.001
 High school or higher21.7 (12.8–30.7)1543.6 (33.8–53.4)579.470.002
Household income
 1st quartile12.0 (1.7–22.4)524.6 (12.3–36.8)152.060.151
 2nd quartile11.5 (1.8–21.3)530.3 (18.3–42.3)254.640.031
 3rd quartile19.2 (6.5–32.0)750.6 (35.9–65.3)288.370.004
 4th quartile25.1 (10.5–39.8)1046.7 (34.0–59.4)374.290.038
Health insurance
 National health insurance17.5 (11.8–23.1)2840.7 (33.5–48.0)10522.26<0.0001
 Medicaid23.9 (0.0–63.3)121.7 (0.0–58.4)10.010.934
Urbanity
 Urban18.5 (11.7–25.3)2141.6 (33.3–49.9)7916.52<0.0001
 Rural14.6 (5.9–23.2)836.3 (19.6–53.0)276.100.014
Smoking
 Nonsmoker13.7 (6.4–21.1)1435.7 (26.5–45.0)5611.090.001
 Past smoker47.9 (25.3–70.4)851.3 (36.0–66.6)300.060.804
 Current smoker14.0 (5.1–22.8)739.9 (24.9–54.8)209.100.003
Alcohol consumption
 No13.3 (6.0–20.6)1342.9 (30.2–55.6)3815.52<0.0001
 Light16.0 (7.1–24.9)737.3 (27.4–47.2)477.900.005
 Moderate39.1 (16.4–61.9)738.7 (17.6–59.7)120.0010.975
 Heavy24.8 (2.8–46.9)247.1 (23.1–71.1)91.8210.177
Awareness of hepatitis B infection
 No14.8 (9.3–20.3)2135.1 (27.1–43.1)7116.17<0.0001
 Yes31.1 (13.7–48.6)860.0 (45.9–74.2)355.850.016

*Based on weighted data; †Based on unweighted data. P values are derived from Rao-Scott Chi-square test (PROC SURVEYFREQ procedure). KNHANES: Korea National Health and Nutrition Examination Surveys; CI: Confidence interval.

Rate of recent hepatocellular carcinoma screening within 2 years *Based on weighted data; †Based on unweighted data. P values are derived from Rao-Scott Chi-square test (PROC SURVEYFREQ procedure). KNHANES: Korea National Health and Nutrition Examination Surveys; CI: Confidence interval.

Factor influencing hepatocellular carcinoma screening tests among hepatitis B virus-infected participants ≥40 years of age

The results of the multivariable logistic regression models for factors associated with the adherence to HCC screening tests are reported in Table 3. Following adjustments for household income, smoking status, awareness of HBV infection, survey year, and individuals in higher income quartiles were more likely to have undergone recent HCC screening (third quartile: Adjusted OR = 3.03, 95% CI: 1.27–7.23; fourth quartile: Adjusted OR = 2.49, 95% CI: 1.08–5.73). Self-awareness of HBV infection was positively related to recent HCC screening (adjusted OR = 2.74, 95% CI: 1.40–5.38). Survey year 2010–2011 was associated with a significantly higher rate of recent HCC screening (adjusted OR = 3.37, 95% CI: 1.95–5.81).
Table 3

Regression models for adherence to hepatocellular carcinoma screening

Variables% (95% CI)*Total numberCrude OR (95% CI)PAdjusted OR (95% CI)P
Gender
 Male42.5 (32.6–52.4)701
 Female33.4 (25.0–41.8)650.68 (0.39–1.19)0.175
Age
 40–49 years38.1 (27.2–48.9)501
 50–59 years40.3 (29.2–51.4)481.10 (0.58–2.10)0.776
 ≥60 years34.4 (23.5–45.3)370.85 (0.43–1.68)0.643
Marital status
 Never married42.3 (23.6–61.0)181
 Married or partnered37.6 (30.8–44.3)1170.83 (0.37–1.86)0.650
Education
 Less than high school33.3 (24.1–42.4)631
 High school or higher41.9 (32.8–51.0)721.46 (0.84–2.54)0.185
Household income
 1st quartile22.3 (12.2–32.5)2011
 2nd quartile28.8 (17.7–39.9)301.49 (0.69–3.21)0.3111.28 (0.56–2.94)0.560
 3rd quartile47.6 (34.2–61.0)353.33 (1.51–7.35)0.0033.03 (1.27–7.23)0.013
 4th quartile45.0 (33.2–56.8)473.00 (1.40–6.41)0.0052.49 (1.08–5.73)0.032
Health insurance
 National health insurance38.4 (31.9–44.9)1331
 Medicaid22.0 (0.0–54.8)20.40 (0.05–3.25)0.387
Urbanity
 Urban39.3 (31.7–46.9)1001
 Rural33.8 (18.8–48.9)350.79 (0.36–1.70)0.540
Smoking
 Nonsmoker33.2 (25.0–41.4)7011
 Past smoker51.1 (36.5–65.7)382.08 (1.03–4.21)0.0421.78 (0.87–3.65)0.117
 Current smoker36.7 (23.3–50.1)271.16 (0.58–2.31)0.6831.14 (0.55–2.37)0.725
Alcohol consumption
 No38.2 (27.3–49.1)511
 Light35.8 (26.6–45.0)540.88 (0.50–1.57)0.645
 Moderate38.7 (19.2–58.2)191.02 (0.40–2.64)0.964
 Heavy45.9 (23.1–68.8)111.40 (0.48–4.11)0.544
Awareness of hepatitis B infection
 No32.9 (25.7–40.1)9211
 Yes57.7 (44.5–70.9)432.76 (1.46–5.22)0.0022.74 (1.40–5.38)0.003
Survey year
 KNHANES II (2001)17.5 (12.0–22.9)2911
 KNHANES V (2010–2011)40.3 (33.2–47.4)1063.54 (2.14–5.85)<0.00013.37 (1.95–5.81)<0.0001

*Based on weighted data; †Based on unweighted data. Crude and adjusted ORs (95% CIs) were calculated using logistic regression (PROC SURVEYLOGISTIC procedure). OR: Odds ratio; CI: Confidence interval; KNHANES: Korea National Health and Nutrition Examination Surveys.

Regression models for adherence to hepatocellular carcinoma screening *Based on weighted data; †Based on unweighted data. Crude and adjusted ORs (95% CIs) were calculated using logistic regression (PROC SURVEYLOGISTIC procedure). OR: Odds ratio; CI: Confidence interval; KNHANES: Korea National Health and Nutrition Examination Surveys.

DISCUSSION

Given the considerable burden and overall poor prognosis of HCC,[112] early diagnosis through screening enables curative treatments, and, therefore, has the potential to reduce liver-related mortality.[31314] It is important to investigate changes in the use of HCC screening to understand how screening is being conducted in practice following the introduction of a nationwide HCC screening program in Korea. This study revealed a significant increase in recent HCC screening from 2001 to 2010–2011. In 2001, only 17.5% of respondents had undergone HCC screening test; however, 40.3% of HBV-infected participants had been screened for HCC within the preceding 2 years in 2010–2011. This substantial increase in HCC screening may be partially explained by NCSP. Since 2003, the Korean government has provided individuals at high-risk for developing HCC for free or with a 90% subsidy for HCC screening services.[815] This organized screening program may contribute to the increase in HCC screening. However, no prominent increase in HCC screening among individuals with low household income was detected. Moreover, the participation rate of HCC screening in the low-income group remained low, even though screening services were offered free of charge by the NCSP. HCC screening programs are different from those of other solid cancers, such as stomach, breast, cervical, or colorectal cancers, in that they target not a general population but a high-risk population.[7] Therefore, omission from the target population might cause underuse of HCC screening tests among individuals in the low-income group. The target population for HCC screening in Korea NCSP included individuals aged ≥40 years with liver cirrhosis, HBV or HCV infection. The NCSP HCC screening program comprises two stages. First, the NCSP identifies the high-risk population for HCC among the lower 50% of NHI beneficiaries by screening a computerized medical claims database stored in the NHI Corporation within the past 2 years. The NCSP also analyzed serologic tests for HBsAg and HCV antibody to identify the high-risk group among Medicaid recipients. The second stage involves active surveillance among these high-risk individuals.[15] Therefore, individuals with HBV infection who had never undergone a health check-up might be missing from the target population group. Consequently, the opportunity to make use of free HCC screening services would have been lost in this missing population. The lower participation rate among the low-income group may also have been due to their unawareness of HBV infection status, and lack of information regarding the nationwide cancer screening program and the benefits of HCC screening. We also found that moderate-to-high household income, awareness of HBV infection status, and survey year were associated with increased use of recent HCC screening. The association between household income and HCC screening in this study was similar to a previous report that participants with higher income were more likely to use HCC screening tests.[8] In general, individuals with higher household income are more likely to undergo screening for colorectal, gastric, breast, and cervical cancer.[16] In addition, self-awareness of HBV infection was significantly related to adherence with the HCC screening program. Several reports have shown that awareness of HBV infection significantly affected participation in HCC screening programs.[8917] In this report, 16.3% of HBV-infected participants aged ≥40 years were aware of their HBV infection status in 2001. However, the rate of infection awareness among HBV carriers ≥40 years of age was 21% in 2010–2011, which was not significantly increased compared to that in 2001. These results imply that the identification of HBV-infected individuals among the general population group is important for HCC surveillance among HBV-infected persons. Therefore, to increase the low rate of HCC screening use, a national policy should encourage HBsAg screening programs to identify HBV-infected persons, as well as improve patient adherence to HCC screening among HBV-infected individuals. This study had several limitations. First, causal associations could not be examined due to the cross-sectional design. Second, this study defined recent HCC screening use as that performed within the previous 2 years to make uniform the measurement in the two survey periods. The guidelines released jointly by the Korean Association for the Study of the Liver and the National Cancer Center recommended regular screening every 6 months on the basis of tumor doubling time.[6] Therefore, the primary outcome in this study does not represent the recommended HCC screening criteria. Moreover, previous studies reported that the rate of participation in regular HCC screening (every 6 months) was lower compared to that of irregular or lifetime HCC screening.[818] Nevertheless, this study that revealed relatively few participants had undergone recent HCC screening within the previous 2 years. Third, we relied on self-reported data to determine whether a subject had actually been screened and when the screening was performed. Therefore, information and recall bias might have interfered. Self-reporting is likely to overestimate cancer-screening rates.[19] Therefore, this limitation does not seem to overstate our finding of underuse of HCC screening among the study population. Fourth, the screening rate for HCC included organized screening programs and opportunistic screening. In Korea, opportunistic screening is widely accessible, in addition to nationwide organized screening programs. Finally, other factors influencing HCC screening use, such as a family history of HCC, or replicative state of HBV, or other co-morbidities, were not investigated. Despite these limitations, this study had several strengths. First, it was the first to analyze changes in HCC screening rates following the implementation of organized, nationwide HCC screening programs among HBV-infected groups targeted for screening. A substantial increase in HCC screening in HBV-infected individuals following implementation of the nationwide screening program provides lessons for government's HCC screening policy in areas endemic for HBV. Second, we used data representative of the Korean population. Therefore, we could evaluate the nationwide change in the utilization of HCC screening. Third, we also identified potential factors related to underuse of screening. To improve the efficiency of national HCC screening program and reduce socioeconomic disparities, identification of proper screening targets for active surveillance is a crucial step in HBV-endemic areas. We anticipate that our results might bring about improvements in HCC screening of high-risk individuals. In conclusion, the rate of adherence to HCC screening within the past 2 years among HBV-infected Korean people aged ≥40 years has more than doubled in 2010–2011 compared to 2001. However, the HCC screening rate among the high-risk group remained suboptimal despite the implementation of a nationwide screening program. Household income and awareness of HBV infection were positively associated with HCC screening in this study population at high-risk for HCC. These results suggest that multiple strategies, including encouragement for HBV-infected persons to attend HCC screening, as well as more efficient identification of HBV-infected subjects unaware of their infection, are urgently needed to maximize the advantages of HCC screening.

Financial support and sponsorship

This study was supported by a research grant from the Korean Association for the Study of the Liver (the Research Supporting Program of the Korean Association for the Study of the Liver).

Conflicts of interest

There are no conflicts of interest.
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9.  Factors associated with compliance with recommendations for liver cancer screening in Korea: a nationwide survey in Korea.

Authors:  Boyoung Park; Kui Son Choi; Mina Suh; Ji-Yeon Shin; Jae Kwan Jun
Journal:  PLoS One       Date:  2013-06-28       Impact factor: 3.240

10.  Cancer statistics in Korea: incidence, mortality, survival and prevalence in 2010.

Authors:  Kyu-Won Jung; Young-Joo Won; Hyun-Joo Kong; Chang-Mo Oh; Hong Gwan Seo; Jin-Soo Lee
Journal:  Cancer Res Treat       Date:  2013-03-31       Impact factor: 4.679

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  5 in total

Review 1.  Patient-, Provider-, and System-Level Barriers to Surveillance for Hepatocellular Carcinoma in High-Risk Patients in the USA: a Scoping Review.

Authors:  Eliza W Beal; Mackenzie Owen; Molly McNamara; Ann Scheck McAlearney; Allan Tsung
Journal:  J Gastrointest Cancer       Date:  2022-07-26

2.  Knockdown of Decoy Receptor 3 Impairs Growth and Invasiveness of Hepatocellular Carcinoma Cell Line of HepG2.

Authors:  Xiao-Na Zhou; Guang-Ming Li; Ying-Chen Xu; Tuan-Jie Zhao; Ji-Xiang Wu
Journal:  Chin Med J (Engl)       Date:  2016-11-05       Impact factor: 2.628

3.  Efficacy of Real-world Entecavir Therapy in Treatment-naïve Chronic Hepatitis B Patients.

Authors:  Yan-Di Xie; Hui Ma; Bo Feng; Lai Wei
Journal:  Chin Med J (Engl)       Date:  2017-09-20       Impact factor: 2.628

4.  A Case Series of Liver Abscess Formation after Transcatheter Arterial Chemoembolization for Hepatic Tumors.

Authors:  Wei Sun; Fei Xu; Xiao Li; Chen-Rui Li
Journal:  Chin Med J (Engl)       Date:  2017-06-05       Impact factor: 2.628

5.  Kinetics of Hepatitis B Surface Antigen Level in Chronic Hepatitis B Patients who Achieved Hepatitis B Surface Antigen Loss during Pegylated Interferon Alpha-2a Treatment.

Authors:  Ming-Hui Li; Lu Zhang; Xiao-Jing Qu; Yao Lu; Ge Shen; Shu-Ling Wu; Min Chang; Ru-Yu Liu; Lei-Ping Hu; Zhen-Zhen Li; Wen-Hao Hua; Shu-Jing Song; Yao Xie
Journal:  Chin Med J (Engl)       Date:  2017-03-05       Impact factor: 2.628

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