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Department of Epidemiology, School of Public Health, The Fourth Military Medical University, Xi’an, Shaanxi, 710032, ChinaAcademy of Preventive Medicine, Shandong University, Jinan, ChinaShandong Provincial Key Laboratory of Infectious Disease Control and Prevention, Shandong Center for Disease Control and Prevention, Jinan, China.
Academy of Preventive Medicine, Shandong University, Jinan, ChinaShandong Provincial Key Laboratory of Infectious Disease Control and Prevention, Shandong Center for Disease Control and Prevention, Jinan, China.
Academy of Preventive Medicine, Shandong University, Jinan, ChinaShandong Provincial Key Laboratory of Infectious Disease Control and Prevention, Shandong Center for Disease Control and Prevention, Jinan, China.
Academy of Preventive Medicine, Shandong University, Jinan, ChinaShandong Provincial Key Laboratory of Infectious Disease Control and Prevention, Shandong Center for Disease Control and Prevention, Jinan, China.
Academy of Preventive Medicine, Shandong University, Jinan, ChinaShandong Provincial Key Laboratory of Infectious Disease Control and Prevention, Shandong Center for Disease Control and Prevention, Jinan, China.
Academy of Preventive Medicine, Shandong University, Jinan, ChinaShandong Provincial Key Laboratory of Infectious Disease Control and Prevention, Shandong Center for Disease Control and Prevention, Jinan, China.
Academy of Preventive Medicine, Shandong University, Jinan, ChinaShandong Provincial Key Laboratory of Infectious Disease Control and Prevention, Shandong Center for Disease Control and Prevention, Jinan, China.
The prevalence rates of hepatitis B surface antigen (HBsAg) and antibody against hepatitis B core antigen (anti-HBc) showed sustained decreases from 2006 to 2014 in Shandong Province, China.
•
The emerging peak of HBsAg prevalence in those aged 20–29 years seen in the 2014 survey should be taken seriously.
•
Students and farmers may become the high-risk populations for HBV infection, and sexual transmission may be the main route of transmission in students.
•
Extending the hepatitis B vaccination program to students and farmers might be the priority intervention for HBV infection in future in Shandong Province, China.
Abstract
Background
Tremendous progress has been made in hepatitis B virus (HBV) prevention and control in the last 30 years in China, but it continues to be a major public health problem. The most recently reported population-based seroepidemiological survey on HBV in Shandong Province in China was published in 2006, and an updated baseline for HBV prevalence was badly needed in the province to identify the change in HBV epidemiology in the last decade.
Methods
Two population-based cross-sectional serosurveys were performed among the population aged 1–59 years in the same sample areas in Shandong Province, China in 2006 and 2014, respectively. Data on demographic characteristics were collected. A blood sample was obtained from each person and was tested for hepatitis B surface antigen (HBsAg), antibody against HBsAg (anti-HBs), and antibody against hepatitis B core antigen (anti-HBc).
Results
Overall, the prevalence rates of HBsAg, anti-HBs, and anti-HBc were 3.39% (95% confidence interval (CI) 2.51–4.26), 44.96% (95% CI 41.34–48.57), and 24.45% (95% CI 22.19–26.71), respectively, among the population aged 1–59 years in the 2006 serovsurvey; the corresponding prevalence rates were 2.49% (95% CI 1.81–3.17), 48.27% (95% CI 45.63–50.92), and 22.56% (95% CI 20.14–24.97), respectively, in 2014. The prevalence rates of HBsAg and anti-HBc were lower in 2014 than in 2006. Conversely, the prevalence of anti-HBs showed an increase. However, none of these differences were statistically significant (all p> 0.05). The prevalence of HBsAg showed an increase among persons aged 20–24 years in 2014 (3.83%) compared with 2006 (2.98%) (t = 0.45, p = 0.67). Among all occupation groups, the prevalence of HBsAg was lower in 2014 than in 2006, while the prevalence of anti-HBc showed moderate increases in students and farmers (all p> 0.05). The prevalence of HBsAg decreased more obviously in urban areas (65.49%) than rural areas (7.07%) from 2006 to 2014.
Conclusions
The epidemiology of HBV infection has changed in Shandong Province, China over the last decade. More attention should be paid to HBV infection among students and farmers.
Hepatitis B virus (HBV) infection continues to be a major public health problem worldwide, with high levels of morbidity and mortality. It was estimated that about 248 million individuals were positive for hepatitis B surface antigen (HBsAg) globally in 2010 (
Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010.
). A recent global burden of disease study indicated that HBV infection was the tenth leading cause of death worldwide, with about 786 000 HBV-related deaths every year (
Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010.
An effective and safe hepatitis B vaccine has been available since 1981. Although the vaccination coverage rate varies in different countries, the implementation of universal hepatitis B vaccination in infants has resulted in a sharp decrease in many parts of the world (
). Universal hepatitis B vaccination accompanied by blood screening, improvements in safe injection practices, and other comprehensive measures may change the epidemiology of HBV infection, as has been reported in northern and north-western European, the Middle East, and China (
Evidence for a change in the epidemiology of hepatitis B virus infection after nearly two decades of universal hepatitis B vaccination in South Africa.
Population-Based Multicentric Survey of Hepatitis B Infection and Risk Factors in the North, South, and Southeast Regions of Brazil, 10-20 Years After the Beginning of Vaccination.
Prevalence of hepatitis B and C virus infections in the general Chinese population. Results from a nationwide cross-sectional seroepidemiologic study of hepatitis A, B, C, D, and E virus infections in China, 1992.
International Hepatology Communications.1996; 5: 62-73
). Shandong Province is located in the east of China and has the second largest population in the country. Hepatitis B vaccine was first recommended for infants in the province in 1992 and has been provided to infants without charge since 2002. Data from the Shandong Center for Disease Control and Prevention (CDC) indicate that coverage with the hepatitis B vaccine has remained at a very high level (above 96%) among infants in the province since 2002; furthermore, the prevalence of HBsAg decreased from 8% in 1992 to 1.36% in 2006 among children aged 1–14 years (
A significant reduction in hepatitis B virus infection among the children of Shandong Province, China: the effect of 15 years of universal infant hepatitis B vaccination.
), there have been very few population-based studies since 2006. It is unclear whether the changes in HBV prevalence have been sustained in the province over the last decade.
The aim of this study was to assess the shift in epidemiology of HBV infection among individuals aged 1–59 years between the years 2006 and 2014, and to provide a new baseline for HBV infection in Shandong Province, China.
Methods
Study population and sampling method
Shandong Province has an area of 156 700 km2 and a population of approximately 98 million. Two population-based cross-sectional HBV serosurveys were conducted in the same 12 counties of the province in 2006 and 2014, respectively. The representativeness of the sample area has been documented previously (
A significant reduction in hepatitis B virus infection among the children of Shandong Province, China: the effect of 15 years of universal infant hepatitis B vaccination.
A multi-stage, stratified, random sampling method was used in both surveys, but details differed. In the 2006 serosurvey, the 12 counties were chosen at random, following which two or three towns from each county were chosen by systematic sampling. Then one village was selected from each town by simple random sampling. Finally, all of the population aged 1–4 years was involved in the study, the population aged 5–14 years was selected by systematic random sampling, and the population aged 15–59 years was selected by cluster sampling based on the family unit. In 2014, the same 12 counties were selected, following which 24 villages were identified in the 12 counties (two per county) by probability proportional to size (PPS) sampling. Finally, the population aged 1–4, 5–14, 15–29, and 30–59 years, respectively, were enumerated and selected by simple random sampling.
Investigation
Similar investigation methods and questionnaires were used in both serosurveys. A face-to-face investigation was completed by trained staff from the local CDC. Standardized questionnaires were used to collect the basic information of the participants including sex, birth date, education level, occupation (available for persons aged above 18 years), ethnicity, residential area, and history of immunization with hepatitis B vaccine. History of immunization with hepatitis B vaccine was obtained by checking the immunization certificate for participants under 15 years of age and by recall for those over 15 years of age.
Specimen collection and laboratory testing
Approximately 5 ml of venous blood was obtained from each participant. All serum specimens were stored at −20 °C at Shandong provincial CDC and were then transferred to the China CDC for testing. All samples were tested for HBsAg, antibody against HBsAg (anti-HBs), and antibody against hepatitis B core antigen (anti-HBc) by enzyme-linked immunosorbent assay (ELISA). For the 2006 serosurvey, ELISA reagents for HBsAg and anti-HBs testing were purchased from InTec Products, Inc., and anti-HBc detection reagents were purchased from Shanghai Kehua Bio-engineering Co., Ltd. For the 2014 serosurvey, all HBV seromarker detection reagents were purchased from Beijing Wantai Biological Pharmacy Enterprise. For specimens with uncertain results, Abbott EIA reagents were used for reconfirmation testing.
Statistical analysis
Data were inputted into an Epi Data 3.02 software database and analyzed using SAS 9.13 software. Appropriate sampling weights were constructed for sample datasets. In the 2006 serosurvey, the weight for each person i could be expressed as follows: wi = w1 × w2 × w3 × w4 × wadj, where w1 is the reciprocal of the inclusion probability of county, w2 is the reciprocal of the inclusion probability of town, w3 is the reciprocal of the inclusion probability of village, w4 is the reciprocal of the inclusion probability of person i within the selected village, and wadj is an adjustment factor for person i such that the sum of weights equals the actual size of the Shandong Province population in 2005. In the 2014 serosurvey, the weight for each person i could be expressed as follows: wi = w1 × w2 × w3 × wadj, where w1 is the reciprocal of the inclusion probability of county, w2 is the reciprocal of the inclusion probability of village, w3 is the reciprocal of the inclusion probability of person i within the selected village, and wadj is an adjustment factor for person i such that the sum of weights equals the actual size of the Shandong Province population in 2010.
Proportions were used to describe the sociodemographic characteristics of the participants. The Taylor series linearization methods were used to estimate variance. The point estimates and their estimated 95% confidence intervals (CIs) were used to evaluate the prevalence of HBV seromarkers. The t-test was used to compare the prevalence in different groups. p-Values of less than 0.05 were considered statistically significant. The prevalence rates of HBV seromarkers in the 2014 serosurvey were compared to those in the 2006 serosurvey.
The 12 counties investigated were divided into three geographic areas. The eastern area included Zhifu, Penglai, Shibei, and Gaomi; the middle area included Junan, Guangrao, Yiyuan, and Laicheng; the western area included Leling, Xuecheng, Zoucheng, and Ningyang. The urban area included Zhifu, Shibei, Laicheng, and Xuecheng, while the rural area included Penglai, Gaomi, Junan, Guangrao, Yiyuan, Leling, Zoucheng, and Ningyang. Hepatitis B vaccine coverage was defined as the percentage of persons who had received one or more doses of hepatitis B vaccine.
Quality control
The designs of both serosurvey programs were based on expert demonstrations and pilot investigations. All investigators were trained by the researchers from Shandong CDC. All fieldwork followed standard operating procedures. In order to ensure a high response rate, appropriate appointments and visiting times were considered. The data analysis was performed by specialist epidemiological and statistics groups.
Ethical issues
Both serosurveys were approved by the China CDC Ethics Committee. A written informed consent agreement was obtained from each individual before the investigation.
Results
Characteristics of the study populations in the 2006 and 2014 serosurveys
Overall, a total of 7601 samples were analyzed in the 2006 serosurvey and 5528 samples in the 2014 serosurvey. The male to female ratio was 0.91:1 in the 2006 serosurvey and 0.95:1 in the 2014 serosurvey. The proportions of persons in the different age groups, occupation groups, and residential areas were similar in the two serosurveys. The characteristics of these two survey populations are shown in Table 1.
Table 1Characteristics of the study populations in the 2006 and 2014 serosurveys.
Overall prevalence of HBV serological markers in 2006 and 2014
Overall, the prevalence rates of HBsAg, anti-HBs, and anti-HBc were 3.39% (95% CI 2.51–4.26), 44.96% (95% CI 41.34–48.57), and 24.45% (95% CI 22.19–26.71), respectively, among the population aged 1–59 years in the 2006 serosurvey. The corresponding prevalence rates were 2.49% (95% CI 1.81–3.17), 48.27% (95% CI 45.63–50.92), and 22.56% (95% CI 20.14–24.97), respectively, in 2014. The prevalence rates of HBsAg and anti-HBc were lower in 2014 than in 2006. Conversely, the prevalence rate of anti-HBs showed an increase. However, the differences in these HBV serological markers between the two serosurveys were not statistically significant (all p> 0.05) (Figure 2).
Figure 2Prevalence of HBV serological markers among the population aged 1–59 years in 2006 and 2014. Bars indicate the 95% confidence interval.
Age-specific prevalence of HBV seromarkers in 2006 and 2014
The prevalence rates of HBsAg, anti-HBs, and anti-HBc in the different age groups differed significantly in both the 2006 serosurvey and the 2014 serosurvey (all p< 0.05). Two prevalence peaks of HBsAg were observed in 2006, among adults aged 25–34 years and 45–54 years. Similarly, two prevalence peaks of HBsAg were observed among adults aged 20–29 years and 40–49 years in 2014. Overall, the prevalence of anti-HBs decreased gradually with age and the prevalence of anti-HBc increased with age in both surveys.
The prevalence of HBsAg decreased from 1.36% in the 2006 survey to 0.21% in the 2014 survey among children aged 1–14 years (t = 2.28, p = 0.05). The prevalence of HBsAg was lower in the 2014 survey when compared to the 2006 survey in the age groups of 25–34 years and 45–59 years, but a statistically significant difference was found only in the age group of 50–54 years (t = 4.68, p< 0.01). Remarkably, the prevalence of HBsAg showed an increase among persons aged 20–24 years in 2014 (3.83%) compared with 2006 (2.98%) (t = 0.45, p = 0.67). The prevalence of anti-HBs was similar among children aged 1–14 years in 2006 and 2014 (t = 1.98, p = 0.08), but was significantly higher among persons aged 15–49 years in 2014 compared with 2006 (t = 2.40, p = 0.04). The prevalence of anti-HBc decreased among persons aged 1–29 years from 2006 to 2014 (t = 0.05, p = 0.82), and was similar among persons aged over 30 years (t = 1.60, p = 0.24) (Figure 3).
Figure 3Age-specific prevalence of HBV seromarkers in 2006 and 2014. (a) Comparison of the prevalence of HBsAg in 2006 and 2014. (b) Comparison of the prevalence of anti-HBs in 2006 and 2014. (c) Comparison of the prevalence of anti-HBc in 2006 and 2014.
Prevalence of HBV serological markers by sex, occupation, and residential area in 2006 and 2014
The prevalence rates of HBsAg, anti-HBs, and anti-HBc were all higher in males than in females in both surveys. In the 2006 survey, the highest prevalence of HBsAg was identified in public service workers (7.72%), followed by workers (4.75%), while in the 2014 survey, the highest prevalence of HBsAg was in farmers (3.49%), followed by workers (3.37%). Cadre showed the highest prevalence of anti-HBs (56.75%) in 2006, while students showed the highest prevalence of anti-HBs (69.82%) in 2014. The prevalence rates of both anti-HBs and anti-HBc were higher in urban areas than in rural areas in both surveys. The highest prevalence rates of anti-HBs and anti-HBc were both obtained in the eastern area in both surveys.
The prevalence rates of HBsAg and anti-HBc decreased in 2014 compared with 2006 among both males and females, but a statistically significant decrease was identified only for HBsAg prevalence in females. Conversely, the prevalence of anti-HBs showed an increase from 2006 to 2014. Among all occupation groups, the prevalence of HBsAg was lower in 2014 compared with 2006, but a statistically significant decrease was identified only in public service workers (t = 3.93, p < 0.01). The prevalence of anti-HBc showed moderate increases in students and farmers and decreases in workers, cadre, public service workers, and other occupations from 2006 to 2014 (all p > 0.05). A significant decrease in HBsAg prevalence was found in urban areas from 2006 to 2014 (t = 8.05, p = 0.02), with a drop of 65.49%. The prevalence of HBsAg decreased in all three geographic locations (eastern, central, and western areas) from 2006 to 2014, but a statistically significant drop was found only in the eastern area (t = 3.34, p = 0.04). A significant increase in the prevalence of anti-HBs was found in the eastern region from 2006 to 2014 (t = 7.42, p< 0.01) (Table 2).
Table 2Prevalence of HBV markers among the population aged 1–59 years by sex, occupation, and residential area in 2006 and 2014.
p<0.01 for the comparison of the prevalence of anti-HBs between 2006 and 2014.
30.81 (23.65–37.98)
23.63 (9.47–37.80)
Central
2545
1873
2.34 (0.53–4.14)
1.77 (0.44–3.09)
46.44 (40.34–52.53)
46.99 (40.89–53.10)
22.72 (17.58–27.86)
19.81 (15.58–24.05)
Western
2510
1822
3.99 (3.09–4.88)
3.09 (0.32–5.86)
41.86 (34.27–49.45)
47.94 (40.76–55.13)
23.31 (21.61–25.02)
23.43 (18.32–28.54)
CI, confidence interval; HBsAg, hepatitis B surface antigen; anti-HBs, antibody against hepatitis B surface antigen; anti-HBc, antibody against hepatitis B core antigen.
a p< 0.05 for the comparison of the prevalence of HBsAg between 2006 and 2014.
b p< 0.01 for the comparison of the prevalence of anti-HBs between 2006 and 2014.
Seroprevalence of HBV markers by hepatitis B immunization status
The prevalence of HBsAg among vaccinated persons was 2.33% in 2006 and 1.26% in 2014; this was lower than the prevalence in unvaccinated persons in both years (3.90% and 3.98%, respectively). However, only the difference in 2014 was statistically significant (t = 2.92, p = 0.02). Similarly, the prevalence rates of anti-HBc among vaccinated persons in 2006 (14.42%) and 2014 (15.17%) were lower than those in unvaccinated persons (30.24% and 30.82%, all p< 0.01). Conversely, the prevalence rates of anti-HBs in 2006 (65.51%) and 2014 (62.95%) were higher among vaccinated persons than among unvaccinated persons (33.06% and 34.88%, all p< 0.01).
The prevalence of HBsAg among vaccinated persons in 2014 was significantly lower than that in 2006 (t = 3.68, p < 0.01). The prevalence rates of both anti-HBs and anti-HBc among vaccinated persons in 2006 were similar to those in 2014 (all p > 0.05). Likewise, the prevalence rates of HBsAg, anti-HBs, and anti-HBc among unvaccinated persons in 2006 were similar to those in 2014 (all p> 0.05) (Figure 4).
Figure 4Prevalence of HBV seromarkers by hepatitis B immunization status in 2006 and 2014. (a) Comparison of the prevalence of HBsAg by history of hepatitis B vaccination in 2006 and 2014. (b) Comparison of the prevalence of anti-HBs by history of hepatitis B vaccination in 2006 and 2014. (c) Comparison of the prevalence of anti-HBc by history of hepatitis B vaccination in 2006 and 2014. Bars indicate the 95% confidence interval.
The prevention and control of HBV infection has been amongst the highest priorities for public health in China. Although Shandong Province has made tremendous progress in HBV control over the past 20 years, the number of HBV-infected individuals remains large. In the present study, changes in the epidemiology of HBV infection among the general population over the last decade were observed in Shandong Province, China. This study obtained evidence of the recent community-based status of HBV epidemiology and allowed the effects of the efforts towards HBV control in Shandong Province over the last decade to be evaluated.
The prevalence of HBsAg varies greatly across different regions and populations. Regions are classified according to HBsAg prevalence into high (HBsAg prevalence rate ≥8%), higher-intermediate (5–7.99%), lower-intermediate (2–4.99%), and low (<2%) prevalence areas (
). According to the present study, Shandong Province remains an intermediate prevalence area. The provincial HBV serosurvey in 1992 found that the overall prevalence of HBsAg was 6.4% among the population aged 1–59 years in Shandong Province. The prevalence of HBsAg was high among all age groups in 1992 due to the absence of hepatitis B vaccination. HBsAg prevalence has decreased dramatically since 1992, and this decrease was accompanied by an increase in the prevalence of anti-HBs among people aged <25 years in 2006. A sustained decrease in HBsAg prevalence was found from 2006 to 2014 in this study, although the difference was not statistically significant. Although hepatitis B vaccination, blood screening, use of antiviral drugs, health education, and other effective strategies could also have contributed to the drop in HBsAg prevalence, a mathematical model analysis indicated that newborn vaccination could have accounted for more than 50% of the reduction in the total HBV prevalence from 1992 to 2006 in China (
). The contribution rate of newborn vaccination increased with the increase in hepatitis B vaccination coverage. This suggests that the implementation of universal infant HBV immunization might play a key role in HBV control and that the high hepatitis B vaccination coverage should be maintained.
The prevalence of HBsAg varied greatly among the different age group populations in both the 2006 and 2014 surveys in this study, which is consistent with previous studies (
). This correlation may be mainly due to the wide difference in the newborn hepatitis B vaccination coverage rate and cumulative numbers of patients with HBV infection. The prevalence of HBsAg in 2014 showed a sustained decrease among persons aged 1–14 years compared with 2006, which might be mainly related to the high hepatitis B vaccination coverage of newborns in the last decades (
). A catch-up program of hepatitis B vaccination was conducted among children under 15 years old in China in 2009–2011. Hepatitis B immune globulin (HBIG) has been provided to newborns of HBsAg-positive mothers free of charge since July 2011 in Shandong Province, China.
reported that the maternal screening rate for HBsAg during pregnancy or at delivery increased from 70.7% in 2004 to 96.9% in 2012 and that the coverage of HBIG increased from 85.0% before July 2011 to 92.1% after July 2011 in Shandong Province. These may all have contributed to the sustained decrease in HBsAg prevalence from 2006 to 2014.
Two age-peaks for HBsAg prevalence were observed in both the 2006 and 2014 surveys in this study, but the peak age differed. The peak at 40–49 years in the 2014 survey might represent a shift in the peak at 25–34 years in the 2006 survey. However, the emerging peak at 20–29 years in the 2014 survey should be taken seriously. It is well known that HBV infection is transmitted perinatally, by percutaneous or mucosal exposure to infected blood and various body fluids, or sexually (
). Mother-to-child transmission was regarded as the main route for HBV infection in Shandong Province before this study. The high prevalence of HBV among young people in this study suggests that they may have been infected by mother-to-child transmission because of the prevalent peak in 40–49-year-olds in 2014. Hepatitis B vaccine coverage was less than 50% among young people aged 20–29 years in the 2014 survey. Therefore, although the finding of a high risk of HBV infection among young people should be investigated further, it is suggested that hepatitis B vaccine be given to young people susceptible to HBV.
Some previous studies have shown the prevalence of HBsAg to be higher in males than in females (
). The present study also found the same tendency in both surveys. The reason for the higher prevalence of HBV in males has remained unclear to date. Some studies have reported that females are more likely to clear HBsAg than males (
), which might partly explain this result. Besides this, males usually engage in more social activities than females in China and might face a higher risk of becoming infected during social activities.
Contrary to the prevalence of anti-HBc in the other occupation groups, a moderate increase was seen in students from 2006 to 2014 in this study, which suggests that students over 18 years of age might become a population at high risk of HBV infection. It is well known that HBV and HIV share the same modes of transmission. The proportion of students among HIV-infected individuals increased from 1.9% in 2005 to 13.0% in 2012 in China (
). Over the same period, the proportion of reported HIV/AIDS cases infected through heterosexual or homosexual transmission increased from 27.8% to 91.2% (
). Another study showed that 8.3% of students aged 15–35 years had sexual experience, and only 48.5% used a condom in the first sexual intercourse during the years 2010 to 2015 in China (
). Thus, it could be inferred that sexual transmission may be the most common route of HBV transmission in students. In this study, 65.59% of students in the 2014 survey were born after universal infant hepatitis B vaccination and 76.34% had received the hepatitis B vaccination. The necessity of hepatitis B vaccine booster doses among healthy individuals remains controversial (
). However, according to the present results, it may be necessary to provide hepatitis B vaccination to students over 18 years of age who have not completed three doses of hepatitis B vaccine and to conduct studies on the booster dose among those who have completed a full course of hepatitis B vaccine in infancy.
This study also found an increase in anti-HBc prevalence among farmers from 2006 to 2014, suggesting a high risk for HBV infection among them. A low coverage of hepatitis B vaccine (<30%) and a high proportion of the population susceptible to HBV (about 50%) were found in the 2014 survey in this study, which is similar to the findings of another study performed in rural areas of China (
). Although the reason for the increase in anti-HBc prevalence among farmers should be studied further, it is suggested that hepatitis B vaccination be recommended to farmers in China.
The greatest strength of this study is the simultaneous analysis of changes in the HBV epidemic status in Shandong Province in two population-based serosurveys. These were designed by the same team, with similar populations investigated and similar sampling methods, and were conducted in the same 12 representative counties. Furthermore, the data analysis used similar statistical methods by computing sampling weights. However, this study also had some limitations. First, samples in the 2006 serosurvey and 2014 serosurvey were tested with different detection reagents by different staff, which may have resulted in some observational bias. However, all of the detection reagents were selected based on evaluation compared to Abbott EIA reagents using a panel of 153 standard reference sera. For specimens with uncertain results, Abbott EIA reagents were used for reconfirmation testing. Second, the immunization information of adults was based on their memory and so might be subject to some recall bias. Third, both serosurveys were cross-sectional in design. Thus, it was difficult to establish causal relationships. Nevertheless, this study provides important demographic insights into HBV prevalence over the last decade.
In conclusion, the overall epidemic patterns of HBV have changed over the last decade according to the two population-based serosurveys in Shandong Province. Students and farmers may become the high-risk populations for HBV infection, and sexual transmission may be the main route of transmission in students in Shandong Province. Extending the hepatitis B vaccination program to students and farmers might be the priority intervention for HBV infection in future in Shandong Province.
Funding
This work was supported by grants from the National Science and Technology Key Projects on ‘Major Infectious Diseases such as HIV/AIDS, Viral Hepatitis Prevention and Treatment’ (No. 2012ZX10004701), from the Shandong Medical and Health Science and Technology Development Programs (No. 2011HD006, 2015WS0285), and from Taishan Scholar Program of Shandong Province (No. ts201511105).
Conflict of interest
The authors declare that they have no conflict of interest.
Acknowledgements
We thank the CDCs of Zhifu, Penglai, Shibei, Gaomi, Junan, Guangrao, Yiyuan, Laicheng, Leling, Xuecheng, Zoucheng, and Ningyang and relevant personnel for their contribution to this study.
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