Decade-Long Analysis of Hepatitis Trends Among International Travelers at Shanghai Port (2013–2023)

Introduction

Viral hepatitis remains a significant global health challenge, encompassing a range of infections – primarily hepatitis B (HBV), hepatitis C (HCV), hepatitis D (HDV), and hepatitis E (HEV) – that can lead to severe liver damage and other systemic complications. Hepatitis is characterized by high incidence rates, strong infectivity, widespread transmission, and diverse transmission routes, all of which impose substantial economic and social burdens on affected individuals and communities [1]. While hepatitis A virus (HAV) generally causes acute, self-limiting illness, chronic forms of the disease, including HBV, HCV, and HDV, are associated with long-term liver damage, cirrhosis, and liver cancer [2].

Globally, the age-standardized incidence rate of viral hepatitis in 2019 was 3615.9 per 100 000 individuals, with substantial disparities observed across different regions, socioeconomic statuses, and healthcare systems. The highest age-standardized incidence rates were observed in parts of sub-Saharan Africa and East Asia, underscoring the regional burden of the disease [3]. HBV remains a leading global cause of mortality, ranking among the top 10 causes of death worldwide. In 2019, chronic HBV infection was responsible for approximately 820 000 deaths, primarily due to liver cirrhosis and liver cancer [4]. In China, HBV was responsible for 162 000 deaths due to liver diseases in 2019 alone, and the number of liver cancer deaths attributable to chronic HBV infection has been steadily increasing [5]. Between 2015 and 2019, liver cancer deaths in China linked to HBV infection increased by 7.05%, reflecting the continued burden of chronic HBV infection in the population.

The globalization of travel and trade has increased cross-border mobility, presenting new challenges for infectious disease surveillance and control. As one of the busiest international ports in China, Shanghai Port has experienced a significant rise in both inbound and outbound traffic, which complicates monitoring infectious diseases, including viral hepatitis. In 2019, it handled 420 million tons of cargo and more than 30 million passengers. They come from different parts of the world, such as Asia, Europe, the Americas, and elsewhere, for purposes ranging from tourism and business to immigration. The sheer traffic volume and the population diversity at Shanghai Port make it a unique setting for potential hepatitis transmission. Travelers from different international regions may carry various strains of hepatitis viruses, making it an ideal site for the epidemiological study of hepatitis among migrants and the implementation of global prevention guidelines. The movement of individuals through this primary gateway highlights the importance of understanding hepatitis prevalence in this population, as this information is critical for public health surveillance and intervention strategies.

Despite the importance of Shanghai Port as a central hub for international travel, there have been few comprehensive, longitudinal studies examining hepatitis infection rates among individuals passing through this port. While several studies have explored viral hepatitis prevalence in specific regions or populations (eg, healthcare workers and high-risk communities), few have focused on populations at ports of entry, which are a high-risk group for cross-border disease transmission. This study addresses this gap by epidemiologically analyzing hepatitis surveillance data from individuals undergoing medical examinations at Shanghai Port between 2013 and 2023. The primary objective was to describe the distribution and temporal trends of viral hepatitis among inbound and outbound populations. By identifying patterns of disease prevalence, this research will provide valuable insights into the transmission dynamics of hepatitis and inform targeted public health interventions. In addition, deriving ways in which hepatitis spreads in these environments can guide specific measures of prevention and control – such as creating vaccination programs tailored to the conditions and health education campaigns – which is the only way to mitigate the spread of the virus in more and more linked regions.

The findings of this study will contribute to developing more effective strategies for monitoring and controlling hepatitis at major international ports, with the ultimate goal of reducing the infection and detection rates of viral hepatitis among travelers. This effort is critical in minimizing the risk of international transmission of hepatitis and mitigating the related public health burden, including morbidity and mortality from chronic liver diseases.

Material and Methods

STUDY POPULATION:

The study population consisted of individuals who entered or exited Shanghai and underwent initial infectious disease screening at the SITHC from January 2013 to December 2023. This cohort encompasses diverse groups, including laborers, exchange students, tourists visiting relatives, and individuals involved in international marriages. Demographic information such as age, gender, and occupational categories was collected from the Shanghai Entry-Exit Administration System. All participants underwent face-to-face interviews using a standardized questionnaire, with quarterly investigator training achieving a mean inter-rater agreement of Kappa=0.86. This study conforms to the principles of the Declaration of Helsinki. Notification data were collected under the China Epidemics Act; hence, no ethics approval was required.

SCREENING PROTOCOLS:

The examination protocols encompassed routine physical assessments and targeted laboratory investigations. In alignment with the standards outlined in the records of the SITHC, comprehensive physical exams were conducted, which included internal medicine and surgical evaluations. These assessments involved electrocardiograms, ultrasound scans, and chest X-rays.

For all individuals undergoing testing, venous blood samples were collected, and serum was subsequently separated following the addition of anticoagulants.

LABORATORY TESTING:

Hepatitis virus surface antigens (HAV, HBV, HCV, HDV, and HEV) were detected using a double-antibody sandwich enzyme-linked immunosorbent assay (ELISA). Additionally, alanine aminotransferase (ALT) serum levels and other relevant biomarkers were measured. All reagents used for testing were sourced from qualified suppliers, and all laboratory instruments had been validated for accuracy and reliability.

Testing procedures were carried out with strict adherence to standardized protocols, following standardized protocols and adhering strictly to the manufacturer’s instructions for each reagent. Confirmatory testing was performed on samples that initially tested positive during the screening process. These confirmatory tests were conducted using reagents from the same manufacturer (but from different batches) or from various manufacturers. Only when both initial and confirmatory tests yielded positive results was an individual classified as infected with viral hepatitis. To ensure consistency across the 10-year study, 10% of samples were re-tested annually with original assays, showing 98.2% concordance (Cohen’s κ=0.93).

STATISTICAL ANALYSIS:

Statistical analyses were performed using SPSS (version 26.0, Chicago, IL, USA) and Microsoft Excel. The Kolmogorov-Smirnov test was used to assess the normality of continuous variables. Data are presented as means±standard deviations for continuous variables and as numbers/percentages for categorical variables. The chi-squared test (χ²) was employed to compare categorical variables such as demographic characteristics and hepatitis detection rates across different years. Temporal trends in hepatitis detection were assessed using the Cochran-Armitage trend test. In the case of non-normally distributed continuous endpoints, the Mann-Whitney U-test was used to compare. A 2-sided P value of less than 0.05 was considered a statistically significant difference.

Results

TRENDS IN HEPATITIS-POSITIVE DETECTION RATES AMONG INTERNATIONAL TRAVELERS:

The average hepatitis detection rate among individuals undergoing medical examinations at Shanghai Port from 2013 to 2023 was 0.57%, as shown in Figure 1. This rate peaked 2016 at 1.13%, indicating an upward trend from 2013 to 2016. However, a decline began in 2017, with fluctuations noted in the subsequent years.

Among outbound travelers, the average detection rate was 0.19%, with the highest rate recorded in 2016 at 0.45%. Similar to the general trend, this group exhibited a similar trend, with a rise in detection rates from 2013 to 2016, followed by a decline from 2017 onwards. In contrast, inbound travelers had a higher average hepatitis detection rate of 0.94%, which peaked at 1.75% in 2016. This group also showed an increasing trend up to 2016, followed by a decline from 2017 to 2019. Notably, a slight increase was observed in 2020; however, the overall trend continued to decline after 2020. These observed differences in detection rates across the study period were significant (P<0.01).

DEMOGRAPHIC AND EPIDEMIOLOGICAL CHARACTERISTICS OF HEPATITIS-POSITIVE TRAVELERS:

The study analyzed 4246 hepatitis-positive travelers with a mean age of 41.4±18.5 years, with 66.9% being males. Primary regions of origin included China (32.5%), Southeast Asia (10.9%), East Asia (16.7%), West-Central Asi a(2.39%) South Asia (1.46%), and other regions which reflecting regions with high HBV/HCV prevalence according to WHO reports. The immigration duration distribution was: <1 year (31.5%), 1–5 years (44.8%), and >5 years (23.7%). Baseline clinical characteristics showed HBV mono-infection in 58.3%, HCV in 29.1%, and coinfection in 12.6%.

Among the outbound travelers diagnosed with hepatitis, males accounted for 68.03% of cases, significantly higher than females, who accounted for 31.97%. The highest detection rate was observed in the 41–50 age group (31.63%), followed by the 31–40 age group at 29.41%. Regarding occupation, laborers were the largest proportion (67.42%), followed by international students (12.87%). The peak year for hepatitis detection was 2016, with 21.6% of all cases recorded. These cases’ primary regions of origin included Asia (comprising Hong Kong, Macao, Taiwan, East Asia, and Southeast Asia), North America, and Europe.

Among inbound travelers, males also predominated (61.37%). The highest detection rate was found in the 21–30 age group (41.84%). International students accounted for the largest proportion of hepatitis cases among occupations (38.19%), with the highest percentage recorded in 2016 (26.09%).

For both inbound and outbound travelers, hepatitis B accounted for most cases, representing 93.43% of hepatitis diagnoses among outbound travelers and 86.88% among inbound travelers, followed by hepatitis C. Detailed data can be found in Table 1.

COMPARISON OF DEMOGRAPHIC CHARACTERISTICS OF HEPATITIS DETECTION AMONG INTERNATIONAL TRAVELERS ACROSS DIFFERENT YEARS:

Statistically significant differences (P<0.05) were observed in the demographic characteristics of hepatitis-positive individuals among inbound travelers at Shanghai Port over the years. Specifically, the proportion of hepatitis cases among individuals aged 21–50 decreased, while the proportions in the 51–60 and ≥61 age groups increased. Furthermore, there was an increasing trend in hepatitis cases among inbound travelers coming to China for study, international marriages, and employment. Notably, the proportion of hepatitis B cases rose significantly, while the proportion of hepatitis C cases showed a significant decline. Detailed data are presented in Table 2.

Similarly, among outbound travelers, significant differences (P<0.05) were observed in the demographic characteristics of hepatitis-positive individuals across different years. Significant variations were noted in the distribution of hepatitis types, age groups, and occupations. The proportion of individuals aged 20 and below increased, while the 21–30 age group fluctuated but remained relatively high. The proportion of individuals in the 31–40 age group increased, while the proportions in the 41–50 and 51–60 age groups declined, and the proportion of hepatitis cases among individuals aged 61 and above decreased. There was a growing trend of hepatitis cases among outbound travelers traveling for tourism, family visits, study abroad, and immigration. Among these travelers, the proportion of hepatitis B cases increased while the proportion of hepatitis C cases declined. Detailed data are presented in Table 3.

Discussion

LIMITATIONS AND GENERALIZABILITY:

Although this study points out essential trends in hepatitis prevalence among international travelers at Shanghai Port, some limitations should be recognized. One limitation is a geographical restriction of the survey to Shanghai Port, which may limit the generalization of results to other settings and restrict the generalizability of the findings to other regions. Thus, differences in healthcare quality, screening practices, and vaccination coverage across regions may have influenced the results. Furthermore, the study relied on data from routine health check-ups at the port, which may not include the entire variety of hepatitis cases, especially those in asymptomatic individuals or those who do not undergo screening, which may have failed to provide a complete understanding of the dynamics of hepatitis transmission and help identify effective prevention strategies. Further studies should also examine the impact of different healthcare infrastructures on hepatitis control, expand the geographic scope, and include a broader range of entry and exit points.

Conclusions

This study shows the importance of strengthened surveillance, preventive measures, and public health education in managing viral hepatitis among international travelers. The findings of this study point out the need to continue such efforts in surveillance, vaccination, and health education complemented by integrating advanced diagnostic technology to minimize the risk of hepatitis transmission at international ports. Strengthening these measures would ensure global public health protection and reduction of the burden of viral hepatitis worldwide.