Prevalence of sexually transmitted infections among foreigners living in Guangzhou, China: a cross-sectional study (2010–2017)

Background The prevalence of HIV/HCV/HBV/ Treponema pallidum is an essential health issue in China. However, there are few studies focused on foreigners living in China. This study aimed to assess the prevalence and socio-demographic distribution of HIV, HBV, HCV, and T. pallidum among foreigners in Guangzhou in the period of 2010–2017. Methods A cross-sectional study was conducted to screen serological samples of 40,935 foreigners from 2010 to 2017 at the Guangdong International Travel Health Care Center in Guangzhou. Samples were tested for hepatitis B surface antigen (HBsAg), anti-HCV, syphilis antibody (anti-TPPA) and anti-HIV 1 and 2. We collected secondary data from laboratory records and used multiple logistic regression analyses to verify the association between different factors and the seroprevalence of HIV/HBV/HCV/ T. pallidum. Results The prevalence of HBV/HCV/HIV/ T. pallidum was 2.30, 0.42, 0.02, and 0.60%, respectively, and fluctuated slightly for 7 years. The results of multiple logistic regression showed that males were less susceptible to HBV than females (odds ratio [OR] = 0.77, 95% CI: 0.67–0.89). Participants under the age of 20 had a lower risk of HBV (OR = 0.25, 95% CI: 0.18–0.35), HCV (OR = 0.06, 95% CI: 0.02–0.18), and T. pallidum (OR = 0. 10, 95% CI: 0.05–0.20) than participants over the age of 50. Participants with an education level below high school were more likely to have HBV (OR = 2.98, 95% CI: 1.89–4.70) than others, and businessmen (OR = 3.02, 95% CI: 2.03–4.49), and designers (OR = 3.83, 95% CI: 2.49–5.90) had a higher risk of T. pallidum than others. Co-infection involved 58 (4.20%) total cases, and the highest co-infection rate was observed for HBV and T. pallidum (2.60%). Conclusion The prevalence of HBV/HCV/HIV/ T. pallidum was low among foreigners in Guangzhou. Region, gender, age, educational level, and occupation were risk factors for positive infection.


Background
Sexually transmitted infections (STIs) have been recognized as major public health problems in many countries, especially in developing countries [1]. Hepatitis B virus (HBV) infection is considered to be a serious public health problem worldwide, especially in less developed countries. It is estimated that 70% of new chronic HBV infections occur in low-income countries [2]. More so, The Polaris Observatory's collaborators reported in a survey of 128 countries that the global average HBV prevalence rate was 4.9%, with China, India, Nigeria, Indonesia, and the Philippines accounting for more than 57% of all HBsAg-positive cases [3]. The major burden from HCV infection comes from chronic infection [4], as 184 million individuals worldwide are chronic carriers of HCV [5,6]. HIV has been spreading from highrisk populations to the general population [7], and 37 million individuals are living with HIV globally. In addition, around six million individuals are infected with T. pallidum [8]. Although T. pallidum had been eliminated from China in the 1960s by providing free screening and treatment, the first resurgent cases were recognized in China in 1979, and China's national surveillance data show a disturbing steady spread of the disease across the country [9]. T. pallidum has been found to increase HIV infection by two to five times. HIV infection may also increase the spreading of other sexually transmitted diseases, leading to epidemiological synergies between HIV and other STIs [10]. Thus, awareness of co-infection is important because shared transmission pathways and mechanisms may suggest common preventive interventions. In addition, HBV, HCV, HIV, and syphilis can also be transmitted by mother-to-child or iatrogenic transmission, such as contaminated blood or unsterilized dental needles and syringes.
Guangdong is a province in the south of China with an estimated population of 300,000 foreigners. Guangzhou is the capital city of Guangdong. A population of foreigners lives in Guangzhou mostly for economic reasons. Currently, the prevalence of STIs among this population has not been adequately confirmed. To assess the prevalence of HIV, HBV, HCV, and T. pallidum among foreigners living in Guangzhou, we designed a cross-sectional study from 2010 to 2017.

Study design, setting, and subjects
A cross-sectional study was approved by the "Guangdong International Travel Healthcare Center Institutional Review Board Committee." All foreigners arriving in Guangzhou should attend Guangdong

Statistical analysis
The difference in the prevalence of STIs between groups was compared using the χ2 tests. Multiple logistic regression analyses were performed to explore the factors associated with seropositivity. The statistically significant variables, according to the χ2 tests, were included in the multiple logistic regression models to compute the adjusted odds ratios (OR) with 95% confidence intervals (CI). The significance level was set at P < 0.05. All of the analyses were performed using SPSS 20.0.

Sociodemographic characteristics
Of the 40, 935 participants, 23,309 (56.94%) were male and 17,626 (43.06%) were female. The average ages of the participates were 32.59 ± 11.86 years, with a range of 0-97 years (supplementary Table 1). As shown in Table 1, 45.90% of the participants were undergraduate students (N = 18,791), while 72.75% had a college education level or less. The majority of participants were from Europe (31.93%) and North America (22.21%). About 29.56% were students, followed by businessmen (24.08%).

Prevalence of STIs
The prevalence of HBV, HCV, HIV, and T. pallidum was 2.30, 0.42, 0.02, and 0.60%, respectively (Table 1), and fluctuated slightly over the 7 years covered by the study (Fig. 1). It was found that 58 (4.2%) cases had multiple infections (Fig. 2), and the highest coinfection rate was observed for HBV and T. pallidum (2.6%) (supplementary Table 1). As shown in Table 2, females had a higher prevalence of HBV (χ2 = 7.58, P = 0.01) than males (see Table 2, Fig. 3). There were no differences over the exam year among the STIs. The seroprevalence of HIV, HBV, HCV, and T. pallidum presented was different by geographical regions (see Table 2, Fig. 3). There was a significant difference in the seropositivity of HBV between the different age groups (χ2 = 14.15, P = 0.01). Educational level differences were also observed in the seroprevalence of HBV (χ2 = 14.94, P = 0.01) and T. pallidum (χ2 = 14.09, P = 0.01). Considering the occupation, there were significant differences for HBV (χ2 = 64.21, P < 0.001), HCV(χ2 = 26.19, P < 0.001) and T. pallidum (χ2 = 155.94, P < 0.001). However, perhaps as a consequence of the low number of HIV positive cases, the seropositivity of HIV was not different among the different social demographic characteristics.

Discussion
There is an epidemic in China of sexually transmitted diseases and the potential for its continued growth in the future. In addition to sexual transmission, these diseases can also be transmitted through mother-tochild transmission, hospital transmission and so on, so controlling and preventing the spread of STIs are now on the agenda [11,12]. China set out to expand the comprehensive control program consisting of primary and secondary prevention strategies to ensure that STIs can be prevented and infected individuals can be diagnosed and treated in a timely fashion, especially high-risk individuals [13]. However, available data about the prevalence of STIs in foreigners are limited. This is the first large-scale study that detected the seroprevalences of HBV, HCV, HIV, and T. pallidum among foreigners in China.
Of the 40, 935 participants involved, 3.20% (N = 1311) had a single infection, and 0.14% (N = 58) had multiple infections. A recent study in China showed that the prevalence of HBV in people aged 1-4 years, 5-14 years, and 15-29 years was 0.32, 0.94, and 4.38%, respectively [14], in this research, the seropositivity of HBV was 2.30% (N = 943), with the increase of age, the HBV infection rate gradually increased and peaked in the group aged over 50 years, which was in accordance with data for the general population. Foreigners from Africa had the highest proportion of positive HBV rate (5.84%), which is higher than the 4.7% reported in Ethiopia, and lower than the 7.51, 11.2, and 14.96% reported in Benin [15], Cameroon [16], and Burkina Faso [17], respectively.
HCV seroprevalence among foreigners was 0.42%, which is similar to the 0.43% reported in the general population in 2006 in China [18], and it is significantly lower than 2.8%, the average level in the world [19]. Similarly, Africa had the highest rate of HCV infection (0.76%), a value that is higher than the 0.5% reported in Portharcourt [20] and the 0.4% in Ethiopia [21].
Recently, it has been reported that the seroprevalence of T. pallidum ranged from 0.31 to 0.70% among blood donors in different areas of China [22][23][24]. In our study, the seroprevalence of T.pallidum (0.60%) was similar in Guangzhou (0.66%) in 2010 [22], and higher than in Nanjing(0.36%) and Xi'an [23]. Africa and South America had the highest rate of T.pallidum infection. In sub-Saharan Africa, T. pallidum still remains a severe public health problem [25]. When compared with African countries, the seroprevalence of T. pallidum infection in our study was significantly lower.
The seroprevalence of HIV in this study was 0.02%. The prevalence rate of HIV infection reported in Guangzhou and Nanjing is 0.02 and 0.08%, respectively [26], whereas in Western China the prevalence of HIV in donors was 0.31% [27,28]. It is worth noting that there were seven HIV infection cases in total, and five cases were undergraduates, suggesting that college students are still the main group of HIV infection. The prevalence of STIs co-infection was 4.20% in foreigners, and the HBV/ T. pallidum co-infection had the maximum proportion. There were no cases involving HIV with any other pathogens. It is possible that the policy related to HIV infection in the country of origin may explain the low prevalence observed in this research. For instance, some travellers may not be allowed to go abroad due to a HIV positive test in their country. There are several limitations to this study that should be mentioned. First, this article used the secondary data, so the genotypes of various sexually transmitted diseases pathogens were not clear. Second, HIV cases were too small to perform a multiple linear regression, decision trees, or other statistical methods used for analysis [29]. Third, all foreigners who arrive in Guangzhou will accept a physical examination, but some data are incomplete and we removed these data from our study, which may bias the results.

Conclusion
In conclusion, the epidemiologic data presented in this paper showed the presence of STIs prevalence in foreigners living in Guangzhou. This study showed a low prevalence of STIs among foreigners. Some prevalence were consistent with the local trends. During the survey period, there was no significant decline trend in the prevalence of HBV, HCV, HIV, and T. pallidum, so we highlight the need to strengthen the current surveillance program. More observation studies on STIs burden, risk factors, and interventions are needed to provide a solid base for planning and policy change [30,31]. Furthermore, it is essential to take comprehensive measures including this particular group to control and prevent sexually transmitted infections.