Prevalence of HIV infection among foreign applicant to residency in Shanghai, China, 2005-2016

doi:10.21203/rs.3.rs-32658/v1

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Prevalence of HIV infection among foreign applicant to residency in Shanghai, China, 2005-2016

https://doi.org/10.21203/rs.3.rs-32658/v1

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Background

Shanghai is an international city which has high proportion of entry travelers from all over the world. The HIV(human immunodeficiency virus)infection status of this population can reflect the global trend of HIV prevalence. Thus, a retrospective epidemic investigation was conducted to clarify the prevalence and characteristics of HIV infection among entry travelers who apply to residency in Shanghai.

Methods

Totally 50830 entry travelers who applied to residency in Shanghai(2005-2016)were included. The HIV infection rate was confirmed based on the detection of HIV-1 antibody.

Results

Among all the recruited entry travelers, 245 persons were determined HIV positive with infection rate of 0.48%. The detection rate of HIV in male was significantly higher than that in female (χ 2 =62.584, P <0.0001). Those aged 18-30 years, 31-40 years and >40years accounted for 34.3%, 39.6% and 26.1% of the infected population. There was no increase in trend of HIV prevalence rates among the sampling years (Cochran-Armitage Z=2.543, P=0.111). Proportions of individuals infected through homosexual transmission increased over the study period (Cochran-Armitage Z=5.41, P<0.001), while the proportion infected through heterosexual declined over time (Cochran-Armitage Z=3.38, P =0.001).

Conclusion

The rate and characteristics of HIV infection among foreign applicant to residency in Shanghai were clarified in the study. The results would have provided the necessary epidemiological data for monitoring the HIV epidemic among entry international travelers and to further contribute to the establishment of relevant policies and regulations for HIV control and prevention.

Infectious Diseases

HIV (human immunodeficiency virus)

prevalence

travelers

Since the AIDS epidemic peaked in 1993, it turned to be theleading cause of death among 25 to 44-year-old people, and it hadbecome the eighth most common cause of death worldwide^[1].Although human immunodeficiency virus (HIV) infection and mortalityrates have been declining because of the highly activeantiretroviral therapy and effective prevention measures globally,about 35.3 million people are living with HIV worldwide, HIVinfections are considered to be the global threat of present era^[2,3]. China'sState Council promulgated and implemented the "AIDS prevention andcontrol regulations" in March 1st, 2006, to clear the workrequirements and tasks of inspection and quarantine system. In May30th, 2007, AQSIQ examined and approved the "port AIDS preventionand control measures", the port entry&exit personnel AIDSquarantine, monitoring, prevention and control and financialsecurity has specific provisions and requirements. On April 24 of2010, the executive meetings of the State Council adopted “theDecision of the State Council on Amending‘Detailed Rules for theImplementation of the Law of the People's Republic of China onFrontier Health Quarantine Inspection’”, which clearly stipulatedthat the entry of foreign AIDS patients was no longer restricted.This regulation is consistent with most developed countries.

Shanghai is a major destination of international business andtrade which has a large population of cross-border travelersconsequently. Entry travelers and their activities often lead tothe spread of infectious diseases in China and even on a globalscale ^[4]. Moreover, such a large floatingpopulation could promote HIV cross-border transmission, leading toa higher HIV prevalence in the world. Strengthening surveillanceand attention to this group is crucial to the prevention ofHIV/AIDS, particularly in the border areas where trade and touristsare flooding. In addition, the investigation of temporal changes inHIV infection and the associated risk factors could be importantfor the prevention of HIV in this bridge population. Although HIVinfection among cross-border travelers has been reported in othermajor cities ^{[2, 5]}, the HIV related epidemiccharacteristics of these population in Shanghai are still unclear.Therefore, in order to clarify the HIV epidemic characteristicsamong entry travelers, a large-scale retrospective study on HIVscreening was conducted on cross-border travelers who entered Chinathrough Shanghai ports from 2005–2016 and a further analysis wasperformed. The objective of this research was to describe theepidemiological and characteristic of HIV infection amonginternational entry travelers in Shanghai to help policy makersidentify and address the specific needs for HIV prevention, controland treatment.

Study population and data collection

From January 2005 to December 2016, there were about 5 thousandentry travelers on average in Shanghai annually. Those foreignapplicants who apply for a stay in China for one or more years needto finish health examinations in Shanghai International TravelHealthcare Center, which affiliated to Shanghai Entry-ExitInspection and Quarantine Bureau, responsible for the healthassessment and epidemiological surveillance of people entering andexiting Shanghai. Routine examinations included blood routine test,serum chemistries test and the detections of major infectiousdiseases. All applicants who completed the health examination inShanghai International Travel Healthcare Center were forced toperform the HIV test. Before the entry, the applicant who hadvoluntarily declared HIV positive had to re-examinated again toconfirm the diagnosis. In the main, initial screening was carriedout with an enzyme-linked immunoassay (ELISA) or an enzymeimmunoassay (EIA). Samples which were screened to be reactive wererepeated in duplicate with the same assay. If two of three testresults were positive, the sample was transmitted to FDA-approvedsupplemental/confirmatory assays, HIV-1 Western Blot (GeneticSystems HIV-1 Western Blot, Bio-Rad Laboratories, Redmond,Washington, US) and/or an immunofluorescent antibody (IFA) test(Fluorognost HIV-1 IFA, Waldheim Pharmazeutika, GmbH, Vienna,Austria) would be done. The diagnosis of HIV was based on HIVassays approved by Chinese Food and Drug Administration (FDA).Detection methods and quality control are strictly referred to thesame period "National AIDS detection technical specifications" and"National AIDS detection work management measures"^[6].Aface-to-face interview was conducted in a private room to gatherinformation on socio-demographic characteristics [age, gender,nationality, travel history, occupation, education, familysituation and risk behaviors of transmission] for those with finaldiagnosis of HIV. The respondents who did not complete the surveywere regarded as missing data and were not included in thestatistical scope of the study.

All HIV patients’ nations were classified as developed,developing and underdeveloped countries respectively. For thecurrent 2016 fiscal year, low-income economies were defined asthose with a GNI per capita, calculated using the World Bank Atlasmethod, of $1,045 or less in 2014; middle-incomeeconomies were those with a GNI per capita of more than$1,045 but less than $12,736; high-incomeeconomies were those with a GNI per capita of $12,736or more; Lower-middle-income and upper-middle-income economies wereseparated at a GNI per capita of$4,125^[7].

Data Analysis

The statistical analysis was carried out using SPSS, version22.0 software package (SPSS Inc., Chicago, IL, USA).Characteristics between the groups were compared using χ2 tests.Cochran-Mantel-Haenszel was used to compare the differences of thetotal population while controlling for time factors. Time trendswere calculated using Cochran-Armitage trend test. The results withP values < 0.05 were considered to be statisticallysignificant.

Characteristics of HIV positive travelers

From 2005 to 2016, a total of 50830 travelers who had entered inChina through Shanghai port had finished HIV infection screeningtest in Shanghai International Travel Healthcare Center. The annualrecruited populations (range 2640-5764) were not differentsignificantly among the sampling years. According to ELISA and WBresults, 245 individuals were detected to be infected with HIV,resulting in an infection rate of 0.48%. Amnong the 245 HIVinfected cross-border travelers entering at Shanghai border, 215(87.8%) were male and 30 (12.2% ) were female, with a male-to-female ratio of 7.17:1. The detection rate of HIV in male wassignificantly higher than that in female (χ2=62.584，P<0.0001).The age range of this population was 18-69 years old (median, 34 .2years). Those aged 18-30 years, 31-40 years and >40yearsaccounted for 34.3%, 39.6% and 26.1% of the infected population,respectively. Most of the positive cases were employed (53.88%) andhad a second or higher degree (81.22%). Moreover, 54.70% of thepositive cases were not married and 40.82% of them were fromlow-income countries.

Table 1 Demographic characteristic of positivecases

Subjects

Proportion(%)

Total

245

100%

Gender

male

215

87.76%

female

12.24%

Age

18-30

34.3%

31-40

39.6%

>40

26.1%

Current employmentstatus

Employed

132

53.88%

Unemployed

15.51%

Student

22.04%

Housewife/ husband

8.57%

Education

Less than secondary

18.78%

Secondary or higher

199

81.22%

Marital status

Never married

134

54.70%

Married orcohabitating

18.37%

Previouslymarried

26.94%

Host country

high-income countries

22.86%

middle-income countries

36.33%

low-income countries

100

40.82%

Risk behaviors oftransmission

Heterosexual

24.90%

Homosexual

142

57.96%

Blood/Plasma

3.27%

Injecting drugs

0.82%

Unknown/others

9.80%

Condom use

never

18.37%

sometimes

37.55%

Almost always

36.73%

always

4.08%

Infection rates over the years

Infection rates over the years were listed in Table 2. Althoughthe annual detection rates were different, the results from trendanalysis showed that there was no increase in trend of HIVprevalence rates among the sampling years (Cochran-Armitage Z=2.543，P =0.111). Trend analysis based on gender classificationindicated that neither male（Z =1.944，P =0.163）nor women（Z=0.198,P=0.656）had increase trend of HIV positive rates .

Table 2 HIV antibody positive rates among entry travelers2005-2016

Year	Male	Female	Total
2005	65(10/1532)	18(2/1108)	45(12/2640)
2006	54(10/1854)	8(1/1202)	36(11/3056)
2007	59(13/2198)	15(2/1374)	15(15/3572)
2008	58(15/2588)	39(6/1532)	51(21/4120)
2009	45(12/2665)	14(2/1445)	34(14/4120)
2010	80(15/1878)	12(2/1676)	48(17/3554)
2011	84(19/2254)	9(2/2136)	48(21/4390)
2012	85(20/2353)	10(2/2023)	50(22/4376)
2013	65(17/2604)	20(4/1969)	46(21/4573)
2014	99(29/2934)	5(1/2062)	60(30/4996)
2015	59(27/4541)	18(2/1128)	51(29/5669)
2016	77(28/3633)	19(4/2131)	56(32/5764)
Total	69(215/31034)	15(30/19796)	48(245/50830)

* positive rate: number in 10000 persons (positive number / numberof samples)

The change of transmission route

Proportions of individuals infected through homosexualtransmission increased over the study period (Cochran-Armitage Z=5.41，P<0.001), while the proportion infected throughheterosexual declined over time (Cochran-Armitage Z =3.38，P=0.001). The proportion infected through injecting drug declinedover time (Z=3.52，P<0.001). With the change in major HIV riskfactors, the heterosexual spreading of HIV was gradually increasingto be the main transmission route, compared to syringe/needlesharing. (Figure 1.)

Epidemiological characteristics of infectious diseases havechanged dramatically requiring necessitate health care workers tounderstand the status of these diseases, especially for AIDS andother pandemics disease ^[8–10]. Efforts andinvestments have been made globally to strengthen countries’ HIVmonitoring and evaluation (M&E) capacity^[11]. Cross-border travelerswith an HIV infection may cause local HIV transmission and aredefined as a bridge population ^[12]. Shanghai has the largestcross-border population entering China from countries around theworld. Cross-border travel is important for culture and commercebut also leads to the spread of infectious diseases. Therefore,it’s important to analyze HIV prevalence and demographiccharacteristics in this population. This was the first study whichdisplayed the HIV infection rate and their characteristics amongentry travelers over such a long time span, with such a large-scalepopulation in Shanghai.

From 2005 to 2016, there were 50830 international personsentering Shanghai who finished health examination in ShanghaiInternational Healthcare Center. In this crossing borderpopulation, a total of 245 (0.48%) travelers were determined as HIVpositive. Overall, we found that the HIV infection rate among entrytravelers in Shanghai did not show an increasing tendency overthese years, contributed by global HIV/AIDS prevention and controlefforts, such as promoting condoms in Southeast Asian countries andimplementing the Asian regional AIDS project, had receivedinternational attention and achieved good results.

After the HIV infected persons were found, the epidemicsituations were reported to the CDC epidemic reporting system, andthe related data were handed over to the local health department.In recent years, the Shanghai international travel healthcarecenter has strengthened the follow-up supervision of the entry ofAIDS patients, and established foreign liaison files for foreignHIV infected persons. Health education for the HIV infected personswas carried out to provide information about disease diagnosis andtreatment and conduct high risk behavior intervention. With thelocal disease control departments, medical institutions, foreignembassies and other information interoperability, jointcooperation, explore overseas HIV infection health counseling andtreatment measures. AIDS patients who do not want to return to thecountry need to be treated by providing health consultation anddesignated medical institutions to receive paid medical treatment.Using the existing conditions, according to local conditions, theentry-exit personnel health examination site could be settled as aconsulting base. We tried to make full use of newspapers,magazines, radio, television and other mass media to answer typicalquestions; to establish International Travel Health Advisorycontact, by using of websites, cellphone app and other ways toanswer questions raised by travelers on AIDS prevention and controlwork. With the local health administration, Family PlanningCommission, Red Cross and other departments, through public welfareperformances, on-site distribution brochures, free distribution ofcondoms and other means were undergoing.

In the last decade, we had seen a dramatic change in thedemographic structure of the population of people living with HIV(PLWH) ^[13]. This study found that HIV infectionof entry travelers in Shanghai also had certain demographiccharacteristics. From the perspective of age-specific HIVprevalence, the major age population of HIV infected travelers was18–40 years (73.90%). Overall, an estimated of 5 millionyoung people aged 15–24 were living with HIV in 2009 and accountedfor 41% (about 890,000 cases) of new HIV infections globally^[14].HIV is disproportionately afflicting young people worldwideglobally, especially in the developing countries. The similar trendpersisting was founded in our study. According to the diagnostictests, those with positive results was divided into three groups,(more than 40 years old, 31 to 40 years old, less than30 years old), working men aged 31 to 40 had the highestincidence whereas working women had a very low incidence (nearzero). The results are consistent with Wang’s research, they foundthat travelers aged 21–30 and 31–40 were the most commonly infectedindividuals among entry travelers in Yunnan Province^[2].

In addition, HIV infection was more frequently detected amongindividuals with occupations such as businessman and entertainers.Furthermore, from a view of marriage, unmarried (single or othermarital status) applicants had higher proportion of infectioncompared to those married group (54.70%vs18.37%). In general,people with better education and better cognitive ability havehealthier behaviors and lower HIV infection rate^[15].Nevertheless, our study found that most of the infected people werehighly educated. The entry travelers are divided into high-incomecountries, middle-income countries, and low-income countries basedon the host country ^[7]. Our data showed that most of thepositive cases were from middle- and low-income countries.

From the view of transmission, our data implied that sexualcontact was the major high risk behavior,especially in those menhave sex with men (MSM). In the meantime, a study in the USreported the most common HIV transmission route had changed tohomosexual contact in men, while injection drug users were rankedthe third^[16].We also deemed that the major HIVinfection route had been shifted from intravenous drug use tosexual contact in this study.

Monitoring of HIV infections in high-risk populations wasparticularly important for preventing the spread. This study foundthat those who did not use condom accounted for a large proportionin the positive cases. Inconsistent condom uses and severalrisk-taking behaviors were also reported among young people inUnited States (African-Americans aged 18–21) and Uganda^[17].Insufficient HIV-related knowledge and low self-awareness of riskmight be associated with an increasing number of AIDS. Thus,promotion and acceptance of sex education, accurate andage-appropriate information on HIV appeared to be the needed inorder to interrupt the spread of HIV.

Since this was a record-based study, some of the applicantrecords might be incomplete. The face to face interviews were onlyconducted in the HIV population, the characteristics of HIVnegative population could not be obtained. Therefore, thedemographic characteristics of them could not be compared.Furthermore, the sample may not be representative of the totalpopulation of entry travelers in China. At present, most foreignersin China are short-term immigration, some of them go back and forthmany times, the time of staying in China is less than one year eachtime, and the mobility is relatively large. China's law onlyapplies to the foreign applicants who apply for residence in Chinato carry out AIDS monitoring, so there is no effective monitoringmeasures and methods for most of the short-term immigrants.

According to the relevant provisions, entry foreigners holdingHIV antibody test negative proof of overseas public hospitals couldbe exempted from inspection. However, in the past years of work,many cases of these population, the HIV test were found positive.At the same time, the public security, inspection and quarantine,education, human resources and social security departments hadfound that some foreign health inspection materials provided byforeigners were incomplete or fraudulent. This part of thepopulation was the potential spread of AIDS population, however,the supervision of them was more difficult.

This study was one of few studies based on the certainpopulation that have been conducted in China. Although there werelimitations and incomplete information, we still believed that thisstudy could help us understand the dynamics of HIV transmissionamong international travelers to some extent. The findings of thisstudy highlighted the information gap in this area and helped usfill in a small part of it.

Our data from Shanghai International Travel Healthcare Centermore than a decade, suggested a target for HIV/AIDS prevention andcontrol efforts for international travelers. The rate andcharacteristics of HIV infection among foreign applicant toresidency in Shanghai were clarified in the study. The resultswould have provided the necessary epidemiological data formonitoring the HIV epidemic among entry international travelers andto further contribute to the establishment of relevant policies andregulations for HIV control and prevention.

Ethics approval and consent to participate

The design of this research was reviewed by Shanghai Entry-ExitInspection and Quarantine Bureau and approved by Shanghai MedicalEthics Committee. All personally identifiable information for thestudy population was stripped and the individual researchidentification number was assigned before the data set was sent toinvestigators for analyses.

Consent for publication

Written informed consent for publication was obtained from allparticipants.

Availability of data and material

All data are fully available without restriction.

Conflicting interests

All authors declare they have no conflict of interest.

Funding

None

Authors' contributions

QJ, XJ, ZPQ and ZR collaborated in the design of the study. QJand XJ developed the survey instruments. QJ, ZPQ and ZR oversaw thedata collection. QJ and ZR did the statistical analysis and alsowrote the initial drafts. All authors reviewed and edited thereport and all take responsibility for its integrity and theaccuracy of the analysis.

Acknowledgements

We would like to thank all the participants of this study andall staff of HIV/AIDS case reporting system in ShanghaiInternational Healthcare Center.

Authors' information

Jia Qin: Shanghai International Travel Healthcare Center,Shanghai, 200335, China

Jing Xia: Shanghai International Travel Healthcare Center,Shanghai, 200335, China

Peiqin Zhu: Shanghai International Travel Healthcare Center,Shanghai, 200335, China

Ru Zhou: Department of General Surgery, RuiJin Hospital / LuWanBranch, School of medicine, Shanghai Jiaotong University, Shanghai,200020, China

Corresponding author: Ru Zhou

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Prevalence of HIV infection among foreign applicant to residency in Shanghai, China, 2005-2016

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Abstract

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Background

Methods

Study population and data collection

Data Analysis

Results

Discussion

Strengths And Limitations

Conclusion

Declarations

References

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