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Prevalence of HIV and syphilis infections among long-distance truck drivers in China: a data synthesis and meta-analysis

Open ArchivePublished:October 11, 2012DOI:https://doi.org/10.1016/j.ijid.2012.07.018

      Summary

      By 2009, 46 national sentinel surveillance sites had been established for long-distance truck drivers (LDTDs) in China, but the overall disease burden of HIV and syphilis among LDTDs has remained unclear. This study aimed to summarize the prevalence levels of these infections from available published peer-reviewed studies through a comprehensive systematic review and meta-analysis. Forty-six eligible articles were selected in this review. The pooled prevalence estimates of HIV and syphilis among Chinese LDTDs during 1995–2010 were 0.19% (95% confidence interval (CI) 0.15–0.24%) and 0.86% (95% CI 0.70–1.06%), respectively, corresponding to a 3.33 (95% CI 2.40–4.62) and 1.65 (95% CI 1.35–2.03) times higher risk of infection among LDTDs than the general Chinese population. However, these infection risks were much lower than those of LDTDs in other developing country settings and at-risk groups in China. Current surveillance resources have been disproportionately focused on LDTDs and should be diverted to other at-risk groups.

      Keywords

      1. Introduction

      By the end of 2011, approximately 780 000 (95% confidence interval (CI) 620 000–940 000) people were living with HIV/AIDS in China,
      Ministry of Health of the People's Republic of China
      2010 Estimates for the HIV/AIDS epidemic in China.
      corresponding to a national prevalence of 0.058% (95% CI 0.046–0.070%).
      Ministry of Health of the People's Republic of China
      2010 Estimates for the HIV/AIDS epidemic in China.
      In 2011, the majority (81.6%) of people newly diagnosed with HIV (n = 48 000) were infected through sexual means, including 52.2% through heterosexual exposure and 29.4% through homosexual exposure.
      Ministry of Health of the People's Republic of China
      2010 Estimates for the HIV/AIDS epidemic in China.
      Of those infected through heterosexual exposure, approximately three-quarters were infected through a non-spousal pathway, indicating that extra-marital relationships are an important factor contributing to HIV transmission. In addition, the diagnosis of syphilis among the general Chinese population increased 3.55-fold from 6.5 cases per 100 000 individuals in 1999 to 23.1 cases per 100 000 individuals in 2009,
      • Chow E.P.
      • Wilson D.P.
      • Zhang L.
      HIV and syphilis co-infection increasing among men who have sex with men in China: a systematic review and meta-analysis.

      Ministry of Health of the People's Republic of China, Joint United Nations Programme on HIV/AIDS, World Health Organization. China health statistics yearbook 2010. Ministry of Health of the People's Republic of China, UNAIDS, WHO; 2010.

      reaching a prevalence level of between 0.33% and 0.71% among sexually active young Chinese adults.
      • Hesketh T.
      • Tang F.
      • Wang Z.B.
      • Huang X.M.
      • Williams D.
      • Cubitt D.W.
      • et al.
      HIV and syphilis in young Chinese adults: implications for spread.
      It has long been perceived that male clients of female sex workers (FSWs) can act as a potential bridge for HIV and other sexually transmitted infections (STIs) to their regular female partners.
      • Voeten H.A.
      • Egesah O.B.
      • Ondiege M.Y.
      • Varkevisser C.M.
      • Habbema J.D.
      Clients of female sex workers in Nyanza Province, Kenya: a core group in STD/HIV transmission.
      Long-distance truck drivers (LDTDs) – in the Chinese context defined as truck drivers who have undertaken at least three overnight trips in the past 3 months

      Chinese Center for Disease Control and Prevention, Institute for STD and AIDS Prevention and Control. Operating manual of national AIDS sentinel surveillance protocol. Beijing: Chinese Center for Disease Control and Prevention; 2011.

      – typically have frequent sexual encounters with FSWs during their trips
      • Pandey A.
      • Benara S.K.
      • Roy N.
      • Sahu D.
      • Thomas M.
      • Joshi D.K.
      • et al.
      Risk behaviour, sexually transmitted infections and HIV among long-distance truck drivers: a cross-sectional survey along national highways in India.
      • Sunmola A.M.
      Sexual practices, barriers to condom use and its consistent use among long distance truck drivers in Nigeria.
      • Malta M.
      • Bastos F.I.
      • Pereira-Koller E.M.
      • Cunha M.D.
      • Marques C.
      • Strathdee S.A.
      A qualitative assessment of long distance truck drivers’ vulnerability to HIV/AIDS in Itajai, southern Brazil.
      and are often regarded as a proxy group for male clients in many international settings.
      • Pandey A.
      • Benara S.K.
      • Roy N.
      • Sahu D.
      • Thomas M.
      • Joshi D.K.
      • et al.
      Risk behaviour, sexually transmitted infections and HIV among long-distance truck drivers: a cross-sectional survey along national highways in India.
      • Sunmola A.M.
      Sexual practices, barriers to condom use and its consistent use among long distance truck drivers in Nigeria.
      • Malta M.
      • Bastos F.I.
      • Pereira-Koller E.M.
      • Cunha M.D.
      • Marques C.
      • Strathdee S.A.
      A qualitative assessment of long distance truck drivers’ vulnerability to HIV/AIDS in Itajai, southern Brazil.
      • Jing J.
      [HIV/AIDS surveillance in China].
      Due to extensive time away from their families, it has been suggested that LDTDs in China are more likely to solicit FSWs,
      • Marck J.
      Resistances to behavioural change to reduce HIV/AIDS infection.
      • Tian X.
      • Jiang L.
      • Fan B.
      • Zhang J.
      • Wang Y.
      • Huang H.
      • et al.
      [Study on HIV/AIDS prevention and interventions for long distance truck drivers].
      • Xu Y.
      • Zhu J.
      • Mo X.
      • Liang H.
      • Zhou J.
      • Li P.
      [Analysis of HIV/AIDS related knowledge, attitude, behavior in long distance truck drivers in Nanning City].
      and they often patronize ‘low-tier’ FSWs from roadside settlements/hotels, who are generally poorly educated with limited knowledge and awareness of HIV, with a relatively high prevalence of HIV.
      • Bai Y.
      [Survey of knowledge behaviors and HIV infection among commercial sex workers from high, middle and low level places].
      The previous literature has reported an HIV prevalence among ‘low-tier’ FSWs of about 14.2–20.9%,
      • Wang G.
      • Ding G.
      • Wang H.
      • Xu J.
      • Chang D.
      • Gu J.
      [Two cross-sectional surveys on HIV/STI infection among female sex workers in a county of Yunnan Province].
      • Li Q.
      • Xu J.
      • Wang W.
      • Wang G.
      • Chang D.
      • Wang N.
      [Survey of high risk behaviors and HIV/STD infection among FSWs from different venues of Kaiyuan City].
      • Li R.
      • Liu Z.
      • Xu C.
      [Analysis of HIV surveillance among female sex workers in Luxi City, Yunnan Province, 2005–2007].
      much higher than that among ‘high-tier’ FSWs (0.8–2.9%).
      • Li R.
      • Liu Z.
      • Xu C.
      [Analysis of HIV surveillance among female sex workers in Luxi City, Yunnan Province, 2005–2007].
      • Nong L.
      • He B.
      • Zhou Y.
      • Liang S.
      • Liang F.
      • Bi S.
      • et al.
      [Survey on prevalence of HIV and syphilis among female sex workers].
      • Zhang J.
      • Li Y.
      • Wimai E.J.
      • Ka M.N.
      • et al.
      [Analysis on result of HIV screening test among female sex workers in Aksu, Xinjiang].
      Levels of condom use among LDTDs are low with both FSWs (48.2%)
      • Qiu R.
      • Wang F.
      [Investigation on AIDS related knowledge, behavior and the status of HIV infection among 314 male long distance truck drivers in Guixi City].
      and their regular female partners (24.7–35%)
      • Zhang M.
      • Fang P.
      [Analysis on HIV related risk behaviors among married Chinese long-distance trucker drivers].
      • Zhang C.
      • Jia Y.
      [KAP about AIDS prevention of long distance truckers in Datong City, a survey of 1000 cases].
      • Chen S.
      • Mo X.
      • Mo J.
      • Bin F.
      • Zhu J.
      [Investigation on AIDS related knowledge, attitude and behavior among long distance truck drivers in Nanning City in 2007].
      in the last sexual act. The Chinese LDTDs have been regarded as a population with a high risk of acquiring, as well as spreading, HIV and syphilis through sexual contacts, both locally and in distant areas.
      • Azuonwu O.
      • Erhabor O.
      • Frank-Peterside N.
      HIV infection in long-distance truck drivers in a low income setting in the Niger Delta of Nigeria.
      HIV and STI epidemic markers among LDTDs have been monitored in China through its established sentinel surveillance system since 1995.
      • Qu S.Q.
      • Sun X.H.
      • Zheng X.W.
      • Shen J.
      [National sentinel surveillance of HIV infection in China from 1995 to 1998].
      However, these surveillance results have not been published in a systematic manner and the overall disease burden of HIV and syphilis among LDTDs remains unclear. This study aimed to collate and summarize the prevalence of HIV and syphilis among LDTDs in China from available published peer-reviewed studies through a comprehensive systematic review and meta-analysis. This analysis will provide important evidence that directs effective surveillance efforts and strategies for HIV in China.

      2. Methods

      2.1 Search strategy

      Two investigators (XZ, EPFC) performed a systematic review of published research articles by searching the Chinese and English databases independently. Electronic databases used in this review included PubMed, China National Knowledge Infrastructure (CNKI), Wanfang Data, and CQVIP (Chinese Scientific Journals Fulltext Database) for the period 1995 to August 2011. Keywords used in the database search included “Long-distance truck driver” AND (“HIV” OR “AIDS” OR “STI” OR “sexually transmitted infections” OR “syphilis”) AND “China”. This review was conducted and reported according to the PRISMA (Preferred Reporting Items for Systematic Reviews and Meta-Analyses) statement issued in 2009.
      • Moher D.
      • Liberati A.
      • Tetzlaff J.
      • Altman D.G.
      Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement.

      2.2 Study selection

      Studies were eligible for inclusion in the systematic review if they met the following criteria: (1) study published in Chinese or English language; (2) study reported the prevalence level of HIV and/or syphilis among LDTDs in China; (3) reported infections had to have been diagnosed in a laboratory using a qualified serologic testing method; (4) study design and sample size had to be reported. We excluded review papers, non-peer-reviewed local/government reports, conference abstracts, presentations, and studies with a small sample size (n < 30). If the same study data were published in both English and Chinese databases, the articles published in Chinese were excluded from the review. Disagreements with regard to the study criteria were decided by a third investigator (LZ). The quality of studies was assessed using a validated quality assessment tool.
      • Boyle M.H.
      Guidelines for evaluating prevalence studies.

      2.3 Data abstraction

      We extracted the following information from all eligible studies: first author and year published, study location, study period, sample size, percentage of male respondents in the study, testing method for syphilis and HIV infection, and the prevalence of HIV and syphilis infection. Data were stored in Microsoft Access 2007.

      2.4 Statistical analysis

      Meta-analyses were carried out using the Comprehensive Meta-Analysis software (v2.0, Biostat, Englewood, NJ, USA). Heterogeneity was tested by Cochran Q-test (p < 0.10 represents statistically significant heterogeneity) and the I2 statistic (I2 = 25, 50, and 75 represents low, medium, and high heterogeneity, respectively). Since all meta-analyses in this study showed low and insignificant heterogeneities, a fixed-effect model was used to calculate the effect rate of pooled prevalence estimates and 95% CI. Publication bias was measured by the Begg and Mazumdar rank correlation (p < 0.05 represents statistically significant publication bias). Odd ratios and their 95% CI for the prevalence of the diseases were calculated to compare the risk of infection between Chinese LDTDs and the general adult population.

      3. Results

      Our search identified 336 articles from four electronic databases (PubMed = 1; CQVIP = 29; CNKI = 177; Wanfang = 129). We excluded 177 articles due to a lack of relevance or duplicated titles from different databases. We screened the abstracts of the remaining 159 articles and excluded a further 55 articles (49 articles were qualitative research and six were review papers). Full-text screening was conducted of the 104 articles and 58 were excluded due to the absence of any prevalence data reported (n = 55) and duplicated studies based on the same data source (n = 3). The remaining 46 studies
      • Qiu R.
      • Wang F.
      [Investigation on AIDS related knowledge, behavior and the status of HIV infection among 314 male long distance truck drivers in Guixi City].
      • Zhang M.
      • Fang P.
      [Analysis on HIV related risk behaviors among married Chinese long-distance trucker drivers].
      • Cai Y.
      • Chen M.
      [Survey of infectious status of HIV and syphilis in male truck divers in 2005–2006].
      • Chen M.
      • Xu F.
      [Survey on HIV/AIDS knowledge among Chinese long-distance truckers].
      • Chen X.S.
      • Yin Y.P.
      • Gong X.D.
      • Liang G.J.
      • Zhang W.Y.
      • Poumerol G.
      • et al.
      Prevalence of sexually transmitted infections among long-distance truck drivers in Tongling, China.
      • Cheng X.
      • Wang F.
      • Xiao Y.
      [Analysis on the data of HIV sentinel surveillance in 2002–2006 in Anhui Province].
      • Deng F.
      • Zhu F.
      • Zhang Y.
      [Epidemiological survey on HIV/AIDS in Anlu city (2002–2007)].
      • Deng J.
      • Xiao S.
      • Zhang Y.
      • Song Y.
      [Analysis on the epidemic characterization and trend of AIDS in Huangshi].
      • Deng L.
      • Feng L.
      • Zhang W.
      • Wang X.
      • Li Y.
      [Analysis on HIV monitoring among LDTDs in Guandu District, Kunming City].
      • Qu S.Q.
      • Sun Z.H.
      • Zheng X.W.
      • Chen J.
      [National sentinel surveillance of HIV infection in China from 1995 to 1998].
      • Feng L.
      [Analysis on HIV surveillance among long-distance truck drivers in China].
      • Guo W.
      • Zang X.
      • Zhang X.
      • Wei Y.
      • Sun X.
      • Yuan X.
      [HIV sentinel surveillance report on male long distance truck drivers in Lanzhou City, Gansu Province].
      • He B.
      • Nong L.
      • Lu Z.
      • He C.
      • Zhang J.
      • Li W.
      [Survey on HIV and syphilis infection among long-distance truck drivers].
      • Ji W.
      • Wei H.
      • Lv J.
      [Analysis on AIDS monitoring results of high- risk groups in 2008–2009 in Qilihe].
      • Jia C.
      • Yang H.
      • Xu X.
      • Li L.
      • Liu G.
      • Xing H.
      • et al.
      [Seroepidemiological and molecular epidemiological study on HIV infecion in Jiangsu Province].
      • Ke X.
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      • Deng J.
      • Chen W.
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      • Wu X.
      • et al.
      [HIV infection rate in the different groups of high-risk AIDS population in Huangshi City].
      • Leng B.
      • Zhang L.
      • Zhang H.
      • Xu K.
      [Survey on HIV knowledge and sexual behaviors among long-distance truck drivers in Zhoukou City, Henan Province].
      • Li B.
      • Liang L.
      • Zhao H.
      • Bai G.
      • Zhao C.
      • Chen Z.
      [Status of sentinel montoring of HIV/AIDS in Hebei Province].
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      [Study on promoting safer behaviors among long-distance truck drivers].
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      [Analysis of data from HIV surveillance sentinel sites in Jiangsu Province in 2000].
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      • Bai J.
      [Analysis on cognitive survey of AIDS prevention and treatment knowledge in long distance men driver from Shangluo City in 2009].
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      [HIV seroepidemiological survey among targeted population in Yulin City, Guangxi Province].
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      • Qian Y.
      • Wang T.
      [Analysis of HIV/AIDS surveillance data in Shandong Province in 2007].
      • Lin B.
      • Shi F.
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      • Meng Y.
      • Guo J.
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      • et al.
      [Analysis of HIV and syphilis serological testing result among high risk population in Karamay].
      • Liu X.
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      [Analysis on HIV/AIDS surveillance data of Shandong Province in 2004].
      • Liu X.
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      [AIDS surveillance mechanism and its results in Henan Province].
      • Liu Y.
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      • Fu X.
      • Chen Z.
      [Surveillance on HIV infection and HBsAg among high risk populations in Yingcheng City, Hubei Province].
      • Lu H.
      • Hu X.
      [Investigation and analysis on HIV infection in Huaibei].
      • Lu Y.
      • Guo J.
      • Su P.
      • Gu Y.
      • Zhang W.
      [Survey on HIV infection and related behaviours among long-distance truck drivers in Guandu District, Kunming City, Yunnan Province].
      • Nong L.
      • He B.
      • Zhang J.
      • Li B.
      [Serological detection on HIV and syphilis of long-distance truck driver in Pingxiang, 2004–2010].
      • Osman J.
      • Zhang M.
      • Zhang L.
      [Analysis of HIV/STD surveillance in Urumqi from 2000 to 2003].
      • Peng G.
      • Zhang Y.
      • Jiang H.
      [Analysis of epidemic characteristics of HIV/AIDS in Hubei Province].
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      • Zhou P.
      [Epidemiological analysis on the newly discovered HIV/AIDS in Suizhou City (2007–2009)].
      • Wang C.
      • Gao X.
      • Sun F.
      • Sai L.K.
      • Na Y.L.
      [Study on HIV infection among long-distance truck drivers in Lli District, Xinjiang Autonomous Region].
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      • Chen F.
      [Investigation on the HIV infection and behavior of 5 kinds of people in Dangyang City (2006)].
      • Wei X.
      • An Z.
      • Wang H.
      • Feng X.
      • Pang S.
      • Cao W.
      • et al.
      [Data analysis on STI sentinel surveillance among high-risk populations in Shihezi City in Xinjiang Autonomous Region].
      • Wen Z.
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      • Jiang W.
      • et al.
      [Analysis of the HIV/AIDS surveillance data in the Three Gorges area of Xingshan County].
      • Xi S.
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      • Zhou X.
      • Wang Z.
      [KAP study on HIV/AIDS among long-distance truck drivers in China].
      • Xu X.
      • Liu S.
      • Zhang J.
      [Analysis of AIDS sentinel surveillance in Huhhot in 2009].
      • Yan J.
      • Ji W.
      • Wei H.
      [Study on 400 long-distance truck drivers for HIV, hepatitis C and syphilis infection in Qilihe in 2009].
      • Yang J.
      • Yu A.
      • Jin A.
      • Zhang C.
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      • Zhan X.
      • Chen H.
      • Jiang H.
      [Analysis of the results of HIV surveillance in Hubei Province in 2003].
      • Zhou W.
      • Zhao J.
      • Li P.
      [Survey of AIDS-related knowledge and behaviors among male long-distance truck drivers in Ningbo City].
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      • Yang J.
      • Pan X.
      • Yang Q.
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      • Li X.
      • et al.
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      (two in English and 44 in Chinese) were eligible for the quantitative synthesis. Meta-analyses were performed to estimate the prevalence of HIV (46 articles, 74 prevalence estimates) and syphilis (23 articles, 33 prevalence estimates) infections among LDTDs. The selection process is illustrated in the Supplementary Material (Figure S1) and the details of each study are shown in Table 1.
      Table 1Studies reporting the prevalence of HIV and syphilis infection among Chinese long-distance truck drivers
      Prevalence of HIV infection
      First author, published yearLanguageStudy periodStudy locationType of studyLaboratory test for HIV infectionSample sizeNumber of HIV infectionsHIV prevalenceQuality assessment score
      Cai, 2007
      • Cai Y.
      • Chen M.
      [Survey of infectious status of HIV and syphilis in male truck divers in 2005–2006].
      Chinese2005–2006Ningbo (Zhejiang)Cross-sectionalELISA70800.00%6
      Chen, 2008
      • Chen M.
      • Xu F.
      [Survey on HIV/AIDS knowledge among Chinese long-distance truckers].
      Chinese2005Ningbo (Zhejiang)Cross-sectionalELISA30300.00%6
      Chen, 2006
      • Chen X.S.
      • Yin Y.P.
      • Gong X.D.
      • Liang G.J.
      • Zhang W.Y.
      • Poumerol G.
      • et al.
      Prevalence of sexually transmitted infections among long-distance truck drivers in Tongling, China.
      English02/2000–05/2000Tongling (Anhui)Cross-sectionalELISA55000.00%8
      Cheng, 2009
      • Cheng X.
      • Wang F.
      • Xiao Y.
      [Analysis on the data of HIV sentinel surveillance in 2002–2006 in Anhui Province].
      Chinese2003Anqing (Anhui)Cross-sectionalELISA38700.00%5
      Cheng, 2009
      • Cheng X.
      • Wang F.
      • Xiao Y.
      [Analysis on the data of HIV sentinel surveillance in 2002–2006 in Anhui Province].
      Chinese2004Anqing (Anhui)Cross-sectionalELISA40900.00%5
      Cheng, 2009
      • Cheng X.
      • Wang F.
      • Xiao Y.
      [Analysis on the data of HIV sentinel surveillance in 2002–2006 in Anhui Province].
      Chinese2005Anqing (Anhui)Cross-sectionalELISA42010.20%5
      Cheng, 2009
      • Cheng X.
      • Wang F.
      • Xiao Y.
      [Analysis on the data of HIV sentinel surveillance in 2002–2006 in Anhui Province].
      Chinese2006Anqing (Anhui)Cross-sectionalELISA41800.00%5
      Cheng, 2009
      • Cheng X.
      • Wang F.
      • Xiao Y.
      [Analysis on the data of HIV sentinel surveillance in 2002–2006 in Anhui Province].
      Chinese2007Anqing (Anhui)Cross-sectionalELISA42210.20%5
      Deng, 2009
      • Deng F.
      • Zhu F.
      • Zhang Y.
      [Epidemiological survey on HIV/AIDS in Anlu city (2002–2007)].
      Chinese2002–2007Anlu (Hubei)Cross-sectionalELISA67000.00%5
      Deng, 2005
      • Deng J.
      • Xiao S.
      • Zhang Y.
      • Song Y.
      [Analysis on the epidemic characterization and trend of AIDS in Huangshi].
      Chinese2000–2002Huangshi (Hubei)Cross-sectionalELISA43600.00%6
      Deng, 2011
      • Deng L.
      • Feng L.
      • Zhang W.
      • Wang X.
      • Li Y.
      [Analysis on HIV monitoring among LDTDs in Guandu District, Kunming City].
      ChineseN/AKunming (Yunnan)Cross-sectionalELISA40030.75%7
      Feng, 2008
      • Feng L.
      [Analysis on HIV surveillance among long-distance truck drivers in China].
      Chinese1997–2006Golmud (Xinjiang)Cross-sectionalELISA419330.07%7
      Feng, 2008
      • Feng L.
      [Analysis on HIV surveillance among long-distance truck drivers in China].
      Chinese2001Golmud (Xinjiang)Cross-sectionalELISA41720.48%7
      Feng, 2008
      • Feng L.
      [Analysis on HIV surveillance among long-distance truck drivers in China].
      Chinese2005Golmud (Xinjiang)Cross-sectionalN/A40110.25%7
      Guo, 2010
      • Guo W.
      • Zang X.
      • Zhang X.
      • Wei Y.
      • Sun X.
      • Yuan X.
      [HIV sentinel surveillance report on male long distance truck drivers in Lanzhou City, Gansu Province].
      Chinese04/2010–05/2010Lanzhou (Gansu)Cross-sectionalN/A40000.00%5
      He, 2006
      • He B.
      • Nong L.
      • Lu Z.
      • He C.
      • Zhang J.
      • Li W.
      [Survey on HIV and syphilis infection among long-distance truck drivers].
      Chinese10/2004–11/2004GuangxiCross-sectionalELISA36800.00%7
      Qu, 2000
      • Qu S.Q.
      • Sun Z.H.
      • Zheng X.W.
      • Chen J.
      [National sentinel surveillance of HIV infection in China from 1995 to 1998].
      Chinese1997Urumqi (Xinjiang)National sentinel studyELISA40010.30%6
      Qu, 2000
      • Qu S.Q.
      • Sun Z.H.
      • Zheng X.W.
      • Chen J.
      [National sentinel surveillance of HIV infection in China from 1995 to 1998].
      Chinese1998Urumqi (Xinjiang)National sentinel studyELISA40020.50%6
      Ji, 2010
      • Ji W.
      • Wei H.
      • Lv J.
      [Analysis on AIDS monitoring results of high- risk groups in 2008–2009 in Qilihe].
      Chinese2009Qilihe (Gansu)CohortN/A40010.25%4
      Ji, 2010
      • Ji W.
      • Wei H.
      • Lv J.
      [Analysis on AIDS monitoring results of high- risk groups in 2008–2009 in Qilihe].
      Chinese2008Qilihe (Gansu)CohortN/A28400.00%4
      Jia, 2002
      • Jia C.
      • Yang H.
      • Xu X.
      • Li L.
      • Liu G.
      • Xing H.
      • et al.
      [Seroepidemiological and molecular epidemiological study on HIV infecion in Jiangsu Province].
      Chinese1995–2000JiangsuCohortELISA76510.13%5
      Ke, 2008
      • Ke X.
      • Xiao S.
      • Deng J.
      • Chen W.
      • Xiong F.
      • Wu X.
      • et al.
      [HIV infection rate in the different groups of high-risk AIDS population in Huangshi City].
      Chinese2004–2007Huangshi (Hubei)Cross-sectionalELISA69500.00%5
      Leng, 2010
      • Leng B.
      • Zhang L.
      • Zhang H.
      • Xu K.
      [Survey on HIV knowledge and sexual behaviors among long-distance truck drivers in Zhoukou City, Henan Province].
      Chinese2009Zhoukou (Henan)Cross-sectionalELISA40000.00%7
      Li, 2010
      • Li B.
      • Liang L.
      • Zhao H.
      • Bai G.
      • Zhao C.
      • Chen Z.
      [Status of sentinel montoring of HIV/AIDS in Hebei Province].
      Chinese1997–2006HebeiCross-sectionalELISA632200.00%6
      Li, 1999
      • Li H.
      • Chen J.
      • Liang S.
      • Zhang K.
      • Liang F.
      • Liu W.
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      ELISA, enzyme-linked immunosorbent assay; N/A, laboratory test method not mentioned in the study; RPR, rapid plasma reagin; TPHA, Treponema pallidum hemagglutination assay; TPPA, Treponema pallidum particle agglutination assay; TRUST, toluidine red unheated serum test; WB, Western blot.

      3.1 Study characteristics

      Among 46 eligible articles, all reported the study location, covering 14 Chinese provinces. The study sampling size ranged from 47 to 12 119 (median 402, interquartile range 366–711). Only one-quarter of the studies (12/46) reported the gender composition of the respondents, among which 11 studies reported 100% male respondents and one reported 99.3% male respondents. Types of studies on HIV prevalence included national sentinel studies (n = 15), cross-sectional studies (n = 28), cohort studies (n = 2), and a baseline survey from an intervention study (n = 1). Among 22 articles reporting the prevalence of syphilis infection, five were national sentinel studies and 17 were cross-sectional studies.

      3.2 Prevalence of HIV and syphilis

      Correlation analysis showed that there was no significant association between HIV infection and the study period (r = −0.165, p = 0.167). The pooled estimate of HIV prevalence among Chinese LDTDs was 0.19% (95% CI 0.15–0.24%) during 1995–2010 (Table 2). Significant publication bias (Begg rank correlation, p = 0.005) and low heterogeneity (I2 = 0, p = 0.941) were found across studies. In comparison, the prevalence of syphilis infections was 0.86% (95% CI 0.70–1.06%) among LDTDs, with a significant publication bias (p < 0.001) and medium heterogeneity (I2 = 46.053; p = 0.002). Similarly, there was no significant correlation between the study period and the prevalence of syphilis infection (r = 0.228, p = 0.218). In contrast, the prevalence levels of HIV and syphilis among the general population were 0.057% (95% CI 0.042–0.071%)

      Ministry of Health of the People's Republic of China, Joint United Nations Programme on HIV/AIDS, World Health Organization. China health statistics yearbook 2010. Ministry of Health of the People's Republic of China, UNAIDS, WHO; 2010.

      and 0.52% (95% CI 0.33–0.71%),
      • Hesketh T.
      • Tang F.
      • Wang Z.B.
      • Huang X.M.
      • Williams D.
      • Cubitt D.W.
      • et al.
      HIV and syphilis in young Chinese adults: implications for spread.
      • Hesketh T.
      • Ye X.J.
      • Zhu W.X.
      Syphilis in China: the great comeback.
      respectively (Table 2). LDTDs were found to be 3.33 (95% CI 2.40–4.62) and 1.65 (95% CI 1.35–2.03) times more at risk of being infected with HIV and syphilis, respectively.
      Table 2Relative risk and 95% confidence intervals for the prevalence of HIV/STIs among long-distance truck drivers in comparison with the general population in China
      InfectionPooled prevalence estimate in LDTDs from meta-analysis, % (95% CI)Reported prevalence mean in general population, % (range)Relative risk of infection (95% CI)
      HIV0.19 (0.15–0.24)

      (See Supplementary Material, Figure S2)
      0.057 (0.042–0.071)

      Ministry of Health of the People's Republic of China, Joint United Nations Programme on HIV/AIDS, World Health Organization. China health statistics yearbook 2010. Ministry of Health of the People's Republic of China, UNAIDS, WHO; 2010.

      3.33 (2.40–4.62)
      Syphilis0.86 (0.70–1.06)

      (See Supplementary Material, Figure S3)
      0.52 (0.33–0.71)
      • Hesketh T.
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      • Wang Z.B.
      • Huang X.M.
      • Williams D.
      • Cubitt D.W.
      • et al.
      HIV and syphilis in young Chinese adults: implications for spread.
      • Hesketh T.
      • Ye X.J.
      • Zhu W.X.
      Syphilis in China: the great comeback.
      1.65 (1.35–2.03)
      CI, confidence interval; LDTD, long-distance truck driver; STI, sexually transmitted infection.

      4. Discussion

      Chinese LDTDs are one of the at-risk populations regularly monitored by the national HIV sentinel surveillance in China.
      • Qu S.Q.
      • Sun X.H.
      • Zheng X.W.
      • Shen J.
      [National sentinel surveillance of HIV infection in China from 1995 to 1998].
      However, this practice is not based on sound scientific evidence within China, but relies purely on findings from other developing countries, where LDTDs have been found to be particularly vulnerable to HIV.
      • Voeten H.A.
      • Egesah O.B.
      • Ondiege M.Y.
      • Varkevisser C.M.
      • Habbema J.D.
      Clients of female sex workers in Nyanza Province, Kenya: a core group in STD/HIV transmission.
      • Pandey A.
      • Benara S.K.
      • Roy N.
      • Sahu D.
      • Thomas M.
      • Joshi D.K.
      • et al.
      Risk behaviour, sexually transmitted infections and HIV among long-distance truck drivers: a cross-sectional survey along national highways in India.
      • Sunmola A.M.
      Sexual practices, barriers to condom use and its consistent use among long distance truck drivers in Nigeria.
      • Jing J.
      [HIV/AIDS surveillance in China].
      In contrast to the high HIV prevalence reported in Africa (56% in South Africa,
      • Ramjee G.
      • Gouws E.
      Prevalence of HIV among truck drivers visiting sex workers in KwaZulu-Natal, South Africa.
      17.8% in Kenya,
      • Jackson D.J.
      • Rakwar J.P.
      • Richardson B.A.
      • Mandaliya K.
      • Chohan B.H.
      • Bwayo J.J.
      • et al.
      Decreased incidence of sexually transmitted diseases among trucking company workers in Kenya: results of a behavioural risk-reduction programme.
      and 10.0% in Nigeria
      • Azuonwu O.
      • Erhabor O.
      • Frank-Peterside N.
      HIV infection in long-distance truck drivers in a low income setting in the Niger Delta of Nigeria.
      ) and other Asian countries (15.9% in India
      • Gawande A.V.
      • Vasudeo N.D.
      • Zodpey S.P.
      • Khandait D.W.
      Sexually transmitted infections in long distance truck drivers.
      • Manjunath J.V.
      • Thappa D.M.
      • Jaisankar T.J.
      Sexually transmitted diseases and sexual lifestyles of long-distance truck drivers: a clinico-epidemiologic study in south India.
      and 5.3–7.0% in Guinea
      • Diallo B.L.
      • Alary M.
      • Rashed S.
      • Barry A.
      [HIV prevalence, associated risk factors and evolution among truck drivers from 2001 to 2007 in Guinea].
      ), Chinese LDTDs sustained a relatively low HIV prevalence (0.19%, 95% CI 0.15–0.24%) throughout 1995–2010. Similarly, the prevalence of syphilis infection among LDTDs is as high as 21% in India,
      • Gawande A.V.
      • Vasudeo N.D.
      • Zodpey S.P.
      • Khandait D.W.
      Sexually transmitted infections in long distance truck drivers.
      • Manjunath J.V.
      • Thappa D.M.
      • Jaisankar T.J.
      Sexually transmitted diseases and sexual lifestyles of long-distance truck drivers: a clinico-epidemiologic study in south India.
      but we estimate only 0.86% (95% CI 0.7–1.06%) among Chinese LDTDs. This indicates that Chinese LDTDs experience a much lower risk of HIV infection than the level originally perceived during the early phase of the HIV epidemic in China. This could be due to several reasons. First, China has maintained a low-level concentrated epidemic of HIV and syphilis.
      • Azuonwu O.
      • Erhabor O.
      • Frank-Peterside N.
      HIV infection in long-distance truck drivers in a low income setting in the Niger Delta of Nigeria.

      WHO, UNAIDS, UNICEF. Epidemiological fact sheet on HIV and AIDS 2008. WHO; 2008. Available at: http://www.who.int/countries/en/ (accessed March 13, 2012).

      Second, it is reported that LDTDs in other developing countries are more likely to solicit FSWs (68.5–86%)
      • Azuonwu O.
      • Erhabor O.
      • Frank-Peterside N.
      HIV infection in long-distance truck drivers in a low income setting in the Niger Delta of Nigeria.
      • Atilola G.O.
      • Akpa O.M.
      • Komolafe I.O.
      HIV/AIDS and the long-distance truck drivers in south-west Nigeria: a cross-sectional survey on the knowledge, attitude, risk behaviour and beliefs of truckers.
      • Botros B.A.
      • Aliyev Q.M.
      • Saad M.D.
      • Michael A.A.
      • Sanchez J.L.
      • Carr J.K.
      • et al.
      HIV infection and associated risk factors among long-distance truck drivers travelling through Azerbaijan.
      in comparison to those in China (19–30%),
      • Deng L.
      • Feng L.
      • Zhang W.
      • Wang X.
      • Li Y.
      [Analysis on HIV monitoring among LDTDs in Guandu District, Kunming City].
      • Guo W.
      • Zang X.
      • Zhang X.
      • Wei Y.
      • Sun X.
      • Yuan X.
      [HIV sentinel surveillance report on male long distance truck drivers in Lanzhou City, Gansu Province].
      • Zhang C.L.
      • Jia Y.S.
      [KAP about AIDS prevention of long distance truckers in Datong City, a survey of 1000 cases].
      with consistently lower condom use (15–32%)
      • Azuonwu O.
      • Erhabor O.
      • Frank-Peterside N.
      HIV infection in long-distance truck drivers in a low income setting in the Niger Delta of Nigeria.
      • Ramjee G.
      • Gouws E.
      Prevalence of HIV among truck drivers visiting sex workers in KwaZulu-Natal, South Africa.
      • Atilola G.O.
      • Akpa O.M.
      • Komolafe I.O.
      HIV/AIDS and the long-distance truck drivers in south-west Nigeria: a cross-sectional survey on the knowledge, attitude, risk behaviour and beliefs of truckers.
      • Bwayo J.J.
      • Mutere A.N.
      • Omari M.A.
      • Kreiss J.K.
      • Jaoko W.
      • Sekkade-Kigondu C.
      • et al.
      Long distance truck drivers. 2: knowledge and attitudes concerning sexually transmitted diseases and sexual behaviour.
      than in China (53–64%).
      • Zhang C.
      • Jia Y.
      [KAP about AIDS prevention of long distance truckers in Datong City, a survey of 1000 cases].
      • Deng L.
      • Feng L.
      • Zhang W.
      • Wang X.
      • Li Y.
      [Analysis on HIV monitoring among LDTDs in Guandu District, Kunming City].
      • Xu X.
      • Liu S.
      • Zhang J.
      [Analysis of AIDS sentinel surveillance in Huhhot in 2009].
      • Yao J.
      • Tian X.
      • Wang Y.
      • Zhang J.
      • Huang H.
      • Fan B.
      • et al.
      [Voluntary counseling and testing for HIV/AIDS at major parking lot for long-distance trucks in Shanghai].
      In addition, LDTDs also demonstrate a much lower risk of HIV and syphilis infections than other at-risk populations in China. For example, the current HIV and syphilis prevalences among Chinese men who have sex with men (MSM) are 5.3% and 13.5%,
      • Chow E.P.
      • Wilson D.P.
      • Zhang L.
      HIV and syphilis co-infection increasing among men who have sex with men in China: a systematic review and meta-analysis.
      • Chow E.P.
      • Wilson D.P.
      • Zhang J.
      • Jing J.
      • Zhang L.
      Human immunodeficiency virus prevalence is increasing among men who have sex with men in China: findings from a review and meta-analysis.
      representing a 27.9 and 15.7 times higher odds of infection risk than LDTDs, respectively. The prevalences of HIV and syphilis among FSWs are 0.6% and 6.9%, respectively,
      • Poon A.N.
      • Li Z.
      • Wang N.
      • Hong Y.
      Review of HIV and other sexually transmitted infections among female sex workers in China.
      and the risks of infection are 3.16 and 8.02 times higher than in LDTDs. Both MSM and FSW are populations defined according to their high risk sexual behaviors, whereas the term LDTD refers to an occupation that may potentially include individuals with diversified sexual behaviors. However, surveillance resources and efforts have been invested at a disproportionately high level to LDTDs. The latest statistics indicate that 46 national HIV sentinel sites had been designated to monitor LDTDs countrywide but only 25 for MSM in 2009.
      • Wang N.
      • Wang L.
      • Wu Z.
      • Guo W.
      • Sun X.
      • Poundstone K.
      • et al.
      Estimating the number of people living with HIV/AIDS in China: 2003–09.
      As LDTDs mostly acquire HIV from FSWs, extra surveillance resources should be prioritized and directed to strengthen the surveillance of HIV transmission among FSWs while maintaining regular monitoring and effective interventions among LDTDs.
      Chinese LDTDs have traditionally been regarded as a proxy group for male clients of FSWs. A recent large survey among 1840 male clients conducted in five Chinese cities reported the prevalence of HIV and syphilis infections to be 0.11% and 1.6%, respectively.
      • Wang L.
      • Gao L.
      • Guo W.
      • Wang L.
      • Li D.M.
      • Yan R.X.
      • et al.
      [Characteristics of AIDS related behaviors and HIV prevalence among commercial sex worker clients in selected cities in China, 2009].
      Consistent with this, other past studies have also reported similar HIV and syphilis disease burdens among male clients.
      • Li G.
      • Xia D.
      [Study on behavioral changes among clients of commercial sex workers in Beijing from 2005 to 2008].
      • Li R.
      • Tong W.
      • Zhao Z.
      • Xiong B.
      • Yang W.
      [AIDS surveillance results and epidemic trend from 1992 to 2004 in Dalian City].
      • Yang Y.
      • Li Q.
      • Yu X.
      • Wang Y.
      • Ruan G.
      [Investigation on AIDS/STD knowledge infection and high risk behavior among client].
      • Lu L.
      • Jia M.
      • Zhang X.
      • Luo H.
      • Ma Y.
      • Fu L.
      • et al.
      [Analysis for epidemic trend of acquired immunodeficiency syndrome in Yunnan Province of China].
      However, despite these similarities, Chinese LDTDs were found mostly to engage with roadside FSWs, who represent a subgroup of ‘low-tier’ FSWs with greater risk behaviors than the average FSW population.
      • Li Q.
      • Xu J.
      • Wang W.
      • Wang G.
      • Chang D.
      • Wang N.
      [Survey of high risk behaviors and HIV/STD infection among FSWs from different venues of Kaiyuan City].
      • Li R.
      • Liu Z.
      • Xu C.
      [Analysis of HIV surveillance among female sex workers in Luxi City, Yunnan Province, 2005–2007].
      • Nong L.
      • He B.
      • Zhou Y.
      • Liang S.
      • Liang F.
      • Bi S.
      • et al.
      [Survey on prevalence of HIV and syphilis among female sex workers].
      Previous studies have indicated a substantially lower level of condom usage and higher HIV/STI prevalence among roadside FSWs than in those of high-class entertainment establishments.
      • Bai Y.
      [Survey of knowledge behaviors and HIV infection among commercial sex workers from high, middle and low level places].
      • Zheng Z.J.
      • Gu H.
      • Zhang J.Y.
      • Wei B.H.
      • Wang S.Q.
      [A survey of awareness of AIDS and sexual behavior in roadside sex workers].
      • Jin Y.
      • Yin G.Q.
      • Bao W.S.
      • Liu C.B.
      • He L.F.
      • Mao B.B.
      • et al.
      [Effect of health education and behavioral intervention of AIDS/STD among female attendants of roadside inn].
      Additionally, Chinese LDTDs have low levels of knowledge and awareness of HIV/AIDS and are less likely to use condoms with their regular and commercial sexual partners.
      • Zhang C.
      • Jia Y.
      [KAP about AIDS prevention of long distance truckers in Datong City, a survey of 1000 cases].
      • Chen S.
      • Mo X.
      • Mo J.
      • Bin F.
      • Zhu J.
      [Investigation on AIDS related knowledge, attitude and behavior among long distance truck drivers in Nanning City in 2007].
      • Cai Y.
      • Chen M.
      [Survey of infectious status of HIV and syphilis in male truck divers in 2005–2006].
      • Chen M.
      • Xu F.
      [Survey on HIV/AIDS knowledge among Chinese long-distance truckers].
      • Zhang C.
      • Ruan S.
      • Shi Z.
      • Yang H.
      • Zhu Y.
      • Jia Z.
      • et al.
      [Survey of HIV/AIDS related knowledge and behavior among high risk population Jinan city].
      Further, the fact that only 19–30% of LDTDs reported having sex with FSWs in the last 12 months,
      • Deng L.
      • Feng L.
      • Zhang W.
      • Wang X.
      • Li Y.
      [Analysis on HIV monitoring among LDTDs in Guandu District, Kunming City].
      • Guo W.
      • Zang X.
      • Zhang X.
      • Wei Y.
      • Sun X.
      • Yuan X.
      [HIV sentinel surveillance report on male long distance truck drivers in Lanzhou City, Gansu Province].
      • Zhang C.L.
      • Jia Y.S.
      [KAP about AIDS prevention of long distance truckers in Datong City, a survey of 1000 cases].
      suggests that a large proportion of LDTDs is not sexually exposed to HIV/STIs. In addition, with the large expansion of the inter-provincial road network, the previous main traffic routes for long-distance transportation are rapidly being replaced by national motorways that enable high traffic flow and restricted access for pedestrians.
      • Wang X.L.
      [Impact analysis of freeway construction on economic development in China].
      This may have resulted in a reduction in the likelihood of truck drivers patronizing roadside FSWs. The limited proportion of patronizing LDTDs but greater risk behaviors with low-tier FSWs provides a probable explanation for the comparable HIV/STI prevalence levels between LDTDs and male clients. However, the substantial differences in their risk behaviors indicate considerable limitations in seeing LDTDs as a proxy group for male clients from the perspective of surveillance.
      Several limitations should be noted in our study. Out of 31 provinces in China, our review only covers the prevalence of the diseases in 14 provinces. Two provinces with a high HIV prevalence (Sichuan and Guangdong), which have more than 50 000 people were living with HIV/AIDS, have no published data. This may have led to the significant publication biases detected in the meta-analyses on HIV and syphilis prevalence. Additionally, due to the limited number of available studies, we were unable to stratify and investigate the geographical and temporal trends in the epidemics of the burden of diseases among Chinese LDTDs.
      In conclusion, the risks of HIV and syphilis infections are significantly higher among Chinese LDTDs than the general Chinese adult population, but much lower than LDTDs in other developing country settings and at-risk groups in China. LDTDs in China may not be a good proxy for male clients in general as only a small proportion of LDTDs bought sex from FSWs. This indicates that the current surveillance resources have been disproportionately allocated to LDTDs. More resources should be directed to other at-risk groups in China while sustaining the current level of surveillance efforts in LDTDs.
      Funding source: This study was supported by the Australian Government Department of Health and Ageing, the University of New South Wales, the Endeavour Awards (Award ID: 2744_2012), the World Bank Global HIV/AIDS Program, grant number 2008ZX10001–003 from the Ministry of Science and technology in China, and grant number FT0991990 from the Australian Research Council.
      Ethical approval: No ethical approval was needed for this study.
      Conflict of interest: No conflict of interest to declare.

      Appendix A. Supplementary data

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