Changes in Prevalence of HIV or Syphilis among Male Sex Workers and Non-Commercial Men Who Have Sex with Men in Shenzhen, China: Results of a Second Survey

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Abstract

Background

A previous time-location sampling survey (TLS) was performed in 2008 to evaluate the HIV or syphilis infection rate among male sex workers (MSWs) and non-commercial men who have sex with men (ncMSM) in Shenzhen, China. This is a second TLS performed in 2014. This article describes the findings and changes in the prevalence of HIV and syphilis.

Methods

TLS was used to collect information as a second cross-sectional survey to an earlier TLS assessment. Data on behavior (e.g., sexual history and sexual behavior) were analyzed. Blood specimens were drawn for HIV and syphilis testing. To determine the changes in the prevalence of HIV and syphilis, we analyzed these results and compared them to the results of our first survey.

Results

A total of 965 participants were recruited, including 489 MSWs and 476 ncMSM. Overall, the prevalence of HIV was 9.7%: 2.9% for MSWs and 16.8% for ncMSM (P<0.001). 10.9% of the 965 participants tested positive for syphilis: 4.5% among MSWs and 17.4% among ncMSM (P<0.001). The HIV prevalence in MSWs decreased from 4.5% in 2008 to 2.9% in 2014 (P = 0.143) but increased in ncMSM (7.0% in 2008 vs 16.8% in 2014, P<0.001). Decreased syphilis rates were observed in both MSWs (12.9% in 2008 vs 4.5% in 2014, P<0.001) and ncMSM (20.2% in 2008 vs 17.4% in 2014, P = 0.221).

Conclusions

Overall, there was a decline in the prevalence of HIV and syphilis in MSWs but not in ncMSM. The study indicated the need for continued efforts to improve public health, particularly to counter the rising rate of HIV in ncMSM.

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Most cited references 17

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HIV prevalence in China: integration of surveillance data and a systematic review.

Lei Zhang, Eric Chow, Jun Jing … (2013)

Asian HIV epidemics are concentrated among particular behavioural groups, but large variations exist in epidemic types, timing, and geographical spread between countries and within countries, especially in China. We aimed to understand the complexity of HIV epidemics in China by systematically analysing prevalence trends by data source, region, population group, and time period. We collected HIV prevalence data from official national sentinel surveillance sites at the provincial level from Jan 1, 1995, to Dec 31, 2010. We also searched PubMed, VIP Chinese Journal Database (VIP), China National Knowledge Infrastructure, and Wanfang Data from Jan 1, 1990, to Dec 31, 2012, for independent studies of HIV prevalence. We integrated both sets of data, and used an intraclass correlation coefficient test to assess the similarity of geographical pattern of HIV disease burden across 31 Chinese provinces in 2010. We investigated prevalence trends (and 95% CIs) to infer corresponding incidence by region, population group, and year. Of 6850 articles identified by the search strategy, 821 studies (384,583 drug users, 52,356 injecting drug users, 186,288 female sex workers, and 87,834 men who have sex with men) met the inclusion criteria. Official surveillance data and findings from independent studies showed a very similar geographical distribution and magnitude of HIV epidemics across China. We noted that HIV epidemics among injecting drug users are decreasing in all regions outside southwest China and have stabilised at a high level in northwest China. Compared with injecting drug users, HIV prevalence in female sex workers is much lower and has stabilised at low levels in all regions except in the southwest. In 2010, national HIV prevalence was 9·08% (95% CI 8·04-10·52) in injecting drug users and 0·36% (0·12-0·71) in female sex workers, whereas incidence in both populations stabilised at rates of 0·57 (0·43-0·72) and 0·02 (0·01-0·04) per 100 person-years, respectively. By comparison, HIV prevalence in men who have sex with men increased from 1·77% (1·26-2·57) in 2000, to 5·98% (4·43-8·18) in 2010, with a national incidence of 0·98 (0·70-1·25) per 100 person-years in 2010. We recorded strong associations between HIV prevalence among at-risk populations in each province, supporting the existence of overlap in risk behaviours and mixing among these populations. HIV epidemics in China remain concentrated in injecting drug users, female sex workers, and men who have sex with men. HIV prevalence is especially high in southwest China. Sex between men has clearly become the main route of HIV transmission. Copyright © 2013 Elsevier Ltd. All rights reserved.

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HIV and Syphilis Co-Infection Increasing among Men Who Have Sex with Men in China: A Systematic Review and Meta-Analysis

Eric Chow, David Wilson, Lei Zhang (2011)

Background This study aims to estimate the magnitude and changing trends of HIV, syphilis and HIV-syphilis co-infections among men who have sex with men (MSM) in China during 2003–2008 through a systematic review of published literature. Methodology/Principal Findings Chinese and English literatures were searched for studies reporting HIV and syphilis prevalence among MSM from 2003 to 2008. The prevalence estimates were summarized and analysed by meta-analyses. Meta-regression was used to identify the potential factors that are associated with high heterogeneities in meta-analysis. Seventy-one eligible articles were selected in this review (17 in English and 54 in Chinese). Nationally, HIV prevalence among MSM increased from 1.3% during 2003–2004 to 2.4% during 2005–2006 and to 4.7% during 2007–2008. Syphilis prevalence increased from 6.8% during 2003–2004 to 10.4% during 2005–2006 and to 13.5% during 2007–2008. HIV-syphilis co-infection increased from 1.4% during 2005–2006 to 2.7% during 2007–2008. Study locations and study period are the two major contributors of heterogeneities of both HIV and syphilis prevalence among Chinese MSM. Conclusions/Significance There have been significant increases in HIV and syphilis prevalence among MSM in China. Scale-up of HIV and syphilis screening and implementation of effective public health intervention programs should target MSM to prevent further spread of HIV and syphilis infection.

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China AIDS policy implementation: reversing the HIV/AIDS epidemic by 2015

Zunyou Wu, Allen Wang, Roger Detels … (2010)

In the past decade, tremendous efforts have been made and impressive achievements have been obtained in accelerating universal access for HIV prevention, treatment and care and support worldwide. For example, between 2003 and 2008, the number of people receiving antiretroviral therapy (ART) increased 10-fold—from 400 000 to 4 000 000—corresponding to 42% of 8.8 million people who needed treatment for HIV. 1 , 2 Overall, the availability and coverage of HIV prevention, treatment and care continued to expand in low- and middle-income countries. In low- and middle-income countries in 2008, ART for adults and children averaged 42% (40–47%) and the percentage of pregnant women living with HIV receiving ART drugs to prevent mother-to-child transmission averaged 45% (37–57%). 2 Yet, these achievements have not stopped the epidemic, with approximately 2.3 million persons being infected annually, 3 outpacing the annual increase in the number of people receiving treatment. 2 Progress on achieving HIV goals has been uneven across and within countries. 1 Many gaps and challenges still remain. China is among the countries that have committed to achieve the Millennium Development Goals by 2015. Remarkable progress has been made in promoting HIV prevention, treatment care and support in China in recent years. 4 In particular, China is one of only a few low- and middle-income countries in which domestic funds account for the major proportion of their HIV/AIDS program funding. 5 This supplement of the International Journal of Epidemiology, entitled ‘China's AIDS Policy Implementation’, has assembled 11 papers describing various of aspects of China's response to the HIV/AIDS epidemic. Policies for stigmatized infectious diseases, such as AIDS, are politically sensitive. Early in the HIV epidemic, China initiated many projects to respond to the HIV/AIDS epidemic, but an effective national HIV/AIDS policy was not developed. The outbreak of severe acute respiratory syndromes (SARS) in Beijing in 2003 6 triggered rapid mobilization of public health policies for a broad range of health challenges. China initially responded slowly to SARS, and the consequences of slow action motivated subsequent rapid implementation of HIV national policies. China recognized the potential consequences of a generalized epidemic on the economic well-being, quality of life and mortality that HIV may cause. China's public health sector committed to anticipate issues and to develop and implement effective HIV policies before health problems became out of control. China soon launched its first 5-year action plan, which had a significant impact: ‘Four Frees and One Care’ policy (See Sun et al. 7 ). This policy provided access to free HIV testing, ART and prevention of HIV mother-to-child transmission. Globally, successful control of the epidemic of HIV/AIDS requires strong international collaborations. International projects on HIV have greatly contributed in facilitating China's national AIDS response. 8 Over 20 years, China has participated in 267 collaborative international projects to stop the HIV/AIDS epidemic, receiving ∼USD$526 million from over 40 international organizations. Initially, these were stand-alone projects providing technical support for surveillance, training, advocacy for public awareness, and to support effective, but politically sensitive, pilot projects. These projects are now fully integrated into the overall national AIDS responses. Beyond providing critical financial support, these international projects created the opportunity to introduce the best practices in use globally into China, accelerating the formulation of AIDS policies, strengthening providers’ capacity, improving the development of grass-roots social organizations and establishing a platform for communication and experience sharing with the international community. 8 , 9 The international contributions decreased over time, as the importance of sustainable government support became apparent, so that today international financial support reflects only one-third of the total monetary resources for the China's AIDS program. With this international support, civil societies (non-government organizations) have been initiated and grown strong and active over the past 20 years. Organizations for civil societies were non-existent 20 years ago, but now organizations have changed from being mere spectators to being active implementers of social change. 9 These civil society organizations have played a significant role in providing specialized prevention and treatment services to marginalized groups, such as men who have sex with men and people infected and affected by HIV/AIDS. 9 However, the capacity of civil society to play a more important role within the national plan, to establish a vibrant communication network, to learn from each other and interact with the government sector needs to be improved in order to function as effective implementers of HIV policies within communities. Prevention of new HIV infections has always been the top priority in the overall response to HIV/AIDS. Fortunately, China's AIDS epidemic, in general, still remains limited to at-risk groups, associated with injecting drug use, sex work and male-to-male sexual contact. The HIV epidemic was initially driven by injecting drug use. In response, China has developed and rapidly expanded its national methadone maintenance treatment program (see Yin et al. 10 ). Recognition of this achievement has been received from both international and domestic communities (United Nations Program on HIV/AIDS, 2008). However, many challenges remain. As Yin and colleagues outline in this issue, China's methadone treatment program can be improved by: (i) expanding the coverage of methadone maintenance treatment and the number of its beneficiaries; (ii) increasing accessibility of services; (iii) improving the quality of services offered, increasing the range of services offered at clinics and introducing referral systems between related services; (iv) implementing on-going staff training to improve the quality of their services, increase their understanding of drug addiction and enhance their professionalism; and (v) mobilizing multi-sector cooperation, especially at local levels, to ensure that clients can enjoy uninterrupted treatment. 10 Globally, sexual contact is the major mode of HIV transmission and has now become a major mode of HIV spread in China. In 2009, China estimated that among 48 000 new HIV infections, 75% were caused by sexual contact. Rou et al. 11 describe in detail how China has responded to the threat of increasing sexual transmission of HIV. These efforts may partially explain why China's HIV prevalence has remained low among sex workers and the general public. However, China's national policy implementers have identified new strategic directions to continue to ensure that HIV remains low among sex workers and that sexual transmission of HIV does not increase further. China expanded its antiretroviral (ARV) treatment program very rapidly. The national free ART program started in 2002. 12 By the end of 2009, over 80 000 patients had received ARV treatment. 13 Dou et al. 14 describe baseline characteristics of patients enrolled in ART program between 2002 and 2009. Marginalized groups were receiving less ART, such as injecting drug users, who account for 32.2% of people living with HIV/AIDS 15 but only 15.5% of patients in the ART program. 14 Without equally treating the marginalized groups, the millennium development goal will be hard to achieve. China's Comprehensive AIDS Response Program (China CARES), 16 described by Han et al. in this issue, is the single largest AIDS project, covering 83.3 million people in 127 program sites in 28 provinces. This demonstrates that scaling-up HIV prevention, treatment and care activities in rural China is possible and effective. The number of people being tested for HIV in project sites increased by 67%, and the number of patients enrolled into the free ART program increased by 23 000 between 2005 and 2007. Ninety-three per cent of HIV-infected pregnant women and 85.5% of their newborns received ART prophylaxis. China CARES has provided a good model for promoting universal access to HIV prevention, treatment care and support. Laboratories are an essential infrastructure for HIV testing and monitoring CD4 level and viral load. An HIV laboratory network system has been established and improved in China, which is comprised of 8273 local screening laboratories, 254 confirmatory laboratories, 35 provincial confirmatory central laboratories and 1 National AIDS Reference Laboratory. 17 Between 2002 and 2009, more than 220 million specimens were tested for HIV antibody at screening laboratories in the network. This laboratory network can perform laboratory tests from simple antibody tests to sophisticated CD4 cell enumeration, viral load, early infant diagnosis, drug resistance genotyping, HIV-1 subtyping and incidence assays. Thus, the system provides a basis for monitoring the epidemic and improving treatment of patients. China has established an HIV laboratory quality assurance system. However, the coverage and quality assurance programs still need to be further strengthened, particularly at the local level. Monitoring and evaluation (M&E) activities include activities that describe the HIV epidemic and associated health challenges (hepatitis C virus, human papilloma virus and sexually transmitted infections); documenting implementation practices; and evaluating the impact of national programs. M&E activities are key to providing feedback, which allows continuous quality improvement. China has made remarkable progress in improving the quality and reach of its data sources. Greater transparency has been a stated goal of China's current M&E activities (see Wang et al. 18 ). The participation of the international community in developing better estimates of HIV/AIDS occurrence has had a substantial impact on improving data quality. China is among a few countries that have made tremendous efforts in achieving accurate estimates over the past 6 years on the scope, sites and extensiveness of its epidemic. As described by Wang et al., 18 China's public health leaders from each province reviewed its national HIV/AIDS estimates collectively in 2003, 2005, 2007 and 2009. These reviews served both to build capacity at the provincial level and to generate data that more accurately reflect China's heterogeneous epidemic. These improvements in data quality and data availability have improved the precision of HIV/AIDS estimates, providing information that is critical to setting public health goals and evidence-based policies. China's new unified, web-based HIV/AIDS information system is unique globally. 19 It was implemented within a 9-month period in 2004, with consistent quality improvement since that time. Few countries have data systems that combine HIV testing, prevention, treatment and care information on the same platform. China uses a web portal to monitor HIV cases in real-time nationally, including data from all provinces. The information system has improved the efficiency of data collection, reporting, analysis and use, as well as data quality and security. This system facilitates integration of all international or domestic AIDS projects into one national AIDS program. It is also a powerful tool to support policy makers by allowing China to monitor changes over time and to quickly identify new disease outbreaks, as well as implementing the national HIV/AIDS program and program evaluation (see Mao et al. 19 ). The national AIDS program has been facilitated by setting annual goals for core indicators and holding local implementers accountable to monitor AIDS policy implementation. 20 This process continues today, as China is now setting the 2015 program goals. Commitment to controlling HIV/AIDS epidemic at the highest policy levels is an important first step for prevention and care, but even more important is implementation, as well as monitoring of implementation to assure that the commitment has been translated into action. Policies to stop HIV have made substantial progress in the areas of expanding access to methadone maintenance (from 8 to 690 sites in 5 years). To achieve the millennium development goals, China must work even harder and more vigorously.

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Author and article information

Contributors

Ruan Yuhua: Role: Editor

Journal

Journal ID (nlm-ta): PLoS One

Journal ID (iso-abbrev): PLoS ONE

Journal ID (publisher-id): plos

Journal ID (pmc): plosone

Title: PLoS ONE

Publisher: Public Library of Science (San Francisco, CA USA )

ISSN (Electronic): 1932-6203

Publication date (Electronic): 9 December 2016

Publication date Collection: 2016

Volume: 11

Issue: 12

Electronic Location Identifier: e0167619

Affiliations

[1 ]Department of Preventive Medicine, Shantou University Medical College, Shantou, Guangdong, China

[2 ]Shenzhen Center for Disease Control and Prevention, Guangdong, China

National Center for AIDS/STD Control and Prevention, China CDC, CHINA

Author notes

Competing Interests: The authors declare no conflict of interest.

Conceptualization: JZ KL.
Data curation: YH YZ.
Formal analysis: YH YZ.
Funding acquisition: JZ.
Investigation: YH YZ.
Methodology: JZ KL YH.
Project administration: JZ KL.
Resources: JZ.
Supervision: JZ KL.
Visualization: YH JZ YZ.
Writing – original draft: YH YZ.
Writing – review & editing: YH.

* E-mail: keli1122@ 123456126.com (KL); szhaojin@ 123456gmail.com (JZ)

Article

Publisher ID: PONE-D-16-20687

DOI: 10.1371/journal.pone.0167619

PMC ID: 5147921

PubMed ID: 27935980

SO-VID: 405731fa-ce6f-4948-ac7c-90a6e0695010

License:

This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

History

Date received : 23 May 2016

Date accepted : 8 November 2016

Page count

Figures: 0, Tables: 4, Pages: 12

Funding

Funded by: funder-id http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 81573211 and 81270043

Award Recipient : Jin Zhao

Funded by: National Natural Science Foundation of Guangdong Province

Award ID: 2014A030313772

Award Recipient : Jin Zhao

Funded by: Shenzhen Technology and Research Fund

Award ID: JCYJ20140410171018515

Award Recipient : Jin Zhao

This work was supported in part by grants from the National Natural Science Foundation of China (81573211 and 81270043), the National Natural Science Foundation of Guangdong Province (2014A030313772), Shenzhen Technology and Research Fund (JCYJ20140410171018515 and JCYJ20140416104959068) and the Medical Key Laboratory of Shenzhen. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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Changes in Prevalence of HIV or Syphilis among Male Sex Workers and Non-Commercial Men Who Have Sex with Men in Shenzhen, China: Results of a Second Survey

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Abstract

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Most cited references 17

HIV prevalence in China: integration of surveillance data and a systematic review.

HIV and Syphilis Co-Infection Increasing among Men Who Have Sex with Men in China: A Systematic Review and Meta-Analysis

China AIDS policy implementation: reversing the HIV/AIDS epidemic by 2015

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