China is a low HIV-prevalence country (∼0.05%) with pockets of high transmission. The country's first AIDS case was identified in 1985 and by 2005, official estimates placed the number of people living with HIV in China at 650 000 (range: 540 000–760 000) [1,2]. As China's HIV epidemic has grown, the surveillance system established to monitor it has evolved alongside, building on case reporting to include annual sentinel surveillance and behavioural surveillance surveys. Although China's HIV surveillance system now covers all of China's 31 provinces, autonomous regions, and municipalities, many challenges remain due to the large population and geography. We present a description and historical overview of the development of China's HIV/AIDS surveillance system.
Overview of China's HIV epidemic
China's HIV epidemic has experienced three main phases: (1) sporadic cases (1985–1988); (2) localized spread (1989–1994); and (3) localized with local generalized epidemic (1995-present) . During the initial phase just 22 cases were identified in seven provinces and all were non-indigenous . Infections were identified in 18 tourists and overseas Chinese and four people infected by imported blood products .
In the second period the first indigenous cases were identified. These were among 146 injecting drug users (IDU) in Ruili, a county in Yunnan Province which lies along the Myanmar border. The infection spread inland to other areas in the Dehong prefecture  and by 1994 HIV had been identified in 21 provinces  and was rising among IDU, female sex workers (FSW), sexually transmitted disease (STD) patients and Chinese workers returning from abroad.
The third phase began in 1995. In these past twelve years, the disease has spread from IDU in south-western Yunnan to neighbouring Guangxi and Sichuan and all the way to north-western Xinjiang. A feature of this period was the large number of cases identified among paid blood donors in the mid-1990s . By the end of 1998, HIV had been reported in all 31 provinces.
The history of HIV/AIDS surveillance in China
Concurrent with the epidemic, HIV surveillance has followed three stages. The first stage (1984–1994) largely involved passive surveillance; i.e. case reporting by hospitals and centers for disease control (CDC) to provincial and national authorities. In 1986, the Ministry of Health added HIV to its list of notifiable diseases and later, in 1989, the Infectious Disease Prevention and Care Law was issued making the reporting of HIV and AIDS cases a legal requirement. Cases were reported simultaneously through a special HIV/AIDS reporting system and a national notifiable infectious disease epidemic reporting system. By the end of 1994, 1774 HIV/AIDS cases had been identified, with 65 AIDS patients, in 21 provinces .
During the first phase, two groups were also specifically targeted for HIV antibody testing: (1) foreigners who would be living in China for more than 1 year; and (2) FSW, particularly those whose clients included foreigners. Testing was mainly at the provincial level by inspection and quarantine agencies responsible for HIV testing among people entering and leaving China and cases that were identified were reportable to provincial authorities within 12 h of diagnosis .
In provinces with early reports of HIV, provincial sentinel surveillance sites were established to conduct surveys among key high risk groups, including drug users, STD clinic attendees, and FSW and their clients. However, these sentinel surveillance sites did not follow standardized protocols. Based on surveillance findings, further epidemiologic investigations were conducted, including cohort studies among drug users in Yunnan province [11–13].
The second stage of HIV surveillance in China saw the initiation of active surveillance. A national HIV/AIDS sentinel surveillance system was established in 1995 to augment case reporting data and more completely reflect HIV patterns and trends across China. Serial cross-sectional surveys were conducted among the most at risk populations, using a single, standardized protocol, and laboratory testing methods. Annual surveys were conducted at fixed sites, fixed times, and with target sample sizes of 400 people, although a minimum of 250 was acceptable. Participants were tested anonymously and completed a short questionnaire about their engagement in high risk behaviours; e.g. FSW were asked about condom use; drug users were asked about injecting and needle sharing .
In 1995, 42 national sentinel surveillance sites were established in 23 provinces, covering STD clinic attendees, FSW, drug users, and long-distance truck drivers. Additional sites continued to be added based on the epidemic situation and available resources. Target populations increased to include pregnant women from 1997 and paid blood donors in 1998 and 1999 (Table 1). By 1998, there were 98 national sentinel surveillance sites. Provincial sentinel surveillance sites were also established in areas where the coverage and number of national sites were insufficient.
Sentinel surveillance results have documented the rapid spread of HIV among drug users. In Urumqi, Xinjiang, for example, HIV prevalence among drug users rose from 0% in 1995 to 28.8% in 1998. Similarly, in Guangxi and Guangdong provinces, HIV prevalence rose from around 1% in 1997 to 12.8% to 10.4%, respectively, in 1998. Alongside increases in HIV prevalence, rates of injection drug use and needle sharing have risen. In other populations during this period, HIV prevalence remained relatively low, but with indications of potential risk .
Special surveys were also conducted during this phase among populations of special interest and concern. For example, former commercial plasma donors were investigated [16,17], the results of which directly led to government intervention to shut down illegal plasma collection stations and the issuance of a Blood Donation Law in 1998.
The third and current stage of China's HIV surveillance system has seen the development of comprehensive surveillance. In 1998, the World Health Organisation (WHO) and UNAIDS put forward the concept of Second Generation Surveillance for HIV (SGS) . SGS has built on the existing HIV serological surveillance and AIDS case reporting systems (first generation surveillance) and added behavioural surveillance surveys (BSS). In 2000, with support from the World Bank Health IX Loan Project and the China-UK HIV/AIDS Prevention and Control Cooperative Project, behavioural surveillance pilot sites targeting high risk populations, vulnerable populations, and the general population were established in Fujian, Xinjiang, Guangxi and Shanxi (World Bank), as well as Yunnan and Sichuan (China-UK). Based on these experiences, Chinese experts adapted international best practice  to China's situation under an approach termed comprehensive surveillance. This approach established a foundation for comprehensive data collection, data analysis and data sharing based upon the integration of HIV and STD surveillance, and the integration of biological and behavioural surveillance. In this way, a comprehensive HIV/STD surveillance system was created to analyze the current HIV situation and trends, and to provide evidence to guide the formulation of strategic HIV/AIDS prevention and care policies and programmes. To guide the expansion of comprehensive HIV surveillance approaches, the Ministry of Health and the Chinese National Center for HIV/AIDS Prevention and Control (NCAIDS) issued two key documents in 2002: Standards for HIV Surveillance and HIV/AIDS and STD Comprehensive Surveillance Guidelines (Draft).
During this phase, the sentinel surveillance system has been continuously expanding and developing. By the end of 2006, there were 393 national HIV sentinel surveillance sites in all 31 provinces, and a total of eight population groups covered by sentinel surveillance surveys (Table 1). In addition, 370 provincial sentinel surveillance sites have been established, with the majority following the national HIV surveillance protocol, adapted to provincial needs. Different projects have provided support for the establishment of sentinel sites targeting key populations not included in routine national surveillance surveys, such as migrant workers, entertainment establishment workers, incarcerated populations, blood donors, sailors, and hospital staff. Since 2006, data from provincial sentinel surveillance sites, including sites supported by various projects, are reported to NCAIDS for compilation and analysis. These data are used to calculate national HIV estimates, and allow for active monitoring of the epidemic in different places and populations.
Behavioural surveillance is a key feature of comprehensive HIV surveillance. Behavioural surveillance utilizes epidemiological investigation methodologies to periodically conduct cross-sectional surveys among specific populations and collect HIV-related behavioural data. By observing behavioural changes over time, behavioural surveillance acts as an early warning system for potential epidemics, facilitates interpretation of changes in an epidemic, and can be used to inform and evaluate HIV intervention strategies. Starting in 2004, 42 pilot behavioural surveillance sites were established in 19 provinces covering six key populations; drug users, female sex workers, men who have sex with men, STD clinic attendees, long-distance truck drivers and students (16-24 years old). By the end of 2006, there were 159 national behavioural surveillance sites in 27 provinces.
China's current HIV surveillance system
Currently, China is working to more thoroughly integrate HIV surveillance activities into a single, comprehensive system. These activities include HIV/AIDS case reporting, HIV sentinel surveillance, HIV behavioural surveillance, and special epidemiological surveys.
In order to increase the quality and timeliness of HIV case reporting, the Ministry of Health established a web-based HIV/AIDS case reporting system based on the China infectious disease prevention information system. The system was launched in March 2005, and all agencies performing HIV tests report cases through the web site (Fig. 1). This system has increased the timeliness of HIV/AIDS case reporting. In addition, data are also collected on individual risk factors, estimated time of exposure, and CD4 test results.
HIV/AIDS web-based case reporting, HIV sentinel surveillance and behavioural surveillance are being integrated into a single protocol and implementation plan, with a single training programme for each level of staff working on HIV surveillance. First, NCAIDS staff will provide training to provincial level CDC staff working in HIV/AIDS and provincial staff will, in turn, provide training to staff at township and county levels. National and provincial level experts will monitor the progress of HIV surveillance work, providing technical guidance and assessments to ensure that surveillance work is proceeding according to the requirements outlined in the protocol.
By the end of 2006, a cumulative total of 191 565 HIV/AIDS cases had been reported, including 47 713 AIDS patients and 13 632 deaths. Surveillance data indicate that HIV among high risk populations is escalating. For example, HIV prevalence among FSW rose from an average of 0.02% in 1996 to an average of 0.51% in 2005. Similarly, among drug users, HIV prevalence has risen from an average of 1.95% in 1996 to an average of 7.54% in 2005 (Fig. 2). Moreover, risk behaviours have increased, with the median proportion of IDU among drug users increasing from 32.6% in 1995 to 64.1% in 2005, and the proportion of IDU sharing needles increasing from 39.6% to 46.8%. In contrast, surveillance data among FSW show encouraging increases in condom use (Table 2), with the median proportion of always using condoms in commercial sexual contacts in the last month increasing from 10.0% in 1995 to 38.7% in 2005, and that of never using any condom decreasing from 70.6% in 1995 to 10.0% in 2005.
There are, however, wide geographic variations in HIV prevalence (Fig. 2). For example, in parts of Xinjiang, Yunnan and Sichuan, HIV prevalence among drug users is over 50%; in Jiangsu, Zhejiang, Inner Mongolia and Liaoning, HIV prevalence among drug users remains under 5%. In some parts of Yunnan, Chongqing, Hunan, Guangdong, Guangxi and Sichuan, HIV prevalence among FSW is greater than 1%. In addition, in some parts of Yunnan, Henan and Xinjiang, HIV prevalence is over 1% among pregnant women, people screened for HIV before marriage, and patients screened before receiving clinical care, suggesting that HIV is moving from high risk groups to the general population.
Beginning in late 2004, special epidemiologic surveys were conducted in Henan province to screen all former commercial plasma donors . The results were similar with former surveys [16,17]. Also in that year, an epidemiological investigation was conducted in the FPD communities in Wenxi County, Shanxi Province, and revealed no evidence of the further spread of the HIV/AIDS epidemic from these communities . Following this, the Ministry of Health directed a nationwide HIV screening campaign among former commercial plasma donors . In 2005, the Ministry of Health, Ministry of Justice, Ministry of Public Security and other agencies jointly implemented mass HIV screening in compulsory drug detoxification centres, detention centres, prisons and other closed settings , which later became routine HIV testing for all new inmates. The results from mass screening were similar to those of the sentinel surveillance. Screening has facilitated early detection of HIV cases and early treatment and intervention for people testing HIV positive . Surveys have also been conducted among other vulnerable populations, including migrant labourers [24–26] and MSM [27,28], and to estimate HIV incidence . Data generated from screening and epidemiological surveys have provided useful evidence for policy makers at both the local and national level to guide decisions about HIV prevention and care strategies and resource allocation. These data have also been included in annual joint assessment reports [1,30].
These special epidemiological surveys also include molecular epidemiology research, which was accomplished in 2005, and identified the transmission routes of different HIV-1 subtypes in China (Fig. 3) . The detection of the transmission routes of the subtypes also further elucidated the special characteristics of the HIV/AIDS epidemic in different regions in China. The map in Figure 3 also illustrates a path of spread of the epidemic compatible with the development of epidemic's historical stages.
In addition to these important epidemic findings, the aforementioned Standards for HIV Surveillance and HIV/AIDS and STD Comprehensive Surveillance Guidelines have provided technical guidance for the quality assurance and quality control (QA/QC) for the surveillance of HIV/AIDS. Accordingly, the national and provincial CDCs conduct regular evaluation and examination of the operations and outputs of the HIV/AIDS surveillance work performed by subordinate CDCs yearly, for both case reporting and sentinel surveillance, using a series of technical and management indicators assessing the accuracy, timeliness and work completion rates of reporting, distribution of infrastructure, quality of human resources, etc.
Although the surveillance network in China has come a long way in the past two decades, there are several limitations to the system. Gaps in sentinel surveillance data include an uneven distribution of sentinel surveillance sites, wide variations in the quality of the data collected, and insufficient coverage of the most at-risk populations. Emerging risk groups are also poorly covered. For example, China has an estimated 120 million internal migrants who generally have poor HIV knowledge and may be vulnerable to infection , but among whom there is no targeted surveillance. Behavioural surveillance data are still weak and need to be expanded and improved. Data on the socioeconomic effects of HIV in China are also weak, and the data that are available are not analyzed in a timely fashion.
Further, while the work to test incidence has began in China in supplement to the surveillance of prevalence, there remains tremendous space to improve the laboratory method, i.e. HIV-1 BED-IEA introduced to China by the US CDC, currently under application in China, while searching for new alternatives.
In recent years, a large amount of valuable data has been collected from sources other than surveillance, including laboratory testing, prevention, treatment, care and support programs. However, most places have limited capacity to analyze and use these data and as a result, a large amount remains underutilized. In addition, there has been little integration of these data, data sharing or experience sharing across project sites, places and agencies. In 2006, NCAIDS began to integrate HIV case reporting, sentinel surveillance, behavioural surveillance, special surveys, voluntary counselling and testing and treatment and care data to better understand the epidemic.
The leadership and management of strategic information needs to be strengthened further to make better use of organizational capacity for data collection, analysis, integration and timely dissemination of related information, to provide data to support HIV prevention and care strategies and to promote multisectoral involvement in the HIV response. Within these organizations, staff capacity needs to be enhanced and operational research is needed to identify successful testing strategies that include voluntary counselling and testing as a central feature.
In summary, the HIV surveillance network in China has expanded considerably since the first HIV case was identified in the country, particularly in last decade, and now covers most risk groups in China. However, the system needs to remain dynamic so that it can adapt to the changing profile of the epidemic, and needs to be strengthened in certain areas.
The authors report no conflicts of interest.
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