Chinese Medical Journal 2010;123(23):3495-3500
HIV/AIDS epidemic and the development of comprehensive surveillance system in China with challenges

WANG Lu,  WANG Ning

WANG Lu (National Center for AIDS/STD Control and Prevention, Chinese Centre for Disease Control and Prevention, Beijing 102206, China)

WANG Ning (National Center for AIDS/STD Control and Prevention, Chinese Centre for Disease Control and Prevention, Beijing 102206, China)

Correspondence to:WANG Ning,National Center for AIDS/STD Control and Prevention, Chinese Centre for Disease Control and Prevention, Beijing 102206, China (Tel: 86-10-58900906. Fax:86-10-58900906. E-mail:wangnbj@163. com)
Keywords
comprehensive surveillance system; acquired immune deficiency syndrome
Abstract
AIDS is the most severe infectious disease that has appeared in the second half of the 20th century. Since the United States Center of Disease Control & Prevention (US CDC) reported the first case of HIV carrier in the men who had sex with men (MSM) population in 1981, HIV/AIDS had spread globally. By the end of December 2008, UNAIDS and WHO estimated that there were 3340 million (3110–3580 million) infected with HIV/AIDS worldwide.1 While the HIV/AIDS epidemic in Asia began later than the epidemic in Europe, America and Africa, experts predict that countries in Asia, especially in three countries, China, India and Indonesia, which have a population of more than 100 million, will have the world’s largest number of HIV/AIDS in the near future.
 
The spread of HIV/AIDS has no borders. The first reported AIDS case in China was identified in a 34-year-old American Argentina tourist in 1985 and Yunnan Province identified 146 cases of HIV infection among drug users (DUs) in 1989, which marked the beginning of the HIV epidemic in China.2,3 At that time, the main route of transmission was through injected drug use, as well as from commercial plasma donations. Currently, new epidemic trends have emerged in China and sexual transmission has become the leading route of HIV transmission. While the HIV epidemic in China is still mainly concentrated in high-risk populations, evidence shows that the epidemic is spreading to the general population.4
 
NATIONAL HIV/AIDS EPIDEMIC IN CHINA
 
Slowing down the growth of the HIV/AIDS epidemic
Since 2005, a marked improvement has been made in various AIDS control measures, national surveillance methods and analysis, and civil society participation in HIV/AIDS awareness campaigns and activities. These changes have helped to blunt the growth rate of new HIV/AIDS infections. Based on national case reporting data, by the end of 2009, there were a cumulative number of 326 000 HIV/AIDS cases. Among those, 107 000 cases were AIDS patients, and reported deaths attributed to AIDS were 54 000. The growth rate of newly reported cases decreased from 9.0% in 2006 to 5.8% in 2009 (Figure 1). By the end of 2009, it was estimated that 740 000 people were living with HIV/AIDS (PLWHA) in China, down by 40 000 cases in comparison to 2007 reports. New infections also decreased, from 50 000 in 2007 to 48 000 in 2009. But from 2007 to 2009, the number of reported AIDS patients increased by 20 000. Data from sentinel surveillance showed a stable HIV prevalence among intravenous drug users (IDUs), female sex workers (FSWs), sexually transmitted infection (STI) clinic patients, and pregnant women. Of particular note, HIV prevalence among MSM increased substantially (Figure 2). This suggests that, except for MSM, new infections are stable among other sub-groups.5,6
 
Sexual contact continues to be the major route of transmission and homosexual transmission increases significantly
Among the estimated 740 000 PLWHA in 2009, 59.0% of the infections were attributed to sexual transmission. And among heterosexual transmission, sexual transmission by a spouse accounted for one-third of the cases. Among the estimated 48 000 new infections, 74.7% were attributed to sexual transmission, a sharp increase from 56.9% in 2007. Homosexual transmission increased the most and was one of the most important transmission routes for new cases in 2009. Both homosexual and heterosexual transmissions had increased gradually over time (Figure 3).
 
Sentinel surveillance data from 2008 and 2009 reported >1% prevalence and a rapid increase in reported HIV among MSM. An investigation targeting MSM in 61 cities from 2008 to 2009 found an average HIV prevalence of 5% among MSM in medium and large cities. In major cities of southwest China such as Guiyang, Chongqing, Kunming, and Chengdu, HIV prevalence was >10%, suggesting rapid spread among this sub-group. Thus, MSM has become one of the important drivers for the HIV/AIDS epidemic in China (Figure 4).
 

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Figure 1. Annual reported HIV/AIDS cases in China between 1985 and 2009.
Figure 2. HIV sentinel surveillance data on DUs, FSWs, STD clinic patients, pregnant women and MSM from 1995 to 2009.
Figure 3. Annual transmission constitute of reported HIV/AIDS cases in China between 1985 and 2009.
Figure 4. HIV sentinel surveillance data on MSM from 2002 to 2009.
 
National HIV/AIDS epidemic situation is an overall low prevalence, but concentrated in certain high-risk areas
Since 1998, except Hongkong, Macao, and Taiwan, each of the other 31 provinces, autonomous regions and municipalities has reported cases of HIV/AIDS. As of December 2009, 90.5% (2787/3080) of the counties and districts in China had reported cases. Case reports through the web-based system indicated a large range of diversity in reporting across provinces. The six provinces with the most reported cases, Yunnan, Guangxi, Henan, Sichuan, Xinjiang and Guangdong, accounted for 70%–80% of total reports nationwide. The seven provinces, cities and autonomous regions with the least number of reported cases were Tibet, Qinghai, Ningxia, Inner Mongolia, Tianjin, Gansu, and Hainan. The total number of reported cases from these seven provinces comprised less than 1% of the total case load (Figures 5 and 6). Regions including Dehong prefecture, and Honghe prefecture of Yunnan Province, Yining city and Urumqi Tianshan district of Xinjiang were among the high HIV/AIDS epidemic hotspots. Regions with rapid increases in the number of reported cases since 2007 included Butuo county, Shaojue county, Meigu county and Yuexi county of Liangshan prefecture of Sichuan Province, Luzhai county and Liujiang county of Liuzhou city, Babu district of Hezhou city of Guangxi. Although the epidemics in Zhumadian city and Weishi county of Henan Province were high in the past, they have been stabilized in recent years. According to the 2009 estimates, six provinces were estimated to have more than 50 000 cases each. These six provinces represented 61.8% of the total estimated cases. Each of nine provinces was estimated to have between 10 000 and 50 000 cases. Eight provinces were estimated to have less than 5000 cases each. These eight provinces comprised 2.3% of the total estimated cases (Figure 7).
 

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Figure 5. Geographic distribution of cumulative reported HIV positive cases in China (through the end of 2009).
Figure 6. Geographic distribution of cumulative reported AIDS cases in China (through the end of 2009).
Figure 7. Geographic distribution estimated cases in China in 2009.
 
The highest prevalence of HIV/AIDS was detected among drug users, especially among IDUs, with varying geographic diversity. Sentinel surveillance showed hotspots of HIV/AIDS infections clustered in Yunnan, Xinjiang, Sichuan, Guangxi, Guizhou, and Guangdong provinces,7,8 where the HIV prevalence rates among drug users are over 50%. In comparison, the HIV prevalence among commercial sex workers (CSWs) were lower in most of regions, province-specific HIV prevalence rates over 1% clustered in Yunnan, Xinjiang, Guangxi, Sichuan, and Guizhou provinces. In high epidemic regions, HIV infection among pregnant women is high. HIV prevalence in pregnant women-specific sentinel sites has continually increased from 1997 through 2008, reaching >1% in 2003. The cumulative number of MTCT cases from Henan, Yunnan, Guangxi, Xinjiang and Anhui provinces comprised 78.1% of the total estimated MTCT cases in the country.
 
HIV/AIDS affected more people and transmission modes have diversified
Case-reporting data showed a considerable increase in HIV among people aged 50 and over. People aged 50–64 years comprised 6.1% of reported cases in 2006. This figure increased to 10.6% in 2009. Males accounted for a disproportional number of HIV/AIDS cases in the group over 65 years old, with a male-to-female gender ratio of 4.4:1. Sexual contact was the major transmission route.5
 
The number of reported HIV positive students is gradually increasing. With expansion of the migrating population, imported HIV infection through marriage has been reported in various places across the country. Surveys among immigrant wives in Shandong, Shanxi, Jilin, Anhui, and Jiangsu suggest that a link may exist between imported HIV infections, sexual transmissions within a serodiscordant couple, and MTCT.
 
In summary, China is a low prevalence HIV/AIDS epidemic country. However, high epidemics are currently occurring in concentrated areas, and HIV is being transmitted from most at risk populations (MARPS) to the general population. Promotion of HIV/AIDS prevention programs is urgently needed. Government leadership and active involvement of the entire society are needed to effectively implement strategies for prevention, control and treatment of HIV/AIDS.
 
DEVELOPMENT OF THE INTEGRATED MONITORING SYSTEM OF HIVAIDS IN CHINA
 
Monitoring of the HIV/AIDS epidemic directly impacts the determination of the HIV/AIDS policies and the distribution of resources. An accurate understanding of the HIV/AIDS epidemic situation is integral to understanding and foreseeing the impact of the AIDS epidemic on the society at large. Therefore, comprehensive monitoring of the AIDS epidemic in China plays a very important role in HIV/AIDS prevention work.
 
HIV/AIDS surveillance is one of the core strategies of China’s HIV/AIDS prevention and control
HIV/AIDS surveillance is the continuous, systematic collection, and analysis of the distribution information about HIV/AIDS infection and related factors in all types of people in order to provide timely and reliable information. This surveillance information is used to help formulate AIDS prevention and control measures, as well as to assess the efficacy of implemented strategies.9,10 The AIDS Monitoring System in China consists of three main areas: case reporting, epidemiological sentinel survey- llance, and special surveys (mainly for AIDS epidemic estimation and predictions, estimating the size of high-risk populations, etc).
 
In China, AIDS surveillance has gone through three phases: passive surveillance, coexistence of passive surveillance and active surveillance, and comprehensive surveillance. Case reporting, which belonged to the passive monitoring stage, was used from 1985 to 1995. In 1995, the national HIV sentinel surveillance system, which incorporated both passive monitoring and active monitoring phases, was established. Beginning in 1999, behavioral surveillance was piloted in selected provinces and cities and in 2004 became formally integrated into the HIV/AIDS Comprehensive Surveillance System also known as “Comprehensive surveillance of Surveillance” (Figure 8).11,12
 

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Figure 8. The development of the AIDS monitoring system in China.
 
The AIDS case reporting system began in 1985, as part of the paper report card system to track infectious diseases. The “AIDS Epidemic Network Reporting System” was launched in July 2005 to start a national network of direct reporting. All information of previous reported cases was transferred into the system. Currently, the entire AIDS epidemic direct reporting network provides real-time statistics, and uses the “Data Analysis and Statistics” module in the system platform to provide monthly, quarterly, and annual HIV/AIDS epidemic reports. This reporting system provides a wealth of information that helps to aid AIDS prevention strategies and enhances the ability and speed of our country to respond to the AIDS epidemic in the field with both AIDS prevention and control.
 
AIDS sentinel surveillance was established in 1995 and the 42 sentinel sites covered sexually transmitted disease (STD) patients, CSWs, drug users and long-distance truck drivers,13 with maternal and MSM sentinel sites established at a later time. This “second generation surveillance” concept, introduced in 1998 by the WHO and UNAIDS, refers to the combination of basic serological and clinical surveillance (S&CS) and the behavioral surveillance survey (BSS).14 The international cooperation projects were launched in 1998 to target behavioral surveillance among high-risk groups, vulnerable groups and the general population in selected provinces and cities in China. In 2004, an additional 42 behavioral surveillance sites (which included HIV antibody testing) were established across the nation to survey six specific subpopulations: DUs, CSWs, STD patients, long-distance truck drivers, young students and pregnant women. By the end of 2008, there were 1080 serological HIV sentinel sites in China (681 serological sentinel and 399 integrated sentinel sites). Sentinel surveillance sites for CSWs and STD patients covered 31 provinces and sentinel sites for drug users covered 28 provinces.
 
In 2009, the serological surveillance system and comprehensive surveillance systems were integrated into “Chinese AIDS Sentinel Surveillance System”. China developed and used the “National Program on HIV Sentinel Surveillance (2009 Edition)” in order to create this country-specific, newly integrated surveillance system. This system had a total of 1312 sentinel sites that provided data, which was used to compile the “2009 National HIV Sentinel Surveillance Report”. In 2010, the national AIDS sentinel sites were recategorized and the number of sites was expanded to 1888 covering eight categories of HIV/AIDS-related populations, monitoring 87 hepatitis C virus (HCV) surveillance sites, and covering five high-risk populations for HCV. As the number of surveillance sites increases, the surveillance system will be continuously improved and enhanced.
 
Since 2003, the same estimation methods, drafted in collaboration between the Ministry of Health, WHO and UNAIDS, have been used to estimate the AIDS epidemic in China once every two years, a total of four times. Data accumulated over the years from the AIDS comprehensive surveillance system were used to write the “Joint Assessment of HIV/AIDS Prevention, Treatment and Care in China” reports.
 
Two changes and the integration of AIDS surveillance system in China
Change from passive surveillance to active surveillance
The change in the surveillance system reflects the continually changing and growing AIDS epidemic in China. Passive surveillance is based on case reporting which records the three distributions of the new cases each year and accumulated cases over the years. However, it is acknowledged that there are a number of HIV/AIDS cases that go undetected, so the number of reported cases can not fully reflected the trend of the AIDS epidemic. Because of the continual increase in the HIV infection rate among specific populations as reported through passive surveillance, active surveillance was put in place to better gauge and understands the HIV/AIDS epidemic in China.
 
Change from first generation surveillance to second generation surveillance
HIV/AIDS epidemic trends can be better predicted with information from thorough surveys and studies of high-risk behavior among a population. Surveillance based on case reports and serology does not account for behavioral characteristics, so it is limited to detect infection prevalence but is relatively ineffective in curtailing future infections. With the establishment of the comprehensive surveillance system, there was a change from the first generation of serological surveillance to the second generation of behavioral surveillance. The behavioral information among specific populations collected by the comprehensive surveillance provided a more accurate picture of the current and future AIDS epidemic in China.15
 
The integration of the biological and behavioral surveillance
The AIDS sentinel surveillance system in 2009 reflected integrated the biological and behavioral surveillance systems, saving resources and improving the quality of information, to better depict the HIV/AIDS epidemic in China. In 2010, AIDS sentinels were recategorized and redistributed in order to reflect changes of the AIDS epidemic trends and to give a more representative picture of various populations.
 
CHALLENGES IN HIV/AIDS EPIDEMIC AND SURVEILLANCE IN CHINA
 
With the development and changes of the AIDS epidemic, the HIV sentinel surveillance system faces new problems and challenges;16 several important aspects are summa- rized below.
 
Quality of the current HIV/AIDS case reporting system
The current HIV network reporting system has covered all of the counties (cities, districts) at the national level. But due to the imbalance of regional human resources, material resources, social and cultural needs and socio-economic development, the quality of HIV network reporting varies greatly by locale. Future efforts should focus on improving the accuracy, timeliness and sensitivity of the network reporting system to a more uniform standard.
 
Location of surveillance sites
As the HIV/AIDS epidemic disperses from concentrated areas across China, there needs to be an increased number of sites. In addition, there is a need for an improved methodology that is used to choose the location of sentinel sites. It is often difficult to find CSWs and methadone maintenance treatment users (MMT) because of the illicit activities they participate in and their fear of repercussions. Each surveillance site faces unique challenges according to the characteristics of its local HIV/AIDS epidemic, socioeconomic and geopolitical climate, as well as availability of human resources. At a large number of surveillance sites, there is a dearth of public health workers and doctors, thus overextending the staff. This can lead to a high turnover in staff.
 
Selection of monitoring group
Over time, China’s HIV/AIDS epidemic has spread from concentrated high-risk groups to the general population, increasing the breadth of the population affected by HIV/AIDS. The selection of specific groups for monitoring needs to reflect the epidemic’s development. For example, monitoring sites for CSWs currently exist in most areas of those 31 provinces. There are a large number of CSWs and clients, but one of the major challenges to monitoring sex workers is that they are a “floating” or highly mobile population, and thus often are undetected by our survey methods. So although surveillance shows that the rate of HIV infection in CSWs is low, there may be a large proportion of the population that goes undetected, which would mean that the rate of HIV infection in CSWs, in actuality, may be significantly higher.
 
In recent years, case reporting suggests that sexual transmission has become the main route of transmission in China’s epidemic. Combined with sentinel surveillance, the data suggest that there is a significant proportion of this sexual transmission that is heterosexual transmission that occurs outside of commercial sex work. In other words, monitoring the HIV epidemic trend requires changes due to new heterosexual transmission and monitoring CSWs is no longer enough. There should be more consideration given to heterosexual transmission between married couples or regular partners. Because of the differences between the population sizes of drug users and sex workers, the changes in the composition of transmission in the case report system cannot be used to explain the changes in the situation of infection in different high-risk populations. In addition, there is a need for improved analysis and verification of collected data in order to accurately assess the HIV/AIDS epidemic. In summary, more work needs to be done in order to reach out and monitor sensitive populations, such as CSWs and MSMs. Moreover, additional research should be conducted to understand the role of heterosexual transmission, outside of commercial sex work, and how it relates to China’s HIV/AIDS epidemic. 
 
Estimation and prediction of HIV/AIDS epidemic
Estimations and predictions of the HIV/AIDS epidemic are based on the comprehensive analysis of data from the case reporting system, sentinel surveillance system, and special epidemiological surveys. Accuracy of the estimation results is dependent on the applicability of the model and data accuracy. More needs to be done in order to empower local governments to actively participate in HIV/AIDS estimations and projection work, in order to enable local officials to effectively combat the HIV/AIDS epidemic in their communities.
 
Standardization of collection, analysis and use of surveillance data
Random sampling or convenience sampling methods were used in surveillance, although they do not abide by the strictest requirements of the sentinel surveillance program, which requires continuous sampling. The “off-line input, online transference” approach was used in the current data management system. Because of limitations of human resources and computer network infrastructure in some areas, it was difficult to collect and report sentinel surveillance data in a timely manner.
 
RECOMMENDATIONS
 
Strengthen the construction of local personnel resources
Staff training at the local level needs to be strengthened and there should be training provided particularly for staff that are responsible for monitoring.  National or provincial CDCs should provide technical support and supervision for high-risk HIV/AIDS areas and areas with limited capacity to conduct quality monitoring. In addition, problems that arise in surveillance should be detected and dealt with immediately.
 
Deciding on sentinels site’s reasonability and standardized operations
Geographical distribution, population representation and a large enough sample size should be considered when setting a sentinel surveillance site. Through the course of the operation, the national and provincial CDCs should make every effort to conduct data audits and the county-level CDC should strengthen the training of investigators to improve the quality of investigations. Quality control should be conducted on all aspects of the operation when the sentinel site is running.
 
Integrating resources and strengthening data analysis
The sentinel surveillance system was integrated in 2009, and then revamped in 2010. There needs to be improved data analysis at all levels among surveillance staff in order to understand the HIV/AIDS epidemic situation in China.
 
In summary, the development of the AIDS comprehensive surveillance system of China has been adapted to the changing HIV/AIDS climate. Over time, the system has changed from passive to active surveillance and from biological surveillance to behavioral surveillance. The present work of resources integration, improvement of surveillance quality, and the enhancement of data analysis and utilization will promote an improved AIDS comprehensive surveillance system.
 
REFERENCES
 
1.  Joint United Nations Program on HIV/AIDS (UNAIDS) and World Health Organization (WHO). AIDS epidemic update. Geneva: UNAIDS and WHO; 2009: 7.
2.  Zhang KL, Ma SJ. Epidemiology of HIV in China. BMJ 2002; 324: 803-804.
3.  Zheng XW. Advanced in epidemiology (VIII). Beijing: China Science and Technology Press; 1995: 25-64.
4.  State Council AIDS Working Committee Office, UN Theme Group on AIDS in China. A Joint Assessment of HIV/AIDS Prevention, Treatment and Care in China. Beijing: SCAWCO and UNTG; 2007: 4.
5.  Ministry of Health of China, UN Theme Group on HIV/AIDS in China and World Health Organization. 2009 update on the HIV/AIDS epidemic in China. Beijing: Chinese Center for Disease Control and Prevention, 2009. (Accessed at http://www.chinaaids.cn/n16/n1193/n4073/307442.html)
6.  Wang L, Wang N, Wang LY, Li DM, Jia MH, Gao X, et al. The 2007 estimates for people at risk for and living with HIV in China: progress and challenges. J Acquir Immune Defic Syndr 2009; 50: 414-418.
7.  Wang L, Wang L, Wang LY, Ding GW, Li DM, Gao X, et al. Analysis of core indicators of behavioral surveillance surveys among female sex workers from 2005 to 2007. Chin J AIDS & STD (Chin) 2009; 15: 140-142.
8.  Wang L, Ding ZW, Ding GW, Guo W, Wang L, Qin QQ, et al. Data analysis of national HIV comprehensive surveillance sites among female sex workers from 2004 to 2008. Chin J Prev Med (Chin) 2009; 43: 1009-1015.
9.  Li LM. Epidemiology (the fourth edition). Beijing: People’s Medical Publishing House; 2000: 145.
10.  AIDS prevention and control, 2006. (Accessed at http://www.gov.cn/zwgk/2006-02/12/ content_186318.htm)
11.  Wu ZY. Current challenge of AIDS epidemic surveillance in China. Dis Surveill 2009; 24: 819-821.
12.  Li DM, Wang L, Wang LY, Wang L, Gao X, Qin QQ, et al. HIV sentinel surveillance system in China: the history and the current. Chin J Prev Med (Chin) 2008; 42: 922-925.
13.  Zheng XW. Strengthening comprehensive monitoring capacity of AIDS/STD in our country. China J Prev Med (Chin) 2001; 2: 13-14.
14.  WHO, UNAIDS. Guidelines for second generation HIV surveillance. Geneva: WHO and UNAIDS; 200: 22-23.
15.  Zeng G. Secondary generation of HIV/AIDS surveillance. Chin J AIDS & STD (Chin) 1998; 4: 49-50.
16.  Wang N. HIV control and prevention in China: situation and challenges. Chin J Prev Med (Chin) 2004; 38: 291-293.