UNAIDS estimated that at the end of 2001, between 800 000 and 1.5 million Chinese people had acquired HIV infection. This figure coincides with estimates from the Chinese Ministry of Health; however, neither systematic population-based surveillance nor blood donor surveillance currently exist [1,2]. In the absence of successful interventions, the United Nations estimates that HIV prevalence in China will reach 10 000 000 by 2010.
China is suffering from several concomitant HIV epidemics. HIV was first recognized in the early 1990s among injecting drug users (IDU) in far western and southern provinces. HIV is now found in IDU in every province, and official surveillance data indicate that 39% of IDU in Xinjiang Province (in the northwest), and more than 50% of IDU in Yunnan Province (in the south) are HIV seropositive .
A second epidemic among blood plasma donors was reported in 1998 . Plasma donors in central provinces developed HIV through use of unsafe blood transfusion procedures and reuse of contaminated medical equipment. In some areas entire villages have been profoundly affected by AIDS [5,6]. In one Henan Province study, among 208 women who donated blood or received a transfusion between 1992 and 1996, 50% were HIV positive .
Heterosexual transmission of HIV is increasingly important. Since the introduction of market reforms in the 1980s, sexually transmitted disease (STD) incidence has dramatically increased in China (Fig. 1). Between 1990 and 1998 in China, syphilis incidence increased 20-fold .
While large segments of the Chinese population still have a low risk of sexually transmitted infection (STI) and HIV , major demographic changes are underway. The goal of this review is to focus on two groups that may fuel China's HIV epidemic: young, poor, unmarried men or ‘surplus’ men and female sex workers (FSW). While HIV and STI seroprevalence are more traditional metrics for the heterosexual spread of HIV, the male heterosexual risk generally has not been a focus of research in China. More specifically, a major demographic shift already underway could have major implications for the spread of HIV and STI in China.
Surplus men: young, single poor men or ‘bare branches’
Today in China the young, poor unmarried are called guang gun – bare branch, since without marriage growing new branches on the family tree is impossible. Traditional preference for male children re-emerged after the end of the Maoist era (1949–1976) when policies fostered gender equality [10–12]. Post-Mao policies have encouraged son preference though the de-collectivization of agriculture, the one child family planning policy, and the diffusion of ultrasound technology that enabled sex selective abortion [13,14].
The sex ratio at birth (SRB) is the number of males born per 100 females in a given population, and is naturally approximately 106 . Census data from 2000 report China's nationwide uncorrected sex ratio for children aged 0–4 years was 120.2 compared to 105 in 1980 (Fig. 2). Using 2000 census figures and accounting for under-reporting of female births, China has 8.5 million more men than women among cohorts born between 1980 and 2000 . Demographers believe that this surplus has been driven primarily by elective abortion of females .
China has previously witnessed a surplus of men related to migration. In 1933 the Shanghai Civic Association's statistics show that men outnumbered women 130 to 100 in the Chinese section of the city, and official statistics for the entire city show similar sex ratios [18,19]. This imbalance developed as a result of permanent migration from rural areas and transient groups of sailors. STI were rampant. The Police Surgeon and Municipal Health Officer for Shanghai noticed that the spread of STI was mostly associated with the population “consisting mainly of young unmarried men, [who] are particularly liable to suffer from those evils” and who according to a contemporary sociologist, “demand sexual satisfaction and yet cannot afford to go through all the procedures of ceremonial courtship” [20,21].
Demographics of surplus men
Current demographic estimates place the number of surplus men between the ages of 20 and 23 years at approximately 640 000 individuals; by 2020, the number of surplus men between the ages of 20 and 40 years is predicted to increase to a cumulative 8.5 million . Provincial mean SRB from 1989 permit a more precise province-by-province analysis: surplus men will be found in the eastern, southern and southwestern provinces, including Zhejiang, Jiangsu, Shandong, Guangdong, Sichuan, and Hainan . Ultrasound machines capable of prenatal sex determination were standard at city hospitals by the mid-1990s, and are common in many townships today. Within a province, there appear to be slightly more surplus men in towns and the countryside, and slightly fewer in cities . Furthermore, since a poor family may be expected to have greater son preference for economic reasons, more surplus men will be expected in poor rural areas.
Educational and economic characteristics of surplus men
The anticipated surplus male will be unmarried, poor, unemployed, and lacking education. Currently, among unmarried Chinese aged 35–39 years, approximately 88% are male; 99% of all females aged 30–34 years are married . Among unmarried men, 74% have not graduated from senior high school. Among rural unmarried men, 97% do not have high school degrees and 40% are illiterate . Analysis of the 2000 China National Census confirms this pattern, with 89% of all unmarried men not completing senior high school . Surplus men in China will likely have fewer opportunities for education, and subsequently fewer employment opportunities. A recent analysis of China's impending demographic shift warned that surplus men will tend to be poor and cause substantial social unrest .
China's traditional system of bride prices, typically paid by the groom's family to the conjugal unit, exacerbates problems surplus men face in finding a wife . Increased bride prices due to a relative scarcity of available brides will create challenges for poor rural Chinese males to get married, while affluent urban Chinese men will be less affected [30,31]. Confirming these trends, a recent study from rural China showed that bride prices have increased significantly, giving women more options in choosing a suitor . As a result of their limited economic resources, surplus men will migrate to other areas for jobs and/or brides. Given established migration patterns, surplus men in China will move eastward and southward, from rural to urban areas, and from towns to cities .
Male sexual risk behaviors among migrants and the unemployed
While no studies have examined the sexual risk behaviors of surplus men, there are a number of reports on migrant workers, who may have similar characteristics. China's 100–150 million liudong renkou ‘floating migrant population’ are largely young poor, single men, typically from the countryside [34,35]. They constitute a substantial portion of the underclass in cities and towns. Given their transient lifestyle, systematic studies of this group are difficult. However, a recent report looked at over 2000 rural to urban migrants in two large Chinese cities, and found increased sexual risk taking behaviors among migrants, and demographic analysis from a different study in south China supports the finding of increased risk of STI and HIV among migrant populations [36,37].
These findings are also confirmed by other studies. For example, a workplace survey of 1845 unmarried migrant workers in east China found substantial gaps in HIV knowledge and infrequent condom use . A convenience sample of 506 migrants found that nearly half reported multiple sex partners, 89% inconsistently used condoms, 12% reported selling blood since leaving their last residence, and 9% admitted illicit drug use . A study of stall workers in Fuzhou, a city in the eastern province of Fujian, found that 13% had STI . Finally, a recent population-based survey in China showed that 11.1% of Chinese men aged 20–24 years had unprotected sex with a sex worker .
Operational definition of surplus men
Since the term ‘surplus men’ has come from the demography literature into a broader HIV and STD framework, a more precise definition of this group is essential for epidemiologic, behavioral, and prevention activities. Based on the SRB and the traditional marriage customs described above, we know that this group will be unmarried. And since we know this group of men was born between 1980 and 2000, the group of men can be described as young – less than 30 years old. Importantly, the young unmarried men (students, young professionals) delaying marriage until their late 20s are not part of the group being discussed. In order to exclude this group, a certain level of poverty separates true surplus men from their more affluent young professional counterparts. Hence, a reasonable operational definition of surplus men would be young, poor, unmarried men. While this group is certainly at greater risk of migration and some subsets of migrants may completely overlap with surplus men, even young, poor, unmarried men in a local area may have greater risk of STI and HIV.
Female sex workers in China
Given that surplus men will be unlikely to find marital partners, the expansion of female sex work to meet greater demand may occur. Sexually transmitted infections and female sex work have flourished in China during various periods in the past century .
Sex work in the twentieth century in China has been well studied. Shanghai had as many as 100 000 FSW by 1935, making it one of the most common means of employment for women in the city . The Shanghai Municipal Council issued photo identification cards certifying weekly physician examinations for women in the sex trade during that time. Women with STI had their cards destroyed, and brothels supporting such FSW were in danger of being closed by the police . Syphilis prevalence was 19%, substantially greater than the estimate of syphilis prevalence across the UK and USA at the time [45,46]. Shanghai's extensive inter-regional and international migration created a foundation for sexual network mixing and increased sexually transmitted infection.
The 1950s witnessed sweeping changes instituted under Mao Zedong, in both the practice of commercial sex work and prevalence of STI. Campaigns targeting sex work using re-education camps and stiff fines were used; STI control through mass screening coupled with antibiotic therapy was a national priority and an act of patriotism. By the late 1950s, STI virtually disappeared from infectious disease clinics .
As a market economy developed during the 1980s, STI and an active sex work industry re-emerged. According to Chinese statistics, the number of FSW in China soared from 25 000 in 1985 to 246 000 in 1992 to 420 000 in 1996, although many sources suggest that this is a significant underestimation of the true numbers [48,49]. By 2000 the Chinese Public Security office estimated 4–6 million sex workers nationwide, a 160-fold increase since 1985 . A 2001 US State Department report on China estimated the number of sex workers at 10 million .
There are at least 12 distinct types of sex workers in China, ranging from courtesans or escorts to brothel-based sex workers to freelance street walkers, with a diversity of work organization, income, clientele, and employment status . In general, FSW tend to be young, unmarried, with limited education, having migrated from poor rural areas to towns or cities [53–55]. An active sex industry can be found within townships and rural areas, providing male farmers opportunities for nearby sex outside of marriage [56–59]. There are sex workers near factories (gongpeng nu, factory girl) whose clients are factory or construction workers; low income sex workers (zhanjie nu, street standing girl) are also likely to provide sex services to poorer male clients . Thus, China's diverse FSW population would likely be able to accommodate low income surplus men in rural and urban areas.
Female sex workers’ sexual risk behaviors
Studies of sex worker behaviors provide some insight about condom use and STI risk. Across 19 reporting provinces an average of 51% of FSW never used a condom in 2000 (range, 8–88%) . While a number of condom use campaigns have been instituted since these official reports, a core group of FSW does not consistently use condoms. A 2002 community-based study of Beijing FSW found that 39% of those surveyed did not consistently wear a condom . Another recent study revealed similar findings, demonstrating approximately 15–30% of sex workers from a community sample regularly used condoms .
Not surprisingly, STI are common among FSW in China. A community study of 966 commercial sex workers in Guangdong Province (in south China) found that 14% had syphilis, 32% had chlamydia, 8% had gonorrhea, 12.5% had trichomoniasis, and 1.4% were HIV positive . Sentinel surveillance data suggest that three provinces – Yunnan, Guangdong, and Guangxi – have had increasing HIV seroprevalence among FSW from 1996 to 2000 (Fig. 3) . Increases in HIV seroprevalence among sex workers in the southern part of China during the last several years are concerning given known STI trends.
The epidemic of STI and China's economic development
Economic growth in China during the past 10 years has been unparalleled, but also accompanied by tremendous regional inequalities [66,67]. Even taking into consideration variations in cost of living, income inequality has increased, providing disposable income among the newly wealthy to purchase sex. In a population-based study of chlamydia seroprevalence in China, men with higher incomes and men who socialized or traveled more were more likely to have unprotected paid sex, and women in a steady relationship with high income man were at a greater risk of chlamydia infection .
Furthermore, provinces with more STI also have the highest pace of economic development, and probably a larger pool of high income men at risk. The province with the largest STI incidence in 2000 was Shanghai at 312 reported STI cases per 100 000 individuals. This was followed by Zhejiang Province at 216 cases per 100 000, and then Beijing, Jiangsu, Guangdong, Tianjin, and Hainan. Given the increasing numbers of wealthy businessmen in these locations, it is not surprising that STI burden is largest in the most rapidly expanding urban and eastern coastal areas of China. These coastal provinces with high STI prevalence also overlap with some of the provinces where China will have greater numbers of surplus and migrant men (Fig. 4) .
How do these studies relate to the STI risk of surplus men? Substantial regional variation in income also encourages migration of the poor to find better jobs. Poor migrant males moving from rural areas to urban areas in search of better jobs will engage in high risk sexual behaviors that place them at risk for HIV infection, especially the unmarried and young . While the poorest surplus males will not have money to purchase sex, variations in price per sex act and extent of sex work in relatively poor areas suggests that a substantial number of surplus men may buy sex. In addition, among poor surplus men, the immediate costs of paying a sex worker are less than the long-term investments necessary to find a bride. The variation of commercial sex available as described above virtually assures that even poor surplus men will be able to find and afford sexual services.
Surplus men's role in future HIV transmission: bridging populations
Quantifying the increased sexual risk of China's surplus men is essential to understanding the importance of this emerging group. Probability of HIV transmission depends on viral transmission efficiency, number of people exposed, and duration of infectiousness . However, since only a broad estimate for each of these variables exists in China, such approximations would be purely hypothetical. As such, a more useful exercise is to consider how a concentrated HIV epidemic like China's could turn into a generalized one based on a new bridging male population, the surplus men. The potential for surplus men will be explored along two levels: from high to low heterosexual risk, as well as from IDU to heterosexual transmission.
Given the known (single, poor, unmarried) and anticipated (high risk sex with FSW, migration, low education) characteristics of surplus men, there may be a high risk of heterosexual HIV bridging between high and low risk populations. Many surplus men will migrate from rural to urban areas, as has already been discussed. Before the young unmarried poor men find wives, they are likely to have a greater risk of acquiring STI and HIV from FSW in urban areas. However, once they earn money and become more stable, there would likely be a transition from high risk partners (FSW) to low risk partners (similarly poor women in urban or rural areas).
Examples of male bridging populations are worthy of further consideration to predict transition from a concentrated epidemic to a generalized one. In Cambodia an active male bridging population was found among military men for whom the general social norms did not apply, and group dynamics promoted buying sex . This study found that social factors (military group dynamics, living near a port city) more than individual characteristics mediated whether or not a man had sex with both high and low risk women. A male bridging population was also discovered in a sub-Saharan Africa analysis . Male bridging populations mediated by mobility and non-standard group norms accelerated a generalized heterosexual HIV epidemic in Cambodia, and similar social forces should be analyzed when predicting the future heterosexual HIV epidemic of China.
Beyond heterosexual bridging, the concomitant high prevalence of injecting drug use within some surplus men could have substantial consequences for heterosexual transmission. There are no studies in China that directly assessed HIV status, injecting drug use, and secondary transmission among groups of young poor single men. One study from Yunnan Province found that among those IDU with HIV, approximately 69% were unemployed and 67% were single . The phenomena of injecting drug use heterosexual transmission or drugs for sex has not been described in China, but might be expected in coming years as the surplus men increase in number.
Preventing HIV in China
There is no doubt that China will face an extraordinary male surplus in the next 20 years, and a great number will be single, poor, undereducated, and underemployed migrants. The extent to which these surplus men seeking sex will overlap with sex workers in terms of price and place remains hypothetical. However, historical examples of true male surpluses in China combined with available data about HIV/STI seroprevalence among FSW and migrant men make this issue fundamental to the future of the HIV epidemic.
Beyond traditional STI/HIV prevention services, targeting high risk sex workers and potential clients is paramount to successful prevention activities. Recent evidence from outside China shows that high risk individuals are often more likely to meet sexual partners in non-random locations . Sociologists in China have studied the locations and habits of sex workers and migrant groups that may resemble surplus men [76,77].
High risk women and the prevention of HIV
Focusing interventions at beauty parlors, salons, other types of brothels, and female re-education centers holds great potential . China and several other counties in Asia have mandatory sex worker re-education centers where FSW are detained by police, tested without consent for HIV and other STI, and then released. Fundamental human rights issues are at stake, and the basic rights of these often already marginalized women needs to be addressed . Since female re-education centers likely hold some of the poorest and most vulnerable sex workers, interpreting the large amount of epidemiologic data emerging from such centers is challenging. Furthermore, re-education centers and police crackdowns may promote FSW mobility that increases their risk of STI and distances them from regular health care and the stability of their local social structure.
Reform within mandatory FSW re-education centers could start with acknowledging their STI risk, providing STI/HIV education, and introducing informed consent for STI/HIV surveillance testing performed. Legal reform for sex workers could make the profession safer, decrease the incidence of STI, and substantially slow the spread of heterosexual HIV transmission . Conversely, any policy that drives sex work underground may make detection and proper treatment of STI more difficult . Recent provincial policies point towards a more effective official relationship with sex workers. China's first provincial regulation on AIDS Prevention and Control in Yunnan was implemented on 1 March 2004, and includes condom promotion and STI education for incarcerated women . Zhejiang, Guangdong, and Hubei Provinces have introduced similar provincial laws that promote condom use or distribution in specific locations [83,84].
FSW frequently lack the negotiating experience and social capital to refuse unprotected commercial sex, making client and brothel manager involvement in STI prevention especially important . In addition, identifying and improving the health of migrant men must become a national priority for the public health infrastructure in China. Interventions and prevention activities for surplus men focused at construction sites, unemployment centers, bus stations, railroad stations, and other places where rural to urban poor single migrants are found may be particularly useful .
High risk men and HIV prevention
Preventing HIV among heterosexual men is an important issue that has remained at the margins of HIV prevention. Since some parts of southern China have an HIV seroprevalence rate of approximately 1–2%, prevention of a generalized HIV epidemic is especially important. In order to prevent the surplus male population from becoming a bridging population, condom use among both high risk and low risk partners should be encouraged. Furthermore, large groups of men (police, military) should receive targeted education, prevention, and other interventions. Currently in China, men receive routine HIV testing when entering the military. Broader screening to include STI on entry to the military and HIV and STI when leaving the military (and potentially returning with STI to their low risk previous partners) should be considered.
Targeting male clients, boyfriends, or brothel personnel is certainly a challenging task that has made literature on the topic sparse, although there has been promising work in this area. Studies in the field have shown that sampling men from brothels  and bars, nightclubs, and lounges (apart from brothels)  are both feasible methods of accessing this high risk population.
Construction sites are worthy of special consideration. China's fast paced economy, most notably in eastern urban centers, has created two groups of men at increased risk of STI which did not exist 20 years ago: wealthy traveling businessmen and poor migrant men. Employer-based STI prevention would allow both management and workers in a business to benefit from education, and many businesses have attached clinics which could be utilized for interventions. Since HIV prevention has been shown to be cost effective in many developing countries, business leaders may be more likely to become partners in STI prevention and related interventions . In addition to construction sites and other work specific areas, China's centrally organized system of tracking people who are unemployed may be a useful area to target interventions.
Understanding the social determinants of HIV in China requires a broad demographic outlook. The root causes of male preference in China are the same ones that make HIV prevention challenging among female sex workers – discrimination, gender inequality, and poverty. Empowering FSW with educational and economic opportunities has been suggested in other settings and should be considered in China today [89,90]. While there are many programs that benefit poor women in China, none have specifically focused on poor sex workers .
While this paper did not discuss the implications of China's bare branches on the other components of the HIV epidemic (blood donation, men who have sex with men), preliminary behavioral evidence from China's floating population supports a substantial risk for HIV transmission via non-heterosexual means as well. More demographic, behavioral, and epidemiologic data is needed about the growing number of MSM in China .
China does not stand alone as an Asian nation with both surplus men and potential for expanded heterosexual HIV epidemics. Since the male surplus will likely have a significant impact on the development of China's HIV epidemic, it would be important to explore similar demographic changes in other countries with heterosexual HIV epidemics, including India, Myanmar, and Viet Nam.
China is undergoing a social and economic transformation of historic proportions. The dramatic changes inaugurated in the 1980s have paved the way for bare branches – poor, migratory, unemployed, and unmarried men. A major demographic shift is taking place in a country that comprises one-fifth of the world's population, creating a new STI risk group. Meanwhile, HIV seroprevalence from FSW in several Chinese provinces suggest that an expanded heterosexual HIV epidemic may already be underway, and the diversity of sex workers in China could accommodate this emerging risk group. Current surveillance has neglected the emerging male surplus subpopulation. As this demographic shift occurs, it will be imperative to appreciate the evolving sexual risk of China's young, unmarried males.
We are indebted to the China National STD Control Center for helping to facilitate analysis and exchange. This article was presented in part at the Third International Conference on AIDS and other Infections in Guangxi, China from Dec 1–3, 2004.
Sponsorship: This study was supported by the National Institutes of Health Fogarty AIDS International Training and Research Program (Grant D43 TW01039) through the UNC Fogarty Center.
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