International Journal of Gynecology and Obstetrics 128 (2015) 18–22
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CLINICAL ARTICLE
HIV, other sexually transmitted infections, and risk behaviors among female sex workers in Liuzhou, China Yin-Guang Fan a,1, Jin-Ji Liu b,1, Yu-Jing Zhang a, Se-Ying Dai a, Ming-Qiang Li b, Dong-Qing Ye a,⁎ a b
Department of Epidemiology and Biostatistics, School of Public Health, Anhui Medical University, Hefei, China Liuzhou Center for Disease Control and Prevention, Liuzhou, China
a r t i c l e
i n f o
Article history: Received 8 January 2014 Received in revised form 9 July 2014 Accepted 27 August 2014 Keywords: Female sex worker Hepatitis C HIV Risk behavior Syphilis
a b s t r a c t Objective: To determine the prevalence of infections with HIV and hepatitis C virus (HCV), and of syphilis among female sex workers (FSWs) in Liuzhou, China, along with levels of HIV-related knowledge and frequencies of risk behaviors. Methods: A cross-sectional survey was conducted between July 2012 and January 2013. FSWs (aged ≥16 years; reported receiving payment for sex in previous 6 months) working at 58 selected commercial sex establishments (level 1 [N¥300 per transaction], level 2 [¥100–300], or level 3 [b¥100]) completed a questionnaire and provided blood samples for testing. Results: Of 622 participating FSWs, 7 (1.1%) had HIV infection, 67 (10.8%) syphilis, and 44 (7.1%) HCV infection. Consistent condom use during commercial sex encounters in the past month was reported by 412 (66.2%) FSWs. Inconsistent condom use was most likely in FSWs working in level 3 establishments (odds ratio [OR] 1.85; 95% CI 1.02–3.39), with a regular partner (OR 1.65; 95% CI 1.12–2.45), and who used illicit drugs (OR 2.10; 95% CI 1.24–3.54). Inconsistent condom use was least likely in FSWs with high HIV awareness (OR 0.29; 95% CI 0.18–0.48) and who had had a previous HIV test (OR 0.51; 95% CI 0.34–0.76). Conclusion: Further prioritized and combined programs aimed at FSWs are needed to prevent HIV transmission in China. © 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction In China, the annual reported number of individuals living with HIV/AIDS has been increasing, reaching 780 000 in 2011 [1]. Injecting drug use was the most common mode of infection until 2007, when heterosexual contact became the main transmission mode [1,2], the proportion of cases resulting from heterosexual transmission increased from 11.3% in 2005 to 38.9% in 2007 and 76.3% in 2011 [3]. How to prevent further sexual transmission is the great challenge in the control of the HIV epidemic in China. Since the Chinese economic reform began in the 1980s, sexually transmitted infections (STIs) have re-emerged [4]. In the same period, the number of female sex workers (FSWs) has grown, with the figure reaching 4–10 million by 2004 [4,5]. FSWs are vulnerable to HIV and STIs, their rates of infection are higher than are those of the general population [6]. In 2009, government estimates suggested that 0.33%–0.94% of FSWs were living with HIV [7], but the prevalence has been as high as 8.3%–10.3% [8,9]. In one study in Yunnan [9], 4.8%–53.2% of FSWs
reported having had STIs in the past, and 13.0%–90.6% tested positive for at least one STI. Guangxi Zhuang Autonomous Region is located in South Central China. The HIV prevalence in this region is the second highest among the 31 provinces of mainland China [10]. Liuzhou is a city in the north of Guangxi, with a population of 3.7 million. Commercial sex trade flourishes in the city because the economy has been growing in recent years. By the end of 2010, 9982 people in Liuzhou were living with HIV/AIDS [11]. According to a report from the Chinese Ministry of Health [1], Guangxi Zhuang Autonomous Region is one of five provinces where more than 1% of FSWs are living with HIV. However, no FSWs tested in one study in Liuzhou [12] were HIV positive, and the prevalence was 0.5% in another investigation [13]. The aim of the present study was to determine the prevalence of infections with HIV and hepatitis C virus (HCV), and syphilis among FSWs in Liuzhou. A secondary aim was to identify the risk factors associated with inconsistent use of condoms.
2. Materials and methods ⁎ Corresponding author at: Department of Epidemiology and Biostatistics, School of Public Health, Anhui Medical University, 81 Meishan Road, Hefei, Anhui, 230032, China. Tel.: +86 551 65167726; fax: +86 551 65161171. E-mail address: [email protected] (D.-Q. Ye). 1 These authors contributed equally.
A cross-sectional study was conducted between July 1, 2012, and January 4, 2013. FSWs aged at least 16 years who reported receiving payment for sex in the previous 6 months were eligible for inclusion. Participants had to be willing to undergo testing and HIV/STI counseling.
http://dx.doi.org/10.1016/j.ijgo.2014.07.024 0020-7292/© 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
Y.-G. Fan et al. / International Journal of Gynecology and Obstetrics 128 (2015) 18–22
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The study protocol was approved by the ethics committee of Anhui Medical University. All participants provided informed consent. Participants were recruited using multistage sampling methods. Liuzhou has one urban district and five counties. To enable an assessment of STIs in both urban and rural areas, the urban district and one county were selected for inclusion. Liujiang County was randomly selected using a simple random sampling method. The sampling scheme was based on the map of commercial sex establishments maintained by the Liuzhou Center for Disease Control and Prevention (CDC) and Liujiang CDC, and all the sexual establishments in the map were identified by a pilot study. The identified sex establishments in the two areas were categorized into three levels according to the mean income of FSWs per transaction: at level 1 establishments, more than 300 Yuan were earned per transaction (e.g. bars, saunas, nightclubs, and karaoke bars); at level 2 establishments, 100–300 Yuan were earned per transaction (e.g. massage parlors and hair salons); and at level 3 establishments, less than 100 Yuan were earned per transaction (e.g. restaurants and inns). A sample of 10% of the establishments in each level was used: three level 1, 11 level 2, and 44 level 3 establishments were selected by local outreach workers by convenience sampling. An anonymous questionnaire was developed and validated in a pilot study of 15 FSWs. The questionnaire consisted of three parts: demographic information, HIV-related knowledge, and sexual and HIV risk behaviors. HIV-related knowledge was evaluated by eight questions, to which participants needed to answer yes or no. Participants who gave at least six correct answers were deemed to have high awareness. They were also asked to rate their HIV-related knowledge (none, little, some, and a lot) and their risk of HIV infection (very likely, likely, unlikely and very unlikely). A regular sexual partner was defined as a man who was not a client and with whom the FSW had sexual contact, such as a boyfriend or husband. The survey was conducted face-toface by an interviewer in a private room. Approximately 10–15 minutes were needed to complete each questionnaire. Blood samples (3 mL from the median cubital vein) were obtained from FSWs by qualified doctors after the questionnaire was completed. The samples were tested in the Laboratory Department of Liuzhou CDC. They were screened for HIV antibodies by enzyme-linked immunosorbent assay (ELISA; Beijing Modern Gaoda Biotechnology Co, Beijing, China) and positive tests were confirmed by a HIV-1 western blot (Diagnostics HIV Blot 2.2, Genelabs, Singapore). Participants who had HIV infection were referred to their local CDC. Syphilis was detected by a rapid plasma reagin test (Xindi Biological Pharmaceutical Engineering Co., Nanjing, China) and positive tests were confirmed by Treponema pallidum particle agglutination assay (Beijing Modern Gaoda Biotechnology Co, Beijing, China). The presence of antiHCV antibody was detected by ELISA. FSWs who had syphilis or HCV infection were referred to the infectious diseases outpatient clinics of local hospitals. Data were entered into a database twice and matched using EpiData 3.1 (The EpiData Association, Odense, Denmark). Analysis was done using SPSS 10.01 (SPSS Inc, Chicago, IL, USA). Differences between FSWs at the three levels were assessed by univariate analysis. The χ2 test and linear-by-linear association test (trend tests) were used for proportional variables, and Fisher exact tests were used for contingency tables when more than 20% of the cells had expected counts less than five or one cell had an expected count of less than one. The one-way analysis of variance test was used for continuous variables. Independent risk factors of inconsistent condom use were assessed using logistic regression analysis. Variables significant in the univariate analysis were included in a multivariate model. All testing was twosided, and P ≤ 0.05 was considered statistically significant.
level 1 establishments, 210 (33.8%) at level 2 establishments, and 312 (50.2%) at level 3 establishments. A total of 535 (86.0%) FSWs came from Guangxi. Most were of Han or Zhuang ethnic origin (Table 1). Few respondents had attended high school, and most were older than 25 years. Age increased with level (trend test χ2 = 106.641; P b 0.001), as did the proportion of FSWs who were married or cohabiting (trend test χ2 = 217.699; P b 0.001). A regular sexual partner was reported by 359 (57.7%) FSWs. The proportion reporting a regular sexual partner increased with the level of establishment (Table 1), and the trend was significant (trend test χ2 = 12.829; P b 0.001). Of the 622 participants, 7 (1.1%) were identified as HIV positive (Table 2). Only 26 (4.2%) participants reported that they had had an STI in the past year, but the screening showed that 67 (10.8%) had syphilis and 44 (7.1%) were positive for HCV antibodies. The proportion of FSWs with each of the infections was highest in level 3 establishments, but the difference was significant only for syphilis (P b 0.001) (Table 2). Sixteen (2.6%) FSWs had syphilis and HCV infection, and 2 (0.3%) had syphilis and HIV infection. Among the 67 participants who tested positive for syphilis, 60 (89.6%) reported that they had never had an STI. Consistent condom use during commercial sex encounters in the past month was reported by 412 (66.2%) FSWs. Only 178 (57.1%) FSWs from level 3 establishments reported always using a condom. Overall, 21 (3.4%) FSWs overall reported never using condoms. A total of 96 (15.4%) had not used a condom in the most recent commercial sex encounter. The most common reasons for not using condoms were refusal by clients and regular clients (Table 2). Among the 359 FSWs who had regular partners, 70 (19.5%) had not used a condom during the most recent sex with their partner. This proportion is a little higher than that of FSW who did not use a condom with clients, but the difference was not significant (χ2 = 2.675; P = 0.102). Table 3 shows the proportions of FSWs who responded correctly to each of the eight HIV-related knowledge questions. Overall, 442 (71.1%) participants got at least six correct answers. There was a significant difference in awareness among the three levels: 88 (88.0%) of 100 FSWs from level 1 establishments answered correctly at least six times compared with 162 (77.1%) of 210 from level 2 and 192 (61.5%) of 312 from level 3 establishments (χ2 = 31.488; P b 0.001). The proportion of FSWs with high awareness decreased as the level of establishment increased (trend test χ2 = 31.098; P b 0.001). Some participants (194, 31.2%) thought that they knew only a little about HIV. Of the 24 FSWs who reported a high degree of HIV-related knowledge, only four (16.7%) answered correctly to at least six of the HIV-related questions. A total of 501 (80.5%) FSWs thought that they were unlikely to have been infected with HIV. Use of illicit drugs was reported by 112 (18.0%), of whom 31 (27.7%) had injected heroin previously. Approximately 45% of participants had undergone HIV testing previously (Table 4). First intercourse when younger than 18 years was reported by 345 (55.5%) FSWs. Overall, 390 (62.7%) participants had worked as a FSW for more than 12 months, and 357 (57.4%) had worked in more than one establishment. More than one client per day on average was reported by 340 (54.7%) FSWs, and 190 (30.5%) had three or more clients daily (Table 4). Significant variables in the univariate analysis were entered into the multivariate logistic regression model for inconsistent condom use (Table 5). Inconsistent condom use was significantly more likely in FSWs working in level 3 establishments than in those working in level 1 establishments (P = 0.045). Other significant risk factors in the multivariate analysis were a regular partner (P = 0.012) and illicit drug use (P = 0.006). High awareness of HIV (P b 0.001) and a previous HIV test (P = 0.001) were significant protective factors.
3. Results
4. Discussion
All 622 FSWs who worked in the 58 commercial sex establishments selected agreed to participate. Among the FSWs, 100 (16.1%) worked at
In the present study, the prevalences of HIV and HCV infections and syphilis among FSWs were high, whereas the rates of condom use
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Table 1 Demographic characteristics.a Characteristic Ethnic origin Han Zhuang Other Education levelb Primary school or below Middle school High school and above Age group, yb b25 25-30 30-40 ≥40 Marital status Single or regular sexual partner Married or cohabiting Separated or divorced Regular sexual partner a b
Level 1 (n = 100)
Level 2 (n = 210)
Level 3 (n = 312)
Total (n = 622)
χ2
P value
5.012 58 (58.0) 36 (36.0) 6 (6.0)
96 (45.7) 100 (47.6) 14 (6.7)
145 (46.5) 143 (45.8) 24 (7.7)
299 (48.1) 279 (44.9) 44 (7.1)
52 (52.0) 42 (42.0) 6 (6.0)
174 (82.9) 30 (14.3) 6 (2.9)
191 (61.2) 111 (35.6) 10 (3.2)
417 (67.0) 183 (29.4) 22 (3.5)
36 (36.0) 56 (56.0) 4 (4.0) 4 (4.0)
14 (6.7) 52 (24.8) 94 (44.8) 50 (23.8)
32 (10.3) 52 (16.7) 81 (26.0) 147 (47.1)
82 (13.2) 160 (25.7) 179 (28.8) 201 (32.3)
66 (66.0) 34 (34.0) 0 46 (46.0)
96 (45.7) 98 (46.7) 16 (7.6) 112 (53.3)
87 (27.9) 191 (61.2) 34 (10.9) 201 (64.4)
249 (40.0) 323 (51.9) 50 (8.0) 359 (57.7)
0.286
–
b0.001
–
b0.001
53.790
b0.001
13.029
0.001
χ2
P value
1.306 16.591 2.243 1.818 370.004
0.527 b0.001 0.326 0.403 b0.001
5.119
0.077 b0.001
2.531
0.282
Values are given as number (percentage) unless indicated otherwise. Tested by Fisher exact test.
Table 2 Prevalence of HIV, syphilis, and HCV infection, and patterns of condom use.a Variable
Level 1 (n = 100)
HIV Syphilis HCV History of STI Condom use during commercial sex in the past month Never Sometimes Often Always Did not use condom in the most recent commercial sex encounter Reason for not using condoms in the most recent commercial sex encounter b Refusal by clients Regular clients No condom available Other Did not use condom during most recent sex with regular partnerc
Level 2 (n = 210)
Level 3 (n = 312)
Total (n = 622)
1 (1.0) 8 (8.0) 4 (4.0) 6 (6.0)
1 (0.5) 10 (4.8) 14 (6.7) 6 (2.9)
5 (1.6) 49 (15.7) 26 (8.3) 14 (4.5)
7 (1.1) 67 (10.8) 44 (7.1) 26 (4.2)
6 (2.9) 14 (14.0) 10 (10.0) 76 (76.0) 14 (14.0)
15 (4.8) 16 (7.6) 30 (14.3) 158 (75.2) 24 (11.4)
21 (3.4) 23 (7.4) 96 (30.8) 178 (57.1) 58 (18.6)
53 (8.5) 136 (21.9) 412 (66.2) 96 (15.4) –
10 (71.4) 2 (14.3) 0 2 (14.3) 8 (17.4)
8 (33.3) 4 (16.7) 12 (50.0) 0 17 (15.2)
21 (36.2) 19 (32.8) 2 (3.4) 16 (27.6) 45 (22.4)
39 (40.6) 25 (26.0) 14 (14.6) 18 (18.8) 70 (19.5)
Abbreviations: HCV, hepatitis C virus; STI, sexually transmitted infection. a Values are given as number (percentage) unless indicated otherwise. b Tested by Fisher exact test. c The number of FSWs who had regular partner was 46 in level 1, 112 in level 2, and 201 in level 3.
were low. The prevalence of HIV infection among FSWs in Liuzhou (1.1%) is much higher than the national prevalence (0.04% in 2009) [14]. This finding is in line with that from other studies in Guangxi Table 3 Questions to assess participants’ HIV-related knowledge.a Questions
Correct answer (n = 622)
1. Can a person who looks healthy carry HIV? 2. Can a person be infected with HIV by transmitting blood or blood products? 3. Can a person be infected by HIV when sharing needles with HIV carriers? 4. Can condom use reduce the risk of HIV spread? 5. Can the risk of HIV spread be reduced by maintaining one sexual partner who does not have HIV infection? 6. Can pregnant women with HIV transmit the virus to their children? 7. Can HIV be transmitted by eating with HIV-positive individuals or patients with AIDS? 8. Can HIV be transmitted by mosquito bites?
391 (62.9) 529 (85.0)
a
Values are given as number (percentage).
511 (82.2) 500 (80.4) 481 (77.3) 524 (84.2) 441 (70.9) 282 (45.3)
Zhuang Autonomous Region [12,13]. However, the prevalence of HCV infection (7.1%) was higher than has been reported in other investigations in Guangxi (0.5%–0.92%) [15,16]. The syphilis prevalence (10.8%) was similar to previously reported values for the same region (5.33%–6.4%) [15,17]. Among the participants, those who worked in level 3 establishments were most likely to report inconsistent condom use. One possible explanation for this finding is that FSW from these establishments were older, less educated, and had less HIV-related knowledge than did those from other establishments. Alternatively, the fact that FSWs working in level 3 establishments had more clients each day could have meant they were less likely to report consistent condom use [18]. Condom use was less frequent during sex with regular partners than with clients. Again, the reason might be that a high proportion of FSWs with regular sexual partners worked in level 3 establishments and so were older and more likely to be married. Indeed, Reza-Paul et al. [19] found that married FSWs were less likely to use condoms in commercial sexual encounters. Therefore, FSWs with regular partners might be at increased risk of transmitting HIV or other STIs from their clients to their regular partners.
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Table 4 Illicit drug use and sexual behaviors.a Characteristic
Level 1 (n = 100)
Level 2 (n = 210)
Level 3 (n = 312)
Total (n = 622)
Illicit drug use Injected heroin previously Previous HIV test Age at first intercourse, y b14 14–18 18–22 ≥22 Time as a female sex worker, mo b6 6–12 12–24 ≥24 Number of establishments 1 2 3–5 ≥5 Average number of clients per day ≤1 2 ≥3
37 (37.0) 14 (14.0) 42 (42.0)
50 (23.8) 10 (4.8) 108 (51.4)
25 (8.0) 7 (2.2) 126 (40.4)
112 (18.0) 31 (5.0) 276 (44.4)
4 (4.0) 88 (88.0) 8 (8.0) 0
4 (1.9) 102 (48.6) 88 (41.9) 16 (7.6)
3 (1.0) 144 (46.2) 129 (41.3) 36 (11.5)
11 (1.8) 334 (53.7) 225 (36.2) 52 (8.4)
30 (30.0) 12 (12.0) 24 (24.0) 34 (34.0)
42 (20.0) 38 (18.1) 68 (32.4) 62 (29.5)
72 (23.1) 38 (12.2) 64 (20.5) 138 (44.2)
144 (23.2) 88 (14.1) 156 (25.1) 234 (37.6)
32 (32.0) 42 (42.0) 16 (16.0) 10 (10.0)
130 (61.9) 72 (34.3) 4 (1.9) 4 (1.9)
103 (33.0) 83 (26.6) 59 (18.9) 67 (21.5)
265 (42.6) 197 (31.7) 79 (12.7) 81 (13.0)
79 (79.0) 21 (21.0) 0
118 (56.2) 36 (17.1) 56 (26.7)
85 (27.2) 93 (29.8) 134 (42.9)
282 (45.3) 150 (24.1) 190 (30.5)
a
χ2
P value
50.330 22.135 6.474 68.659
b0.001 b0.001 0.039 b0.001
21.157
b0.001
101.438
b0.001
109.099
b0.001
Values are given as number (percentage) unless indicated otherwise.
As previous studies [20,21] have revealed, inconsistent condom use is related to poor knowledge about HIV. The present study found that FSWs with high HIV awareness were more likely to use condoms during commercial sex encounters. The proportion of FSWs with high awareness was lowest at level 3 establishments, where individuals were more likely to be older and have received less education. In addition, FSWs who had ever had an HIV test were more likely to report consistent condom use
during commercial sex encounters, which should encourage a broadening of HIV testing among FSWs and other high-risk populations. The association between inconsistent condom use and illicit drug use is well documented [22]. The present study confirmed this association, with a 2.10-fold increase in risk among FSWs who reported illicit drug use. These FSWs might want to earn more money from clients so they can buy illicit drugs, which would reduce their ability to negotiate
Table 5 Univariate and multivariate logistic regression model for inconsistent condom use. Variable
Univariate analysis P value
Level of establishment 1 2 3 Marital status Single Married or cohabiting Separated or divorced Ethnic origin Han Zhuang Other High awareness of HIV No Yes Self-awareness of HIV-related knowledge None A little Some A lot Self-awareness of risk of HIV infection Very likely Likely Unlikely Very unlikely Regular partner No Yes Illicit drug use No Yes Previous HIV test No Yes Abbreviations: OR, odds ratio; CI, confidence interval.
Multivariate analysis OR (95% CI)
P value
OR (95% CI)
0.884 0.002
1.00 1.04 (0.60–1.82) 2.23 (1.34–3.72)
0.968 0.045
1.00 0.99 (0.53–1.84) 1.85 (1.02–3.39)
0.002 0.079
1.00 1.76 (1.22–2.52) 1.72 (0.94–3.35)
– – –
– – –
b0.001 0.246
1.00 1.96 (1.38–2.79) 1.49 (0.76–2.93)
– – –
– – –
b0.001
1.00 0.32 (0.22–0.46)
b0.001
1.00 0.29 (0.18–0.48)
0.187 0.014 0.976
1.00 1.72 (0.77–3.86) 2.86 (1.24–6.58) 1.02 (0.29–3.58)
– – – –
– – – –
0.027 0.078 0.267
1.00 5.60 (1.22–25.66) 3.83 (0.86–16.98) 2.39 (0.51–11.08)
– – – –
– – – –
0.004
1.00 1.66 (1.18–2.35)
0.012
1.00 1.65 (1.12–2.45)
0.045
1.00 1.54 (1.01–2.34)
0.006
1.00 2.10 (1.24–3.54)
b0.001
1.00 0.43 (0.30–0.61)
0.001
1.00 0.51 (0.34–0.76)
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safe sex with the clients. In addition, illicit drugs may influence FSWs’ ability to practice safe sex [23]. The present study has several limitations. First, because commercial sex work is illegal in China, it was not possible to randomly select FSWs. The participants were recruited by a convenience method according to a map of commercial sex establishments, and all the FSWs surveyed were from one city. Therefore, generalizability is limited and the findings might not be applicable elsewhere. Second, sexual behavior is a sensitive topic in China and is not often discussed. Thus, during the survey, it is possible that some participants may have under-reported commercial sex and other risk behaviors. Finally, like all other community-based studies, the findings are subject to volunteer and social desirability biases [24]. Although the prevalence of HIV infection was not very high among FSWs in Liuzhou, the prevalence of STIs and poor condom use suggest that HIV could spread rapidly in this group. Prevention strategies have already been established for FSWs—e.g. the “100% condom” campaign, peer education, and voluntary counseling and testing—but more education programs targeting this group are urgently needed and present programs should be further strengthened. Furthermore, more attention should be paid to the FSWs who work in a lower level of establishment, use illicit drugs, and have a regular partner. Effective monitoring and new interventions are urgently needed to prevent the spread of HIV/AIDS from FSWs to the general population in China. Acknowledgments
[4]
[5] [6] [7]
[8]
[9]
[10]
[11] [12] [13] [14] [15]
[16] [17]
This study was funded by The Global Fund to Fight AIDS (CSO2012-21) and the program of technical support for Liuzhou, which was authorized by the Chinese National Center for AIDS/STD Control and Prevention.
[18]
[19]
Conflict of interest [20]
The authors have no conflicts of interest. [21]
References [22] [1] China Ministry of Health UNAIDS, UNAIDS, World Health Organization. Estimates for the HIV/AIDS Epidemic in China. http://www.moh.gov.cn/cmsresources/mohyzs/ cmsrsdocument/doc13944.pdf; 2011. Published 2011. Accessed August 21, 2014. [2] Zhao J, Song F, Ren S, Wang Y, Wang L, Liu W, et al. Predictors of condom use behaviors based on the Health Belief Model (HBM) among female sex workers: a crosssectional study in Hubei Province, China. PLoS One 2012;7(11):e49542. [3] Zhou Y, Li X, Zhang C, Tan G, Stanton B, Zhang X, et al. Rates of HIV, syphilis, and HCV infections among different demographic groups of female sex workers in Guangxi
[23]
[24]
China: evidence from 2010 national sentinel surveillance data. AIDS Care 2013; 25(11):1433–41. Yang C, Latkin C, Luan R, Wang C, Nelson K. HIV, syphilis, hepatitis C and risk behaviours among commercial sex male clients in Sichuan province, China. Sex Transm Infect 2010;86(7):559–64. Hong Y, Li X. Behavioral studies of female sex workers in China: a literature review and recommendation for future research. AIDS Behav 2008;12(4):623–36. Nguyen NT, Nguyen HT, Trinh HQ, Mills SJ, Detels R. Clients of female sex workers as a bridging population in Vietnam. AIDS Behav 2009;13(5):881–91. Wang L, Wang N, Wang L, Li D, Jia M, 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(4):414–8. Wang H, Wang N, Chen RY, Sharp GB, Ma Y, Wang G, et al. Prevalence and predictors of herpes simplex virus type 2 infection among female sex workers in Yunnan Province, China. Int J STD AIDS 2008;19(9):635–9. Wang H, Wang N, Bi A, Wang G, Ding G, Jia M, et al. Application of cumulative odds logistic model on risk factors analysis for sexually transmitted infections among female sex workers in Kaiyuan city, Yunnan province, China. Sex Transm Infect 2009;85(4):290–5. Guangxi Center for Disease Control, Prevention (Guangxi CDC). Update on HIV/AIDS epidemic in Guangxi. Workshop of NIAA A venue-based HIV and alcohol risk reduction among female sex workers in China; July 19–21, 2009. Guilin, Guangxi, China. Feng X, Li M, Pan J, Liu J. Analysis on the epidemic characteristics of HIV/AIDS in Liuzhou from 1996 to 2010. Med Pest Control 2011;27(10):921–3. Zhang Y, Lin H, Feng W, Shan G, Zhang T. Syphilis and HIV infection status among commercial sexual workers in Liuzhou, Guangxi. J Trop Med 2011;11(3):337–9. Bai Y, Weng Y, Feng W. Sentinel Surveillance of AIDS in Liuzhou, 2008. Prev Med Inf 2010;26(7):527–30. Fu S, Sun L, Meng X, Ding Z, Wang L. Surveillance of AIDS among female sex workers in China, 1995–2009. Dis Surveill 2010;25(11):850–3. Lin R, Quan X, Ye R, Huang Z, Ning J. Investigation on core indicator of behavioral surveillance among female sex workers in Yulin, 2009–2011. Chin Trop Med 2012; 12(6):700–24. Bai Y, Zhang J, Ouyang Y. Analysis on monitoring results of AIDS among female sexual workers in Liuzhou City in 2010. Med Pest Control 2012;28(9):964–6. Qin W, Liu H, Fengxiang L, Huang C, Zhou F. Sentinel surveillance of syphilis in female sex workers in Nanning city, 2007–2009. Dis Surveill 2011;26(2):106–9. Huang Y, Henderson GE, Pan S. Cohen MS.HIV/AIDS risk among brothel-based female sex workers in China: assessing the terms, content, and knowledge of sex work. Sex Transm Dis 2004;31(11):695–700. Reza-Paul S, Beattie T, Syed HU, Venukumar KT, Venugopal MS, Fathima MP, et al. Declines in risk behaviour and sexually transmitted infection prevalence following a community-led HIV preventive intervention among female sex workers in Mysore, India. AIDS 2008;22(Suppl. 5):S91–S100. Jung M, Arya M, Viswanath K. Effect of media use on HIV/AIDS-related knowledge and condom use in sub-Saharan Africa: a cross-sectional study. PLoS One 2013; 8(7):e68359. Vian T, Semrau K, Hamer DH, Loan le TT, Sabin LL. HIV/AIDS-Related Knowledge and Behaviors Among Most-at-Risk Populations in Vietnam. Open AIDS J 2012;6:259–65. Chen Y, Li X, Zhou Y, Wen X, Wu D. Perceived peer engagement in HIV-related sexual risk behaviors and self-reported risk-taking among female sex workers in Guangxi, China. AIDS Care 2013;25(9):1114–21. Wang B, Li X, Stanton B, Zhang L, Fang X. Alcohol use, unprotected sex, and sexually transmitted infections among female sex workers in China. Sex Transm Dis 2010; 37(10):629–36. Hong Y, Zhang C, Li X, Fang X, Lin X, Zhou Y, et al. HIV testing behaviors among female sex workers in Southwest China. AIDS Behav 2012;16(1):44–52.
Contents lists available at ScienceDirect
International Journal of Gynecology and Obstetrics journal homepage: www.elsevier.com/locate/ijgo
CLINICAL ARTICLE
HIV, other sexually transmitted infections, and risk behaviors among female sex workers in Liuzhou, China Yin-Guang Fan a,1, Jin-Ji Liu b,1, Yu-Jing Zhang a, Se-Ying Dai a, Ming-Qiang Li b, Dong-Qing Ye a,⁎ a b
Department of Epidemiology and Biostatistics, School of Public Health, Anhui Medical University, Hefei, China Liuzhou Center for Disease Control and Prevention, Liuzhou, China
a r t i c l e
i n f o
Article history: Received 8 January 2014 Received in revised form 9 July 2014 Accepted 27 August 2014 Keywords: Female sex worker Hepatitis C HIV Risk behavior Syphilis
a b s t r a c t Objective: To determine the prevalence of infections with HIV and hepatitis C virus (HCV), and of syphilis among female sex workers (FSWs) in Liuzhou, China, along with levels of HIV-related knowledge and frequencies of risk behaviors. Methods: A cross-sectional survey was conducted between July 2012 and January 2013. FSWs (aged ≥16 years; reported receiving payment for sex in previous 6 months) working at 58 selected commercial sex establishments (level 1 [N¥300 per transaction], level 2 [¥100–300], or level 3 [b¥100]) completed a questionnaire and provided blood samples for testing. Results: Of 622 participating FSWs, 7 (1.1%) had HIV infection, 67 (10.8%) syphilis, and 44 (7.1%) HCV infection. Consistent condom use during commercial sex encounters in the past month was reported by 412 (66.2%) FSWs. Inconsistent condom use was most likely in FSWs working in level 3 establishments (odds ratio [OR] 1.85; 95% CI 1.02–3.39), with a regular partner (OR 1.65; 95% CI 1.12–2.45), and who used illicit drugs (OR 2.10; 95% CI 1.24–3.54). Inconsistent condom use was least likely in FSWs with high HIV awareness (OR 0.29; 95% CI 0.18–0.48) and who had had a previous HIV test (OR 0.51; 95% CI 0.34–0.76). Conclusion: Further prioritized and combined programs aimed at FSWs are needed to prevent HIV transmission in China. © 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
1. Introduction In China, the annual reported number of individuals living with HIV/AIDS has been increasing, reaching 780 000 in 2011 [1]. Injecting drug use was the most common mode of infection until 2007, when heterosexual contact became the main transmission mode [1,2], the proportion of cases resulting from heterosexual transmission increased from 11.3% in 2005 to 38.9% in 2007 and 76.3% in 2011 [3]. How to prevent further sexual transmission is the great challenge in the control of the HIV epidemic in China. Since the Chinese economic reform began in the 1980s, sexually transmitted infections (STIs) have re-emerged [4]. In the same period, the number of female sex workers (FSWs) has grown, with the figure reaching 4–10 million by 2004 [4,5]. FSWs are vulnerable to HIV and STIs, their rates of infection are higher than are those of the general population [6]. In 2009, government estimates suggested that 0.33%–0.94% of FSWs were living with HIV [7], but the prevalence has been as high as 8.3%–10.3% [8,9]. In one study in Yunnan [9], 4.8%–53.2% of FSWs
reported having had STIs in the past, and 13.0%–90.6% tested positive for at least one STI. Guangxi Zhuang Autonomous Region is located in South Central China. The HIV prevalence in this region is the second highest among the 31 provinces of mainland China [10]. Liuzhou is a city in the north of Guangxi, with a population of 3.7 million. Commercial sex trade flourishes in the city because the economy has been growing in recent years. By the end of 2010, 9982 people in Liuzhou were living with HIV/AIDS [11]. According to a report from the Chinese Ministry of Health [1], Guangxi Zhuang Autonomous Region is one of five provinces where more than 1% of FSWs are living with HIV. However, no FSWs tested in one study in Liuzhou [12] were HIV positive, and the prevalence was 0.5% in another investigation [13]. The aim of the present study was to determine the prevalence of infections with HIV and hepatitis C virus (HCV), and syphilis among FSWs in Liuzhou. A secondary aim was to identify the risk factors associated with inconsistent use of condoms.
2. Materials and methods ⁎ Corresponding author at: Department of Epidemiology and Biostatistics, School of Public Health, Anhui Medical University, 81 Meishan Road, Hefei, Anhui, 230032, China. Tel.: +86 551 65167726; fax: +86 551 65161171. E-mail address: [email protected] (D.-Q. Ye). 1 These authors contributed equally.
A cross-sectional study was conducted between July 1, 2012, and January 4, 2013. FSWs aged at least 16 years who reported receiving payment for sex in the previous 6 months were eligible for inclusion. Participants had to be willing to undergo testing and HIV/STI counseling.
http://dx.doi.org/10.1016/j.ijgo.2014.07.024 0020-7292/© 2014 International Federation of Gynecology and Obstetrics. Published by Elsevier Ireland Ltd. All rights reserved.
Y.-G. Fan et al. / International Journal of Gynecology and Obstetrics 128 (2015) 18–22
19
The study protocol was approved by the ethics committee of Anhui Medical University. All participants provided informed consent. Participants were recruited using multistage sampling methods. Liuzhou has one urban district and five counties. To enable an assessment of STIs in both urban and rural areas, the urban district and one county were selected for inclusion. Liujiang County was randomly selected using a simple random sampling method. The sampling scheme was based on the map of commercial sex establishments maintained by the Liuzhou Center for Disease Control and Prevention (CDC) and Liujiang CDC, and all the sexual establishments in the map were identified by a pilot study. The identified sex establishments in the two areas were categorized into three levels according to the mean income of FSWs per transaction: at level 1 establishments, more than 300 Yuan were earned per transaction (e.g. bars, saunas, nightclubs, and karaoke bars); at level 2 establishments, 100–300 Yuan were earned per transaction (e.g. massage parlors and hair salons); and at level 3 establishments, less than 100 Yuan were earned per transaction (e.g. restaurants and inns). A sample of 10% of the establishments in each level was used: three level 1, 11 level 2, and 44 level 3 establishments were selected by local outreach workers by convenience sampling. An anonymous questionnaire was developed and validated in a pilot study of 15 FSWs. The questionnaire consisted of three parts: demographic information, HIV-related knowledge, and sexual and HIV risk behaviors. HIV-related knowledge was evaluated by eight questions, to which participants needed to answer yes or no. Participants who gave at least six correct answers were deemed to have high awareness. They were also asked to rate their HIV-related knowledge (none, little, some, and a lot) and their risk of HIV infection (very likely, likely, unlikely and very unlikely). A regular sexual partner was defined as a man who was not a client and with whom the FSW had sexual contact, such as a boyfriend or husband. The survey was conducted face-toface by an interviewer in a private room. Approximately 10–15 minutes were needed to complete each questionnaire. Blood samples (3 mL from the median cubital vein) were obtained from FSWs by qualified doctors after the questionnaire was completed. The samples were tested in the Laboratory Department of Liuzhou CDC. They were screened for HIV antibodies by enzyme-linked immunosorbent assay (ELISA; Beijing Modern Gaoda Biotechnology Co, Beijing, China) and positive tests were confirmed by a HIV-1 western blot (Diagnostics HIV Blot 2.2, Genelabs, Singapore). Participants who had HIV infection were referred to their local CDC. Syphilis was detected by a rapid plasma reagin test (Xindi Biological Pharmaceutical Engineering Co., Nanjing, China) and positive tests were confirmed by Treponema pallidum particle agglutination assay (Beijing Modern Gaoda Biotechnology Co, Beijing, China). The presence of antiHCV antibody was detected by ELISA. FSWs who had syphilis or HCV infection were referred to the infectious diseases outpatient clinics of local hospitals. Data were entered into a database twice and matched using EpiData 3.1 (The EpiData Association, Odense, Denmark). Analysis was done using SPSS 10.01 (SPSS Inc, Chicago, IL, USA). Differences between FSWs at the three levels were assessed by univariate analysis. The χ2 test and linear-by-linear association test (trend tests) were used for proportional variables, and Fisher exact tests were used for contingency tables when more than 20% of the cells had expected counts less than five or one cell had an expected count of less than one. The one-way analysis of variance test was used for continuous variables. Independent risk factors of inconsistent condom use were assessed using logistic regression analysis. Variables significant in the univariate analysis were included in a multivariate model. All testing was twosided, and P ≤ 0.05 was considered statistically significant.
level 1 establishments, 210 (33.8%) at level 2 establishments, and 312 (50.2%) at level 3 establishments. A total of 535 (86.0%) FSWs came from Guangxi. Most were of Han or Zhuang ethnic origin (Table 1). Few respondents had attended high school, and most were older than 25 years. Age increased with level (trend test χ2 = 106.641; P b 0.001), as did the proportion of FSWs who were married or cohabiting (trend test χ2 = 217.699; P b 0.001). A regular sexual partner was reported by 359 (57.7%) FSWs. The proportion reporting a regular sexual partner increased with the level of establishment (Table 1), and the trend was significant (trend test χ2 = 12.829; P b 0.001). Of the 622 participants, 7 (1.1%) were identified as HIV positive (Table 2). Only 26 (4.2%) participants reported that they had had an STI in the past year, but the screening showed that 67 (10.8%) had syphilis and 44 (7.1%) were positive for HCV antibodies. The proportion of FSWs with each of the infections was highest in level 3 establishments, but the difference was significant only for syphilis (P b 0.001) (Table 2). Sixteen (2.6%) FSWs had syphilis and HCV infection, and 2 (0.3%) had syphilis and HIV infection. Among the 67 participants who tested positive for syphilis, 60 (89.6%) reported that they had never had an STI. Consistent condom use during commercial sex encounters in the past month was reported by 412 (66.2%) FSWs. Only 178 (57.1%) FSWs from level 3 establishments reported always using a condom. Overall, 21 (3.4%) FSWs overall reported never using condoms. A total of 96 (15.4%) had not used a condom in the most recent commercial sex encounter. The most common reasons for not using condoms were refusal by clients and regular clients (Table 2). Among the 359 FSWs who had regular partners, 70 (19.5%) had not used a condom during the most recent sex with their partner. This proportion is a little higher than that of FSW who did not use a condom with clients, but the difference was not significant (χ2 = 2.675; P = 0.102). Table 3 shows the proportions of FSWs who responded correctly to each of the eight HIV-related knowledge questions. Overall, 442 (71.1%) participants got at least six correct answers. There was a significant difference in awareness among the three levels: 88 (88.0%) of 100 FSWs from level 1 establishments answered correctly at least six times compared with 162 (77.1%) of 210 from level 2 and 192 (61.5%) of 312 from level 3 establishments (χ2 = 31.488; P b 0.001). The proportion of FSWs with high awareness decreased as the level of establishment increased (trend test χ2 = 31.098; P b 0.001). Some participants (194, 31.2%) thought that they knew only a little about HIV. Of the 24 FSWs who reported a high degree of HIV-related knowledge, only four (16.7%) answered correctly to at least six of the HIV-related questions. A total of 501 (80.5%) FSWs thought that they were unlikely to have been infected with HIV. Use of illicit drugs was reported by 112 (18.0%), of whom 31 (27.7%) had injected heroin previously. Approximately 45% of participants had undergone HIV testing previously (Table 4). First intercourse when younger than 18 years was reported by 345 (55.5%) FSWs. Overall, 390 (62.7%) participants had worked as a FSW for more than 12 months, and 357 (57.4%) had worked in more than one establishment. More than one client per day on average was reported by 340 (54.7%) FSWs, and 190 (30.5%) had three or more clients daily (Table 4). Significant variables in the univariate analysis were entered into the multivariate logistic regression model for inconsistent condom use (Table 5). Inconsistent condom use was significantly more likely in FSWs working in level 3 establishments than in those working in level 1 establishments (P = 0.045). Other significant risk factors in the multivariate analysis were a regular partner (P = 0.012) and illicit drug use (P = 0.006). High awareness of HIV (P b 0.001) and a previous HIV test (P = 0.001) were significant protective factors.
3. Results
4. Discussion
All 622 FSWs who worked in the 58 commercial sex establishments selected agreed to participate. Among the FSWs, 100 (16.1%) worked at
In the present study, the prevalences of HIV and HCV infections and syphilis among FSWs were high, whereas the rates of condom use
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Table 1 Demographic characteristics.a Characteristic Ethnic origin Han Zhuang Other Education levelb Primary school or below Middle school High school and above Age group, yb b25 25-30 30-40 ≥40 Marital status Single or regular sexual partner Married or cohabiting Separated or divorced Regular sexual partner a b
Level 1 (n = 100)
Level 2 (n = 210)
Level 3 (n = 312)
Total (n = 622)
χ2
P value
5.012 58 (58.0) 36 (36.0) 6 (6.0)
96 (45.7) 100 (47.6) 14 (6.7)
145 (46.5) 143 (45.8) 24 (7.7)
299 (48.1) 279 (44.9) 44 (7.1)
52 (52.0) 42 (42.0) 6 (6.0)
174 (82.9) 30 (14.3) 6 (2.9)
191 (61.2) 111 (35.6) 10 (3.2)
417 (67.0) 183 (29.4) 22 (3.5)
36 (36.0) 56 (56.0) 4 (4.0) 4 (4.0)
14 (6.7) 52 (24.8) 94 (44.8) 50 (23.8)
32 (10.3) 52 (16.7) 81 (26.0) 147 (47.1)
82 (13.2) 160 (25.7) 179 (28.8) 201 (32.3)
66 (66.0) 34 (34.0) 0 46 (46.0)
96 (45.7) 98 (46.7) 16 (7.6) 112 (53.3)
87 (27.9) 191 (61.2) 34 (10.9) 201 (64.4)
249 (40.0) 323 (51.9) 50 (8.0) 359 (57.7)
0.286
–
b0.001
–
b0.001
53.790
b0.001
13.029
0.001
χ2
P value
1.306 16.591 2.243 1.818 370.004
0.527 b0.001 0.326 0.403 b0.001
5.119
0.077 b0.001
2.531
0.282
Values are given as number (percentage) unless indicated otherwise. Tested by Fisher exact test.
Table 2 Prevalence of HIV, syphilis, and HCV infection, and patterns of condom use.a Variable
Level 1 (n = 100)
HIV Syphilis HCV History of STI Condom use during commercial sex in the past month Never Sometimes Often Always Did not use condom in the most recent commercial sex encounter Reason for not using condoms in the most recent commercial sex encounter b Refusal by clients Regular clients No condom available Other Did not use condom during most recent sex with regular partnerc
Level 2 (n = 210)
Level 3 (n = 312)
Total (n = 622)
1 (1.0) 8 (8.0) 4 (4.0) 6 (6.0)
1 (0.5) 10 (4.8) 14 (6.7) 6 (2.9)
5 (1.6) 49 (15.7) 26 (8.3) 14 (4.5)
7 (1.1) 67 (10.8) 44 (7.1) 26 (4.2)
6 (2.9) 14 (14.0) 10 (10.0) 76 (76.0) 14 (14.0)
15 (4.8) 16 (7.6) 30 (14.3) 158 (75.2) 24 (11.4)
21 (3.4) 23 (7.4) 96 (30.8) 178 (57.1) 58 (18.6)
53 (8.5) 136 (21.9) 412 (66.2) 96 (15.4) –
10 (71.4) 2 (14.3) 0 2 (14.3) 8 (17.4)
8 (33.3) 4 (16.7) 12 (50.0) 0 17 (15.2)
21 (36.2) 19 (32.8) 2 (3.4) 16 (27.6) 45 (22.4)
39 (40.6) 25 (26.0) 14 (14.6) 18 (18.8) 70 (19.5)
Abbreviations: HCV, hepatitis C virus; STI, sexually transmitted infection. a Values are given as number (percentage) unless indicated otherwise. b Tested by Fisher exact test. c The number of FSWs who had regular partner was 46 in level 1, 112 in level 2, and 201 in level 3.
were low. The prevalence of HIV infection among FSWs in Liuzhou (1.1%) is much higher than the national prevalence (0.04% in 2009) [14]. This finding is in line with that from other studies in Guangxi Table 3 Questions to assess participants’ HIV-related knowledge.a Questions
Correct answer (n = 622)
1. Can a person who looks healthy carry HIV? 2. Can a person be infected with HIV by transmitting blood or blood products? 3. Can a person be infected by HIV when sharing needles with HIV carriers? 4. Can condom use reduce the risk of HIV spread? 5. Can the risk of HIV spread be reduced by maintaining one sexual partner who does not have HIV infection? 6. Can pregnant women with HIV transmit the virus to their children? 7. Can HIV be transmitted by eating with HIV-positive individuals or patients with AIDS? 8. Can HIV be transmitted by mosquito bites?
391 (62.9) 529 (85.0)
a
Values are given as number (percentage).
511 (82.2) 500 (80.4) 481 (77.3) 524 (84.2) 441 (70.9) 282 (45.3)
Zhuang Autonomous Region [12,13]. However, the prevalence of HCV infection (7.1%) was higher than has been reported in other investigations in Guangxi (0.5%–0.92%) [15,16]. The syphilis prevalence (10.8%) was similar to previously reported values for the same region (5.33%–6.4%) [15,17]. Among the participants, those who worked in level 3 establishments were most likely to report inconsistent condom use. One possible explanation for this finding is that FSW from these establishments were older, less educated, and had less HIV-related knowledge than did those from other establishments. Alternatively, the fact that FSWs working in level 3 establishments had more clients each day could have meant they were less likely to report consistent condom use [18]. Condom use was less frequent during sex with regular partners than with clients. Again, the reason might be that a high proportion of FSWs with regular sexual partners worked in level 3 establishments and so were older and more likely to be married. Indeed, Reza-Paul et al. [19] found that married FSWs were less likely to use condoms in commercial sexual encounters. Therefore, FSWs with regular partners might be at increased risk of transmitting HIV or other STIs from their clients to their regular partners.
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Table 4 Illicit drug use and sexual behaviors.a Characteristic
Level 1 (n = 100)
Level 2 (n = 210)
Level 3 (n = 312)
Total (n = 622)
Illicit drug use Injected heroin previously Previous HIV test Age at first intercourse, y b14 14–18 18–22 ≥22 Time as a female sex worker, mo b6 6–12 12–24 ≥24 Number of establishments 1 2 3–5 ≥5 Average number of clients per day ≤1 2 ≥3
37 (37.0) 14 (14.0) 42 (42.0)
50 (23.8) 10 (4.8) 108 (51.4)
25 (8.0) 7 (2.2) 126 (40.4)
112 (18.0) 31 (5.0) 276 (44.4)
4 (4.0) 88 (88.0) 8 (8.0) 0
4 (1.9) 102 (48.6) 88 (41.9) 16 (7.6)
3 (1.0) 144 (46.2) 129 (41.3) 36 (11.5)
11 (1.8) 334 (53.7) 225 (36.2) 52 (8.4)
30 (30.0) 12 (12.0) 24 (24.0) 34 (34.0)
42 (20.0) 38 (18.1) 68 (32.4) 62 (29.5)
72 (23.1) 38 (12.2) 64 (20.5) 138 (44.2)
144 (23.2) 88 (14.1) 156 (25.1) 234 (37.6)
32 (32.0) 42 (42.0) 16 (16.0) 10 (10.0)
130 (61.9) 72 (34.3) 4 (1.9) 4 (1.9)
103 (33.0) 83 (26.6) 59 (18.9) 67 (21.5)
265 (42.6) 197 (31.7) 79 (12.7) 81 (13.0)
79 (79.0) 21 (21.0) 0
118 (56.2) 36 (17.1) 56 (26.7)
85 (27.2) 93 (29.8) 134 (42.9)
282 (45.3) 150 (24.1) 190 (30.5)
a
χ2
P value
50.330 22.135 6.474 68.659
b0.001 b0.001 0.039 b0.001
21.157
b0.001
101.438
b0.001
109.099
b0.001
Values are given as number (percentage) unless indicated otherwise.
As previous studies [20,21] have revealed, inconsistent condom use is related to poor knowledge about HIV. The present study found that FSWs with high HIV awareness were more likely to use condoms during commercial sex encounters. The proportion of FSWs with high awareness was lowest at level 3 establishments, where individuals were more likely to be older and have received less education. In addition, FSWs who had ever had an HIV test were more likely to report consistent condom use
during commercial sex encounters, which should encourage a broadening of HIV testing among FSWs and other high-risk populations. The association between inconsistent condom use and illicit drug use is well documented [22]. The present study confirmed this association, with a 2.10-fold increase in risk among FSWs who reported illicit drug use. These FSWs might want to earn more money from clients so they can buy illicit drugs, which would reduce their ability to negotiate
Table 5 Univariate and multivariate logistic regression model for inconsistent condom use. Variable
Univariate analysis P value
Level of establishment 1 2 3 Marital status Single Married or cohabiting Separated or divorced Ethnic origin Han Zhuang Other High awareness of HIV No Yes Self-awareness of HIV-related knowledge None A little Some A lot Self-awareness of risk of HIV infection Very likely Likely Unlikely Very unlikely Regular partner No Yes Illicit drug use No Yes Previous HIV test No Yes Abbreviations: OR, odds ratio; CI, confidence interval.
Multivariate analysis OR (95% CI)
P value
OR (95% CI)
0.884 0.002
1.00 1.04 (0.60–1.82) 2.23 (1.34–3.72)
0.968 0.045
1.00 0.99 (0.53–1.84) 1.85 (1.02–3.39)
0.002 0.079
1.00 1.76 (1.22–2.52) 1.72 (0.94–3.35)
– – –
– – –
b0.001 0.246
1.00 1.96 (1.38–2.79) 1.49 (0.76–2.93)
– – –
– – –
b0.001
1.00 0.32 (0.22–0.46)
b0.001
1.00 0.29 (0.18–0.48)
0.187 0.014 0.976
1.00 1.72 (0.77–3.86) 2.86 (1.24–6.58) 1.02 (0.29–3.58)
– – – –
– – – –
0.027 0.078 0.267
1.00 5.60 (1.22–25.66) 3.83 (0.86–16.98) 2.39 (0.51–11.08)
– – – –
– – – –
0.004
1.00 1.66 (1.18–2.35)
0.012
1.00 1.65 (1.12–2.45)
0.045
1.00 1.54 (1.01–2.34)
0.006
1.00 2.10 (1.24–3.54)
b0.001
1.00 0.43 (0.30–0.61)
0.001
1.00 0.51 (0.34–0.76)
22
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safe sex with the clients. In addition, illicit drugs may influence FSWs’ ability to practice safe sex [23]. The present study has several limitations. First, because commercial sex work is illegal in China, it was not possible to randomly select FSWs. The participants were recruited by a convenience method according to a map of commercial sex establishments, and all the FSWs surveyed were from one city. Therefore, generalizability is limited and the findings might not be applicable elsewhere. Second, sexual behavior is a sensitive topic in China and is not often discussed. Thus, during the survey, it is possible that some participants may have under-reported commercial sex and other risk behaviors. Finally, like all other community-based studies, the findings are subject to volunteer and social desirability biases [24]. Although the prevalence of HIV infection was not very high among FSWs in Liuzhou, the prevalence of STIs and poor condom use suggest that HIV could spread rapidly in this group. Prevention strategies have already been established for FSWs—e.g. the “100% condom” campaign, peer education, and voluntary counseling and testing—but more education programs targeting this group are urgently needed and present programs should be further strengthened. Furthermore, more attention should be paid to the FSWs who work in a lower level of establishment, use illicit drugs, and have a regular partner. Effective monitoring and new interventions are urgently needed to prevent the spread of HIV/AIDS from FSWs to the general population in China. Acknowledgments
[4]
[5] [6] [7]
[8]
[9]
[10]
[11] [12] [13] [14] [15]
[16] [17]
This study was funded by The Global Fund to Fight AIDS (CSO2012-21) and the program of technical support for Liuzhou, which was authorized by the Chinese National Center for AIDS/STD Control and Prevention.
[18]
[19]
Conflict of interest [20]
The authors have no conflicts of interest. [21]
References [22] [1] China Ministry of Health UNAIDS, UNAIDS, World Health Organization. Estimates for the HIV/AIDS Epidemic in China. http://www.moh.gov.cn/cmsresources/mohyzs/ cmsrsdocument/doc13944.pdf; 2011. Published 2011. Accessed August 21, 2014. [2] Zhao J, Song F, Ren S, Wang Y, Wang L, Liu W, et al. Predictors of condom use behaviors based on the Health Belief Model (HBM) among female sex workers: a crosssectional study in Hubei Province, China. PLoS One 2012;7(11):e49542. [3] Zhou Y, Li X, Zhang C, Tan G, Stanton B, Zhang X, et al. Rates of HIV, syphilis, and HCV infections among different demographic groups of female sex workers in Guangxi
[23]
[24]
China: evidence from 2010 national sentinel surveillance data. AIDS Care 2013; 25(11):1433–41. Yang C, Latkin C, Luan R, Wang C, Nelson K. HIV, syphilis, hepatitis C and risk behaviours among commercial sex male clients in Sichuan province, China. Sex Transm Infect 2010;86(7):559–64. Hong Y, Li X. Behavioral studies of female sex workers in China: a literature review and recommendation for future research. AIDS Behav 2008;12(4):623–36. Nguyen NT, Nguyen HT, Trinh HQ, Mills SJ, Detels R. Clients of female sex workers as a bridging population in Vietnam. AIDS Behav 2009;13(5):881–91. Wang L, Wang N, Wang L, Li D, Jia M, 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(4):414–8. Wang H, Wang N, Chen RY, Sharp GB, Ma Y, Wang G, et al. Prevalence and predictors of herpes simplex virus type 2 infection among female sex workers in Yunnan Province, China. Int J STD AIDS 2008;19(9):635–9. Wang H, Wang N, Bi A, Wang G, Ding G, Jia M, et al. Application of cumulative odds logistic model on risk factors analysis for sexually transmitted infections among female sex workers in Kaiyuan city, Yunnan province, China. Sex Transm Infect 2009;85(4):290–5. Guangxi Center for Disease Control, Prevention (Guangxi CDC). Update on HIV/AIDS epidemic in Guangxi. Workshop of NIAA A venue-based HIV and alcohol risk reduction among female sex workers in China; July 19–21, 2009. Guilin, Guangxi, China. Feng X, Li M, Pan J, Liu J. Analysis on the epidemic characteristics of HIV/AIDS in Liuzhou from 1996 to 2010. Med Pest Control 2011;27(10):921–3. Zhang Y, Lin H, Feng W, Shan G, Zhang T. Syphilis and HIV infection status among commercial sexual workers in Liuzhou, Guangxi. J Trop Med 2011;11(3):337–9. Bai Y, Weng Y, Feng W. Sentinel Surveillance of AIDS in Liuzhou, 2008. Prev Med Inf 2010;26(7):527–30. Fu S, Sun L, Meng X, Ding Z, Wang L. Surveillance of AIDS among female sex workers in China, 1995–2009. Dis Surveill 2010;25(11):850–3. Lin R, Quan X, Ye R, Huang Z, Ning J. Investigation on core indicator of behavioral surveillance among female sex workers in Yulin, 2009–2011. Chin Trop Med 2012; 12(6):700–24. Bai Y, Zhang J, Ouyang Y. Analysis on monitoring results of AIDS among female sexual workers in Liuzhou City in 2010. Med Pest Control 2012;28(9):964–6. Qin W, Liu H, Fengxiang L, Huang C, Zhou F. Sentinel surveillance of syphilis in female sex workers in Nanning city, 2007–2009. Dis Surveill 2011;26(2):106–9. Huang Y, Henderson GE, Pan S. Cohen MS.HIV/AIDS risk among brothel-based female sex workers in China: assessing the terms, content, and knowledge of sex work. Sex Transm Dis 2004;31(11):695–700. Reza-Paul S, Beattie T, Syed HU, Venukumar KT, Venugopal MS, Fathima MP, et al. Declines in risk behaviour and sexually transmitted infection prevalence following a community-led HIV preventive intervention among female sex workers in Mysore, India. AIDS 2008;22(Suppl. 5):S91–S100. Jung M, Arya M, Viswanath K. Effect of media use on HIV/AIDS-related knowledge and condom use in sub-Saharan Africa: a cross-sectional study. PLoS One 2013; 8(7):e68359. Vian T, Semrau K, Hamer DH, Loan le TT, Sabin LL. HIV/AIDS-Related Knowledge and Behaviors Among Most-at-Risk Populations in Vietnam. Open AIDS J 2012;6:259–65. Chen Y, Li X, Zhou Y, Wen X, Wu D. Perceived peer engagement in HIV-related sexual risk behaviors and self-reported risk-taking among female sex workers in Guangxi, China. AIDS Care 2013;25(9):1114–21. Wang B, Li X, Stanton B, Zhang L, Fang X. Alcohol use, unprotected sex, and sexually transmitted infections among female sex workers in China. Sex Transm Dis 2010; 37(10):629–36. Hong Y, Zhang C, Li X, Fang X, Lin X, Zhou Y, et al. HIV testing behaviors among female sex workers in Southwest China. AIDS Behav 2012;16(1):44–52.
