HIV prevalence and correlated factors of female sex workers and male clients in a border region of Yunnan Province,China

Abstract

Female sex workers (FSWs) and their male clients are vulnerable to HIV infection and serve as a bridge in HIV transmission from the high-risk population to the general, low-risk population. To examine the factors of FSWs and male clients that correlate with the prevalence of HIV infection in the Chinese–Vietnamese border region, a cross-sectional survey was conducted in 2014 in the Hekou county of the Yunnan province of China. We performed a questionnaire survey to collect data on demographics, sexual behavior, and drug use. Blood and urine samples were collected for testing of HIV/sexually transmitted infections and drug use. We found that the prevalence of HIV infection among FSWs was 2.74%, and 15 male clients (2.62%) were HIV-positive. Multivariate logistic regression analysis revealed that herpes simplex virus type 2 infection was a risk factor for HIV infection in FSWs and male clients, suggesting the increased role of sexual transmission in the HIV epidemic in the Chinese–Vietnamese border region. Positive urinalysis result for amphetamine-type stimulants was observed in FSWs with HIV infection. History of drug use was correlated with HIV infection, which increased the HIV infection risk of male clients, confirming that drug use is an important target in future interventions for HIV prevention.

Keywords

Female sex workers male clients of female sex workers commercial sex HIV

Introduction

Heterosexual transmission is recognized to be the primary mode of recent human immunodeficiency virus (HIV)/acquired immune deficiency syndrome (AIDS) epidemic in China.¹ During the first half of 2016, 63,300 people in China were newly infected with HIV, of whom 66.3% were infected through unprotected heterosexual intercourse.^2,3 Female sex workers (FSWs) and their male clients are considered a high-risk population for HIV infection in China owing to the significant role of commercial sexual transmission in the HIV epidemic.^4,5 However, the prevalence of HIV infection in FSWs and male clients varies considerably in different regions of China.^6,7

The Yunnan Province is located in the southwest of China. Owing to its special location near the so-called Golden Triangle, the HIV epidemic in this region has primarily spread through the use of injection drugs for many years.⁸ With the increasing role of sexual transmission in the HIV epidemic, most of the new cases of HIV infection in this region were recently acquired through sexual contact.^9,10 Hekou county is the national border port of the Yunnan province in China that adjoins the Lao Cai province in Vietnam. By the development of economic cooperation between China and Vietnam, an increasing number of people moved across the border into the two countries, including FSWs and their male clients.^11,12 It is estimated that more than 600 Vietnamese FSWs and 100 Chinese FSWs operate in Hekou. The flourishing commercial sex industry also attracted many male clients travelling to Hekou county. Despite the increase in the numbers of FSWs and male client over the years, little is known about the HIV-associated risk factors of FSWs and male clients in this region. This study concentrated on the prevalence of HIV infection in FSWs and their male clients, and examined the risk factors associated with the prevalence of HIV infection in the two groups. Moreover, we studied the correlations of HIV-related risk behaviors and the prevalence of HIV infection in FSWs and their male clients, which might provide suggestions for targets for interventions for HIV prevention.

Methods

Study site and population

This cross-sectional study was conducted from June to December 2014 in Hekou County, the HongHe Prefecture of the Yunnan Province of China. FSWs and male clients were recruited by the local outreach workers and health officials of the Hekou Center of Disease Control and Prevention (CDC). Women were considered eligible for study participation if they were at least 16 years old, reported that they provided sexual services in exchange for money in the past six months, and willing to answer our questions. The eligibility criteria for the male clients were as follows: at least 16 years of age, had a history of paying for sexual services in the past 12 months, and agreed to provide information on demographics, sexual behaviors, and drug use.

Recruitment of participants

Female participants were recruited by using convenience sampling by local health officials, outreach workers, and FSW peer educators from brothel-based commercial sex markets and entertainment venues near the region of the Chinese–Vietnamese border crossing in Hekou county. Our study staff and local health officials approached the male clients of the FSWs when they entered the commercial sex venues. In addition, snowball sampling was used to recruit male participants from the acquaintances of FSWs, their employers, and other male clients. We provided an incentive of 10 CNY (1.5 USD) to the referring person for each enrolled participant. Each participant provided written informed consent before being interviewed or providing specimens. All our study participants were compensated 50 CNY (7.5 USD) for participation in this study. Each participant received a unique personal identity number associated with the fingerprint of the right index finger to avoid duplicate participation.

Data collection

Trained staff and bilingual outreach workers who were fluent in both Chinese and Vietnamese of the Hekou CDC collected data on demographics, and sexual and drug use behaviors through face-to-face interviews by using a structured questionnaire. Quality assurance of the interview and questionnaire was done by graduated students from the Southeast University and National Center for AIDS/STD Control and Prevention (NCAIDS) of the CDC in China.

Study measures

The objective of our survey was to examine the factors that correlated with the prevalence of HIV infection in the population at risk of acquiring HIV in the Chinese–Vietnamese border region. We posed various questions concerning social-demographics, and sexual and drug use behaviors in our questionnaire. Most questions had multiple-choice answers. For example, to assess condom use with the last male client, FSWs were asked ‘In the latest commercial sex, did you use a condom with the male client?’ Response options were ‘yes’ and ‘no.’ In addition, some questions were designed such that the response required was a continuous variable, for example, age and average payment for commercial sex. To facilitate multivariate logistic regression, we transformed the continuous variables into classified variables. For instance, age (years) of male clients was transformed to a variable with three categories (‘0 = 16–24,’ ‘1 = 25–39,’ and ‘2 = ≥40’) in the multivariate logistic regression model with reference to the distribution of the response on age by male clients, and some reference that also focused on male clients of FSWs in Yunan province, China.

Laboratory testing

Blood and urine samples were collected by local physicians of the Hekou County People’s Hospital. Blood samples were cold transported to the laboratory and screened for HIV antibodies by using enzyme-linked immunosorbent assay (ELISA; Organon Teknika, Co., Ltd, Boxtel, the Netherlands), and positive tests were confirmed by HIV-1/2 Western blot assay (HIV Blot 2.2 WBH; Genelabs Diagnostics, Singapore). Blood specimens were also tested for antibodies to herpes simplex virus type 2 (HSV-2) by ELISA (Herpe Select-2 ELISA IgG; Focus Technologies, Cypress, CA, USA). Syphilis (Treponema pallidum) was tested by using the syphilis rapid plasma reagin (RPR Diagnostics kit; Shanghai Kehua, China), and positive specimens were confirmed by using a T. pallidum particle assay (Serodia-TPPA; Fujirebio Inc., Fuji, Japan). Urine samples were tested on-site for narcotics by using morphine-, ketamine-, and amphetamine-type stimulant (ATS) gold conjugate test strips (ABON; Hangzhou, China).

Data analysis

Epidata 3.1 (Odense, Denmark) was used to file the data from the research questionnaires and laboratory tests. SPSS 21.0 (IBM Inc., Armonk, USA) was used to perform statistical analysis. Data with non-normal distribution were described by using median and interquartile range (IQR) values. Chi-square and Fisher’s exact tests were used to examine the difference and associations with univariate analyses. Demographical variables and variables that were significant in the univariate analyses were included in the multivariate logistic regression model. All statistical tests were two sided, with significance determined at P < 0.05.

Ethics approval

This study received approval from the institutional review boards of the NCAIDS of the CDC in China and the Southeast University.

Results

Demographic characteristics

A total of 589 FSWs agreed to participate in this study, but four were excluded because they were younger than 16 years. Therefore, 585 FSWs consisting of 121 Chinese and 464 Vietnamese subjects who met the inclusion criteria finished the questionnaire interview and provided specimens. The median age of the FSWs was 24 years (IQR: 19–28 years), and 67.0% (392/585) had less than nine years of school. A total of 164 female participants (28.0%) were married or cohabiting. Table 1 shows that the demographical variables of age (years), education, and marital status were all significantly different between Vietnamese FSWs and Chinese FSWs.

Table 1.

Demographic characteristics of FSWs (n = 585) in Hekou, China.

Variables	n (%) of FSWs		P
Variables	Vietnamese FSWs (n = 464)	Chinese FSWs (n = 121)	P
Age (years)			<0.001
16–24	341 (73.5)	42 (34.7)
25–34	108 (23.3)	69 (57.0)
≥35	15 (3.2)	10 (8.3)
Education			<0.001
≤6 years	180 (38.8)	16 (13.2)
7–9 years	244 (52.6)	83 (68.6)
≥10 years	40 (8.6)	22 (18.2)
Marital status			<0.001
Married or cohabiting	111 (23.9)	53 (43.8)
Single, divorced, separated or widowed	353 (76.1)	68 (56.2)

FSW: female sex worker.

The total number of male respondents was 573. The median age of the male clients was 35 years (IQR: 22–45 years). The number of male participants with >10 years of education was 108 (18.9%), and 38.7% (222/573) were single, divorced, separated, or widowed. Table 2 shows that the marital status of local male clients of FSWs in Hekou is significantly different to that of other male clients.

Table 2.

Demographic characteristics of male clients of FSWs (n = 573) in Hekou, China.

Variables	n (%) of male clients		P
Variables	Others (n = 484)	Local residents (n = 89)	P
Age (years)			0.353
16–24	90 (18.6)	19 (21.3)
25–39	180 (37.2)	26 (29.2)
≥40	214 (44.2)	44 (49.4)
Education			0.076
≤6 years	163 (33.7)	20 (22.5)
7–9 years	235 (48.6)	47 (52.8)
≥10 years	86 (17.8)	22 (24.7)
Marital status			0.025
Married or cohabiting	287 (59.3)	64 (71.9)
Single, divorced, separated or widowed	197 (40.7)	25 (28.1)

FSW: female sex worker.

Drug use and HIV infection/sexually transmitted infections

A history of drug use was reported by 21 FSWs and 51 male clients. Only three male clients had ever injected drugs. After a urine test, 18 FSWs (3.1%) were identified as drug users, and all of them were positive for ATSs. The number of male respondents who were confirmed as drug users by positive urinalysis for morphine was 13 (2.3%), whereas two also used ATS.

Of our female respondents, 16 (2.7%) were identified as HIV-positive, 268 (45.8%) were infected with HSV-2, and six (1.0%) were syphilis-positive. In the male clients, the HIV and HSV-2 infection rates were 2.6% (15/573) and 13.1% (75/573), respectively. None of the male participants was infected with syphilis.

Sexual behaviors

The median age of sexual debut of the FSWs was 18 years (IQR: 16–21years), and the median age of first commercial sex was 22 years (IQR: 19–26 years). Table 3 describes that 61.2% (358/585) of FSWs ever had a regular noncommercial sexual partner and 191 (32.7%) had a regular sexual partner currently. Of the female participants, 213 (36.4%) had at least one repeated commercial sexual partner. Compared with Chinese FSWs in Hekou, age at first episode of commercial sex, number of male clients per week, and average clients’ payment of Vietnamese FSWs were significantly different.

Table 3.

Sexual behaviors of FSWs in Hekou, China

Variables	n (%) of FSWs		P
Variables	Vietnamese FSWs (n = 464)	Chinese FSWs (n = 121)	P
Age of sexual debut			0.322
<16 years old	78 (16.8)	25 (20.7)
≥16 years old	386 (83.2)	96 (79.3)
Age at first episode of commercial sex			<0.001
<20 years old	275 (59.3)	39 (32.2)
≥20 years old	189 (40.7)	82 (67.8)
Condom use with the last commercial sexual partner			0.073
Yes	427 (92.0)	117 (96.7)
No	37 (8.0)	4 (3.3)
Ever had a regular, noncommercial sexual partner			0.021
Yes	295 (63.6)	63 (52.1)
No	169 (36.4)	58 (47.9)
Currently had a regular, noncommercial sexual partner			0.327
Yes	156 (33.6)	35 (28.9)
No	308 (66.4)	86 (71.1)
Have repeated commercial sexual partner			0.663
Yes	171 (36.9)	42 (34.7)
No	293 (63.1)	79 (65.3)
Number of male clients per week			<0.001
<7	4 (0.9)	92 (76.0)
7–21	161 (34.7)	29 (24.0)
>21	299 (64.4)	0
Average clients’ payment			<0.001
<150 RMB ($22 USD)	332 (71.6)	33 (27.3)
≥150 RMB ($22 USD)	132 (28.4)	88 (72.7)

FSW: female sex worker.

For the male clients, the median age of sexual debut among the male participants was 20 years (IQR: 17–24 years). In addition, the median age at first episode of commercial sex of the male clients was 27 years (IQR: 20–35 years). Table 4 describes that among the male clients of the FSWs, 56.9% (333/573) ever had a regular sexual partner, and 46.3% clients (271/573) currently still had a regular sexual partner. Of the male participants, 32 (5.6%) had repeated commercial sexual partners. More than 80% of male respondents reported that they used a condom with the last commercial sexual partner. Comparisons of the variables of sexual behaviors between local and other male clients in Hekou county in this study showed that there were no significant differences.

Table 4.

Sexual behaviors of male clients of FSWs (n=573) in Hekou, China

Variables	n (%) of male clients		P
Variables	Others (n = 484)	Local residents (n = 89)	P
Age of sexual debut			0.086
<16 years old	34 (7.0)	11 (12.4)
≥16 years old	450 (93.0)	78 (87.6)
Age at first episode of commercial sex			0.456
<20 years old	144 (29.8)	23 (25.8)
≥20 years old	340 (70.2)	66 (74.2)
Condom use with the last commercial sexual partner			0.172
Yes	423 (87.4)	73 (82.0)
No	61 (12.6)	16 (18.0)
Ever had a regular, noncommercial sexual partner			0.317
Yes	277 (57.2)	56 (62.9)
No	207 (42.8)	33 (37.1)
Currently had a regular, noncommercial sexual partner			0.344
Yes	233 (48.1)	38 (42.7)
No	251 (51.9)	51 (57.3)
Have repeated commercial sexual partner			0.308
Yes	25 (5.2)	7 (7.9)
No	459 (94.8)	82 (92.1)
Frequency of commercial sex			0.423
<5 times per month	418 (86.4)	74 (83.1)
≥5 times per month	66 (13.6)	15 (16.9)
Average payment for commercial sex			0.172
<150 RMB ($22 USD)	389 (80.4)	77 (86.5)
≥150 RMB ($22 USD)	95 (19.6)	12 (13.5)

FSW: female sex worker.

Factors that correlate with HIV

Table 5 describes the associated factors of HIV infection of the FSWs by using a logistic regression model. For the univariate level, age (years), education, condom use with the last commercial sexual partner, average clients’ payment, positive HSV-2 test result, and positive urine test for ATSs were considered significantly associated with HIV infection. Multivariate logistic regression analyses showed that a positive HSV-2 test result (OR: 6.8, 95% CI: 1.5–31.4) and a positive urine test result for ATSs (OR: 7.2, 95% CI: 2.0–26.2) were significantly associated with greater odds of HIV infection. However, average clients’ payment ≥150 RMB ($22 USD) (OR: 0.2, 95% CI: 0.1–0.9) was correlated with lower odds of HIV infection among FSWs in Hekou.

Table 5.

Factors correlated with HIV infection among FSWs in Hekou, China

Variable	n	n (%) of HIV infections	Univariate OR (95%CI)	Multivariate OR (95%CI)
Nationality
Chinese	121	0.8	1	1
Vietnamese	464	3.2	4.0 (0.5–30.7)	3.6 (0.5–27.8)
Age (years)
16–24	383	2.1	1	1
25–34	177	2.3	1.1 (0.3–3.6)	1.2 (0.3–3.8)
≥35	25	16.0	8.9 (2.4–32.1)^§	5.7 (0.8–40.6)
Education
≤6 years	196	5.1	1	1
7–9 years	327	1.5	0.3 (0.1–0.9)^†	0.4 (0.1–1.2)
≥10 years	62	1.6	0.3 (0.0–2.4)	0.6 (0.1–4.1)
Marital status
Married or cohabiting	164	4.3	1	1
Single, divorced, separated or widowed	421	2.1	0.5 (0.2–1.3)	0.6 (0.2–1.5)
Age of sexual debut
<16 years old	103	5.8	1
≥16 years old	482	2.1	0.3 (0.1–1.0)
Age at first episode of commercial sex
<20 years old	314	3.5	1
≥20 years old	271	1.9	0.5 (0.2–1.5)
Ever had a regular, noncommercial sexual partner
No	227	3.1	1
Yes	358	2.5	0.8 (0.3–2.2)
Currently had a regular, noncommercial sexual partner
No	394	2.5	1
Yes	191	3.1	1.2 (0.4–3.5)
Have repeated commercial sexual partner
No	372	3.0	1
Yes	213	2.3	0.8 (0.3–2.3)
Number of male clients per week
<7	96	1.0	1
7–21	190	2.1	2.0 (0.2–18.5)
>21	299	3.7	3.6 (0.5–28.5)
Condom use with the last commercial sexual partner
No	41	9.8	1	1
Yes	544	2.2	0.2 (0.1–0.7)^†	0.3 (0.1–1.3)
Average clients’ payment
<150 RMB ($22 USD)	365	3.8	1	1
≥150 RMB ($22 USD)	220	0.9	0.2 (0.1–1.0)^†	0.2 (0.1–0.9)^‡
HSV-2 test
Negative	317	0.6	1	1
Positive	268	5.2	8.7 (2.0–38.6)^‡	6.8 (1.5–31.4)^‡
Syphilis test
Negative	579	2.6	1
Positive	6	16.7	7.5 (0.8–68.4)
History of drug use
No	564	2.5	1
Yes	21	9.5	4.1 (0.9–19.5)
Amphetamine-type stimulants urine test
Negative	567	2.1	1	1
Positive	18	22.2	13.2 (3.8–46.1)^‡	7.2 (2.0–26.2)^†

CI: confidence interval; FSW: female sex worker; HIV: human immunodeficiency virus; HSV-2: herpes simplex virus type 2; OR: odds ratio.

^†

p-value<0.05; ^‡p-value<0.01; ^§p-value<0.001.

The associated risk factors of HIV infection among the male clients of FSWs are shown in Table 6. Positive HSV-2 test result, ever-use of illegal drugs, positive morphine urine test result, and frequency of commercial sex per month were considered significant associated factors of HIV infection at the univariate level. Positive HSV-2 test result (OR: 7.3, 95% CI: 2.4–22.0), history of drug use (OR: 6.2, 95% CI: 2.1–18.3), and frequency for commercial sex per month (OR: 5.5, 95% CI: 1.9–14.9) that associated with greater odds of HIV infection of male clients were retained in the multivariate model.

Table 6.

HIV correlated factors of HIV infection among male clients of FSWs in Hekou, China

Variable	n	n (%) of HIV infections	Univariate OR (95%CI)	Multivariate OR (95%CI)
Age (years)
16–24	109	0.9	1	1
25–39	206	4.4	4.9 (0.6–39.5)	4.5 (0.5–36.4)
≥40	258	1.9	2.1 (0.3–18.5)	2.0 (0.3–17.9)
Education
≤6 years	183	3.3	1	1
7–9 years	282	2.5	0.8 (0.3–2.3)	0.9 (0.3–2.6)
≥10 years	108	1.9	0.6 (0.1–2.8)	0.4 (0.1–1.6)
Marital status
Married or cohabiting	351	1.7	1	1
Single, divorced, separated or widowed	222	4.1	2.4 (0.9–6.9)	2.2 (0.9–6.2)
Residency
Local residents	89	3.4	1	1
Others	484	2.5	0.7 (0.2–2.6)	0.8 (0.2–3.0)
Age of sexual debut
<16 years old	45	4.4	1
≥16 years old	528	2.5	0.5 (0.1–2.5)
Age at first episode of commercial sex
<20 years old	167	1.8	1
≥20 years old	406	3.0	1.7 (0.5–6.0)
Ever had a regular, noncommercial sexual partner
No	240	3.3	1
Yes	333	2.1	0.6 (0.2–1.7)
Currently had a regular, noncommercial sexual partner
No	302	3.64	1
Yes	271	1.48	0.4 (0.1–1.3)
Have repeated commercial sexual partner
No	541	2.4	1
Yes	32	6.3	2.7 (0.6–12.5)
Frequency of commercial sex
<5 times per month	492	1.2	1	1
≥5 times per month	81	11.1	9.3 (3.2–26.9)^§	5.5 (1.9–14.9) ^†
Condom use with the last commercial sexual partner
No	77	5.2	1
Yes	496	2.2	0.4 (0.1–1.3)
Average payment for commercial sex
<150 RMB ($22 USD)	466	2.8	1
≥150 RMB ($22 USD)	107	1.9	0.7 (0.1–3.0)
HSV-2 test
Negative	498	1.4	1	1
Positive	75	10.7	8.4 (2.9–23.8)^§	7.3 (2.4–22.0)^‡
History of drug use
No	522	1.7	1	1
Yes	51	11.8	7.60 (2.6–22.3)^§	6.2 (2.1–18.3)^†
Morphine urine test
Negative	560	2.3	1	1
Positive	13	15.4	7.7 (1.5–38.0)^†	5.8 (0.8–42.1)

CI: confidence interval; FSW: female sex worker; HIV: human immunodeficiency virus; HSV-2: herpes simplex virus type 2; OR: odds ratio.

†

p-value<0.05; ^‡p-value<0.01; ^§p-value<0.001.

Discussion

In this study, the HIV prevalence rates of FSWs and male clients were 2.7% (16/585) and 2.6% (15/573), respectively. Almost no significant difference in HIV infection rates was found between the two groups based on the HIV test results. FSWs have been considered a high-risk population for HIV infection and transmission since the HIV pandemic emerged worldwide.¹³ Male clients of FSWs may also play an important role in the transmission of HIV infection across the China–Vietnam border.

The HIV prevalence in the Vietnamese FSWs in Hekou county (3.2%) was lower than the estimate of Wang et al.¹¹ In addition, an even lower prevalence rate than that in five border provinces of Vietnam.¹⁴ The HIV prevalence among the Chinese FSWs was lower than the HIV prevalence estimated by Li et al.¹⁵ among Chinese street-based FSWs, but higher than that reported by Beyrer et al.¹⁶ Some researchers have indicated that the HIV prevalences among Chinese FSWs in different regions were significantly different.¹⁷ Southwestern China always has higher HIV prevalence among Chinese FSWs than other regions.¹⁸ Compared with some recent studies which reported that the HIV prevalence among Chinese FSWs in Yunnan province was estimated to be more than 10%, the HIV prevalence among Chinese FSWs in Hekou was much lower.^19,20 One possible explanation for the relatively low HIV prevalence in FSWs in this study is that it has greatly decreased owing to the HIV-related attitudes and behaviors of FSWs in Hekou county after years of behavioral interventions and HIV-related health education provided by Hekou CDC and some international nongovernmental organizations. In addition, through the efforts of the outreach workers and FSW peer educators of Hekou CDC, an increasing number of FSWs are willing to participate in HIV/sexually transmitted infection prevention interventions. Most FSWs know how to protect themselves in commercial sexual behaviors. Furthermore, some of them can negotiate condom use with male clients. The difference in HIV prevalence between the Vietnamese and Chinese FSWs was not significant. The relatively low HIV prevalence and the conservative Fisher’s exact tests may be important factors.

For the male clients, 2.6% were infected with HIV. Compared with the HIV prevalence in male clients in Hekou county in 2012 (9.2%) estimated by Reilly et al.²¹ and HIV prevalence of male clients in Kaiyuan city, Yunnan province, in 2010 (6.0%), estimated by Jin et al.,²² the HIV prevalence of the male clients in this study was lower. However, the prevalence was higher than that reported by McLaughlin²³ in China (0.7%) or southwest of China (2.5%). The study region and sample selection may be important factors that affect the estimation of HIV prevalence among male clients.²³ If more male clients from low-fee commercial sexual venues were collected, maybe more positive cases could have been found in the study. In addition, if more illegal drug users, especially injection drug users (IDUs), were recruited, the HIV prevalence among the male clients in Yunnan province, China, would have been higher.^24,25

In this study, we compared social-demographics and sexual behaviors, not only between Vietnamese and Chinese FSWs, but also between local and other male clients. However, the results among FSWs and male clients were statistically quite different. For male clients of FSWs, only marital status was significantly different between local and other male clients. This indicates that the demographic characteristics and sexual behaviors of male clients who are local residents or those from the endemic population are similar. Therefore, uniform HIV prevention interventions can be applied to all male clients in Hekou county. Special measures for any subgroup of male clients are not required. Nevertheless, there were several differences between Vietnamese and Chinese FSWs in terms of social-demographic characteristics and sexual behaviors. Compared with Chinese FSWs in Hekou, Vietnamese FSWs were significantly younger and had a younger age at first episode of commercial sex. Furthermore, the number of male clients per week and average clients’ payment were also significantly different between Vietnamese and Chinese FSWs. This showed that sexual, especially commercial sexual behavior models between Vietnamese and Chinese FSWs are significantly different. Compared with Chinese FSWs, Vietnamese FSWs generally have a greater frequency of commercial sexual encounters but get lower payment from male clients. It highlighted that Vietnamese FSWs in Hekou need more effective safe-sex interventions as they have a greater frequency of commercial sexual partner change than Chinese FSWs. The relatively low payment among Vietnamese FSWs indicated that male clients of Vietnamese FSWs may be different to those of Chinese FSWs, thus it may put Vietnamese FSWs at a greater risk of HIV infection in commercial sex.

The logistic regression results of this study confirmed that FSWs in Hekou of Yunnan, China, are particularly vulnerable to HIV infection by HSV-2 positivity (OR: 6.8, 95% CI: 1.5–31.4) and ATS positivity (OR: 7.2, 95% CI: 2.0–26.4). However, engaging in commercial sex with clients who are willing to make an average payment ≥150 RMB ($22 USD) (OR: 0.2, 95% CI: 0.1-0.9) may reduce the likelihood of HIV infection. The main predictors of HIV infection in the male clients were HSV-2 positivity (OR: 7.3, 95% CI: 2.4–22.0), history of drug use (OR: 6.2, 95% CI: 2.1–18.3), and more frequent commercial sex per month (OR: 5.5, 95% CI: 1.9–14.9). Other studies on factors that correlate with HIV found that condom use, monthly income, and having a regular sexual partner were associated with HIV infection but not significantly in this study.^26–28 Different regions and sample sources may be the most important reason. Moreover, all the study information was collected through self-report by respondents. Some HIV-related factors were not associated with HIV infection in our research probably because of a downward bias.²⁹ Finally, the relatively low number of outcomes (prevalence of HIV infection) may have caused confounding in the multiple logistic regression model.¹¹

For the common HIV infection-related factor, which is HSV-2 positivity, previous studies confirmed that HSV-2 infection may increase the risk of acquiring HIV.³⁰ Some studies also found significant associations between HSV-2 and HIV infections in FSWs and male clients in Yunnan province.^31–33 In this study, the HSV-2 prevalence among the male clients was lower than that reported by Xu et al.²⁴ in Gejiu city, Yunnan province. However, for FSWs, it is observably higher than those in some other studies of HSV-2 prevalence among FSWs in Yunnan province, and this may pose greater risks of HIV acquisition.³⁴ In addition, because sexual transmission is the primary mode for the spread of HSV-2 infection. The association between HSV-2 and HIV infections in this study among FSWs and male clients also emphasizes the increasing role of sexual transmission, especially commercial heterosexual transmission, in the HIV epidemic at China–Vietnam border area.²¹

In this study, drug use is another common factor that correlates with HIV infection in FSWs and male clients. Drug use has been found in some past research studies to be associated with HIV infection, and most of the earliest HIV-positive cases identified in Yunnan province, China, were IDUs.^35,36 Xu et al.³⁷ reported that drug use poses significant risks for both new and established HIV infection among FSWs. Jin et al.²² found that drug use caused a 6.1-fold increased risk among male clients associated with HIV infection in Yunnan, China. In this study, a history of drug use among male clients and positive urine testing for ATSs of FSWs were significant for HIV infection, indicating that drug use is still a salient risk factor for HIV infection in southwestern China. Moreover, ATS is one of the new types of drug widely produced, trafficked, and used recently in Southeast Asia.³⁸ Previous research found that FSWs who have used ATS before commercial sexual behavior are less likely to use condoms with clients,³⁹ suggesting that ATS use may exacerbate the HIV epidemic among FSWs through risky sexual behaviors. Thus, drug use, especially of a new type of drug, is of concern in HIV prevention interventions that target FSWs and male clients in the China–Vietnam border region.

More frequent commercial sex is an individual-related factor associated with HIV infection in male clients. One possible explanation is that clients who visit FSWs more frequently may have a higher rate of commercial sexual partner change, thus making them more likely to have sexual risk with a HIV-positive partner.⁴⁰

Limitations

This study has several limitations. First, we could not obtain a sampling frame and take random selection of samples for our research study because sex work is illegal in China. The participants in this study may not be representative of the overall group of FSWs and male clients in the Chinese–Vietnamese border region. As described in the recruitment methods, the FSWs in our study were located at venues, where outreach workers could approach them easily. Most of the male clients who visited these FSWs were also relatively easy to approach by our research staff. This suggests a selection bias by including participants with a lower risk of HIV infection. Some previous studies showed that FSWs at venues with a higher risk of HIV infection were more likely HIV-positive, suggesting that their male clients may also have a higher risk of HIV infection. However, both FSWs and male clients at venues with a higher risk of HIV infection were difficult to recruit for our study. Therefore, sampling methods that can effectively recruit hard-to-reach subjects, such as respondent-driven sampling, should be considered in future research.⁴¹ Second, as our study included many sensitive issues and the data were collected through a questionnaire interview, FSWs and male clients were subject to social desirability bias. Self-reporting and recall biases among the respondents also affected the correlation of factors with HIV infection. However, the effects caused by these biases were difficult to determine in our study. Third, because urine tests can only identify drug use within one week, the number of drug-using participants might have been underestimated in this study. Drug use is an important factor that is associated with HIV infection in FSWs and male clients in this study, which was discussed in detail earlier. It is interesting that among both FSWs and male clients were several subjects who denied previous drug use but were identified as drug users by a positive urine test result. Therefore, the actual association of HIV infection with drug use may be underestimated. Moreover, the factors that correlate with HIV infection do not determine the causal relationship because of the cross-sectional design of this study.⁴²

Conclusion

FSWs and male clients in the Chinese–Vietnamese border region are vulnerable to HIV infection. Understanding the factors that correlate with HIV infection in the two groups can be helpful in the design and provision of interventions. Health education on safe sex and providing condoms in entertainment venues to encourage condom use as the primary mode of interventions for HIV prevention have been done for many years in China, which targets FSWs but not their male clients. Therefore, effective interventions should be provided to reduce the risk of HIV infection in male clients. As FSWs and male clients in the Chinese–Vietnamese border region are a potential bridge in transborder HIV transmission, further research focusing on the reduction of risk behavior for HIV is important.

Footnotes

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors disclosed receipt of the following financial support for the research, authorship, and/or publication of this article: This work was supported by the mega-projects of national science research for the 12th Five-Year Plan (2012ZX10001-001) and The Fundamental Research Funds of the Central Universities (KYZZ_0077) of China.

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