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Microbicide Acceptability and Associated Factors Among Female Sex Workers and Male Clients in Kaiyuan County, Yunnan Province, China

Wang, Yun MPH*; Jiang, Yan MD, PhD; Lu, Lin MD, MPM; Wang, Guixiang§; Bi, Aimei§; Fang, Hong§; Chang, Dongfang; Gu, Jing; Wang, Wenzhong

JAIDS Journal of Acquired Immune Deficiency Syndromes: February 2010 - Volume 53 - Issue - p S93-S97
doi: 10.1097/QAI.0b013e3181c7de7b
Supplement Article

Objectives: To determine microbicide acceptability and associated factors among female sex workers (FSWs) and their clients in Yunnan, China.

Methods: Kaiyuan County, with high rates of HIV in FSWs, in Yunnan Province was chosen as the study site. Establishments were selected using stratified sampling, and FSWs were recruited using random sampling. Male clients of FSWs were also recruited. In-depth interviews and anonymous questionnaires were used to collect data. An acceptance rate was calculated for each individual variable, and factors associated with acceptability were assessed using multivariate analysis.

Results: Four hundred FSWs and 200 male clients were recruited. Microbicides were acceptable if they prevented HIV transmission effectively and safely, were lubricating, effective up to 24 hours, and <10 China Yuan (CNY) (US $1.50) per use. Eighty-one percent of participants indicated future intention to use microbicides. Factors associated with potential microbicide use included age, establishment stratum, price, perception of risk behavior, and knowledge of AIDS/sexually transmitted infections.

Conclusions: The acceptablitiy of microbmicides is high among FSWs and their clients. Development of effective and affordable microbicides has great potential for controlling sexual transmission of the HIV epidemic in China.

From the *Division of TB Control and Prevention Yunnan Center for Disease Control and Prevention, Yunnan, China; †National AIDS Reference Laboratory, National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing, China; ‡Yunnan Center for Disease Control and Prevention, Yunnan, China; §Kaiyuan Center for Disease Control and Prevention, Yunnan, China; and ‖Division of AIDS Control and Prevention, Kaiyuan Center for Disease Control and Prevention, Yunnan, China.

Supported by the US Center for Disease Control and Prevention Global AIDS Program, 5U62PS022883-5.

Correspondence to: Yan Jiang, MD, PhD, 27 Nanwei Road, National AIDS Reference Laboratory, National Center for AIDS/STD Control and Prevention, China Center for Disease Control and Prevention, Xuanwu District, Beijing 100050, China (e-mail:

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The HIV epidemic continues to grow worldwide. Among the 39.5 million people living with HIV in 2006, new HIV infections accounted for 4.3 million, and 85%-90% of new HIV infections were contracted through heterosexual transmission.1 Interacting synergistically with the HIV epidemic is the epidemic of other sexually transmitted infections (STIs), some of which can exacerbate the infectivity of HIV and the host's susceptibility to HIV infection.2

The effectiveness and use of male and female condoms are limited by the need for women to negotiate their use with their sexual partners.3 Microbicides, which are self-administered prophylactic agents applied to the vagina or rectum in various formulations and by various delivery methods hold great promise for HIV prevention among sexually active people. Microbicides allow women to control its use, instead of depending on men for the use of condoms, can impede transmission of HIV and/or other sexually transmitted pathogens, and some may even provide contraceptive protection.4,5

Increasingly, the major mode of HIV transmission in China is through heterosexual sexual contact, and the burden of HIV infections is among women, especially in female sex workers (FSWs). Sentinel surveillance data indicated that the rate of HIV infection in FSWs increased from 0.02% in 1995 to 1% in 2005,6 and in 2007, 44.7% of new HIV infections were due to heterosexual transmission.7 The urgent need in using microbicides to assist in limiting the sexual spread of HIV in China is clear. This article is the first to present research on male clients of FSWs (herafter referred to as male clients) attitudes toward microbicides in China.

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Study Site

The Kaiyuan County located in Yunnna was selected as the study site. An HIV prevalence of 11.9% (89 of 747) was found among FSWs in Kaiyuan in 2006 that was much higher than both the national (1%)6 and Yunnan provincial average (1.7%).8 This implies great potential of HIV transmission via sexual intercourse.

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Participants, Sampling, and Data Collection

Establishment-based FSWs and their clients were the study participants. These establishments were divided into 3 strata according to the price of sexual service: >60 China Yuan (CNY) (about US $9)-stratum A; 30-60 CNY (about US $4.50 to US $9)-stratum B; <30 CNY (US $4.50)-stratum C. Fifteen establishments each were selected from strata A and B, and 10 establishments were selected from stratum C. FSWs in selected establishments were recruited through random sampling, and no more than 15 FSWs were selected from each establishment.

Male clients were recruited by 1 of 3 methods. The first method was through FSWs recommending their clients, with each FSW limited to recommending 3 male clients. Another method was through snowball sampling, using male clients as seeds referred by FSWs. A third method was through Kaiyuan Center for Disease control and prevention (CDC) employees recommending people they knew who patronized FSWs.

Eligibility was defined as having commercial heterosexual sexual intercourse in the last month, having lived for more than 6 months in Kaiyuan county, and not planning to leave in the next 12 months. Male drug users were excluded.

In-depth interviews and anonymous questionnaires were used to collect data. There were separate questionnaire versions and interview outlines for FSWs and for male clients. The FSW questionnaire comprised 5 parts as follows: (1) sociodemographic characteristics; (2) AIDS/STI knowledge (16 questions); (3) history of gynaecopathia intravaginal drug and lubrication use; (4) sexual history, and (5) attitudes toward microbicides. The male client questionnaires comprised 4 parts as follows: (1) sociodemographic characteristics; (2) AIDS/STI knowledge (14 questions); (3) sexual history, and (4) attitudes toward microbicides. A preliminary survey was conducted to assess the suitability of both the in-depth interview outlines and the questionnaires and were revised as necessary. Questionnaires were completed by all eligible participants, whereas interviews were completed by a subset of the participants.

Informed participant consent was obtained, and subjects were assured that participation was anonymous and all information provided would be confidential. The questionnaire was administered by trained interviewers. An in-depth interview was conducted on FSWs' reported history of engaging in sexual intercourse while using intravaginal drugs. A similar interview was conducted with male clients on their history of sexual intercourse with women using intravaginal drugs.

In total, 420 FSWs and 241 male clients were recruited; 20 FSWs (19 had stopped sex work and 1 was deaf) and 41 male clients (20 were drug users and 21 had never received commercial sexual services) were excluded. Of the eligible participants (400 FSWs and 200 male clients), none refused to participate, and all completed questionnaires. All of the 8 eligible FSWs and 43 eligible male clients completed in-depth interviews.

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Data Analysis

The in-depth interviews were recorded by researchers, and the recorded data were transcribed. Using ATLAS.ti 5.0, researchers coded, compared, sorted, induced, and organized the data to obtain the results. Structured questionnaire data were entered into Epi Data 3.1 (The EpiData Association, Odense, Denmark) and were then analyzed by SPSS 13.0 (SPSS Inc, Chicago, IL) software for descriptive, univariate, and multivariate logistic regression methods to identify the factors associated with the acceptability of microbicides.

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The study protocol was approved by the Institutional Review Board of the National Center for AIDS/STD Control and Prevention of the Chinese Center for Disease Control and Prevention.

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Characteristics of Participants

The demographic and risk characteristics of the 600 participants are reported in Table 1. The average age was 28 years for FSWs and 38 years for male clients. Education obtained was low for both FSWs and clients. The majority were single, separated, or windowed. More than half of FSWs reported previously using a vaginal product.



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Participant Attitudes Toward Potential Microbicide Features

Most participants (73.67%) have never heard of microbicides and as an actual product is still currently unavailable; a description of microbicides was explained in detail to all participants.

Participants were asked to rank in descending order which features of the microbicide (contraception, disease prevention, pleasant to use, convenience, safety, comfort, and cleanliness) they considered to be the most important. Most participants (83.5%) regarded disease prevention, especially impeding the transmission of HIV, as the most important feature (Table 2).



More than half of participants (52.5%) hoped microbicides would be lubricating. Only female participants were asked about potential duration of microbicide effectiveness. The most frequently chosen duration was up to 24 hours (16.25%).

The range of price per application participants could choose was from 1 to 100 CNY. The most frequently chosen price (27.17%) was no more than 10 CNY per use.

Nearly three-quarters of female participants (70%) wanted to insert microbicides into the vagina using an applicator; 22 male clients with a history of anal intercourse also did not mind inserting microbicides into their partner's rectum with their fingers or with an applicator.

More than half of female participants (57.75%) would like microbicides to be available over the counte. Females thought the efficacy of microbicides was the most important feature (47.75%), whereas men were more concerned with the safety of microbicides (59.50%).

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Acceptability of Microbicides

On the premise that microbicides are effective at preventing HIV and STIs, 90.17% of FSW participants were willing to accept changes in their vaginas after the insertion of microbicides, and 70% of male participants were able to accept leakage of microbicides.

The majority of participants (81%) (female and male) indicated that they would purchase and use microbicides in the future, and 78% of participants said they would use this product with their steady partner. After being informed that microbicides currently had an efficacy as low as 40% of the male condom for preventing HIV and STIs, 64% participants still thought it was necessary for China to import this product, whereas 36% of all participants (female and male) expressed that they did not want to use microbicides because they were worried about its safety and were uncomfortable with the idea of inserting something into their vagina/anus.

More than half of female participants (59%) indicated that they would use microbicides when they were unable to negotiate condom use with their commercial partner; however, if they were able to negotioate condom use, only 14.75% of female participants indicated that they would use microbicides in addition to condoms.

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Influence of Microbicides on Sexual Behavior

Two-thirds of female participants (67.5%) thought the use of microbicides would not influence their sexual behavior, but a minority (3.75%) indicated the number of clients they currently had would increase. Meanwhile, nearly a fifth of women (18.25%) thought microbicides would lead to a decrease in condom use.

Among male participants, nearly half (44.5%) thought microbicides would result in a decrease in condom use and nearly a quarter (21%) thought their frequency of commercial sexual intercourse would increase. Among the 22 men who reported a history of anal intercourse, 8 indicated that they would increase their frequency of anal intercourse with microbicide use.

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History of Intravaginal Drug Use

To understand attitudes pertaining to microbicide acceptability in greater detail, females with a history of sexual intercourse while using intravaginal drugs and males who had experienced sexual intercourse with a female using an intravaginal drug were interviewed in depth.

Among the 400 female participants, eight women (2%) had experienced sexual intercourse while using intravaginal drugs, and 2 (25%) reported no change in sensation, whereas 6 (75%) reported a change in sensation. The changed sensations included a feeling of coolness, increased lubrication, and discomfort. The reasons for these women using intravaginal drugs were to treat disease and for pain relief. FSWs who were using the intravaginal drugs were more likely to report having new male partners and/or steady partners.

Among the 200 male participants, 43 (21.5%) had experienced sexual intercourse with females using intravaginal drugs and 10 men (23.26%) reported that they were unaware of any change in sensation. Senstations used to describe the microbicides included the following: cool, sticky, increased lubrication, scorching, and uncomfortable. Almost all of the men (92.59%) were unaware before sexual intercourse that their female partner was using an intravaginal drug. The majority (88.89%) of their female partners were new partners. Twenty-two of the 43 men (51.16%) accepted the practice of using intravaginal drugs although 21 (48.84%) did not.

Men who were more willing to accept the use of intravaginal drugs said that they did not feel any difference in their partners' vagina and that they did not mind whether their female partners used intravaginal drugs or not. Men who were less likely to accept this sexual practice suspected their female partners inserted drugs into their vagina because they were ill.

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Factors Associated With Microbicides Acceptability

Based on the results of the univariate factor analysis, we used logistic regression methods to identify the factors associated with the acceptability of microbicides. The dependent variable was whether participants accepted microbicides or not. Ten independent variables were entered in the model. Gender, lubrication, price, and having taken measures to prevent STIs in the past 6 months were significant (Table 3). Although age, establishment strata, and score of relative AIDS/STI knowledge were not in the last equation, univariate factor analysis showed that they were also factors in microbicide acceptability.



Perception of risk behaviors affected the acceptability of microbicides among all participants (Table 4). Knowledge of STIs and AIDS was also a factor in affecting microbicide acceptability among female participants.



FSWs who scored more questions about STDs and AIDS correctly (at least 10 of 16 questions) (n = 319) had a higher acceptance rate of using microbicides (93%) than those who scored fewer questions correctly (n = 33, acceptance rate: 83%, χ2 = 6.85, P = 0.03).

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Overall acceptability of microbicides was high, indicating the potential market for microbicides among people engaging in high-risk sexual behavior is good. Participants also believed that such products should be available to women if proven to be safe and effective.

Some participants indicated that they would decrease condom use if microbicides became available. If microbicides do lead to a decrease in condom use and become a method of soliciting customers, our results are likely to be discouraging. At present, microbicides have an efficacy as low as 40% of the male condom for preventing HIV and STIs9; therefore, even if their future efficacy is increased to 80%, microbicides should not be absolutely substituted for condoms. These results give an early warning that providers must deliver accurate messages to users and not exaggerate or hide the real efficacy of microbicides. At the same time, sex education should be improved among FSWs and male clients in order for informed decisions to be made.

The covert use of microbicides has been related to sexual partner type,10 and women might be more inclined to use microbicides covertly with a new partner believing he would be less likely than a regular partner to notice anything unusual in the vagina.3 However, in our study, men who engaged in sexual intercourse with new female partners using intravaginal drugs were aware of their use. They did not punish or censure these women because the men thought their relationship was casual and they did not want to spend energy arguing with the women. In view of this fact, microbicides can be a method through which FSWs can persist in getting protection when their male clients refuse to use a condom in casual relationships.

Younger participants were more likely to accept microbicides compared with older participants, and it has been reported that age is a factor in influencing choice regarding microbicide type.11 The higher the price of microbicides, the lower the acceptability, although participants from higher priced establishments were more likely to accept microbicides than those from lower priced establishments. A positive perception of risky sexual behavior and a strong knowledge of STIs and AIDS were helpful for the acceptance of microbicides indicating sex education should be strengthened.

The efficacy of microbicides in preventing HIV was a critical factor influencing acceptability. This indicates that although each participant had different preferences concerning the physical characteristics of microbicides, the efficacy of microbicides was the basis of its acceptability.

Compared with female participants, male participants exhibited more caution concerning microbicides. Caution among men and the impact of male condom use on female decisions showed that male attitudes were an important factor in deciding whether to take preventive measures or what type of preventive measures to take. Therefore, health education for men, especially for male clients, is extremely important.

Most participants choose to insert microbicides with an applicator, indicating both men and women hoped to have clean and safe insertion methods. The sensation of microbicides in the vagina is also a factor influencing acceptability of microbicides; therefore, insertion method and sensation of use will need to be carefully designed to encourage maximum acceptance of product use.

Our study was conducted in Kaiyuan county, Yunnan province, where the rate of HIV transmission through unprotected sexual intercourse is high, and many HIV/AIDS projects have been implemented. Therefore, these FSWs were likely to be more knowledgable about AIDS and were more eager to obtain preventive measures to protect themselves, resulting in high microbicide acceptability. Additionally, most FSWs wanted microbicides to be lubricating. This preference was related to FSWs habit of using lubricants during sexual intercouse. The acceptability of microbicides was also influenced by the local AIDS epidemic and female vaginal practices. These results are consistent with several international studies.12-15

As far as we know, this was the first time in Kaiyuan county and in Yunnan province that a group of male sexual clients was directly surveyed. We explored 3 recruitment methods. Of the 3 methods, recommendation of male clients was not reliable, whereas both methods of FSW and Kaiyuan CDC employee recommendation were more reliable. Nonetheless, the CDC employee recommendation method required more time than FSW recommendation as the participants recommended by the employees of Kaiyuan CDC were extremely concerned about potential exposure of their identity and insisted on being interviewed in locations they had suggested. From this perspective, CDC employee recommendation was not efficient and it does not lend itself to quality control. Therefore, for this study, FSWs' recommendation was the most efficient and reliable method of male client recruitment.

This study had a number of limitations. First, participants were assessed on the likelihood of a hypothetical microbicide; therefore, it is inevitable that some questions were answered subjectively. Second, the population of male clients has not been comprehensively described in Kaiyuan county, so our sampling methods were restricted, and random sampling was not possible. For this population, we used recruitment via personal recommendation. The shortcoming of such a method is that participants are familiar with the person who introduced them, and therefore, a representative sample of the male client population is unlikely to be obtained. Third, there are many factors influencing the acceptability of microbicides, and our study may not have investigated all factors. In addition, our study site was limited to 1 county with a high HIV/AIDS prevalence; therefore, it is possible that our results are not representative of other locations in China.

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Our study found that microbicides is acceptable to both FSWs and their clients in Kaiyuan Yuanna, if they provide protection from HIV infection effectively and safely, and affordable. In view of China's large population and the increasing rate of HIV transmission via unprotected sex, the development of effective, safe, and affordable microbicides has a great potential in controlling sexual transmission of HIV epidemic.

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The authors would like to thank Naomi Juniper for her assistance in the preparation of this article and thank Adrian Liau for editing assistance.

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acceptability; China; FSWs; male clients; microbicides

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