Chinese Medical Journal 2012;125(16):2819-2825
Health-related attitudes and risk factors for sexually transmitted infections of Chinese women who have sex with women

WANG Xiao-fang,  Jessie L. Norris,  LIU Ying-jie,  Kathleen H. Reilly,  WANG Ning

WANG Xiao-fang (National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China)

Jessie L. Norris (National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China)

LIU Ying-jie (Institute for AIDS/STD Control and Prevention, Beijing Chaoyang District Center for Disease Control and Prevention, Beijing 100021, China)

Kathleen H. Reilly (National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, Beijing 102206, China)

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

Correspondence to:WANG Ning,National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention, 155 Changbai Road, Changping District, Beijing 102206, China (Tel: 86-10-58900905. Fax:86-10-58900905. E-mail:wangnbj@163.com)
Keywords
women who have sex with women; lesbian, gay, bisexual, transgender; HIV/AIDS; sexual transmission; sexually transmitted infection
Abstract
Background  Previous studies have shown evidence of health-related risk behaviors among women who have sex with women (WSW), such as sex with men, multiple bisexual partners, and drug use. Women who have sex with women have also been known to avoid routine physical examinations and conceal their same-sex history from physicians, which can affect their ability to receive an accurate diagnosis and treatment. No previous research has targeted women who have sex with women in China. We sought to describe women who have sex with women in China and explore risk factors for their reproductive tract infections (RTI)/sexually transmitted infections (STI).
Methods  Participants were recruited through outreach in venues and online for a cross-sectional study. Data were collected using interviews and laboratory tests.
Results  We recruited 224 women who have sex with women. In the year preceding their participation in the study, 92% (206/224) of women reported sexual relations with women. The RTI rates were: gonorrhea (15.8%), chlamydia (3.5%), syphilis (0.5%), bacterial vaginosis (14.4%), hepatitis B virus (HBV) (0.9%), hepatitis C virus (HCV) (0.5%), and candidiasis (6.9%). No HIV or herpes simplex virus (HSV) positive cases were detected. Factors associated with gonorrhea infection were non-Beijing local residency (odds ratio (OR)=2.1, 95% confidence interval (CI): 1.2–3.8) and genital-genital contact (OR=3.1, 95% CI: 1.3–7.2); factors associated with curable STI (excluding bacterial vaginosis, candidiasis, HBV and HCV) were non-Beijing local residency (OR=1.9; 95% CI: 1.2–3.0) and bleeding during or after sex (OR=18.1; 95% CI: 5.2–62.6); and the factor associated with RTI (including all the infections tested) was bleeding during or after sex (OR=37.8, 95% CI: 11.2–127.4).
Conclusions  Behaviors that may cause RTI/STI exist among Chinese women who have sex with women. Researchers should consider these behaviors when planning corresponding prevention and interventions.
In the 1990s, the health problems and needs of lesbians attracted attention in both the United States and Canada,[i] and over the past ten years more research has been conducted exploring sexual behavior and health among the larger category of women who have sex with women (WSW). The distinction is not just academic. Sexual orientation is not identical to sexual behavior;2-4 in addition to lesbians, WSW can also include bisexual women, heterosexual women, and some women who choose not to identify at all for reasons related to culture, ethnicity, occupation, or peer support groups.5 Several Chinese studies of lesbians have been done in the fields of anthropology and psychological health; however, there have been no studies targeting WSW.6-8
 
Some health related risk behaviors like sex with men,9 multiple bisexual partners,10 and contract marriages (marriages between gay men and lesbian women) exist among WSW. Also, some studies have shown that WSW on average consume more alcohol than heterosexual women, which is a risk factor for STI transmission.11-13
 
Similar to Chinese men who have sex with men (MSM),14 some WSW may identify as homosexual but have a past or current sexual history that includes heterosexual intercourse. Compared with women who only had sex with men, those who reported a history of sex with both women and men showed a higher risk of being infected with an STI.15-17 HIV and sexually transmitted infections (STIs) can be transmitted through the exposure of a mucous membrane, especially if the tissue is cut or torn, to vaginal secretions and menstrual blood in the process of women-women sex.18 Potential HIV transmission between women has been reported in some studies based on case reports.19,20
 
WSW generally avoid routine physical examinations due to either their own lack of perceived need or discrimination from healthcare providers, which can negatively impact their health.21 Previous studies have reported that WSW concealed their same-sex history from physicians.22,23 This can affect their ability to receive an accurate diagnosis and treatment.7
 
This paper aims to describe WSW in China and explore risk factors for their reproductive tract infections (RTI) including sexually transmitted infections (STI).
 
METHODS
 
Participants 
We recruited 224 WSW who were 18 years of age or older and had ever had sexual encounters with other women involving oral, vaginal or anal sex. For the purposes of this study, the category “WSW” was defined to encompass both women who only have sex with women, and women who have sex with women and men. Participants were recruited through outreach in venues and online from September 2010 to April 2011 in Beijing, China.
 
Participants were recruited through advertising the study in LGBT (lesbian, gay, bisexual, transgender) internet resources in Beijing, video and radio dissemination, blog and forum promotion, leaflet distribution and presentations in lesbian and gay bars and non-governmental organizations.
 
Of the 224 WSW recruited, all accepted a physical examination; the blood test was accepted by 216 (96%), the gynecological exam by 202 (90%), and both by 194 (87%) women.
 
Ethics
Trained interviewers explained the purpose, process, benefits and potential risks before obtaining informed consent from participants. Study participation was both anonymous and voluntary. The study was approved by the institutional review board of the Center for Disease Control and Prevention, Chaoyang District, Beijing, China.
 
Survey and interview
After reading and signing an informed consent statement, all 224 participants completed a survey through face-to face interviews with one of three trained interviewers. Participants were interviewed in private rooms. The surveys were reviewed after completion by the principal researcher, who also designed the questionnaire. The content of the survey included demographic information, sexual behaviors and health knowledge, and health seeking behaviors.
 
Participants were also asked if they were aware of the “G-spot” and if they or their partners deliberately sought it during sexual activity. The G-spot was a term firstly coined by Addiego et al24,25 in 1981 to recognize Dr. Grafenberg, who first postulated the existence of the area in 1950. Although the existence of the G-spot is disputed, preliminary research revealed that Beijing WSW often made it the focus of their sexual activity so it was addressed in this study. The G-spot in this study refers to an alleged small but often highly sensitive area on the anterior wall of the vagina, about a third of the way up from the vaginal opening.
 
Clinical specimens
A gynecological examination was conducted by trained physicians and cervical samples were collected for evaluation of Neisseria gonorrhoeae (Gram stain), and Chlamydia trachomatis (Colloidal gold, double antibody sandwich method). Vaginal secretions were tested for candidiasis using wet mount and Gram stain. Bacterial vaginosis (BV) was diagnosed with a BV Quick-test kit (known outside of China as BV-blue™). Syphilis was diagnosed using a Sandwich ELISA, with confirmation by Treponema pallidum haemoagglutination tests and Syphilis reagin tests. HIV was diagnosed by ELISA (Alisei 20100721, Italy). Hepatitis B virus (HBV) was assessed using hepatitis B surface antigen by ELISA (Alisei 20100602, Italy), with confirmation by Chemiluminescence immunoassay (Abbott Laboratories, I2000, America) with Acridinium ester (08164 LF00). Anti-hepatitis C virus (HCV) antibody (ELISA using SLT 20110107 equipment, Beijing, China) was used to test for HCV screening, with confirmation by Chemiluminescence immunoassay (Abbott Laboratories, I2000, USA) with Acridinium ester (04385 LI00). Herpes simplex virus type 2 (HSV-2) was diagnosed with HSV-2 specific IgM ELISA (SLT 20110114 equipment, Beijing, China), with confirmation by ELISA (DIEESSE 410D-J, Italy).
 
In data analysis, STIs were divided into curable and incurable STIs. Curable STIs included gonorrhea, chlamydia, HBV and syphilis. Incurable STIs included BV, HIV, HBV and HSV-2.
 
Each participant was provided an 8-digit identification number and was asked to return 2 weeks later to receive their test results and posttest counseling. All volunteers diagnosed with an STI were examined again and offered appropriate medical treatment.
 
Statistical analysis
Univariable analyses, multivariable analyses and odds ratios calculations were performed as appropriate. Variables significant at P <0.1 in univariable analyses were considered for inclusion in the multivariable regression model, along with variables derived from prior hypotheses. Epidata software (Epidata 3.0 for windows, The Epidata Association, Odense, Denmark) was used to double enter and validate the data. Data analyses were performed using SPSS 17.0 (SPSS Inc., Chicago, IL, USA).
 
RESULTS
 
Participant characteristics
The average age of the 224 women was 25.6 years, and 83.9% (188/224) were 20–29 years old. Of all the women, 33.9% were local residents of Beijing, 93.7% (210/224) had a university-level education and 67.4% (151/224) self-identified as homosexual.
 
All but 10 (95.5% (214/224)) of the women described their marital status as unmarried living alone, with parents, with female partners or other women, or with a man. Of the remaining 10 women, five were divorced or widowed and five were married to men. Two of the five who were married had husbands who were MSM (men who have sex with men) and both couples were in contract marriages stipulating that no sex occurred. One whose husband was MSM and whose parents were not in the same city did not live with her husband, and the other whose parents were in the same city sometimes lived with her husband, who was exclusively homosexual.
 
Prevalence of STI/RTI and sexual behaviors
When asked about sexual behavior with either men or women, 97.3% (218/224) of the women reported engaging in digital- or penis-genital contact, 80.8% (181/224) oral-genital contact, 20.1% (45/224) use sex toys with genital, 6.7% (15/224) anal sex, 1.8% (4/224) fisting, 1.3% (3/224) group sex, 4.5% (10/224), and 0.4% (1/224) phone sex. Digital- or oral-genital contact with women were reported by 91.5% (205/224) and 73.7% of participants, respectively. Moreover, 39.7% (89/224) reported genital-genital contact with other women.
 
In the year preceding their participation in the study, 92% (206/224) of women reported sexual relations with women, 26.8% (60/224) of whom had had sex with two women or more. Of these 206 women, 24.3% (50/206) reported condom use in the last sexual encounter with their female partners, and 48.1% (99/206) reported condom use with their female sexual partners at least once in the last year, generally by using a male condom to protect the fingers during intercourse. The association between attitude toward risk and condom use either at the last sexual encounter or in the last year was not significant in Chi-squared tests (P=0.09, P=0.07, respectively). Of the 206 women who had sex with women in the past year, 102 thought the risk was moderate or high, and 104 thought it was low or very low. Only 29 of the 102 who thought the risk was moderate or high used condoms in the last sexual encounter and only 54 of the same 102 took preventive measures at some time in the past year.
 
Seeking the G-spot
The concept of the alleged G-spot (the Grafenberg spot) was known to 90.6% (184/203) of participants, 65.2% (120/184) of whom mentioned having had their G-spot stimulated by their partner during sex. Of these 184 women, 29.9% (55/184) said they experienced this G-spot stimulation every time, and 35.3% (65/184) experienced it sometimes. More than one-third (36.4% (67/184)) of those noticed the G-spot bleeding during or after sex (excluding bleeding caused by fingernail damage and bleeding during menstruation). A positive association was noted between the frequency of seeking the G-spot and bleeding (P <0.001) (Table 1). The percentage of participants who bled during or after sex increased commensurately with the frequency of seeking the G-spot, including 7 participants who said their partners attempted to stimulate their G-spot every time during sex and reported bleeding often.
 

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Table 1. Associations between bleeding during sex and frequency of seeking the G-spot
 
STI infection rates
Infection rates in this population were 15.8% (32/202) for gonorrhea, 3.5% (7/202) for Chlamydia trachomatis, 0.5% (1/216) for syphilis, 14.4% (29/202) for bacterial vaginosis, 0.9% (2/216) for hepatitis B, 0.5% (1/216) for hepatitis C, and 6.9% (14/202) for candidiasis.
 
There were 26.8% (52/194) of participants who were infected with any STI (BV, gonorrhea, chlamydia trachomatis, hepatitis B and syphilis) and 21.1% (41/194) infected with a curable STI (excluding BV); 31.4% (61/194) were infected with any RTI (above STIs, candidiasis, HBV, or HCV). No woman had a positive HIV or herpes simplex virus test.
 
Gonorrhea infection and associated risk factors
Factors associated with gonorrhea infection in univariable analysis included non-Beijing local residency (OR: 2.2; 95% CI: 1.3–3.7) and genital-genital contact (OR: 2.2, 95% CI: 1.0–4.8). Both non-Beijing local residency (OR: 2.1; 95% CI: 1.2–3.8) and having had genital-genital contact (OR: 3.1, 95% CI: 1.3–7.2) were also significant in the multivariable model.
 
Curable STI associated risk factors
Factors associated with any curable STI in univariable analysis were non-Beijing local residency (OR: 1.6; 95% CI: 1.0–2.4), genital-genital contact (OR: 2.6, 95% CI: 1.3–5.4), bleeding during or after sex (OR: 15.8; 95% CI: 4.7–53.4), and the interaction variable seeking the G-spot bleeding during or after sex (OR: 1.6; 95% CI: 1.1–2.1) (Table 2). Non-Beijing local residency (OR: 1.9; 95% CI: 1.2–3.0), and bleeding during or after sex (OR: 18.1; 95% CI: 5.2–62.6) were significantly associated with any curable STI in multivariable analysis.
 

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Table 2. Factors associated with any curable STI among 194 WSW in Beijing, China
 
RTI associated risk factors
Factors associated with RTI in univariable analysis were age >25 years old (OR: 1.8; 95% CI: 1.0–3.4), genital-genital contact (OR: 2.1; 95% CI: 1.1–4.0), and the interaction variable bleeding during or after sex (OR: 37.8; 95% CI: 11.2–127.4), seeking the G-spot bleeding during or after sex (OR: 1.9; 95% CI: 1.4, 2.5) (Table 3). Only bleeding during or after sex (OR: 37.8; 95% CI: 11.2–127.4) was significant in the RTI multivariable model.
 

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Table 3. Factors associated with any RTI among 194 WSW in Beijing, China
 
STI symptoms and treatment
During the past year, 43.3% (97/224) of participants reported painful urination, abnormal vaginal discharge, or genital ulcers. Of these participants, only 28.9% (28/97) went to a hospital for treatment, 23.7% (23/97) did nothing, 25.8% (25/97) went to pharmacies to buy medicine for themselves and 19.6% (19/97) cleaned the vagina with water or gynecological lotion (douching).
 
Importance of health concerns
Most women indicated gynecological disease (82.1% (184/224)), STIs (34.8% (78/224)), and HIV/AIDS (30.8% (69/224)) as health issues that were of greatest concern to them. A total of 47.8% (107/224) of participants had ever gone to see a gynecologist or practitioner specializing in STIs. However, only 10.3% (11/107) of those who had seen a specialist had told their doctors about their women-women sexual behavior. The reasons given for not disclosing their sexual behavior were: doctors did not ask them (54.2% (52/96)); participant believed it was not necessary to tell (12.5% (12/96)); concern about disclosure of sexual orientation (31.3% (30/96)); and patient had had no women-women sexual encounters since their last doctor visit (2.1% (2/96)).
 
DISCUSSION
 
Along with a complementary manuscript, this is the first reported study in China to explore the relationship between the behavioral factors of WSW and the transmission of STI/HIV.26 In WSW, as with women who have sex with men, genital-genital contact was risk for STI. The very strong association of STI risk with bleeding was a surprise and suggests a serious issue for consideration in counseling around both sex during menstruation and vigorous sexual activity that might cause bleeding.
 
Prior research about WSW sexual health in other countries indicates that up to 44% of WSW have a lifetime history of one or more STIs; however, there is a dearth of research that has examined the specific factors related to infection.27 The foundation of the study sheds some light on information that may help in designing future WSW studies and STI interventions.
 
Both ulcerative and non-ulcerative STIs increase the risk of HIV transmission by augmenting HIV infectiousness and susceptibility through a variety of biological mechanisms.28-30 HIV infection rates of 1.2% and 6.1% have previously been reported among WSW/lesbians.31,32 The risk factors noted for HIV infection among WSW were injection drug use and unprotected sex with males. No HIV-positive WSW was found in the current study, most likely because the study was not conducted in an area with high HIV prevalence. In addition, many participants mentioned they received an annual physical examination provided by their employers, which may indicate that women who already knew their HIV-positive status may not have participated in the survey. One woman accompanied her partner to the survey, but the partner said the woman herself did not take the survey because she had been infected with hepatitis B. It is conceivable, therefore, that women who already knew that they were diagnosed with other STIs (including HIV) may also have chosen not to participate.
 
The sexual behaviors reported by the 224 women correspond to the results of similar studies in other countries, indicating that the most commonly reported sexual activities between women were digital-genital and oral-genital contact.10,33 A Chinese sociological study of women-women sexual behaviors reported that digital-genital contact had a prevalence of 60%–98%, oral-genital contact had a prevalence of 60%–80%, and using sex toys, fisting, anal sex, and sadomasochism had comparatively lower prevalence from 1% (sadomasochism) to 40% (anal sex).34
 
The condom use rate was not significantly higher among women who perceived the risk of HIV and STIs through sex without protective measures as moderate or high, compared to all other women in the survey, which showed that attitude did not definitively influence the corresponding behavior. One participant who had tested positive for Chlamydia appeared very anxious, but in a private discussion after the study she said she still did not take any preventive measures with her female sexual partner because she thought that using a condom might negatively impact their relationship. Interventions should not only promote knowledge and positive health attitudes, but also take into account issues such as culture. Traditional Chinese culture holds that emotionally intimate relationships should be paralleled with equally sexually intimate body contact without barriers. This belief, combined with the thought that the relationship should take precedence over the risk of STI, may lead to low or no condom use during sex.
 
The responses related to the G-spot were surprising because knowledge of the spot has not been openly discussed in China. The existence of the spot is still debated,35 although it has been widely accepted among women, the nonscientific population, and the press.36 “We see the G-spot as a gift that God sends to us lesbians because it can only be stimulated digitally; further, it makes us feel more equal to heterosexual people”, one participant said. Another participant mentioned that WSW, like males in heterosexual relationships, want to satisfy their partners vaginally so they will try anything to bring their partners pleasure. Therefore, they may persistently seek the G-spot even if their initial efforts are not fruitful. The data indicate that most of the WSW participants believed in the existence of the G-spot and its function in stimulating orgasm, leading them to intentionally search for it. The association between seeking the G-spot and bleeding during or after sex suggests that the WSW sexual behavior was influenced by knowledge that was accepted despite not being confirmed scientifically. Because HIV and STIs can spread through vaginal secretions and menstrual blood,37 bleeding caused by G-spot exploration may become a potential source of infection to either the bleeding woman or her partner if she has any open wounds. Sexual education programs should highlight that the existence of the G-spot has not been proven conclusively and the sexual behavior of seeking it should be gentle to avoid bleeding.
 
As for the women’s reluctance to disclose their same-sex behavior to doctors, the main reasons given were doctors’ failure to ask and social discrimination. It is most likely that doctors do not ask a woman whether she has women-women sex because they think WSW health is synonymous with heterosexual women’s health and there is no need to identify women as lesbian or bisexual.38 It may also be because doctors may not even be aware that female homosexual behaviors exist. In addition, doctors may want to avoid causing embarrassment for themselves or the patient, as discussing homosexuality in China is not generally accepted. The health risks of WSW are heightened because their unique characteristics are overlooked by physicians,39 which in turn influence the health-seeking patterns of WSW.38
 
By and large, the general population regards a personal history of at least one same-sex encounter as indicative of homosexual identity. Lesbians in the United States have reported low satisfaction with health services because of negative provider attitudes and a lack of cultural understanding of the context in which their health is shaped.40 Consequently, prior experience with discrimination and homophobia reduces the likelihood of disclosure of sexual orientation during medical consultations.38
 
Differences in health status for WSW result from negative attitudes and experiences within society and the healthcare system, which in turn influences patterns of health-seeking behavior, health-risk factors and specific health issues.38 That 52.2% (117/224) had not seen a gynecologist or a practitioner who specializes in STIs was could be because some participants had no symptoms. Many may have feared discrimination because non-heterosexuality is considered abnormal, which may influence their health-seeking behavior and lead them to skip necessary routine gynecological tests.
 
Limitations of the research include the absence of state-of-the-art STI/RTI diagnostics for all organisms. Some versions of the reagin test (RPR) used to screen for syphilis in this study have a sensitivity of 85.45% and a specificity of 96.1%.41 In one study, using wet mount as a screening method for candidiasis showed a sensitivity of only 61%, although the specificity was nearly 100%.42 In addition, our study used the relatively insensitive Gram stain for gonorrhea. The US CDC does not recommend this method for screening in women due to its “low sensitivity” and “variable specificity”, but it is standard practice in China.43,44 Social acceptability bias and recall bias may also be limitations, given the sensitive and perceived stigmatized nature of some of the history elicited. For this study, all gynecological samples were taken by an experienced physician and observed by an interviewer.
 
The study data demonstrate that Chinese WSW are in need of STI prevention and intervention services. Professionals and members of the general population should expand their knowledge of the sexual practices of WSW (including specific sexual behaviors and attitudes that directly influence sexual health), provide reasonable guidance regarding risky and vulnerable behaviors; and develop strategies for STI intervention programs and their corresponding evaluation. This is necessary not only because of the risk of STI infection among WSW themselves, but also because of possible transmission to men as some WSW engage in sex with men and vice versa, similar to what has been mentioned in other studies.39,45 In addition to promoting sexual health among WSW, practitioners need to develop skills and attitudes that allow non-judgmental sexual history-taking from female patients, without making assumptions about sexuality or sexual behavior, in order to facilitate discussion of the risks that WSW may face. Furthermore, some knowledge regarding safe sex should be disseminated through the general population to avoid misunderstandings that may have harmful health consequences.
 
A British probability survey of 6399 women aged 16–44 years conducted from 1999 to 2001 found that same-sex genital contact was reported by 4.9% of the respondents.46 An Australian random telephone survey of 9134 women demonstrated that 15.1% of the women had had same-sex attraction or sexual experience.47 A study in the United States indicated that women-women sex behavior is increasing due to changes in social norms and public attitudes toward homosexuality over the last two decades.48 The same trend could possibly be true in China; a national Chinese surveys about college students in 1997 showed that women-women sexual contact rates among female college students were 18.1%.49
 
Based on the huge WSW population that might exist in China and the fact that their sexual health status is far from ideal, we should take them into serious consideration when designing and conducting prevention and intervention programs.
Acknowledgements: We would like to acknowledge Professor PAN Sui-ming of the School of Sociology and Population Studies, Renmin University of China, for his assistance with the analysis of bleeding and STI transmission.
 
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  1. Mega-projects of Chinese National Science Research for the 11th Five-Year Plan,No. 2008ZX10001-003;