Sexual health status of women who have regular sexual relations with men who have sex with men in mainland China

Background Men who have sex with men (MSM) are a high-risk group for sexually transmitted diseases (STDs) and human immunodeficiency virus (HIV) infection. In China, the vast majority of MSM feel forced to marry or plan to marry women, according to traditional Chinese culture. Women who have regular sexual relations with MSM, called tongqi in mainland China, live with a high risk of STDs or HIV infection, but these risks are often ignored. Our investigation of this group of the women is a preliminary study that aims to understand the sexual health problems of tongqi and related factors. Methods This study relied on website mobilization and was funded by tongqi. Participants were limited to women who had sex with MSM to whom they were married (in-GWs), whom they had divorced (ex-GWs), or with whom they were friends (GGFs). The data were collected using questionnaire software. Results A total 144 valid surveys were returned from 100 in-GWs, 33 ex-GWs, and 11 GGFs. Average respondent age was 32.8 ± 6.4 years (range 22 to 58 years). Among in-GWs and ex-GWs, over 95% learned that their husbands were MSM after marriage. More than half of respondents had had sex before marriage, and one-third of those women had sex partners other than their husbands. In addition, 35.3% of tongqi had STDs symptoms. About 50% participants had had oral sex with sex partners of MSM and 10% had had passive anal sex, with low condom use during both oral (9.7%) and anal sex (23.1%). Most tongqi had misunderstandings about STDs and HIV and less than 30% had undergone HIV screening. Among participants tested, 5.6% were HIV positive. A total 93.5% of respondents believed that laws should be established to protect the sexual rights of women. Conclusions Women who have regular sexual relations with MSM face adverse sexual health issues and are susceptible to STDs and HIV infection. Measures must be taken to protect the rights and interests of tongqi in mainland China. Electronic supplementary material The online version of this article (doi:10.1186/s12889-017-4096-z) contains supplementary material, which is available to authorized users.


Background
Women who have regular sexual relations with men who have sex with men (MSM) include three subgroups: 1) women who have sex with MSM to whom they are married; 2) those who had sex with MSM to whom they were married but who they later divorced; and 3) women who have regular sexual relations with MSM but who are unmarried (female friends). These women are called tongqi in mainland China, and the three subgroups are respectively designated in-GWs, ex-GWs, and GGFs.
Today, there is a more open attitude toward homosexuality in western countries, with some passing legislation to legalize homosexual marriage. In contrast to these countries, homosexual marriage is illegal in China as well as in many other developing eastern countries. As a result, the status of heterosexual women who are married to MSM varies among different countries worldwide. In developed countries such as the United States or Switzerland, some MSM have regular sex with women or marry women with a different sexual orientation. The political, cultural, and economic backgrounds of such countries permit greater individual freedom of choice and legal protection [1,2]. Few women have regular sex with MSM, and surveys of these women are focused mainly on qualitative psychology [3][4][5]. According to a 2002 survey of MSM in the United States, married MSM were more likely to have unsafe sex than unmarried MSM, thus exposing their wives to a higher risk of human immunodeficiency virus (HIV) infection. Future strategies for the prevention of acquired immunodeficiency syndrome (AIDS) among such women should be more targeted [6]. A 2005 statistical analysis of a large sample of MSM in India indicated that 41.8% of MSM were married to women [7]. Data from a 2010 survey of 443 MSM in Tanzania who did not use injection drugs showed that 29.1% of them were married and 11.9% were separated, divorced, or widowed [8]. Another survey of MSM with HIV/AIDS carried out in India showed that women whose sex partners were MSM were at risk for HIV/AIDS [9]. Surveys of MSM with HIV/AIDS in some countries reveal a high percentage are married or have had sex with heterosexual women; however, few surveys have focused on these women [7,10,11].
Evidence from recent surveys in China has revealed that the marriage status of MSM to women is significantly different from that in Europe and the United States but is similar to that in many developing countries [12,13]. A 2011 survey of 318 MSM infected with HIV in China demonstrated that 37.7% of them were married and in some cases, their wives had also been infected with HIV, a situation that should be urgently addressed [14].
The reasons why MSM marry heterosexual women include traditional moral, philosophical, and religious constraints (in which MSM consider a wife and family to act as a "shield" against negative social opinion), a desire for family life and children [6], and unawareness of one's own sexual identity.
It is worth noting that as a very important group closely related to MSM, tongqi receive little attention and support, a phenomenon that is contrary to the requirements of the theory of social construction [15]. Based on this theory, we conducted a survey of tongqi from 2011 to 2012 that aimed to understand their physical and mental health problems, marital status, and influencing factors.

Procedure
Our survey relied on "Tongqi Homeland", the first webbased grassroots organization for women who have regular sexual relations with MSM in China, established in 2009. This organization provides services to tongqi such as psychological counseling, support, and legal advice for divorce. The survey was mainly mobilized by Tongqi Homeland volunteers, most of who had been married to MSM. Women who participated in the survey were required to meet three conditions: 1) they had had regular sex with MSM (this included in-GWs, ex-GWs, and GGFs); 2) they had confirmed that their sex partners were not heterosexual and had had sex with other men; and 3) they had registered on the Tongqi Homeland website at least 1 month before the survey began.
The survey included three kinds of questions (Additional file 1) for in-GWs, ex-GWs, and GGFs, to set the polygraph. Research assistants provided the women with detailed information about the survey and obtained verbal informed consent. Women consented to participate in the survey anonymously, so records by name were not maintained.
A one-on-one mode of recruitment was used for the survey. Subjects were identified by phone or using the online platform. User keys that could only be used with one computer were automatically generated for all subjects. Survey software (http://www.sojump.com) automatically recorded the reading time and filtered out questionnaires that were submitted in less than 10 min. Links to the questionnaires were not sent over public Internet servers but rather were sent directly to subjects using instant messaging software such as QQ. Surveys were automatically saved and remained active for several hours until completion. User keys were automatically canceled after a questionnaire was completed and submitted. The survey remained active for 3 months (from April to June 2012).
The survey procedure was approved by the Institutional Review Board of the Affiliated Hospital of Medical College, Qingdao University.

Measures
Information on participants' demographic characteristics included age, residence (rural, urban), present residence address, educational background, whether the last marriage was the first marriage (yes, no), and whether the participant had children (yes, no).
Information on participants' sex behaviors included whether they had had sex before marriage, the frequency of their sexual activities, whether participants had had oral or anal sex, whether they had been abused during sexual activity, whether they had sex with men other than their husbands, and the reasons for having sex with other men.
Information on sexually transmitted diseases (STDs) and HIV included four aspects. First, knowledge and attitudes about STDs and AIDS were queried by the following questions: Do a man's normal-looking genitalia indicate that he has no venereal diseases?, Are some STDs still infectious even though they are completely cured?, Can some STDs cause death?, Do women with syphilis, gonorrhea, and other STDs have no clinical manifestations for a long time?, Can AIDS be transmitted through blood, from mother to child, and by sexual contact?, Is it difficult to detect HIV infection because there are often no symptoms for some time?, Is HIV infection similar to AIDS?, Do people with AIDS feel that life is meaningless?, Is the risk of HIV infection higher after learning that sex partners are MSM?, Should women who are the sex partners of MSM undergo testing for HIV infection?
The second aspect of information about STDs or HIV infection and testing included the prevalence of STD/ HIV infection and whether participants had been tested for STDs or HIV. The third involved the use of condoms and whether participants used condoms during vaginal, oral, or anal sex; the frequency of condom use; and whether participants would change their habitual condom use during sex after learning that their sex partners were MSM. Fourth, the topic of abortion was approached by asking whether participants had had an abortion and whether they knew that their sex partners were MSM when deciding to have an abortion.
As for sex education and the right to sex, we asked the following questions: When participants were told that their sex partners are MSM, did they believe that being MSM was a common phenomenon?, After divorcing an MSM, do participants then suspect that all men that they have encountered are MSM?, Can marrying an MSM cause women serious harm?, Should sex outside of marriage be okay when there is no normal sex life in the marriage?, Do MSM who conceal the truth so as to get married seriously harm the rights of women?, Is there a lack of public education about sexuality in the country?, Should there be improvement in education about sexuality?, Should society accept MSM?, Should the rights and interests of MSM be protected so that they do not feel that they must marry women?, Should legal protection of the rights and interests of tongqi be instated?
Attitudes toward homosexuality were also investigated through the multiple-choice question, "What do you think about homosexuality?" Response options given were that it is sexual perversion, a mental illness (psychological barrier), a moral issue, or a normal phenomenon.

Demographic characteristics
A total 147 surveys were returned, 144 of which were valid. Participants included 100 in-GWs, 33 ex-GWs, and 11 GGFs. The average age of participants was 32.8 ± 6.4 years (median 31 years, range 22-58 years).

Sex behaviors
Before marriage, more than half (54.9%, 73/133) of tongqi had had sex with MSM. Of those women, only 28.6% (20/70) took the initiative for sex, 69.0% (49/71) reported that their partners could successfully perform sexual intercourse, and 95.5% (127/133) learned that their husbands were MSM after marriage. A total of 18.4% (23/125) had sex eight times or more per month; 6.4% reported having had sex eight times or more in the last 6 months (6/94). Among participants, 56.5% (70/124) had oral sex with MSM and 10.9% (13/119) Two ex-GWs were infected with HIV as were their exhusbands; one in-GW was not infected with HIV, but her husband was HIV-positive; and one GGF had not undergone testing, but her regular sex partner had tested positive for HIV.

Sex education and the right to sex
When they were told that their sex partners were MSM, most tongqi believed that the phenomenon of MSM was common (92.6%, 126/136); after divorcing, they suspected that all men they had encountered were MSM (61.3%, 19/31). In addition, most women felt that marrying an MSM is harmful to women (81.5%, 106/130), that sex outside of marriage should be okay if there is no normal sex life in the marriage (60.1%, 83/138), that MSM who concealed the truth to get married seriously harmed the rights of women (91.1%, 123/135), and that public education about sexuality was lacking in China (85.0%, 119/140). As a result, a high percentage of tongqi believed that measures should be taken to protect the rights of women and MSM, including improving education about sexuality (92.7%, 127/137), fostering social acceptance of MSM (52.5%, 73/139), safeguarding the rights and interests of MSM so that they do not feel they must marry women (67.6%, 94/139), and enacting legal protection of the rights and interests of tongqi (93.5%, 130/139) ( Table 5).

Discussion
This survey of women whose regular sex partners were MSM represents original exploratory research of sex and reproductive health among tongqi in mainland China.
Traditional Chinese culture highly advocates heterosexual monogamous relationships, with procreation considered the main purpose of sex and marriage [16]. Therefore, nearly all MSM feel obligated to marry women. This survey of women who were married to and whose sex partners were MSM confirmed this fact. It has been estimated that more than 90% of MSM marry women or believe that such marriage is inevitable [17]. In many surveys of MSM during recent years in China, social scholars have pointed out that unmarried MSM generally choose traditional marriage regardless of their true wishes [18].
There are some uncertain factors when estimating the number of tongqi in China. According to a population sample of the National Bureau of Statistics of China in 2012, the number of men whose first marriage was to a woman was 402.871 million [19]. According to data of Pan and Liu et al. [15,17], the total number of MSM in China is 7.614-10.515 million (M = 9.065 million). In addition, there are many women who have sex with men but are unmarried; thus, it can be estimated that there are nearly 10 million tongqi in mainland China. These women are at high risk of STDs and HIV infection related to sexual contact with MSM. Our survey revealed  that the health problems of tongqi are often ignored for extended periods by medical and health care professionals. Sex discrimination (the belief that women are inferior to men) has been a part of traditional Chinese culture since ancient times. This belief has a powerful and widespread influence on Chinese people. The principles of love and marriage are established by the patriarchal authority of the husband, attitudes of male chauvinism (women are expected to show obedience to the father before marriage then obedience to the husband after marriage, the husband controls the wife, and so on), and heterosexism [20]. These often result in stigmatization by sex, placing women at a disadvantage with respect to physical and mental health; their needs, such as an equal right to sex, are usually ignored. Some in the MSM community are firmly opposed to conducting surveys of tongqi for fear of discrimination because of their sex orientation [21]. Thus, carrying out relevant surveys is usually met with great resistance.
One recent survey showed that 60% of heterosexual married people who were under 40 years old had sex two or more times a week. In the last year, men who performed oral sex for women during sexual intercourse accounted for 38.8% of those surveyed; that percentage for women who performed oral sex for men was 35.2%. A total 8.5% of respondents had anal sex. The incidence of self-reported STDs among heterosexual people was 2.5% and that among "non-heterosexuals" was 33.6%; the risk of STDs infection among the latter group was 22.6 times that of the former. A total 9.7% of women reported that they had sex with other men while married [15]. This survey revealed that sex behaviors were clearly different for tongqi after becoming the sex partners of MSM.
A survey of 557 MSM in Nigeria who had had anal sex revealed that 48.1% had had sex with women in the past 2 months. Among those MSM, 45.1% had had anal sex, 74.0% had not taken protective measures, and 66% had had unprotected vaginal intercourse. Bisexual sex among MSM was related to being married to or living with women [22]. A large systematic review of data collected from the published literature showed that only 10% to 20% of younger MSM got married in China, but more than 50% married at older ages, had lower socioeconomic status, or made contact in certain places [23][24][25]. Surveys have also revealed that married MSM were more often infected with STDs or HIV than unmarried MSM [26,27]. According to another survey, less than 50% of MSM with AIDS had told their wives about their disease, and 28.6% of their wives had been infected with HIV [28]. Other surveys have indicated that MSM in China often have STDs. A survey in China of MSM with HIV and syphilis suggested that more than 40% have syphilis [29]. Compared with women sex workers, tongqi are more often infected with HIV because of engaging in unprotected sex with MSM or ignorance of their sex partners' sexual activities with men. This study proved that the level of risk for STD infection among this group of women was high, similar to that of MSM. Tongqi are vulnerable to the spread of STDs or HIV from MSM, a situation that has long been ignored. It is worth noting that the knowledge possessed by tongqi about these risks is far from being effective to prevent and treat STDs and HIV, with only a few women having undergone testing. In this study, most tongqi still had a negative attitude toward STDs or HIV testing, even after having received appropriate information. After learning that their partner was an MSM and having acquired some understanding about the relationship between being an MSM and STDs, some women stated that they would reduce sexual intercourse and increase the use of condoms to prevent sexually transmitted diseases; however, the risks of infection associated with premarital and extramarital sexual behavior remain. Additionally, it is difficult for some in-GWs to divorce their MSM spouses, so they are forced to live with the high risk of STDs for many years. This survey highlighted that most tongqi in our sample were quite positive about sex education. Our study also revealed the important fact that although only a handful of the women surveyed understood that modern science considers same-sex love to be a normal phenomenon within a minority group, most women in the sample were quite positive about sex education owing to their own unique experiences in marriage. A high percentage of the tongqi in our study realized that it was important to legally protect the rights of those with a different sex orientation and gender. Some surveys in China have introduced a perception of MSM that is in the interest of sustainable social development and have explained preliminarily the relationship between the AIDS epidemic among MSM and the protection of human rights [30][31][32]. Today, the lack of awareness about different types of interdependence, interaction, and mutually supportive relationships with respect to sex orientation and gender discrimination can result in the emergence of various human health problems.
"Women and AIDS" by the Joint United Nations Programme on HIV/AIDS (UNAIDS) points out that AIDS prevention among women is often neglected and recommends preventive measures, which are often unable to be controlled by women. This situation could be changed by challenging social ignorance, providing women with support services, creating a safer environment for women, reducing the vulnerability of women through policy reforms, and other similar approaches. Organizations of women and gender in China have reported that gender inequality is the most common type of discrimination and that the intersection between marriage and sexual orientation serves to place women at the greatest disadvantage because multiple social identities must be maintained. These fit with various characteristics of Chinese women whose regular sex partners are MSM. Medical and health care staff in mainland China would benefit from the vigorous promotion of bioethics education on gender and sex equality and protection of the rights and interests of tongqi, to improve awareness about the health of this group. With greater openness and awareness about human rights in Chinese society, it is expected that the number of women who marry MSM will decrease, as will the occurrence of associated health problems.
It should be mentioned that our analysis was from a methodological point of view, which has limitations for the survey of a small part of this social group [15]. The participants in our survey were not randomly selected but were drawn from volunteers via a website. Women who were concerned about and knew their husband's sexual history or who were unhappy in their marriage took part in this survey; thus, the results may not representative of the entire population of tongqi in China. Our survey leaves many questions unresolved. It is conceivable that further social changes will emerge, enabling larger sample surveys to be conducted in the future that address the physical and mental health of tongqi in China.

Conclusions
In traditional Chinese culture, procreation is considered to be the main purpose of sex and marriage; therefore, nearly all MSM feel obligated to marry women. Most of the 144 tongqi surveyed in the present study did not know that their sex partners were MSM before getting married. One-tenth of participants were abused during sexual intercourse. During sex with their MSM sex partners or with other sex partners, some tongqi had had oral sex and anal sex with little or no condom use. Most of the women surveyed had misunderstandings about HIV/AIDS and STDs and some had symptoms of STDs. A few had undergone HIV testing, with 5.6% testing HIV-positive. Most participants felt that there was a great lack of sex education in mainland China and that improvement in sex education was needed. Most participants thought protecting the rights of MSM was also important for the rights of women and that relevant laws should be established to protect women's sexual rights. Taken together, our analyses indicate that women who have regular sexual relations with MSM are often ignored for long periods; they therefore face adverse sexual health issues and are susceptible to HIV and STDs. Proper measures must be taken to protect the rights and interests of tongqi, such as by educating MSM and society as a whole, to improve equality of gender and sex orientation. Abbreviations AIDS: Acquired immunodeficiency syndrome; Ex-GWs: Women who had sex with MSM whom they had divorced; GGFs: Women who had sex with MSM with whom they were friends; HIV: Human immunodeficiency virus; In-GWs: Women who had sex with MSM to whom they were married; MSM: Men who have sex with men; STDs: Sexually transmitted diseases; UNAIDS: Joint United Nations Programme on HIV/AIDS