Fig. 3.1
Incidence rates for most common infection-associated cancers in US women
It is estimated that 4 % of US women engage in sexual relationships with other women [3, 4]. Although population-level data are somewhat limited, it is estimated that 0.3 % of individuals in the US identify as transgender, with a higher percentage of transgender women than men [4]. As previously mentioned, our knowledge of the most basic epidemiologic data for cancer in sexual minority women is hampered by the fact that the SEER program does not include reporting of sexual orientation or gender identity as essential demographic variables for use in characterizing cancer burden. While a number of studies have examined barriers to cancer prevention in lesbian and bisexual women (e.g., Tracy et al. [5, 6], Matthews et al. [7]), particularly breast and cervical cancer, no studies that we are aware of have characterized incidence, prevalence or mortality from these infection-associated cancers for sexual minority women as a population. Consequently, our discussion must focus on earlier disease endpoints such as incident and prevalent infections associated with cancer.
Causes and Prevalence of Sexually Transmitted Viruses
Bacterial infections have been linked to stomach cancer (H. pylori), non-Hodgkin lymphoma (Epstein-Barr), and bladder cancer (Schistosoma haematobium); however, these cancers are relatively rare among women and are presumably even more rare when considered for sexual minority women who comprise such a small proportion of the general population. Of the viral pathogens associated with cancer, nearly all can be transmitted through sexual contact. Consequently, the focus in this chapter will be on cancers that are primarily associated with viral sexually transmitted infections (STIs) known to be associated with cancer (see Table 3.1).
Cervical | Human papillomavirus (HPV), with or without HIV |
---|---|
Anogenital cancers | HPV, with or without HIV |
Oropharyngeal | HPV, with or without tobacco and/or alcohol consumption |
Liver | Hepatitis B (HBV), Hepatitis C (HCV) |
Sexual minority women are at risk of many STIs through skin-to-skin contact, mucosal contact (e.g., mouth to vagina), exposure to vaginal fluids or menstrual blood, and sharing of sex toys. While many STIs are less efficiently transmitted between same sex partners, less efficient transmission is not equivalent to zero risk. The remainder of this section reviews the basic epidemiology of viral STIs associated with cancer in women in general and when available LBT women.
HPV: HPV is a group of viruses that can be sexually transmitted via skin-to-skin contact, including oral-genital and/or digital-genital, and sharing of sex toys. There are more than 50 types of HPV that can infect the anogenital tract [8]; see Munoz et al. [9] for review. Infection with certain high-risk (i.e., oncogenic) strains of HPV can lead to cervical cancer; HPV has also been linked to increased risk of some anogenital (e.g., anal, vulvar, vaginal) and oropharyngeal cancers. Many, though not all, risk factors for HPV are related to sexual behavior. Sexual risk factors include unprotected sexual activity with an infected partner, number of lifetime sex partners and the partners’ sexual history, early age of sexual debut, and inconsistent condom use [10]. Non-sexual risk factors include smoking, number of pregnancies, and genetic factors [10].
HPV infection is sufficiently ubiquitous, with lifetime prevalence of HPV infection estimated at 80 % for women [11]. In a 2007 analysis of data from the National Health and Nutrition Survey (NHANES), Dunne et al. [11] reported an overall annual prevalence of genital HPV infection to be 26.8 % among women between the ages of 14–59. There are relatively few studies that have directly assessed genital HPV infection among women who have sex with women (WSW). In a study of WSW, Marrazzo et al. detected HPV DNA in 30 % of genital tract samples of participants and 19 % of participants who reported no history of sexual intercourse with a male partner [12, 13]. Studies that have focused on the presence of serologic antibodies for HPV 6/11 or HPV 16/18 also confirm that HPV seropositivity did not differ among women with no history of sex with a male partner compared to women with no history of sex with a male partner. These findings suggest that while prevalence of HPV infection in WSW may be lower than what is observed in the general population, WSW are at risk of HPV infection, with and without history of sex with men. In fact, it is possible that WSW are at increased risk of developing HPV-associated cancers because of their behavioral risk profile.
HIV: HIV, the virus that causes Acquired Immune Deficiency Syndrome (AIDS), is a blood borne infection that can be transmitted via sexual contact and sharing of intravenous drug use (IVDU) paraphernalia. Risk factors for HIV infection include unprotected oral, vaginal or anal sexual activity with an HIV-infected partner, substance use, and number of lifetime sexual partners [14]. In 2011, the CDC estimated that 10,257 women 13 and older in the US were newly diagnosed with HIV [10], and approximately 0.5 % of US women are HIV positive [14]. Because female-to-female sexual contact is a much less efficient route for sexual transmission of HIV, the risk of HIV transmission among lesbians is believed to be low. Kwakwa and Ghobrial [15] reported a case of probable female-to-female transmission that was a hypothesized result of sharing of sex toys with an HIV-positive bisexual female partner. More recently, Chan et al. [16] reported a case of female-to-female HIV transmission in a serodiscordant couple from Texas; phylogenetic analysis of the HIV strains infecting each women revealed > 98 % sequence identity for three genes, providing persuasive evidence that HIV was transmitted from the HIV + women to her HIV- partner. As noted in the above section pertaining to risk for HPV infection, some lesbians do engage in high risk sexual behaviors that could increase risk of exposure to HIV. This includes high numbers of sexual partners, history of sexual activity with men, IVDU, and history of sexual activity with partners who are IVDU. Dworkin [17] reports that more than 20 % of IVDU are WSW. The reality is that WSW engage in a wide variety of sexual and other high risk behaviors that may lead to HIV infection with consequent increased risk of other infections associated with cancer.
HIV prevalence among transgender women is believed to be equal to or greater than that observed for other groups at high-risk for contracting HIV (e.g., men who have sex with men). Herbst et al. [18] reviewed studies published from 1990 through 2003 and found a laboratory-confirmed prevalence of 27.7 % among transgender women. More recently, Baral et al. [19] conducted a systematic review of studies published from 2000 to 2011 and noted an HIV prevalence of 21.6 % for transgender women in 5 high-income countries. These estimated rates are significantly higher than rates reported among lesbian, bisexual or heterosexual women.
HBV: Hepatitis B virus (HBV), like HIV, is a blood borne infection that is frequently sexually transmitted. Risk factors for HBV infection include unprotected sex with an infected person, history of multiple sex partners, co-occurring STI, men who have sex with men, IVDU share needles, syringes or other drug equipment, live with a person who has chronic HBV, occupationally exposed to blood, infants of infected mothers, hemodialysis, or travel to countries with moderate to high HBV rates [10]. Custer et al. [20] conducted a systematic review of published studies worldwide and noted that 5.4 % of the population has evidence of past or current HBV infection. More recently, NHANES analysis conducted by Wasley et al. [21] revealed that HBV infection among women is trending downward with a prevalence of 4.5 % for the period from 1988 to 1994 and 3.8 % for the period from 1999 to 2006. Studies of transmission of HBV between female partners are limited. Although not a study of sexual transmission per se, the previously mentioned study by Fethers et al. [22] found an HBV prevalence of approximately 5 % among WSW. This finding suggests that prevalence rates among WSW are similar to those observed for women in the general population; however, it is plausible that the Fethers study over-estimates the true prevalence of HBV in WSW because data for the study were derived from attendees at an Australian STI clinic who likely have a higher risk profile.
Prevalence data for HBV in transgender women is relatively sparse. A US-based study by Nuttbrock et al. reported HBV prevalences ranging from 6.5 to 36 % depending upon racial/ethnic group; HBV prevalence was highest among Hispanic and African American transgender women [23]. Similarly high prevalence of HBV was observed among transgender women from Argentina [19].
HCV: The CDC reports that hepatitis C virus (HCV) infection is the most common chronic blood borne infection in the United States [10]. HCV is most efficiently transmitted through large, repeated percutaneous exposures to infected blood (e.g., typically via IVDU). Although much less common, sexual exposures can also result in HCV transmission. Risk factors with sexual transmission of HVC infection include unprotected sex with an HCV-infected partner, history of multiple partners, presence of other STDs, or sex with trauma [10]. Non-sexual risk factors for HCV transmission include IVDU and sharing of IVDU equipment, needle stick injuries in health care settings, and sharing personal items (e.g., razor, toothbrush) that might be contaminated with traces of HCV-infected blood with an HCV-positive individual.
Analysis of NHANES data for the period from 1999 to 2002 indicates a prevalence of 1.1 % among US women [24]. There is relatively little research on the topic of HCV among lesbian and bisexual women. The largest available study that has examined HCV prevalence in lesbian and bisexual women is the Australian study by Fethers et al. [22]. This study noted a 5 % prevalence of HCV in lesbian and bisexual women seen at an STI clinic. These findings could be interpreted as reflecting greater risk of HBV and HCV in lesbian and bisexual women; however, it is more likely that the Fethers data overestimate the prevalence as women in that study were seeking care for STI and likely engaged in higher risk behaviors that in turn increased risk of these STIs.
As is the case for epidemiologic data for HBV among transgender women, prevalence data for HCV in transgender women is similarly scant. The previously mentioned study by Nuttrock et al. found HCV prevalence rates among transgender women in a US sample to range from 3.6 to 15.7 %, with higher rates observed among Hispanic and African American transgender women.
Genital Herpes: While genital herpes has not been linked directly to cancer, it has been noted that ulcerations that occur during outbreaks, increase the risk of acquiring other STIs, especially HIV [25, 26]. Infection with herpes simplex virus-2 (HSV-2) is the most common cause of genital herpes, although cases of genital herpes associated with herpes simplex-1 (HSV-1) have been reported. Genital herpes infection is typically transmitted via genital-genital contact or oral-genital contact. The biggest risk factor for contracting genital herpes infection is unprotected sexual activity with an infected partner. Other factors that increase risk of HSV-2 infection include early sexual debut, history of STI especially HIV, and number of lifetime sexual partners, and female sex [27–29].
The CDC reports an HSV-2 prevalence of 20.9 % in the general population of women [10]. Like epidemiologic data for HPV infection, the prevalence of HSV-2 among LBT is less well-known. In a study of nearly 400 lesbian and bisexual women, Marrazzo et al. [30] detected HSV-2 in 8 % of participants, most of whom were unaware of their HSV-2 status. In one of the few population-based studies of HSV among WSW Xu et al. used data from the National Health and Nutrition Survey (NHANES) to estimate HSV-2 infection in WSW. Xu et al. found an overall HSV-2 prevalence of 23.8 % and notably higher prevalences in WSW in the past year and WSW ever, 30.3 % and 36.2 %, respectively [31]. When prevalence was analyzed in conjunction with sexual orientation/identity, however, the authors found that among WSW ever, those who identified as lesbian had the lowest prevalence of HSV-2 (8.2 %), while HSV-2 prevalence among women who identified as heterosexual or bisexual was notably higher (45.6 % and 35.9 %, respectively). In a companion editorial, Marrazzo [32] noted that the complex associations between sexual behavior (i.e., WSW) and sexual identity (i.e., lesbian, bisexual, heterosexual) must be considered when evaluating population-level data for STIs as issues of wording, method of data collection, and focus on behavior vs. identity all potentially impact associations yielding over or under-estimates of the true prevalence of not only HSV-2 but presumably of other STIs as well.
Reasons for Differences in Rates from Heterosexual Population
In evaluating the epidemiologic data for the STIs of interest, it is noteworthy that although unique risk factors for each STI-associated cancer exist, there is a high degree of commonality for risk factors among STIs reviewed in this chapter. One of the most significant and consistent risk factors for all of the infectious agents reviewed in this chapter is unprotected sexual activity with an infected partner. Transmission dynamics for infectivity vary for same-sex and opposite-sex pairings, with infectivity appearing higher from male-female sexual encounters. However, two critical caveats must be considered. As noted earlier in this chapter a majority of women who self-define as lesbian have histories of sexual activity with male partners. Further, the work of Marrazzo et al. and the recent report by Chan et al. has provided compelling evidence that women with no history of sexual activity with a male partner can be infected with STIs through sole contact with an infected female partners. It is also noteworthy that WSW and transgender women report higher numbers of lifetime sexual partners than their heterosexual counterparts. Number of lifetime sex partners is another risk factor shared by all of the cancer-associated STIs.
Differences in STI rates among sexual minority women compared to heterosexual women appear to be largely explained by increased rates of STI risk behaviors such as greater number of lifetime partners [33, 35]; unprotected sexual activity with opposite sex partners [22] and same sex partners [35]; exchanging sex for money [36]; and history of intravenous drug use (IVDU) [34, 36, 37]. LBT women tend to report more lifetime sexual partners than heterosexual women. Beyond sexual risk behaviors, LBT women also have higher prevalence of alcohol and substances use [38–42] that may impair judgment in sexual situations leading to greater sexual risk taking. Among transgender women, there are particularly high rates of unprotected anal receptive intercourse and other high-risk sexual behaviors [43–45] (e.g., multiple causal partners, sex work, sex with MSM, alcohol and substance use) placing transgender women at elevated risk for STIs in general and particularly for blood borne STIs such as HIV, HBV, and HCV associated with cancer. Considered together, this suggests that LBT women, as a group, have a behavioral profile that may increase their risk for multiple STIs associated with cancer.
Interventions
Unlike many STIs, vaccines are currently available to prevent transmission of HBV and certain strains of HPV (e.g., strains 6, 11, 16, and 18). The HBV vaccine is recommended for all infants [46] with catch-up vaccination encouraged for children and adolescents born before infant vaccination became a recommendation. HPV vaccines are among those recommended for the general population of women between the ages of 9 to 26 years of age, but available data indicate uptake in the target age group has been modest [47], particularly in the United States. Review of public health efforts targeted to LBT women suggests that sexual minority populations are often not specifically encouraged to obtain such vaccines because their risk for STIs is poorly understood by medical and public health practitioners [48]. Although men who have sex with men (MSM) are viewed as a high-risk population that should obtain both of these vaccinations [49–51], the same perception is not widely held for LBT women. No studies or sexual programs were identified as part of the present review that expressly encouraged vaccination of LBT women with these two vaccines.
While health promotion materials exist that address safe sex practices for sexual minority women, these materials are not always easy to locate [52] and most have not been developed via evidence-based approaches. In a review of lesbian sexual health, Marrazzo [53] noted that no studies have directly assessed effectiveness or even acceptability of STI risk-reduction measures in lesbians. Barrier methods designed to reduce contact with cervicovaginal secretions (e.g., gloves, dental dams, female condoms) are likely effective in reducing risk of STI transmission. Harm reduction strategies for STI prevention include getting tested regularly for STIs and communicating STI status to partners, avoiding fluid exchange, avoiding unprotected contact, avoiding drug and alcohol use before sexual activity, and keeping nails short and groomed [54]. But again, evidence to suggest that LBT women are actively encouraged to engage in harm reduction strategies is currently lacking.
During the last decade, a limited number of small studies have evaluated interventions to reduce HIV and STI risk in transgender populations. Most of these interventions focused on awareness and education of prevention strategies that can reduce risk for STIs, especially HIV. One study found that a community-based sexual health curriculum was successful in improving attitudes about condom use and decreasing sexual risk behaviors [55]. A promising study by Taylor et al. [56] evaluated the Girlfriends behavioral HIV intervention. Using a pre-post design to assess changes in sexual risk behaviors, Taylor et al. found that a group-style risk reduction intervention led to a decrease in number of sexual partners and less unprotected sexual encounters with both male and female partners [56]. In a recent Cochrane review of social marketing interventions to increase STI and HIV testing among MSM and transgender women, it was noted that multi-media social marketing efforts have been effective in increasing HIV testing among MSM, yet no studies have examined this in transgender women [57]. While there appears to be recognition of the unique risk of HIV and other STI transmission for transgender women, this awareness has not been translated into evidence-based interventions that have been broadly implemented.
In general, sexual minority women are not seen by mainstream health practitioners as a priority population for safe sex and STI prevention messages. For example, it has been noted that medical health professionals have poor knowledge of the sexual health needs of LBT women and often do not ask about sexual orientation, sexual behavior or gender identity when taking patient health histories [58].