© Springer International Publishing Switzerland 2015
Ulrike Boehmer and Ronit Elk (eds.)Cancer and the LGBT Community10.1007/978-3-319-15057-4_1818. Current Policy and Research on Cancer in LGBT Communities Internationally
(1)
The Kirby Institute, The University of New South Wales, Sydney, Australia
Abstract
This chapter focuses on cancer policy and research from a number of countries around the world. It endeavours to determine if cancer rates in LGBT communities in these countries differ when compared with the general population. There are few countries with national LGBT-specific policies for screening and managing cancers. No country could be identified where demographic data on sexual identity/orientation were collected in population-based cancer registries. Thus the current knowledge of cancer risk, incidence and mortality in LGBT communities in these countries is gleaned from population-based surveys, results from studies of infection-related cancers, in particular HIV, and from clinical, behavioural and epidemiological research.
As population-based demographic data on sexual identity are unavailable in relation to cancer diagnoses, risk factors as surrogates for cancer risk, such as smoking, excess alcohol consumption and human papillomavirus (HPV) infection are explored. The prevalences of these factors are compared between lesbian, gay, bisexual, transgender and heterosexual populations where possible. General health data are also examined by sexual identity.
The main conclusions of the study are the higher incidence of some risk factors in the LGBT community in many but not all countries, the strong link between HIV and an increased incidence of infection-related cancers, and the issue that unless sexual identity can be documented in census and cancer registry data, population-based data on cancer incidence in LGBT people will remain rare. A “combination prevention” approach to cancer in LGBT communities, similar to that of HIV prevention is proposed.
Introduction
Though there has been an increased focus on LGBT health in recent years, the incidence and risk factors for cancer among LGBT people remain insufficiently studied in countries other than the United States[1]. In most countries, there is scarce high quality statistical information available on LGBT people, as medical systems such as national health and cancer registries do not routinely record diagnoses by sexual orientation. Thus it is not possible to develop estimates that link cancer incidence or mortality to sexual orientation. Consequently, efforts to address cancer disparities associated with sexual orientation are greatly impeded [2, 3]. Other factors contribute to this lack of data. Many LGBT people grew up with legal sanctions on their sexual behaviour and may be reluctant to disclose sexuality in health-related settings, even after homosexuality has been legalised in their country [4]. In a large number of countries, identifying as LGBT remains criminalised and highly stigmatised. Collection of health-related data is close to impossible and as a result there are no data on cancer among LGBT populations available. Due to perceived and actual homophobia, biphobia or transphobia, many LGBT patients do not disclose their sexual orientation to health care providers [5]. Often the issue of sexual orientation is never raised in cancer settings, and the person is presumed to be heterosexual. The current knowledge of cancer risk, incidence and mortality in LGBT communities arises from population based surveys, results from studies of infection-related cancers, in particular HIV, and from clinical, behavioural and epidemiological research. Many studies are small and prone to sampling bias, which limits the generalisability of findings [6]. Obtaining a representative sample of LGBT people is difficult as there is usually no well-defined sampling frame. The recent availability of same-sex marriage registers may offer a new and promising avenue by which a reasonably representative sample may be drawn [7]. As in settings where health care is provided, there may be reluctance to disclose sexual identity in research settings [8, 9]. The LGBT population, like all other populations, is a very heterogeneous group.
Published Policies and Legislation
It is beyond the scope of this chapter to review all global health policies and legislations as they relate to LGBT communities. An on-line search of policies from Canada, Australia and the United Kingdom, limited to English language documents was undertaken. Search terms included “health”, “policy” “health act” “LGBT”, “lesbian”, “gay”, “government” and “federal”. Examples of policies and legislations in these three countries are discussed below. No national cancer-specific LGBT policies could be identified.
a.
Australia
The Australian National LGBTI Health Alliance has estimated that the number of LGBT Australians aged over 65 years will reach 500,000 by 2051 [4]. The Australian Federal Government’s Commonwealth Department of Health and Ageing’s 2012 National Ageing and Aged Care strategy clearly states that LGBT people are a group requiring particular attention due to the past and continuing experience of discrimination. It highlights the limited recognition of LGBT people’s needs by service providers and in policy frameworks and accreditation processes [10]. In the Australian National Women’s Health Policy of 2010, being a lesbian or a bisexual woman is recognised as a social determinant of health. More broadly sexuality, sex and gender identity are also considered to be important determinants of health. The policy declares that for same-sex attracted women, “the fear or experience of insensitive treatment or of blatant discrimination can be a major barrier to accessing appropriate and acceptable health care”. The policy emphasises that in order to minimise the hurdles that same-sex attracted women face when accessing services, it is important to first understand the needs of these groups of women [11].
b.
United Kingdom (UK)
There are an estimated 3.6 million LGBT people living in UK, approximately 5 % of the population. The UK Health Equality Act (2006) prohibits discrimination on the grounds of sexual orientation in the provision of goods and services, including health care [1]. The 2007 Equality Act (Sexual Orientation) Regulations state there should be equal treatment in all public services, including in the National Health Service [12]. A number of non-governmental organisations have released policies and strategies on health issues, including cancer diagnosis and treatment, affecting LGBT communities in the UK. These documents highlight the need to improve the evidence base on cancer in LGBT communities by conducting more research and the need to eliminate obstacles to healthcare access for LGBT people [1, 13].
a.
Canada
In 1996, the Canadian Human Rights Act was amended to explicitly include sexual orientation as one of the prohibited grounds of discrimination [14]. Canada has promoted the equality of same-sex partners, including the legalisation of same-sex marriage in 2005. A question on sexual identity was added to the Canadian Community Health Survey (CCHS) in 2003, which has been very valuable in describing the health and social needs of the Canadian LGBT community. In 2009, 1.1 % of Canadians aged 18–59 reported that they considered themselves to be homosexual (gay or lesbian) and 0.9 % considered themselves to be bisexual [15, 16]. Commentators on the Canadian health system have made observations on the exclusion of LGBT populations from mainstream health promotion research, policy and practice [17]. However, community organisations funded through government sources have worked to develop health promotion programs and policies to increase the visibility of and the services provided to LGBT people [18]. Province-wide guidelines on screening for transgender people for breast, cervical, ovarian, uterine and prostate cancers have been published for British Columbia [19].
Population-Based Studies and Surveys
In 1989, Denmark became the first country to establish marriage-like partnerships with legal implications for same-sex couples. The largest population-based study of cancer among the LGBT community is a Danish cohort study which linked information from the Danish Civil Registration System on men and women in registered same-sex partnerships with the Danish cancer registry and the Danish AIDS registry. Data were linked for the time period between 1989–1997 and results were compared with the general Danish population. 1614 women and 3391 men in same-sex partnerships were included, with an average follow-up of 4.1 years and 4.6 years respectively. Among women, the overall cancer incidence differed little between women in same-sex partnerships and women in the general population, albeit based on wide confidence intervals (relative risk (RR) 0.9 (95 % CI 0.4–1.9). Men in same-sex partnerships were twice as likely to develop cancer compared with men in the general population. However, this was almost entirely a result of extremely high incidence rates of Kaposi’s sarcoma (KS) (RR 136.0, 96–186), non-Hodgkin’s lymphoma (NHL) (RR 15.1, 10.4–21.4) and anal cancer (RR 31.2, 8.4–79.8). The overall cancer incidence rate was not significantly different when these cancers were excluded from the analysis. Though the findings are pivotal, the study does have a number of limitations. No information was available on sociodemographic factors such as education and income, and the study’s authors caution on how representative participants are of all LGB men and women in Denmark [7]. The sample size was relatively small. Further data from these linked registries from 1982 to 2011 were published in 2013. In this updated study, 0.1 % of all partnerships were same-sex marriages and 1.0 % comprised women and 1.9 % men registering same-sex cohabitation. Cohabitation status was a variable created by determining the number and gender of adults sharing the same address as cohort members. Of concern, all-cause mortality was markedly increased in all age groups in same-sex married women (hazard ratio (HR) 1.89, 95 % CI 1.60–2.23) compared with opposite-sex married women, with the greatest differences seen in cancer (HR 1.62, 95 % CI 1.28–2.05) and suicide related mortality (HR 6.4). The mortality rates of men in same-sex marriages had declined since the 1990s. Though still raised when compared with opposite-sex married men, the mortality rates were similar to those among unmarried, widowed or divorced men [20].
Other population-based surveys include the national Canadian Community Health Survey (CCHS). Since 2003, respondents have been asked if they are heterosexual, homosexual (lesbian or gay) or bisexual. In cross-sectional analyses of results for women (60937 heterosexual, 354 lesbian and 424 bisexual), lesbian and bisexual women were more likely to smoke than heterosexual women (odds ratio (OR) 1.77, 95 % CI 1.22–2.57 and 2.04, 95 % CI 1.47–2.83 respectively). Lesbian and bisexual women were twice as likely to report excess alcohol consumption compared with heterosexual women (OR 2.67 (95 % CI 1.67–4.28) and 2.00 (95 % CI 1.30–3.09) respectively) [15]. Gay and bisexual men in the 2003 CCHS had similar rates of daily smoking or excess alcohol consumption as heterosexual men [16].
A national Dutch survey of patients attending general practices was conducted in 2001.19685 people were approached and 65 % participated. Sexuality was reported by 98.2 % of 9684 participants, with 0.6 % identifying as bisexual men, 1.5 % as gay men, 1.2 % as bisexual women and 1.5 % as lesbian women. The SF36 questionnaire, a standardised measure of functional health and wellbeing, was administered and results demonstrated lower acute and general mental health status in LGB people. Cancer rates were not reported. In this study, sexual orientation was not linked to current cigarette smoking in men or women. A lower proportion of LGB people were currently using alcohol, but those who currently used alcohol were more likely to report recent excess consumption (adjusted OR 1.72, 95 % CI 1.17–2.99) [21]. Private Lives 2 is the second national Australian on-line survey of health and well-being of LGBT Australians. It was administered in 2011, with 3835 respondents completing the survey. According to results from the SF36 questionnaire, the general health of male respondents was lower than the national average. The general health of female respondents was lower still, and transgender men and women reported the lowest levels of general health. Only a small numbers of cancers were reported (2.1 % of respondents in total; 2.4 % men, 1.8 % women, 2.5 % transgender women, 0 % transgender men). The most common cancers were skin (19 cases), prostate (16 cases) and breast cancer (12 cases). Of note, breast cancer screening rates did not appear to be lower, with 56.2 % of women aged 50–69 years reporting having a mammogram in past 2 years compared with 55.2 % of similar-aged women in the general population [22].
Risk Factors for Cancer
Much of the existing research and proposed evidence for cancer disparities among LGBT communities is based on differing rates of risk factors for cancer. Behavioural factors such as cigarette smoking and excess alcohol consumption have been associated with a number of cancer types. Nulliparity and being overweight or obese have been associated with breast cancer. Chronic HPV infection has been causally linked with cervical and other ano-genital cancers and cancers of the head and neck (particularly the oropharynx and tonsil). A number of these risk factors, including behaviours and infectious agents, are discussed here.
Cigarette Smoking and Alcohol Consumption
Surveys in Australia show varying rates of smoking among LGBT populations. The National Drug Strategy Household Survey in 2010 showed current smoking rates for the general population at 17.5 %, while the smoking rate for those identifying as homosexual/bisexual was 34.2 % [23]. Descriptive and small studies of transgender health also suggest high rates of smoking. Forty four percent of transgender men and 35.4 % of transgender women in the Private Lives survey smoked on more than five occasions in the preceding month [24]. Among Australian people living with HIV, the HIV Futures study reported a decrease in smoking rates from 54.6 % in 2002 to 30.2 % in 2013 [25]. While rates of smoking have fallen among gay and bisexual men and people with HIV, the Sydney Women and Sexual Health survey shows that the reported high rates of smoking among lesbians and other same-sex attracted women have remained constant between 2006 and 2012 [26]. In the Private Lives survey, 60 % of respondents considered themselves non-smokers, 13.7 % identify as ex-smokers which is comparable with national data where 57.8 % have never smoked and 24.1 % ex-smokers. Reported alcohol use was lower than national averages [22, 23]. Results from a 2007 online survey of 6178 lesbian and bisexual women (LBW) in the UK showed that two thirds of respondents (4118 women) reported a smoking history and 40 % drank at least three times a week [27].
Tobacco has been identified as the most important risk factor for cancer in the UK, with its use linked to 19.4 % of all cancer cases newly diagnosed in 2010. In contrast, infectious agents only accounted for 3.1 % of cancer cases in the UK [28]. In order to address the perceived increase in cigarette smoking among gay men, a UK pilot smoking cessation study was developed. The study aimed to design, recruit and deliver smoking cessation group interventions to gay men in London in consultation with community groups. The intervention was adapted to meet the specific needs of gay men. Of the 98 gay men recruited, 76 attended at least the first session. After 7 weeks, 76 % confirmed they had ceased smoking [29].
Human Papillomavirus Infection
Human papillomavirus (HPV) has been classified by the International Agency for Research on Cancer as a human carcinogen for several cancer types, including anal, cervical, penile, vulval, vaginal and oropharyngeal cancers (in particular tonsillar and base of tongue cancers) [30]. Approximately 85 % of anal cancer is caused by high risk types of HPV, and the high risk type HPV16 is by far the most common cause (90 % of all HPV-related anal cancer) [31].
There have been increasing numbers of studies of prevalence and incidence of ano-genital HPV among men who have sex with men (MSM) in recent years. MSM are consistently more likely than heterosexual men to have anal HPV detected. A systematic review and meta-analysis of studies in MSM that reported prevalence and incidence of anal HPV detection, anal cancer precursor lesions (high grade squamous intraepithelial lesions, HSIL) and anal cancer showed that anal HPV and anal cancer precursors were very common in MSM. In HIV-positive men, the pooled prevalences of anal HPV16 and HSIL were 35·4 % (95 % CI 32·9–37·9) and 29·1 % (95 % CI 22·8–35·4) respectively. In HIV-negative men, the pooled prevalences of anal HPV16 and HSIL were 12·5 % (95 % CI 9·8–15·4) and 21·5 % (95 % CI 13·7–29·3) respectively [32].
Though the great majority of studies identified in this systematic review were from North America, a number of studies on anal HPV from other countries have recently been published. In a cross-sectional Irish study of 113 MSM with detectable HPV DNA, 68 men (42 %) had at least one high risk HPV type detected [33]. A Netherlands cross-sectional study recruited HIV positive (317, 41 %) and HIV negative (461) MSM. Both anal and penile high risk HPV infection were significantly more prevalent in HIV positive MSM (65 % vs 45 %, p < 0.001 and 32 % vs 16 %, p = 0.001 respectively) [34]. The Study for the Prevention of Anal Cancer (SPANC) is a 3-year prospective study of HIV negative and positive gay men aged ≥ 35 years in Sydney, Australia. By March 2013, 342 participants (median age 49 years; 28.7 % HIV positive) had attended a baseline visit. The vast majority of men (85.8 %) had one or more HPV types detected. Almost two thirds had at least one high risk HPV type (64.4 %) and almost a third had HPV16 (30.3 %) detected. Similar to other published studies, the SPANC study found that anal high risk HPV detection was significantly associated with positive HIV status (p = 0.010) [35]. A multi-centre cohort study of 551 HIV positive MSM conducted in Spain between 2007 and 2011 detected anal high risk HPV in 82 % of men [36]. In a cross-sectional study of 445 men with HIV attending public clinics in urban Brazil, men who had sex with women and men (MSWM) and MSM were much more likely than heterosexual men to have anal high risk HPV detected (OR 7.33 and 7.92 respectively) [37].
In-depth interviews and focus groups were conducted in Peru to explore knowledge, attitudes and experiences regarding HPV and genital warts among Peruvian male to female transgender and MSM populations. The study found that knowledge of HPV was limited. Unfortunately, it did not examine knowledge of the association between HPV and cancer [38]. An Italian cross-sectional study assessed knowledge and attitudes towards HPV and HPV vaccination among a random sample of 1000 LGB people. Less than two thirds of participants (60.6 %) had heard of HPV. Knowledge was higher among women and those with higher involvement with LGB community organisations. Though willingness to be vaccinated against HPV was high (73.3 %), only 1.7 % reported being vaccinated [39]. Of 1041 MSM recruited between 2008 and 2009 from community venues in Vancouver, Canada, 71.3 % had heard of HPV and 67.0 % said they were willing to receive HPV vaccine. Interestingly, for MSM aged less than 26 years old, the median time from first sexual contact with males to disclosure of sexual identity to a health care provider was 3.0 years (IQR 1–8 years). Thus many young MSM would already be infected with HPV by the time they self-reported as gay or bisexual. This highlights the limitations associated with delivering vaccination programs for young MSM through health care providers [40].
The incidence of HPV-associated oropharyngeal cancers is rapidly increasing. In 2007, oral HPV detection was measured in 500 MSM (50 % HIV-positive) attending Melbourne Sexual Health Centre, Australia. Oral HPV was found to be significantly associated with HIV infection. One in five HIV positive MSM (19 %) had at least one HPV type detected compared with less than one in ten HIV negative men (7 %, p < 0.001). HPV16 was detected in 4.4 % of HIV positive men compared with 0.8 % of HIV negative men. Other risk factors for oral HPV included smoking, recent tooth-brushing and more lifetime tongue-kissing and oral sex partners [41].
The quadrivalent HPV vaccination provides protection against the two HPV types that are responsible for most ano-genital cancers (HPV16 and HPV18) and the two types that are responsible for most ano-genital warts (HPV6 and HPV11). The vaccine has been proven to be safe and effective in both males and females. An ongoing national school-based, government-funded, HPV vaccination program for females aged 12–13 years commenced in Australia in 2007. The impact of this program has been evaluated in different populations. Among 112 083 new patients attending sexual health services, a decline in number of diagnoses of genital warts was noted for young female residents (p trend <0·0001) after the HPV vaccination program was implemented. There was also a statistically significant decline in genital warts among young heterosexual men (p < 0·0001) which was interpreted as being due to herd protection. There was no change in the number of diagnoses in gay men [42], demonstrating that gay men will gain little if any herd protection from the vaccination of women. The Australian government approved a subsided male HPV vaccination program which commenced in February 2013 and is targeted at high school males aged 12–13 years with a catch up only to the age of 15 [43]. This will clearly benefit very young MSM in Australia. Though HPV-related cancers will be prevented in the decades to come, today’s generation of adult MSM remain unprotected.
HIV-Related Cancers
It is evident that information and data on cancer rates and mortality are far more extensive for gay men with HIV than for LGBT people in general [44]. This is due primarily to the presence of HIV and AIDS registries, which often capture information on sexual behaviours, at least among men diagnosed with HIV. Though an exhaustive review of published literature in this area is beyond the scope of this chapter, the studies discussed here consistently demonstrate the increased risk of cancer among gay and bisexual men living with HIV. In a Scottish study of data linkage from cancer and HIV registries from 1981 to 1996, the incidence of cancer among people living with HIV was 11 times higher than the general population. Among gay and bisexual men, the incidence of cancer was 21 times higher than men in the general population (standardised incidence ratio (SIR) 21.4, 95 % CI 17.4–26.1) [45]. In a Spanish study linking AIDS and cancer registry data, compared with other people living with HIV, MSM and MSWM had the highest rates of Kaposi’s sarcoma (SIR 3003.23) and any invasive cancer (SIR 53.94) and the second highest rates of non-Hodgkin’s lymphoma (after heterosexual men living with HIV, SIR 240.66) [46]. Combined data from 1997 to 1998 on cancer rates among 8385 men (25.8 % homosexual) from two hospital HIV cohorts and a cohort of HIV seroconverters in Italy and France were studied. Observed cancer rates among MSM were compared with expected rates (derived from rates in men in the general population). There were markedly increased observed rates of cancer at any site (SIR 44.2), Kaposi’s sarcoma (SIR 2055), cancer of the salivary glands (SIR 65.5), non-Hodgkin’s lymphoma (SIR 124) and Hodgkin’s disease (SIR 11.2) [47].
Breast Cancer
It is important to emphasise that being a LBW is not in itself a risk factor for breast cancer. The fundamental issue is whether LBW are at greater risk of breast cancer because the risk factors for breast cancer are more prevalent among LBW [5, 48]. These risks include behavioural factors such as excess alcohol consumption and smoking (potentially) [49, 50], reproductive factors such as higher rates of nulliparity and delayed childbirth [51]. There is no consensus on whether these risk factors are indeed more common among LBW.
A threefold increase in fatal breast cancer among LBW has been found in studies from the United States. A recently published systematic review of breast cancer in LBW by UK-based researchers was undertaken in 2009. No published incidence rates of breast cancer could be identified. The review included nine studies of breast cancer prevalence among LBW, mostly small studies of varying methodological quality. Of note, only two were from countries other than the United States (Denmark and UK). These two studies are discussed in this chapter. The authors emphasise that these sparse results validate the call for sexual orientation data to be collected within routine statistics [52]. The UK data included in the systematic review above was an online survey of LBW conducted in 2007. No details of the study methodology are available. Of the 6178 responses, 8 % of LBW reported a diagnosis of breast cancer between ages 50 and 79 [27].
The national UK Lesbians and Health Care Survey was undertaken between 1997 and 1998. 1066 lesbians responded and three quarters of respondents reported that they believed that LW had the same risk of breast cancer as heterosexual women. Twenty one percent of women reported that they never practised breast self-examination; the same proportion as among the general population. However, only 16 % of LBW performed regular monthly breast self-examination, compared with 41 % of women in the general population. Interestingly, 19 % believed their risk of breast cancer was higher than that of heterosexual women [8]. Findings from a national Australian survey showed that Australian LBW aged between 50–69 had similar mammogram rates to the national rates in this age group (56.1 vs 55.2 %), which suggests that Australian LBW are not under-screened for breast cancer [22].
Cervical Cancer
Studies from the United States have found significant differences in prevalence of cervical cancer by sexual orientation. In pooled data from California Health Interview surveys from 2001 to 2005, bisexual women had more than double the prevalence of cervical cancer compared with other women surveyed [2]. However, in the Danish same-sex partnership cohort study described above, invasive cervical cancer rates among women in same-sex relationships were similar to those in opposite-sex relationships. Of note, there was statistically significantly less in situ cervical disease reported in women in same-sex relationships. Although the numbers were small and thus definitive conclusions difficult to make, the authors suggest that this may represent inadequate attendance at screening programs by lesbian women [7].