Health outcomes of sexual and gender minorities after cancer: a systematic review

In this manuscript and in the review conducted, we used “SGM” as a term meant to encompass diverse people whose gender differs from their sex-assigned-at-birth and/or are not heterosexual. While “SGM” is not a term typically used by LGBTQI people to describe themselves, and the authors do not wish to minoritize LGBTQI people, the authors use this acronym, which has been adopted by the NIH, to be inclusive of a wide range of people, including people who do not identify with the words represented in the acronym “LGBTQI.” If a study is focused on a subgroup within the SGM umbrella, the specific subgroup is referred to rather than the broader term “SGM.” Furthermore, the authors acknowledge that the term “survivor” is not universally embraced. Our use of the term, while imperfect, is for the sake of efficiency of wording. We attempt to, whenever is reasonably efficient, refer to people with a history of cancer rather than a cancer “survivor.”

No previous protocol for this study has been published. The search strategy intentionally aimed to cast a wide net before selecting eligible studies for full review. Data were reported following the Preferred Reporting Items for Systematic. Reviews and Meta-Analyses (PRISMA) 2020 guidelines [7, 8].

A medical librarian constructed a comprehensive database search in March 2021. The search was conducted using a combination of keywords in the title or abstract and index terms on PubMed and Embase and keyword in the title or abstract only for Scopus, Web of Science (all databases), PsycINFO, ClinicalTrials.gov, and the Cochrane Central Register of Controlled Trials (Cochrane Library). The search strategy included three distinct concepts that were combined using the “AND” Boolean operator: Sexual and Gender Minorities, Cancer, and Survivor. For the complete PubMed strategy, see Appendix 1. Filters were used to exclude conference abstracts, conference papers, and conference reviews from Embase; no other filters were used. EndNote was used to identify duplicates and additional duplicates were manually removed before screening for inclusion began. Reference lists from review articles that were identified through the database search were then hand searched to identify additional articles for possible inclusion.

Studies were limited to articles published in English that included outcomes of SGM people with a history of a cancer diagnosis. To be included in the review, studies had to investigate and report on at least one physical, psychological, or social patient-reported outcome resulting from impact of a cancer diagnosis and/or treatment: studies with patient experience or satisfaction as the sole endpoint were not included. Commentaries, case studies, abstracts, reviews, dissertations, conference posters, provider-focused trainings and interventions, protocol articles without results, and studies conducted prior to the conclusion of cancer therapy were excluded.

Quality considerations included study design, sampling approach, diversity of sample, measures used, and analytic procedures. Cross-sectional designs, convenience samples, homogenous samples, and non-validated measures were considered limitations. Randomized controlled trials, rigorous qualitative methods, diverse samples, and validated measures were considered strengths.

All included studies were reported in two word tables. Table 1 includes place where study took place, types of SGM subpopulations included, study design, and type of cancer study participants experienced. Appendix 2 reports studies in alphabetical order clustered by age (e.g., AYA) and type of cancer experienced (e.g., breast, colorectal, prostate, various). Studies were synthesized according to experiences of women who have sex with women (WSW), men who have sex with men (MSM), and transgender persons. Given the small number of studies focused on AYA and colorectal cancer survivors, data for these studies were only reported in Appendix 2. Comparisons of SGM subgroups are included in the “Discussion.”

Database searches for peer-reviewed articles focused on health outcomes among SGM persons after definitive treatment for cancer yielded 201 entries in PubMed, 671 in Embase, 344 in Scopus, 279 in Web of Science, 118 in PsycINFO, 12 in ClinicalTrials.gov, and 7 in Cochrane Library’s Central Register of Controlled Trials for a total of 1632 articles. All included articles were required to have SGM people with a history of cancer as a primary focus of the study. Checking for duplicates on EndNote identified 604 duplicates leaving 1028 articles. There were 930 total articles identified for review after manual duplication screen of the EndNote library identified an additional 98 duplicates.

Authors MPC and AA independently reviewed all titles in Excel for these 930 entries. At the title review stage, 796 articles were eliminated. MPC reviewed all abstracts (n = 134), and AA reviewed 10% of the abstracts based on random selection and agreed with MPC on exclusion and inclusion for full-text review. A manual review of reference lists of review articles was conducted to ensure no studies were missed in systematic searches, adding additional 14 articles for abstract review for a total of n = 148 abstracts [9]. Forty-nine studies were eliminated at the abstract review stage leaving n = 99. MPC and AA each reviewed half of the remaining full texts. Full-text articles were reviewed for compliance with the inclusion criteria; reasons for exclusion of 35 articles after full-text review are provided in Fig. 1. The full-text articles included in the final synthesis were n = 64.

Most studies were of people with a history of breast or prostate cancer and were focused on disparities based on sexual orientation. Two studies focused on people who were diagnosed with cancer during adolescence and young adulthood (AYA) and two studies focused on people with a history of colorectal cancer. Most studies were conducted in the USA, Australia, and Canada. See Table 1 for general characteristics of included studies.

Appendix 2 was used as a template for data charting. Studies were sorted by the following demographic groups: adolescent and young adults and studies focused on those diagnosed with breast, prostate, or other cancers, respectively. Lead author and year, location, population of interest including any comparison group(s) when relevant, type of study, design, outcomes, and critical appraisal of each study are reported.

The majority of studies found on SGM people with a history of cancer focused on those who had been diagnosed with breast cancer, mostly comparing lesbians to heterosexual counterparts. Half of the studies on breast cancer were quantitative and analyzed a variety of outcomes from the same two cohorts or subsets of those cohorts [10‐17] and [12, 18‐20]. Given that half of the analyses were conducted in the same two samples of women, extrapolating findings from these studies on SGM with a history of breast cancer should be done with caution. Nevertheless, studies from these two cohorts combined with additional qualitative studies and two mixed methods studies yielded important insights [21‐24].

Participants studied were mostly White, educated, employed, and identified as women. Women who have sex with women (WSW, a term used to be inclusive of lesbian, bisexual, and queer women, and women who do not identify in these ways but partner with women) and heterosexual peers had similar quality of life (QOL) [11, 25] with a few exceptions. WSW with less financial means and those who experienced greater discrimination were more likely to have poorer physical health and increased anxiety and depression [11, 20]. WSW also reported greater stress [26] and less satisfaction with care [24]. In one study, discrimination was associated with anxiety, but resilience and social support buffered this association [26]. Thematic analysis from another study also noted the importance of recognition of partners for psychological wellness, the need for SGM-specific support groups, and the negative impacts of breast cancer treatment on relationships including sexual intimacy [22].

WSW in these studies and their caregivers also showed greater dyadic effects on quality of life compared to heterosexual couples [19]. WSW reported more adaptive coping and improved health behaviors in response to a cancer diagnosis. After cancer diagnoses, WSW with BMI greater than 25 were more likely to lose weight compared with heterosexual counterparts, eliminating a statistically significant pre-diagnosis difference [10]. WSW reported less avoidant coping and anxious preoccupation than heterosexual peers [13, 27] and had similar rates of anxiety and depression [28]. For WSW, having a partner was associated with better sexual function, greater sexual desire, better mental and physical health, and less fear of recurrence compared to heterosexual counterparts [12‐14]. WSW also reported that female partners were a singular and valuable source of support and were able to perceive partner distress, manage home and caretaking, and share a life beyond cancer [24]. In addition, WSW reported being less focused on body image, suffered fewer identity issues due to breast cancer and chose not to have reconstruction more often than heterosexual peers [22, 29, 30]. However, WSW reported more challenges with access to care [31] and experienced more physical complications related to mastectomy and radiation than heterosexual peers [15]. Overall, WSW displayed more resilient behaviors than heterosexual peers, although one study indicated there were no between-group differences in resilience based on sexual practices (WSW vs. heterosexual women) [32].

Counter to other studies, one study demonstrated an association between degree of “outness” (defined in the study as the number of relationships in which people were open about their identity) and higher distress [26], which may suggest increased experiences of stigmatization when people were open about their identities. While WSW did not perceive they were treated differently based on sexual orientation, 39% of WSW in one study said they were assumed to be heterosexual by their health care team [25, 33]. Whether level of outness is linked to discriminatory experiences has not been explored.

Studies on people with a history of prostate cancer primarily focused on genitourinary and relationship changes for men who have sex with men (MSM). Overall, MSM reported more genitourinary challenges than heterosexual peers, including worse urinary and bowel function, lack of ejaculation, changes to erectile function, climacturia, pain during anal sex, penile shortening, loss of libido, and less frequency of sexual activity, although one study demonstrated better sexual function in MSM diagnosed with prostate cancer than that reported in the literature [34‐37]. MSM with HIV reported more significant detrimental effects of treatment than MSM without HIV [38]. One study showed that MSM had greater sexual dysfunction after bicalutamide monotherapy compared to heterosexual peers [39]. One novel study assessed the discussions between MSM and their clinicians regarding sexual and urinary effects of prostate cancer and the treatments offered and noted that while the most common problems reported were loss of ejaculate (93.8%), erectile difficulties (89.6%), change in sense of orgasm (87.0%), loss of sexual confidence (76.7%), changes to the penis (65.8%), increased pain in receptive anal sex (64.8%), urinary incontinence not related to sex (64.2%), and urinary incontinence during sex (49.2%), only loss of ejaculate, erectile difficulties, and nonsexual urinary problems were commonly discussed by clinicians during prostate cancer treatment. Satisfaction with specific rehabilitation options varied widely [40].

In qualitative studies, people with a history of prostate cancer reported fearing rejection and sexual abstinence after treatment: “Afterward I felt like I would never find another partner again and there was a depression” [41]. Among MSM who were dating or seeking casual sex, disclosure was seen as a challenge: “A lot of people hit on me, but I just dread that part in the conversation where I have to go, ‘Well, just so you know, I’m a survivor of prostate cancer and there’s never going to be any cum” [42]. Erectile dysfunction led to break-ups in some cases: “For a month or so it was going really nicely, but about a month in he stopped in the middle of sex one night and he said, ‘I’m sorry, you’re just not hard enough for me.’ I was really upset because I was developing feelings for him” [42]. Loss of spontaneity was another noted adjustment:

“Everything has to be planned ahead of time. How much are you drinking? How much salt did you take? Did you take Cialis? If you’re on a date, you may want to have 100 milligram Viagra in your pocket. If you have any chance of going home with somebody, if you want to leave and do that, you can’t drink a lot beforehand because you don’t want to pee in the guy’s bed. All the stuff I never used to think of, ever. It was just wham, bam, thank you, man. You were much more free. Now, all the spontaneity is gone, which is a shame” [42].

Several studies reported changes to participants’ sense of identity as gay men, resulting in changes to relationships and worse mental health [36, 42‐44]. In one qualitative study, MSM participants describe erectile dysfunction as a persistent problem that is paramount to being “sexually inferior” or “leading to a sense of ‘disqualification’ of the sexual experience” [36]. Another study reported MSM participants feeling unattractive or even disabled [34]. Sexual changes were reported to adversely affect the mental health and identities of MSM. In Ussher et al.’s [36] study, a gay interviewee reported that erectile dysfunction was “the most horrific thing that I’ve ever been through psychologically.” Another respondent indicated decisional regret, preferring to “take my risks with the cancer” if he could go back in time. One MSM interviewee explained his loss of libido as “a profound change in identity” and another said he felt “outside the sexual community” after the change in his sexual function [36]. Two qualitative studies found that renegotiation of exclusivity was one strategy that couples used to cope with physical symptoms and reduced sexual interest of the survivor. Specifically, survivors in this study encouraged partners to obtain sexual satisfaction outside of their relationship [42, 45]. In contrast, some MSM reported more profound intimacy with their partner [36, 42] after cancer diagnosis and treatment.

Several studies demonstrated benefits of MSM’s disclosure of sexual identity to their providers. In one study, MSM who were comfortable disclosing their sexual orientation had greater masculine self-esteem scores, which was linked to greater mental health [46]. Another study demonstrated reduced anxiety and less illness intrusiveness for MSM who had shared their sexual orientation with providers [35].

Studies also highlighted lack of resources and support tailored for MSM [44, 47]. In Ussher et al.’s qualitative study [36], one MSM respondent summarized the issue like this: “Most health care professionals and others working in the prostate cancer field have no understanding of the different ways that prostate cancer can affect gay and bisexual men. Not just sexually, but in the nonsexual side of relationships. It’s as though we’re invisible.” Other MSM described discomfort with a support group that was mostly attended by heterosexual people: “It’s horrifying because there’s this old man talking about sex with the wife. They don’t want to hear about my problem. I didn’t want to hear about theirs. It didn’t work for me” [41]. In the same study, single MSM expressed the need to be extremely independent and not seek out support: “I was alone to recover… I didn’t really want a lot of company. I mean, I’m walking around the house with a catheter tube sticking out of me, it wasn’t really the time” [41]. Other participants noted that they did not want to bother their friends or chose to hire staff to help them rather than seek help from their friends [41].

Only seven studies included transgender and/or genderqueer respondents [21, 22, 31, 48‐51]. Boehmer et al. [31] reported an analysis of BRFSS data from 2014 to 2018 that indicated that transgender men had a higher likelihood of having a cancer diagnosis than cisgender men as well as poorer physical health and more comorbidities compared to cisgender men and cisgender women. Bryson et al. [48] found that intersectional identities impacted the experiences of transgender cancer survivors. Brown and McElroy [21] described health care providers “gender policing” when genderqueer patients made the decision to “go flat” and declined breast reconstruction. These experiences and treatment choices were associated with mixed physical and emotional outcomes. Participants reported being unprepared for early menopause and mental health impacts of hysterectomy. Respondents in another study who identified as “queer,” “questioning,” “genderqueer,” “transgender,” or “other” compared with other SGM people were more likely to report that their current level of support was below average [22]. Kamen et al. [50] and Lisy et al. [51] included transgender respondents in their studies, but the former did not stratify outcomes specific to transgender respondents, and the latter did not decouple gender identity from sexual orientation.

Most studies were either (1) secondary analyses of state-level data where data were available on sexual orientation and gender identity in population surveys or (2) cross-sectional surveys of survivors that could be subject to recall, self-selection, and social desirability bias. Only one study assessed the impact of a therapeutic drug on survivor outcomes [39]. The study was based on binary assumptions about sex and sexual orientation. However, it is singular in demonstrating hormone-based differences in response to cancer pharmacotherapies. A strength among many studies was use of validated measures, although sometimes these had to be adapted to be responsive to the experiences of SGM people. Table 2 catalogs measures used in the included studies.

Most of the studies reviewed were focused on breast cancer for WSW or prostate cancer for MSM. Several studies that synthesized outcomes for people with a history of various cancers indicated worse physical outcomes for SGM compared to heterosexual, cisgender counterparts [91]. However, studies identified no mental health differences between WSW with cancer compared to heterosexual peers. In contrast, a number of studies demonstrated poorer mental health and increased relationship difficulties for MSM with cancer compared to heterosexual peers [92]. In two separate studies, WSW reported lower fear of recurrence while MSM reported greater fear of recurrence compared to heterosexual counterparts [17, 93]. In other studies, MSM were also less likely to be partnered than heterosexual people in contrast to WSW, who were more likely to be partnered [14, 94]. Partner support appeared to buffer negative effects for WSW [13, 17, 29], and partner support was associated with greater reduction in depression [50, 95]. This buffering effect of partnership was not necessarily true for MSM [96]. The heightened dyadic effect of patient-caregiver quality of life shown in Boehmer et al.’s 2020 study [19] highlights the importance of providers including WSW caregivers in cancer treatment discussions.

Additionally, knowledge and competence with SGM health emerged as a critical concern. One study found that SGM who reported their oncologist was not knowledgeable about SGM care reported greater unmet needs and were less likely to disclose their sexual orientation or gender identity to their oncologist [52]. Unmet needs included depression, sadness, cancer-related fears, uncertainty, stress, and sexual dysfunction [52]. Another study found bisexual women who had a history of cancer to be three times more likely to report psychological distress [97]. Bisexual individuals often experience dual discrimination by both mainstream and SGM communities, which may account for this heightened distress. Collectively, these findings support past research that has demonstrated the importance of knowledgeable and unassuming providers in meeting the cancer care needs of SGM persons. For example, a recent study about gender diverse individuals’ satisfaction with care reported discontent with provider assumptions about lesbians wanting breast reconstruction and transgender men wanting hysterectomies; the same study reported that transgender men experienced challenges to male chest reconstruction after breast cancer [98]. Greater clinical and cultural knowledge of SGM concerns and SGM-affirming interventions for concerns are needed.

Since the National Academies 2011 report on SGM health, more studies have been published which examine patient-reported outcomes of SGM people with a history of breast or prostate cancers. However, studies exploring the needs and outcomes of sexual minorities with other cancers as well as studies documenting and addressing the needs of gender minorities are severely limited. Only two studies focused on people with a history of colorectal cancer. One study reported financial challenges of queer colorectal cancer survivors; however, there was no comparison group and no other studies with which to compare the sample. Boehmer et al.’s registry-based study of colorectal cancer survivors showed no differences in patient-reported experiences regarding physician communication, nursing care, or coordination of care, but sexual minorities were more likely to categorize their care overall as “excellent” compared to heterosexual counterparts. A major implication of this study is the potential role of resilience among sexual minorities when facing multiple traumatic events across the lifespan. A weakness of the study was the inability to examine differences in MSM and WSW outcomes within studies due to the aggregation of male and female sexual minorities in the literature. A few studies examined outcomes of people diagnosed with diverse cancers, but overall, more research on people surviving a variety of types of cancer is needed to understand differences in health-related outcomes for SGM survivors.

A critical gap exists in studies focusing on transgender, genderqueer, gender diverse, and intersex patient-reported outcomes. Only seven studies mentioned transgender patients [21, 22, 31, 48‐51]. Of these, one study mentioned the term “intersex,” yet no intersex people were actually included in the study; in addition, sexual orientation was not reported separately from gender identity, conflating multiple constructs [50]. Of note, intersex people often refer to themselves as female or male rather than intersex. Therefore, intersex individuals may be overlooked within some studies under binary sex categories when intersex status is not assessed.

Another critical gap exists in studies focusing on SGM people of color and SGM people with other intersecting marginalized identities. This work is needed to understand the ways that multiple axes of oppression may affect the outcomes of patients after a cancer diagnosis.

Only two studies focused on AYA people with a history of cancer. Desai et al. [99] found greater likelihood of anxiety among sexual minority AYA survivors compared to heterosexual counterparts. Another qualitative study reported that SGM AYA survivors were less concerned with the possibility of infertility and more open to being non-biological parents than heterosexual peers [100]. More work on AYA cancer survivorship that stratifies experiences and outcomes based on sexual orientation and gender identity is needed.

A strength of many of the studies was the use of validated measures. A list of measures is provided in Table 2 for reference. In some cases, measures used were constructed for heterosexual people and were not relevant to SGM populations. This was particularly true of measures focused on sexual function and outcomes. This limitation of existing measures led researchers to sometimes create or adapt instruments for their studies. Validation of measures focused on SGM sexual outcomes is needed to ensure rigor and reliability of research and to allow for comparisons across studies of SGM survivors.

Finally, only two studies were interventional. Kamen et al. [95] found a dyadic exercise intervention for partners to be more effective in reducing depression than a survivor-only intervention. Anderson et al. [46] found that among elderly gay men who were long-term survivors of AIDS and had another serious medical illness (e.g., cancer), psilocybin-supported group therapy was feasible and appeared to have positive effects. This interventional study was novel as a group-based intervention rather than individual-level intervention coupled with pharmacotherapy for clinically demoralized patients [46]. Interventional research to address poorer physical health among lesbians who have been diagnosed with breast cancer and greater sexual challenges for MSM with prostate cancer are needed. Interventional research that provides early and clear information on fertility preservation is also needed for AYA and other survivors regardless of sexual orientation or gender identity.

Notably, a limitation of the current literature on SGM people with a history of cancer is lack of diversity of samples, reliance on cross-sectional studies, and lack of interventional studies. Lack of studies in people diagnosed with cancers other than breast or prostate are also significantly lacking. Greater attention to intersectionality, distinctions among SGM subgroups and reporting of data for transgender, gender diverse, and intersex persons are warranted.

This study was limited to articles published through March 2021 focused on SGM people with a history of cancer that reported at least one post-treatment physical, psychological, or social outcome. The study did not include studies that focused only on experiences of care (such as patient satisfaction) unless at least one health-related patient-reported outcome was also included as an endpoint. For a recent review that includes studies of patient satisfaction [101], care decision-making [102, 103], provider training for improved SGM care [104], supportive care needs [104, 105], and other disparities affecting SGM persons [106], see Kent et al. [107]. These studies were not included here, because our focus was on patient-reported outcomes as a result of cancer and treatment rather than satisfaction or care experiences in treatment.

A major strength of this review is its comprehensiveness in summarizing SGM survivorship research to date due to the systematic search methods [8]. This review contributes uniquely to the literature by providing an update to existing reviews [107], focusing on health outcomes as the endpoints of interest, providing a critical appraisal of studies, comparing differences among SGM subgroups (e.g., research findings relevant to sexual minority women v. sexual minority men), and identifying additional gaps in the research literature. Secondary analyses of primary data sets are also included, unlike existing reviews [107]. Finally, a table of measures used in research focused on SGM cancer survivors is included in Table 2. This summary can assist with scale selection and adaptation for future research to aid in comparisons across studies over time.