Health Outcomes of Sexual and Gender Minorities After Cancer: A Scoping Review

Purpose: Cancer research on sexual and gender minority (SGM) populations is gaining momentum. However, literature on patient-reported health outcomes for SGM people with a history of cancer is limited. The purpose of this review was to examine the nature and extent of research regarding patient-reported health outcomes after cancer treatment among SGM populations. Methods: A systematic search of key words, titles, abstracts, and/or major subjects was conducted in PubMed, Scopus, and CINAHL in September 2019 and in EMBASE in February 2020. Included studies investigated at least one physical, psychosocial, emotional, or functional patient-reported outcome related to cancer diagnosis and/or treatment. Articles that met inclusion criteria were reviewed in their entirety, charted in a Word Table, assessed for quality, and trends within and across studies were reported in addition to each study’s results. Results: Fifty-two studies were included in the �nal analysis; most were quantitative and focused on people with a history of breast and prostate cancer. Most studies were secondary analyses or cross-sectional studies of convenience samples, limiting generalizability. Conclusions: A growing literature describes the patient-reported health outcomes of SGM people with a history of cancer. This study summarizes important between-group differences among SGM and heterosexual, cisgender counterparts that are critical for clinicians to consider when providing care. Implications for cancer survivors: Sexual orientation and gender identity are relevant to cancer survivors’ health outcomes. Clinicians and researchers can build an evidence base to inform care improvements by collecting data on anatomy, sexual orientation, and gender identity in Electronic Health Records and population-based surveys.


Background
Lesbian, gay, bisexual, transgender, queer, and/or intersex (LGBTQI) populations, also known as sexual and gender minorities (SGM), have been largely ignored in research until recently.While it is likely that these populations have been included in previous research, lack of data collection about sexual orientation and gender identity and lack of prioritizing the health of these populations has led to limited knowledge of their speci c needs.Before the National Academies of Sciences 2011 report, The Health of Lesbian, Gay, Bisexual, and Transgender (LGBT) People: Building a Foundation for Better Understanding, few studies investigated disparities in cancer-related health outcomes based on sexual orientation and no studies investigated the outcomes of gender minority people [1].In 2016, the National Institutes of Health (NIH) opened a new o ce dedicated to SGM health research, designating SGM people as a minority population [2].In 2017, the American Society of Clinical Oncology issued a call to action to reduce cancer health disparities for SGM populations [3].However, most oncology practitioners have not been trained to address the needs of SGM people, and most cancer centers have yet to institute explicit policies or routine practices to collect sexual orientation and gender-identity data in the electronic medical record, use gender-neutral language on forms, provide SGM-speci c support services, and/or require SGM cultural humility training for all staff [4].
Lack of training on the clinical and psychosocial needs of SGM patients perpetuates a system in which patients have to teach their clinicians about how to care for them, resulting in suboptimal care and potentially perpetuating stigmatizing behaviors of clinicians [5,6].
Fortunately, cancer research on SGM patients has started to gain momentum.This review aimed to synthesize what is currently known about patient-reported health outcomes of SGM people after de nitive cancer treatment to inform clinical practice and identify gaps in the literature to guide future research.A scoping review was selected rather than a systematic review in order to identify a broad range of relevant literature regardless of study design [7].
Notes on terminology: 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, 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 speci c 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 is for the sake of e ciency of wording.We attempt to, whenever is reasonably e cient, refer to people with a history of cancer rather than a cancer "survivor."

Study selection
Database searches for peer-reviewed articles focused on health outcomes among SGM after de nitive treatment for cancer yielded 242 entries in PubMed, 340 in Scopus, 46 in CINAHL, and 115 in EMBASE.All included articles were required to have SGM people with a history of cancer as a primary focus of the study.Author MPC conducted a review of titles in Excel for these 743 entries.A manual review of reference lists of review articles was conducted to ensure no studies were missed in systematic searches, adding additional articles for abstract review (n=23).Duplicates (n=196) and articles that did not meet eligibility criteria were removed (n=365 during title review; n=140 during abstract review).Full text articles (n=65) were reviewed for compliance with the inclusion criteria; reasons for exclusion after full-text review are provided in Figure 2. The full-text articles included in this study were n=52.

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

Breast cancer survivorship
The majority of studies found on SGM people with a history of cancer focused on breast cancer survivors, mostly comparing lesbian survivors 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 [11][12][13][15][16][17][18]21] and [15,19,20,22,24].Given that half of the analyses were conducted in the same two samples of women, extrapolating ndings 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 one mixed methods study yielded important insights.
Participants studied were mostly white, educated, and employed.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) [12,27] with a few exceptions.WSW with less nancial means and those who experienced greater discrimination were more likely to have poorer physical health and increased anxiety and depression [12,13].WSW also reported greater stress [28].In one study, discrimination was associated with anxiety, but resilience and social support buffered this association [30].WSW in these studies and their caregivers also showed greater dyadic effects on quality of life compared to heterosexual couples [24].
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 signi cant prediagnosis difference [11].WSW reported less avoidant coping and anxious preoccupation than heterosexual peers [16,32].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 [15][16][17]19,21].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 [14,25,54].However, WSW reported more challenges with access to care [23] and experienced more physical complications related to mastectomy and radiation than heterosexual peers [18].Counter to other studies, one study demonstrated an association between degree of "outness" (de ned in the study as the number of relationships in which people were open about their identity) and higher distress [30], 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 [26].Whether level of outness is linked to discriminatory experiences has not been explored.Overall, WSW displayed more resilient behaviors than heterosexual peers, though one study indicated there were no between-group differences in resilience based on sexual practices (WSW vs. heterosexual women) [10].
Prostate cancer survivorship on people with a history of prostate cancer primarily focused on genitourinary and relationship changes for men who have sex with men (MSM).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 [37,50,51].MSM with HIV reported more signi cant detrimental effects of treatment than MSM without HIV [44].One study showed that MSM had greater sexual dysfunction after bicalutamide monotherapy compared to heterosexual peers [43].
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 nd another partner again and there was a depression" [35].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" [45].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" [45].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 [45].
Several studies reported changes to MSM survivors' sense of identity as gay men, resulting in changes to relationships and worse mental health [37,40,45,50].In one qualitative study, MSM describe erectile dysfunction as a persistent problem that is paramount to being "sexually inferior" or "leading to a sense of 'disquali cation' of the sexual experience" [50].Sexual changes were reported to adversely affect the mental health and identities of MSM.In Ussher et al.'s [50] study, a gay interviewee reported that erectile dysfunction was "the most horri c 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 [50].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.Speci cally, survivors in this study encouraged partners to obtain sexual satisfaction outside of their relationship [38,45].In contrast, some MSM reported more profound intimacy with their partner [45,50] after cancer diagnosis and treatment.
Several studies demonstrated bene ts 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 [34].Another study demonstrated reduced anxiety and less illness intrusiveness for MSM who had shared their sexual orientation with providers [36].
Studies also highlighted lack of resources and support tailored for MSM [42,46].In Ussher et al.'s qualitative study [50], one MSM respondent summarized the issue like this: "Most health care professionals and others working in the prostate cancer eld have no understanding of the different ways that prostate cancer can affect gay and bisexual men.Not just sexually, but in the non-sexual 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" [35].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" [35].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 [35].

Transgender cancer
Only four studies included transgender and/or genderqueer respondents [25,54,57,59].Bryson et al. [54] found that intersectional identities impacted the experiences of transgender cancer survivors.Brown and McElroy [25] described health care providers "gender policing" when genderqueer patients made the decision to "go at" 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.Kamen et al. [57] and Lisy et al. [59] included transgender respondents in their study, but the former did not stratify outcomes speci c to transgender respondents, and the latter did not decouple gender identity from sexual orientation.

Critical appraisal
Most studies 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 [43].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 3 catalogs measures used in the included studies.

Differences among SGM populations
Several studies that synthesized outcomes for people with a history of various cancers indicated worse physical outcomes for SGM compared to heterosexual, cisgender counterparts [29].However, studies identi ed 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 di culties for MSM with cancer compared to heterosexual peers [56].In two separate studies, WSW reported lower fear of recurrence while MSM reported greater fear of recurrence compared to heterosexual counterparts [21,48].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 [17,49].Partner support appeared to buffer negative effects for WSW [14,16,21], and partner support was associated with greater reduction in depression [57,58].This buffering effect of partnership was not necessarily true for MSM [37].The heightened dyadic effect of patient-caregiver quality of life shown in [24] highlights the importance of providers including WSW caregivers in cancer treatment discussions.

Gaps in research
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 and 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 one study focused on people with a history of colorectal cancer.This study reported nancial challenges of queer colorectal cancer survivors; however, there was no comparison group and no other studies with which to compare the sample.A few studies examined outcomes of people diagnosed with multiple 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 outcomes.Only four studies mentioned transgender patients [25,54,57,59].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, con ating multiple constructs [59].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.
Only one study was found that focused on AYA people with a history of cancer.This study found that SGM survivors were less concerned with the possibility of infertility and more open to being non-biological parents than heterosexual peers.However, this one qualitative study cannot be assumed to be generalizable.More work on AYA cancer survivorship that strati es 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 3 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 major 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 one study was interventional.Kamen et al.,[58] found a dyadic exercise intervention for partners to be more effective in reducing depression than a survivor-only intervention.Interventional research to address poorer physical health among lesbian breast cancer survivors 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.

Limitations and strengths of this study
This study was limited to articles published in English through February 2020 focused on SGM people with a history of cancer that reported a health-related outcome.The language limitation was due to lack of funding to translate non-English papers for the review.The study did not include studies that focused on experiences of care (such as patient satisfaction) or social support unless at least one health-related patient-reported outcome was an endpoint.By delimiting the literature in this way, important patient experiences are not summarized in this review.This study also did not include cancer prevention or screening studies or provider training interventions to address quality of care for SGM patients, since these studies do not focus on post-therapeutic health outcomes for patients.For a recent review that includes patient experiences and quality of care, see Kent et al. [94].A major strength of this review is its comprehensiveness in summarizing SGM survivorship research to date due to the use of established scoping review methods [7,8] and systematic searches of four databases.

Conclusions
This study summarized important between-group differences among SGM and heterosexual, cisgender counterparts.This review found clear differences in perspectives and health outcomes between WSW and MSM.Thus, researchers should take care to not con ate WSW and MSM when conducting analyses.Gender minority people have been understudied and expanding research in this area will be important to the creation of interventions to improve post-treatment experiences of gender minority people with a history of cancer.Sexual orientation, gender identity, chromosomes, hormone balance, and physical anatomy are separate constructs that should not be con ated.
Finally, attention to intersectionality within SGM populations is critical as people with multiple intersecting aspects of their identity may have drastically different needs, experiences, and outcomes than those of SGM people who identify with only one marginalized population.
It is paramount that anatomy (including intersex status), sexual orientation, and gender identity be documented in Electronic Health Records and population-based surveys.Until these important elds are systematically captured by clinicians and researchers, SGM research will continue to be restricted to small sample sizes that are not powered to detect subgroup differences.Studies focused on heterosexual, cisgender populations will need to be replicated in convenience samples of SGM patients, which is poor stewardship of research funding dollars: Adding sexual orientation, gender identity, and intersex questions to all studies would be more e cient and provide more robust data to inform clinical care.
Finally, a shift to anatomy-and gender-based medicine that accounts for intersectionality is critical to effectively address the needs of SGM people with a cancer diagnosis.Clinicians must be trained on how to tailor medical management based on sexual orientation, gender identity, sexual practices, hormone levels, and physical anatomy rather than by monolithic, binary gender markers.Distinctions between sexual orientation and gender identity in research; structured data collection; and clinician training are critical for evidence-based, quality cancer care to improve health outcomes for SGM people.Furthermore, important cultural distinctions within groups that share sexual orientation, gender identity, and/or intersex categories may yield additional insights regarding within-group differences.Accounting for the diversity of lived experiences of SGM people in research design and analysis will help cancer care better address the needs of diverse populations.In sum, a growing literature describes patient-reported health outcomes of SGM people with a history of cancer, but without systematic registries and/or population-based data collection, data will continue to suffer substantial limitations, thereby reducing utility for clinical practice.

Figure 1 Flow
Figure 1

Table 1
Characteristics of included studies (n=52)

Table 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 multiple 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 in Table2.Critical appraisal consisted of a review of sample recruitment strategy, diversity of the sample (generalizability), study design, use of validated tools (for quantitative studies), innovation, and signi cance.All authors participated in data abstraction and table review for consistency.

Table 2
Summary of Studies of Patient Reported Outcomes from SGM People Diagnosed with Cancer : aOR=adjusted Odds Ratio; DCIS=Ductal Carcinoma In Situ, BrC=Breast Cancer, CRC=Colorectal Cancer, FOR=Fear of Recurrence, PrC=Prostate Cancer, HRQOL=Health Related Quality of Life, MSM=Men who have Sex with Men, SGM=Sexual and Gender Minorities, QOL=Quality of Life, WSW=Sexual Minority Women *Appropriate tests were conducted to compare demographic and clinical characteristics between groups. Abbreviations

Table 3
Summary of Validated Scales used in SGM Survivorship Research.