Disparities in cancer care among sexual and gender minority adolescent and young adult patients: A scoping review

Abstract Background Adolescent and young adult cancer patients (AYAs) who are sexual and gender minorities (SGM) are a rapidly increasing population that experiences unmet cancer‐related needs. Despite emerging awareness, little is known about cancer care and outcomes for this vulnerable population. The purpose of this scoping review was to explore current knowledge and gaps in the literature on cancer care and outcomes for AYAs who identify as SGM. Methods We reviewed empirical knowledge on SGM AYAs by identifying, describing, and critically appraising the literature to date. We conducted a comprehensive search on OVID MEDLINE, PsycINFO, and CINAHL in February 2022. Additionally, we developed and piloted a conceptual framework for appraising SGM AYA research. Results A total of 37 articles were included in the final review. Most studies focused exclusively on SGM‐related outcomes as the primary aim of the study (81.1%, n = 30), whereas others included some focus on SGM‐related outcomes (18.9%, n = 7). The majority of studies included AYAs as part of a broader age range (86.0%, n = 32), and only a few studies examined exclusively AYA samples (14.0%, n = 5). Gaps in scientific evidence on SGM AYAs were seen across the cancer care continuum. Conclusion Numerous gaps in knowledge of cancer care and outcomes exist for SGM AYAs diagnosed with cancer. Future efforts should fill this void with high‐quality empirical studies that reveal unknown disparities in care and outcomes and are inclusive of the intersectionality of SGM AYAs with other minoritized experiences, thereby advancing health equity in meaningful ways.


| BACKGROUND
In 2022, there were an estimated 87,500 new cases of cancer diagnosed in adolescents and young adults (AYAs) between ages 15 and 39 years, comprising 4.5% of all new cancer cases in the United States (US). 1 AYAs experience distinct disparities and challenges including gaps in diagnosis, 2 barriers in accessing care, 2 and potentially added complexities in the impact of cancer on career trajectories and future health. 3 AYAs who are sexual and gender minorities (SGM)-that is, identify as lesbian, gay, bisexual, transgender, queer, and/ or any other noncisgender or nonheterosexual identities (LGBTQ+) 4 -are a rapidly increasing population that experiences unmet cancer-related needs. Nationally representative data on the distribution of SGM across age cohorts in the US are limited. In 2022, Gallup-a private analytic firmestimated that 20.8% of Generation Z (born 1997-2003) and 10.5% of Millenials (born 1981-1996) openly identify as LGBT, whereas only 7.6% of adults born before 1980 openly identify as LGBT. 5 Prior studies have reported that SGM cancer patients face multiple healthcare and psychosocial challenges compared with their non-SGM counterparts 6-8 -for example, higher levels of psychological distress 7,8 and additional barriers to receiving cancer care. 6 Despite emerging awareness of SGM AYAs as a psychosocially and medically vulnerable population and recognition of the need to improve their care, 6,9 the quality of studies addressing SGM needs and experiences can be difficult to evaluate due to incomplete reporting of key elements. Furthermore, quality assessment of individual studies plays a crucial role in building a generalizable, empirical body of literature that enables healthcare professionals to critically evaluate and apply findings in the provision of care. 10 A conceptual framework is missing and needed to prioritize SGM AYA domains that are relevant to the assessment of research quality.
The goal of the current scoping review was to explore current knowledge and gaps in the literature on care and outcomes for AYAs who identify as SGM. Additionally, we responded to a lack of existing tools that adequately appraise the quality of the SGM literature by developing and piloting a novel conceptual framework for assessing the quality of SGM AYA research. Thus, the present review innovatively generates and defines standards for reporting SGM AYA research in the conduct of this scoping review.

| Terminology
Terminology used by authors in this manuscript reflects both the language found in our review of extant literature and our commitment to utilizing language that represents the current cohort of AYAs whose gender identities and sexual orientations are increasingly expansive. More specifically, we used the umbrella terms "sexual and gender minority" (SGM), "sexual orientation and gender identity" (SOGI), "lesbian, gay, bisexual, transgender, queer, plus" (LGBTQ+), and "queer" as revealed in the conduct of our review. Concurrently, we were as specific as possible in the identification of subgroups where applicable. The Human Rights Campaign's glossary of terms 11 was our primary reference for present-day inclusive language. The terms LGBTQ+ and SGM are used interchangeably as are the terms patient and survivor.

| Information sources
Three members of the research team (C.K.C., H.L., and V.A.R.) initially generated search terms (Table 1), which were subsequently reviewed and vetted by all authors. The research librarian (Y.G.) conducted a comprehensive search on OVID MEDLINE, PsycINFO, and CINAHL in February 2022. Search terms used to generate results were arrived at by using keywords and synonymous index terms within our research question and by following guidance from extant reviews of health-related topics for SGM populations.

| Inclusion and exclusion criteria
Studies were included if they met the following seven criteria: (1) English language publication; (2) empirical study, that is, scientific research based on observation or experimentation; (3) reported on a defined patient sample or subsample of patients diagnosed with cancer between ages 15 and 39 years, who may be older at the time of the study; (4) human research; (5) study sample included those investigating research outcomes (i.e., endpoints) related to sexual and gender minority status; (6) examined factor(s) related to a biological, medical, and/or psychosocial aspect related to a cancer diagnosis; (7) examined patients on-or posttreatment. Studies with endpoints that focused on healthcare providers were excluded as were nonempirical publications such as meeting abstracts, editorials, or case reports.

| Search procedures
Search results were compiled in Covidence (Covidence). Five reviewers (C.K.C., E.C., H.L., M.E.R., and V.A.R) participated in the title/abstract screening. Each title/abstract was screened by three reviewers, who resolved disagreements through discussion among them until a consensus was reached. If consensus could still not be reached, then all five reviewers were consulted to arrive at an agreement. A similar process was used to screen the full text of articles reviewed by a total of six reviewers (C.K.C., E.C., H.L., M.E.R., N.J.L., & V.A.R).

| Data analysis
The authors developed a data extraction form in Microsoft Excel (Microsoft) that was populated with search results from Covidence and captured the following information for each study: primary author, year of publication, country of origin, title, study aim, study design, study start date, study end date, method(s) of recruitment, participant characteristics (sample size, age, cancer type, cancer stage, cancer phase, comparison group), study results (cancer outcomes, LGBTQ+ related outcomes, psychosocial outcomes, and physical outcomes), and reviewers' notes on key findings.

| Quality of the evidence
The quality of publications was first calculated by using the relevant Joanna Briggs Institute (JBI) critical appraisal tool 12,13 for the respective study design. The authors then examined SGM AYA research quality by developing and piloting a new conceptual framework that was adapted from considerations for assessing SGM oncofertility praxis 14 (Figure 1).

| RESULTS
In total, 1725 articles were retrieved. After duplicates within and between databases were removed, 1366 records remained ( Figure 2). Of the 1366 articles, 1151 were excluded because they did not meet study inclusion criteria during the title and abstract review. Thereafter, 215 articles were deemed potentially relevant and underwent full-text review. Upon completion of full-text screening 178 articles were removed. Reasons for exclusion of articles were: no patients diagnosed between 15 and 39 years old in the study sample (n = 73); no defined cancer patients in the study sample (n = 46); not an empirical study (n = 30); no sexual and gender minority-related study outcomes (n = 25); provider-focused study (n = 4). A total of 37 articles were included in the final review ( Figure 2). Table 1 characterizes our resulting studies (n = 37). The preponderance of studies included in this scoping review focused exclusively on SGM-related outcomes as the primary aim of the study (81.1%, n = 30), whereas other studies included some focus on SGM-related outcomes (18.9%, n = 7). Most studies included AYAs as part of a broader age range (86.5%, n = 32), and only a few studies used an T A B L E 1 Search terms in scoping review of cancer care and outcomes for sexual and gender minority adolescent and young adults (AYAs). exclusively AYA sample (13.5%, n = 5). Of these 5 articles with exclusively AYA samples, only one study focused exclusively on SGM AYAs-a narrative inquiry with two participants.

Search terms
Methods of recruitment varied with most studies (n = 24) employing more than one method. Approximately one-third of the studies used clinic visits (n = 11) and/or social media (n = 10). Other recruitment approaches included phone (n = 6), postal service (n = 5), email (n = 7), and other in-person contact (n = 5). Considering that nearly half of studies included in our review were qualitative studies (48.6%, n = 18), the majority (40.5%, n = 15) recruited sample sizes of less than 32 participants (Table 1).
More than half of studies included LGBTQ+ participants as part of a larger sample of cancer patients (56.8%, n = 21), while the remaining studies examined exclusively LGBTQ+ cancer patients (43.2%, n = 16). Approximately one third of studies solely focused on one cancer type (breast, gynecological, colorectal, testicular, and acquired immunodeficiency syndrome [AIDS]-defining cancer), while the majority studies represented a variety of cancer types. Of 37 studies, (48.6%, n = 18) were qualitative studies and (43.2%, n = 16) were quantitative studies. Three studies (8.1%) utilized mixed-methods. All quantitative studies applied cross-sectional designs ( Table 2).

| Biomedical outcomes
No studies reported on cancer outcomes such as overall survival, disease-free survival, or progression-free survival ( Table 3).
Only one study reported on other biomedical outcomes for SGM AYAs. 23 Other studies capturing biomedical outcomes reported on a broader age range of SGM cancer survivors and addressed general physical health, fertility, cardiovascular disease, and AIDS-defining cancers that a person with human immunodeficiency virus (HIV) is at high risk of developing. SGM survivors reported significantly greater physical inactivity, compared with cisgender women and men. 16 SGM survivors, especially transgender men survivors, were significantly more likely to report poor physical health and greater medical comorbidities; and transgender women survivors were significantly more likely to report cardiovascular disease compared with cisgender counterparts. 18 Although there was no significant association between sexual orientation and referral to counseling for reproductive compromise after treatment, no women identifying with a known sexual orientation other than heterosexual preserved their fertility. 28 Last, lesbians reported greater tobacco use and bisexual women reported lower odds of having recent mammography. 24

| Psychosocial outcomes
No psychosocial intervention studies were found (Table 3). When investigating psychosocial outcomes, some studies reported the outcomes of SGM AYA cancer survivors compared to their heterosexual counterparts. Thirty-one percent of sexual minority participants met the criteria for clinical depression and 34% met the criteria for clinical anxiety, while 23% of heterosexual participants met the criteria for depression and 20% for anxiety. 22 It follows that the sexual minority group had a significantly higher mean of depression and anxiety scores compared with the heterosexual group. 22 Likewise, bisexual women reported higher psychosocial distress than heterosexual F I G U R E 1 Conceptual framework of foundational progress in sexual and gender minority (SGM) and adolescent and young adult (AYA) research derived from Levin et al.'s 14 schema for assessing sex, gender identity, and sexual orientation in oncofertility research by presenting nine essential domains for high-quality research studies that capture SGM AYAs. 8 24 Sexual minority women who are breast cancer survivors experienced higher levels of stress compared to heterosexual breast cancer survivors. 25 Men who identify as gay, bisexual, and transgender cancer survivors reported greater symptoms of depression than cisheterosexual male cancer survivors. 27 Conversely, sexual minority women in the study sample experienced lower levels of emotional distress compared with the mean mood disturbance score of the scale construction sample which was the heterosexual population. 19 Regarding social support, many studies demonstrated unmet needs or inadequate social support among SGM cancer survivors. SGM participants reported unmet needs for cancer-related social support for themselves and for  their partners, although few reported disclosing their sexual orientation or gender identity to healthcare providers. 21 LGBT cancer survivors reported greater symptoms of depression and greater levels of social/relationship concerns than matched heterosexual cancer survivors. 26 Internalized homophobia among lesbian women treated for early stage breast cancer was associated with greater distress through low self-esteem and perceived unavailability of social support. 29 Moreover, one study found that SGM patients with worse access to care have poorer quality of life (QOL) than non-SGM cancer survivors, 17 and another study reported that instances of isolation and disconnection reinforced fear of cancer and patterns of exclusion among lesbians. 31

| Quality of the evidence
Results from employing JBI critical appraisal tools revealed that all studies in our final review were of high quality, meeting every criterion for trustworthy and relevant findings for their respective research design. Piloting our conceptual framework of foundational progress in SGM AYA research, each co-author calculated frequency ratings of their assigned publications according to the presence or absence of aspects within nine domains ( Figure 1). Results show that the most frequently addressed domains were Implications (n = 29), Nonbinary (n = 28), and Affirming terminology (n = 27).

| DISCUSSION
Our findings in the current scoping review reveal a limited, but growing empirical literature that provides some evidence of disparities in biomedical outcomes and psychosocial outcomes among SGM AYAs. The resulting body of literature was characterized by large gaps in knowledge on cancer outcomes and on outcomes for distinct sub-groups within the SGM AYA patient population.

| Biomedical outcomes
SGM participants reported greater physical inactivity, greater medical comorbidities, greater participation in high-risk behaviors such as alcohol use, and poorer physical health compared with non-SGM controls. 18 This finding may be attributed to conditions associated with SGM status that either predate or may occur irrespective of a cancer diagnosis. For example, SGM in the general population report negative medical experiences, perceive themselves as discriminated against by providers, and have historically low rates of healthcare use. 32,33 As such, SGM AYAs' outcomes may be disadvantaged by a lack of adequate comprehensive health care prior to their cancer diagnosis. It follows that SGM AYAs may have greater potential for treatment and survivorship T A B L E 2 Characteristics of included studies (n = 37). Secondary quantitative data analysis, crosssectional study Biomedical outcomes: transgender men had a significantly higher (>2-fold) number of cancer diagnoses compared with cisgender men, but not cisgender women. Cancer prevalence among gender nonconforming individuals and transgender women was not significantly different from that of cisgender men and cisgender women. Gender nonconforming survivors had significantly greater physical inactivity, heavy episodic alcohol use, and depression compared with cisgender men and cisgender women. Transgender men and survivors were significantly more likely to report poor physical health and greater medical comorbidities and were less likely to report smoking compared with cisgender men and cisgender women. Transgender women survivors were significantly more likely to report diabetes compared with cisgender men and cisgender women and were more likely to report cardiovascular disease compared with cisgender women Captures 2, 5-9

No. of articles
Boehmer et al. 19 USA N = 64, lesbian (n = 55), bisexual (n = 6), partnered with women (n = 3) Semi-structured interviews were followed by a self-administered questionnaire (only survey data were reported in the current study) Psychosocial outcomes: social support was positively associated with a measure of "fighting spirit" and a reverse association between "fighting spirit" and distress. Disclosure of sexual orientation did not have the anticipated positive outcomes, lack of relationship between disclosure, and lower distress or coping. Women in committed relationships were more likely to disclose to providers. A greater perception of social support was present among women who disclosed to providers. Being in a committed relationship had no positive influence on coping or adjustment. Fatalism and cognitive avoidance were unrelated to distress level. Sexual minority women in this sample experience lower levels of emotional distress compared with the mean mood disturbance score of the scale construction sample (heterosexual population). Time since dx was unrelated to coping and mood measures. Membership in cancer-support groups was related to higher distress and more cognitive avoidance coping. Care teams should work toward not being heteronormative and understand the burden of coming out. Suggestions included care teams using inclusive screening and assessment for LGBTQ+ adolescent and young adults, educating providers on inclusive language, and creating safe spaces  nonadherence due to prior negative healthcare experiences that predate their diagnosis of cancer. It is concerning that SGM AYA survivors utilize cancer prevention services, such as mammography with less frequency than their non-SGM peers as a presentation with the later-stage disease in childhood cancer survivors is associated with poor outcomes. 25,34 The finding that bisexual women reported lower odds of recent mammography aligns with the empirical literature that identifies patterns of delayed or declined cancer screening among marginalized groups, especially among those at the intersection of multiple minoritized statuses (e.g., SGM and racial/ethnic minorities). [35][36][37][38] Future studies are advised to test interventions that mitigate stigma and fear of discrimination-two known barriers to receiving prophylactic screenings among these groups.

| Psychosocial outcomes
The finding that SGM AYAs experienced greater clinical depression, anxiety, and psychosocial distress than cis-heterosexual AYAs reflects literature that substantiates minority stress theory among marginalized populations. [39][40][41][42][43] While there are higher rates of psychosocial distress in cancer survivors compared with the general population, there are also higher rates of psychosocial distress in the SGM population compared with the general population. 44,45 The extent to which a cancer diagnosis further exacerbates psychosocial distress in SGM AYA survivors compared with SGM individuals who have not had cancer needs to be assessed.
Further research is needed to develop necessary interventions to alleviate the lifelong impacts of stress processes (e.g., experience of prejudice, expectations of rejection, internalized homophobia) on SGM AYA psychosocial outcomes during and after treatment. A social genomics approach to minority stress among SGM AYAs is needed to further understand the relationship between social determinants of health and cancer's biologic mechanisms. 46 The social determinants of health are defined as the economic, education, healthcare access, built environment, and social conditions in which people live and have been identified as widely contributing to health disparities and inequities. 47 The finding that SGM survivors reported a lack of social support, experiences of isolation or disconnection, and poorer QOL is consistent with literature that demonstrates a lack of appropriate formalized support for SGM AYAs. 8,27,[48][49][50][51][52] Future research is advised to tackle gaps in patient-provider communication and peer-to-peer support programming such that service delivery is appropriately and equitably tailored to LGBTQ+ identity concerns. 53 Furthermore, it is important to understand and incorporate modes of social support among queer communities that exist beyond formalized medical and psychosocial services. A deep tradition of community care and mutual aid-stemming from medical neglect during the HIV/AIDS epidemic-is often upheld among LGBTQ+ groups who divest from formal care due to negative experiences. 54,55

| Gaps in research
Although survival outcomes are the most common primary endpoints in cancer clinical trials, none of the included studies addressed survival outcomes. No studies assessed overall or event-free survival for SGM AYAs for any prevalent cancer type seen in the AYA population. Although recent studies have highlighted racial, ethnic, and socioeconomic disparities in survival for AYAs diagnosed with cancer, the fact that survival outcomes have not been assessed in SGM AYAs is highly concerning. Figure 3 illustrates gaps in scientific evidence on major F I G U R E 3 Gaps in scientific evidence of sexual and gender minority Adolescent and young adults along the cancer care continuum. Adapted from National Institutes of Health. 56 1 No studies found in this area 2 Less than 3 studies found in this area aspects of SGM AYAs' care and outcomes along the National Cancer Institute's cancer care continuum.
Most studies examined AYAs as part of a larger study sample with a broader age range (86.5%, n = 32) and much fewer studies (13.5%, n = 5) focused exclusively on AYAs. Articles that were published in 2020 or later were more likely to include dimensions of gender-that is, nonbinary, transgender-in addition to sex and sexual orientation demographic items. Despite the acknowledgment of noncisgender participants, a critical gap exists in focusing on transgender, genderqueer, gender diverse, and intersex PRO. 57 Only 16 (43.2%) studies included participants who identify as such.
The findings of these studies demonstrate disparate biomedical and psychosocial health outcomes of SGM AYAs compared with their cis-heterosexual counterparts when these outcomes were assessed and reported. Unfortunately, most often studies did not collect or report data on sexual orientation and/or gender identity, and when studies did collect this data, results for AYAs were often combined with data from older SGM survivors.
While these results are critical to address, equal attention to aspects of queer resilience is owed. In some cases, SGM AYAs are less negatively impacted by the psychosocial effects of cancer and treatment. For example, breast cancer survivors who embrace the choice to "go flat"-that is, opt out of reconstruction after bilateral mastectomywere more likely to be genderqueer than cisgender, and these patients found comfort and pride in having modified breasts that more closely aligned with their gender identities. 20 Also, SGM AYAs experienced less romantic partnership distress about infertility arising from cancer than their cis-heterosexual counterparts. 30 Elevating resiliency through a strengths-based lens is of tantamount importance to identifying and eradicating disparate biomedical and psychosocial outcomes for SGM AYAs.

| Conceptual framework of foundational progress in SGM AYA research
We developed and piloted a conceptual framework to assess the quality of scientific evidence on SGM AYAs that derive from Levin et al.'s framework to assess sex, sexual orientation, and gender orientation in oncology research. 14 As shown in Figure 1, our framework reflects Levin et al.'s tripart schema that considers defining the population, measuring the population, and translating research to clinical services, while elaborating upon nine essential domains for high-quality research studies that capture SGM AYAs.
Specifically, Accurate terminology indicates that the study utilizes accurate sexual orientation/gender identity (SO/GI) terminology for today's cohort of SGM AYAs. Dimensions of human sexuality signify that the study correctly utilizes the three dimensions of human sexuality as it relates to the study. Nonbinary means that the study utilizes more than two identities to identify SOGI. Goal of study suggests that the study focuses its primary endpoint on SGM AYA cancer patients. Affirming terminology indicates that the study utilizes affirming SGM terminology that applies to the current cohort of AYAs.
Furthermore, Stakeholder collaboration denotes that the study discloses collaboration on research activities with SGM AYA patients and/or SGM AYA stakeholders in either the research methods or authors' affiliation. Multiple methods to collect SGM identity confirm that the study captures SGM identity via methods that offer both close-ended and open-ended response options. Implications indicate that the study offers practice and/or policy implications that directly address SGM AYA health. Last, Validated frameworks verify that the study utilizes instruments that are validated for SGM AYAs.
Findings revealing the most frequently included domains of SGM AYA research point to trends in research to date in the areas of Implications, Nonbinary, and Affirming terminology. These frequencies suggest that studies in the sampling trend toward providing practice and/or policy implications based on the empirical findings, which bodes well for efficiently translating findings into improved service delivery. A high prevalence of utilizing Nonbinary criteria indicates that studies in the sample measure SOGI as spectrum-based constructs, and that authors produce demographic data accordingly by soliciting more than one, nondichotomous response category for each identity domain. Similarly, a notable presence of Affirming terminology suggests a cultural shift toward endorsing identity affirmation 58 among SGM respondents by employing scientific language that adequately reflects the population of interest.
The least observed domains included Stakeholder collaboration (n = 11), Multiple methods to collect SGM identity (n = 9), and Validated measures (n = 6). Increased stakeholder collaboration between academic investigators and community-based stakeholders is needed. Methodologically, increasing the practice of collecting demographics using multiple methods (e.g., closed-and open-ended response modalities) would improve the production of rigorous and nuanced descriptive data 14,59,60 . Additionally, establishing validated instruments, questionnaires, theories, and frameworks that address the needs and experiences of individuals living at the intersection of SGM and AYA and their identities is critical to advancing the field. To the best of our knowledge, no validated survey instruments to assess SGM AYAs' experiences currently exist.

| Strengths and limitations
This scoping review did not include studies that focused on healthcare providers. Future systematic reviews are encouraged to examine literature that addresses the needs and experiences of our SGM AYA healthcare providers and other stakeholders.
Our study harkens a paradigmatic shift toward inclusive, innovative, and interdisciplinary cancer research with SGM. 61 This interdisciplinary author team comprises researchers with expertise in AYA oncology, social work, information science, and anthropology. Furthermore, the author team includes "embodied researchers" 62,63 whose lived experiences as patient-scientists, physicianscientists, and/or SGM individuals reflect the topics of study. Future author teams are encouraged to incorporate embodied researchers whose diversity of lived experiences reflects upon the literature in question in purposeful and ethical ways. 64

| CONCLUSION
The current study is the first to systematically identify, synthesize, and critique the literature to date on SGM AYAs by developing and piloting a conceptual framework for foundational progress to critically appraise the quality of each contribution. Results point to gaps in scientific evidence on SGM AYAs at numerous points across the cancer care continuum. Future efforts should fill this void with highquality empirical studies that reveal unknown disparities in care and outcomes and are inclusive of the intersectionality of SGM AYAs with other minoritized experiences, thereby advancing health equity in meaningful ways.

ACKNOWLEDGMENTS
The authors thank the scholars of SGM literature that were cited in our review for their foundational work, as well as the AYAs and individuals who participated in these studies for sharing their experiences.