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REVIEW ARTICLE

Digestive Health in Sexual and Gender Minority Populations

Vélez, Christopher MD1,2; Casimiro, Isabel MD, PhD3; Pitts, Robert MD4; Streed, Carl Jr MD, MPH5,6; Paul, Sonali MD, MS7

Author Information
The American Journal of Gastroenterology: June 2022 - Volume 117 - Issue 6 - p 865-875
doi: 10.14309/ajg.0000000000001804

Abstract

Nearly 50 years have passed since the Stonewall Inn Riots in June 1969, a seminal event for the lesbian, gay, bisexual, transgender, queer, intersex, and other sexual and gender diverse minorities' (LGBTQI+ or lesbian, gay, bisexual, transgender, queer, and intersex) rights movement (Table 1). However, sexual and gender minorities (1) (SGM [interchangeable here with LGBTQI+]; Figure 1) still face discrimination and harassment due to their sexual orientation and gender identity (SOGI). Approximately 7.2% of the United States identifies as LGBT, including 20.8% of those in born in Generation Z (1997–2003) (2), although this could be a potential underestimation, given lack of uniform SOGI data collection. The National Institute on Minority Health and Health Disparities has identified SGM communities as a “health disparity population,” (3) further compounded in transgender and intersex individuals (4). Legal issues in access to health insurance, employment, housing, marriage, and retirement benefits drive key social determinants of health (such as smoking, substance use, violence, and homelessness) in SGM populations (3). Health care has contributed to pathology around sex, gender, and sexual orientation and with a center on heteronormativity—where heterosexuality is the expected sexual orientation (5). There is a lack of education and preparedness in health care regarding SGM health (6), and bias (explicit and implicit) is prevalent (7). Understanding disparities in SGM communities is complicated further by lack of uniform SOGI data collection.

T1
Table 1.:
Terminology pertaining to sexual and gender minorities (12)
F1
Figure 1.:
National Institute of Health definition of sexual and gender minorities (SGM).

Broadly, there are higher rates of sexually transmitted infections (STI), substance use, mental health conditions, obesity and eating disorders, cancers (breast, cervical, and anorectal), and cardiovascular disease in SGM communities (8). Transgender patients, especially those of color, are more likely to be uninsured and experience discrimination, and 20% have been denied health care compared with cisgender (a person whose gender identity and expression aligns with their sex assigned at birth) patients (4,9). In addition, SGM individuals have twice the risk of emotional, physical, and sexual trauma compared with heterosexuals (10). A trauma survivor may feel vulnerable (for example, potentially reexperiencing trauma during an anorectal examination), which may affect patient–provider relationships.

This review summarizes the effects of social determinants of health and discrimination on health care access, highlights important digestive diseases to consider in the SGM population (Table 2), and offers solutions to improve and prioritize the health of these communities. The authors are a multidisciplinary panel of physicians who work with SGM individuals offering expert opinion. We aim to highlight SGM-specific issues that affect gastrointestinal (GI) health and highlight fundamental research needs that are currently lacking.

T2
Table 2.:
Digestive disease considerations in sexual and gender minority communities

THE MINORITY STRESS MODEL AND EFFECT ON GI HEALTH

Recognizing the disparate experiences of SGM persons is critical to addressing their health and well-being. The stress of discrimination and structural inequity based on identity is posited as one of the main drivers of health disparities experienced by SGM persons and communities, termed the “minority stress model” (Figure 2) (11–14). Using this model, we can build a better health care experience and system to meet their unique needs. The various social factors that influence care and outcomes of patients with GI concerns vary between SGM persons and straight, cisgender peers (11).

F2
Figure 2.:
Proposed model for how the biopsychosocial stress model and social determinants of health can affect gastrointestinal disease incidence, prevalence, and outcomes in sexual and gender minority populations. Adapted from Caceres et al. (11).

SGM persons experience greater discrimination, violence, rejection, identity concealment, and internalized homophobia that contribute to adverse health outcomes (11,15). Furthermore, there is intersectionality with SGM identity and other factors, including race/ethnicity, age, socioeconomic status, abilities, culture, class, and religion that affect health outcomes (16). Within SGM populations, racial/ethnic minorities are more likely to live in poverty compared with their White peers (17). General stressors and those based on SGM status influence health behaviors associated with GI health, particularly because it relates to an increased tobacco and alcohol use (3,18), which has been consistently linked to victimization and minority stress (19,20).

BOWEL DISORDERS

Sexually transmitted GI syndromes

In the United States, 1 in 5 people experience an STI at any given time, with nearly 26 million STI acquired annually (21). There is a high prevalence of STI among men who have sex with men (MSM) and transgender-diverse persons (22). Unfortunately, SGM patients often experience socioeconomic barriers and discrimination in the health care setting, which inhibit access to care and enhance their risk for STI acquisition (23–25). It is imperative that medical providers caring for SGM patients document a comprehensive sexual history, inquire about risk exposures, and offer testing and treatment based on guidelines (26). Care must be taken to recognize behaviors as conferring increased risk and would be similarly elevated when practiced by non-SGM persons.

There is tremendous anatomic diversity and sexual practices among the SGM populations requiring tailored consideration for STI screening (particularly the GI tract). To complement the sexual history, providers need to document and maintain an anatomical inventory or a record of organs an individual patient has. Data are limited regarding the prevalence of STI among individuals with neo-organs (final organ structure based on a surgical procedure, such as a neovagina in transwomen). Furthermore, those status postvaginoplasty with integrated intestinal grafts carry a risk for inflammatory bowel diseases (IBD) and malignancy, as discussed further (27,28).

Proctitis, proctocolitis, and enteritis are sexually transmitted through oral–anal (cunnilingus or analingus), digital–anal (toy insertion, fingering, and fisting), and genital–anal (anal receptive and insertive) contact in any individual engaging in these activities (SGM and non-SGM alike). A patient with anorectal pain, rectal discharge, or tenesmus should be subjected to testing for acute proctitis. This evaluation includes anoscopy, Gram stain, and laboratory tests to identify herpes simplex viruses, gonorrhea, chlamydia, and syphilis. Of note, lymphogranuloma venereum, a serovar of chlamydia typically more symptomatic, is most commonly diagnosed among MSM (29), and treatment requires a longer course of doxycycline.

Proctocolitis symptoms are similar to proctitis, but causative organisms are different and include Campylobacter spp., Entamoeba histolytica, Shigella spp., Chlamydia spp., and those that cause syphilis. Among immunocompromised patients, cytomegalovirus and other opportunistic infections should be considered. Enteritis, which usually manifests as abdominal cramping and diarrhea, is typically caused by Giardia lamblia, Shigella spp., Salmonella spp., Escherichia coli, Campylobacter spp., and Cryptosporidium spp. Notably, sexually transmitted GI syndromes can resemble IBD both clinically and histopathologically (30). For example, proctitis and proctocolitis can demonstrate mucosal ulcers, granulomas, plasma cell infiltrates, and cryptitis on histopathology, making them indistinguishable from IBD (30). To minimize misdiagnosis and delay in appropriate management, infectious and noninfectious etiologies should be considered when SGM patients who practice anorectal sex present with GI symptoms.

Immunizations are also important for reducing STI, especially sexually transmitted hepatitis viruses. Hepatitis A virus (HAV) outbreaks are sporadic but often involve MSM through oral–anal sexual activity among the unvaccinated (31). HAV vaccination should be offered to all MSM and persons engaging in sexual activities that facilitate transmission (32). The risk factors for hepatitis B virus (HBV) and hepatitis C virus are similar, which include but not limited to condomless sex acts, multiple partners, and other diagnosed STI (33). Patients should be screened for hepatitis C virus and routinely vaccinating for HAV and HBV to promote liver health (26,34,35). However, only approximately 9%–42% of MSM are vaccinated against HBV (9).

GI cancer screening

It is well established that SGM populations experience disparately the effects of cancer with lower screening rates, a higher incidence, and an increased mortality (36). In the United Kingdom, a population survey of 796,594 individuals found lesbian and bisexual women had increased oropharyngeal cancers (odds ratio [OR] 3.2; 85% confidence interval [CI] 1.7–6.0), and bisexual and gay men had higher rates of viral-associated cancers such as Kaposi sarcoma (OR 48.2; 95% CI 22.0–105.6), anal cancer (OR 15.5; 95% CI 11.0–21.9), and penile cancer (OR 1.8; 95% CI 0.9–3.7) (37). Reasons for these disparities include the following: (i) lack of routine SOGI data capture, (ii) inadequate knowledge about the health needs of SGM communities, and (iii) fear of discrimination of the health care system, resulting in decreased care.

Anal squamous cell carcinoma is the fourth most common cause of cancers among people living with human immunodeficiency virus, with an estimated incidence of 160 per 100,000 person-years in the United States and the highest incidence rates being among gay men older than 45 years (38). The Anal Cancer/HSIL Outcomes Research Study found treating anal high-grade squamous intraepithelial lesions decreased the risk of anal cancer by 57% compared with active monitoring (95% CI 6%–80%, P = 0.029) (39). Gastroenterologists should consider screening high-risk populations by anal cytology annually (40). In addition, human papilloma virus (HPV) vaccination should be administered to all eligible patients because it has been found to minimize anal squamous cell carcinoma rates (41). Much debate exists as to who would benefit from screening for (HPV mediated) anal cancer and precancerous lesions (42). While anoscopy is typically used (42), a careful examination of the anus and the perineum can be easily included during a routine colonoscopy in those at an increased risk of HPV-mediated anorectal cancers, such as those practicing receptive anal intercourse, human immunodeficiency virus seropositive, or are immunosuppressed for other reasons. More education is needed in gastroenterology curriculum about anal cancer, HPV risk, and management because it falls under the purview of GI care.

From a GI perspective, care of the neovagina in transgender women merits special consideration. A neovagina refers to a vagina that is constructed in a transgender woman as part of her gender-affirming care. One surgical approach uses intestinal tissue and as such may experience the same disease of the in situ colon (43). The incidence of colorectal cancer developing in these specific neovaginas is unknown, but there is concern that inflammation that may be present may increase the risk of developing malignancy (44). GI providers taking care of transgender women must understand the specifics of the surgery; if a neovagina has been constructed from the sigmoid colon, it likely should be included during colorectal cancer screening. However, there are no data or guidelines to determine the frequency of screening.

ANORECTAL HEALTH

The health of the anorectum and oropharynx is important not only for SGM communities but for any individual engaging in penetration or insertive/receptive intercourse. Among heterosexual men and women, approximately a third of have engaged in oral or anal sex with low rates of barrier protection (45). Given taboos and stigma surrounding anal sex and SGM populations, it is difficult to estimate the prevalence of penetrative practices. However, it is important to recognize that among SGM communities, penetrative anal intercourse is not exclusive to men who have sex with men (46,47). Given the implications in oropharyngeal and anorectal health, a comprehensive sexual history is imperative. However, little has been reported about how often gastroenterologists assess for sexual practices.

While there are rare reports of significant oropharyngeal and anorectal trauma with penetration (48,49), the practice of both oral and anal sex are overwhelmingly safe. Given differences between the vaginal mucosa (which is primed during sexual arousal to facilitate insertion) (50) and anorectal mucosa, adequate lubrication is necessary to reduce the possibility of trauma. In preparation for anal sex, factors that seek to reduce the passage of fecal contents from the anorectum or distal colon during intercourse should be considered (51,52). These include regulation of fecal contents and bowel movement timing and altered eating habits (for example, avoidance of meals before an expected sexual encounter) or increased dietary fiber to promote easier preparation. Enema use is controversial because it may result in anorectal mucosal tears. While dyspareunia from vaginal intercourse is well studied, there is an often overlooked, kindred condition called “anodyspareunia” (pain during receptive anal sex act), which can devastate the sexual quality of life in those who engage in anal sex act (53). It is unknown whether dyspareunia treatments, such as pelvic floor therapy or use of dilators, can affect anodyspareunia, but such interventions are often used empirically (51).

Gastroenterologists are not primed to address concerns about engagement in receptive anal intercourse when patients experience GI illness. This is related to lack of education assessing sexual health and little data to guide management. For example, anal fissures and hemorrhoids may require more aggressive management when engaging in receptive anal sex. While limited data suggest an association between fecal incontinence and penetrative anal intercourse (54,55), it is unlikely strong enough to warrant counseling against anal sex. Irritable bowel syndrome is associated with sexual dysfunction and may be more problematic in those engaging in anal intercourse (56). IBD, particularly ulcerative colitis, can affect the sexual quality of life. Patients may need to be counseled on the avoidance of anal intercourse during flares or immediately after ileal pouch anal anastomosis—with safe resumption once suture lines are healed to reduce the risk of perforation (57). More research is needed to further clarify these questions and improve GI education.

WHOLE GUT/LUMINAL GI HEALTH

Obesity, eating disorders, and disordered gut–brain interactions

The association between sexual orientation and body mass index can be explained by the minority stress model that influences nutrition, physical activity, and alcohol use (13). Eating disorders and body dysmorphia are common in SGM communities, especially among gay men (58). Sexual minority men are more likely to be underweight (59). By contrast, sexual minority women, specifically those that identify as lesbians, were found to be at an increased risk of obesity or overweight (OR 1.41, 95% CI 1.16–1.72 in a study of 93,429 adults) than heterosexual women (59). Obesity has been associated with colorectal cancer in addition to nonalcoholic fatty liver disease (NAFLD) and other chronic diseases, although this has not been shown in meta-analysis (60). Focusing on overall health vs weight alone can lead to positive behavior changes regarding food choice and exercise (61,62).

Furthermore, stress can affect the development and severity of disordered gut–brain interactions (DBGI; formally termed “functional” GI disease). Despite the high prevalence of irritable bowel syndrome and functional dyspepsia in the general population, these diseases and DBGI have been poorly studied in SGM communities (63). Similarly, the incidence of pelvic floor dysfunction remains unknown. With biopsychosocial factors central to DGBI pathophysiology (64), the DGBI burden in SGM communities remains to be determined.

Gender affirmation and gut health in transgender and gender nonbinary patients

Transgender and gender nonbinary (GNB) individuals who choose to undergo hormonal transition or surgical interventions for gender affirmation face unique considerations regarding GI health. Sex hormones are believed to affect GI tract function (65,66); it is unknown how affirming care may alter the GI tract. Feminizing hormone therapy consists of an estrogen and an antiandrogen to suppress testosterone and maintain estradiol at a physiological range for cisgender female individuals. Although spironolactone is the most commonly used antiandrogen, gonadotropin-releasing hormone agonists can also be used. Masculinizing hormone therapy consists of testosterone treatment usually through parenteral or transdermal preparations to achieve testosterone values in the cisgender male range (67). Transgender and GNB patients may also seek gender-affirming surgeries that can have specific GI complications as discussed further. Knowledge of these treatments and further research about their effects are imperative to comprehensively care for these individuals.

LIVER DISEASES AND GENDER-AFFIRMING HORMONE THERAPY

Nonalcoholic fatty liver disease

NAFLD is strongly associated with testosterone levels in cisgender women, even in the absence of androgen excess (68–72). NAFLD is more prevalent in cisgender men compared with that in premenopausal cisgender women and higher in cisgender women with polycystic ovary syndrome. Rates of NAFLD are also higher in cisgender women after menopause compared with those in premenopausal cisgender women (73). In cisgender men, lower levels of testosterone have been shown to be associated with the development of NAFLD (74,75). Cross-sectional studies have shown feminizing hormone therapy with estradiol has a positive effect by increasing HDL cholesterol and lowering LDL cholesterol, but this effect has not been demonstrated in systematic review meta-analyses (76,77).

Masculinizing hormone therapy has been associated with increased BMI (78) and fat redistribution, characterized by increased central/visceral adiposity (79), which increases the risk of dyslipidemia and insulin resistance—both risk factors for NAFLD (80). In a meta-analysis, it has also shown to increase both serum triglycerides (21.4 mg/dL; 95% CI 0.14–42.6) and LDL cholesterol (17.8 mg/dL; 95% CI 3.5–32.1) levels and decrease HDL cholesterol level (−8.5 mg/dL; 95% CI −13.0 to −3.9) at 24 months (76). However, whether or not exogenous testosterone use in individuals assigned female at birth increases NAFLD risk has not been investigated and merits further study. In addition, whether screening for NAFLD in those undergoing gender-affirming hormone therapy and clinical risk factors also remains unknown.

Hepatic adenomas and vascular disorders

Hepatic adenomas are rare benign liver neoplasms that have been shown to be associated with exogenous sex hormone use. In the 1950s, long-term oral contraceptive (OCP) use and hepatocellular adenomas were reported to be as high as 3–4 per 100,000 (81). However, more recent data have not shown an increased risk of adenomas in cisgender women on modern OCP (82). The development of hepatic adenomas has also been linked to exogenous androgen use in cisgender men with hypogonadism and anemia, or androgen used recreationally for body building (81,83–86). Hepatic adenomas in transpatients or GNB patients on gender-affirming hormone therapy have not been widely reported.

Hepatic vascular lesions have also been documented in patients on exogenous steroids (87). Peliosis hepatis is a rare vascular lesion that is characterized by formation of sinusoidal dilatation and blood-filled hepatic spaces (28). Cases of peliosis hepatis have been reported in cisgender women on OCP and in cisgender men on anabolic steroids (88). However, this has not been identified in individuals taking gender-affirming hormone therapy.

SURGICAL CONSIDERATIONS AND CARE OF THE NEOVAGINA

Intestinal vaginoplasty is a modality available for the creation of a neovaginal canal in patients undergoing feminizing surgery who do not have adequate tissue from penile inversion (89). These surgical techniques use intestinal segments from the small or large bowel such as the ileum, sigmoid, or right colon for the creation of a neovagina that provides favorable vaginal sexual function and alleviates gender dysphoria (89–95). Postoperative complications can include surgical site infection, small bowel obstruction, peritonitis, rectovaginal fistulas, rectal injury (96), vaginal stenosis (97), and prolapse (Table 3) (89,98–102). While long-term follow-up studies after intestinal vaginoplasty are scarce, most are low-morbidity procedures, resulting in favorable anatomical outcomes for transfeminine patients (103,104). Although no guidelines exist, patients who have undergone intestinal vaginoplasty should be managed as cisgender females with neovaginas. Thus, providers should obtain a detailed anatomic inventory and ask about neovaginal discharge, bleeding, dyspareunia, or pelvic pain and perform a complete pelvic examination if there are any vaginal symptoms (105). Evidence of suspicious lesions should be biopsied (106), and GI endoscopy may be warranted. Causes of neovaginal bleeding and discharge may include trauma, infection (107), intestinal polyps, IBD, colitis, or carcinoma.

T3
Table 3.:
Management of gastrointestinal complications in intestinal neovaginas

SOLUTIONS: ESSENTIAL STEPS TO TAKE TODAY

Effectively caring for SGM individuals requires sweeping cultural and structural changes in health care (4), starting first with undergraduate and graduate medical education (108). Understanding our own implicit biases regarding sexuality and gender and engaging in self-reflection to mitigate these biases are also needed. Ultimately, meeting the needs of SGM populations requires collaboration with SGM communities, who have for decades been developing care models to meet their own needs (109,110).

The Association of American Medical Colleges has published a comprehensive resource for medical educators, which focuses on providing care for this patient population (4). Implementation of these recommendations would require the following: (i) faculty development on SGM health, (ii) creation of SGM curricular content and appropriate evaluation strategies, (iii) increased exposure to SGM populations in established clinical experiences, (iv) inclusion of SGM health in institutional research priorities, and (v) continued promotion of cultural competency and humility among learners and educators.

Standardizing the collection of SOGI data, including pronouns, while respecting patient's identities is essential (111,112). Such data can facilitate research using electronic health records to systematically study health disparities in this population (113). Table 4 highlights the unanswered questions relevant to GI health in SGM populations. In addition to routinizing appropriate SOGI data collection, respectfully asking about sexual history and practices is important for patient comfort and to assess behaviors, which may be associated with GI disease. This is unfortunately an overlooked skill that is glossed over in medical education but essential for the GI provider. Table 5 highlights the practical ways to ask about pronouns and obtain a sexual history. Establishment of a gender-affirming environment promoting transgender sensitivity and provider knowledge enhances provider–patient trust, reinforces positive interactions, and increases retention in care (114). Resources are available including scripts and toolkits (see Appendix 1, Supplementary Digital Content 1, https://links.lww.com/AJG/C524) (115). In addition, given the disproportionate rates of trauma in SGM populations (116,117), creating safe and inclusive environments are essential. For example, being sensitive to possible sexual trauma while performing anorectal examinations (only when essential) and colonoscopies is imperative.

T4
Table 4.:
GI and hepatology-related research needs in sexual and gender minority populations
T5
Table 5.:
Sexual health model and patient interview in sexual and gender minorities (118)

Furthermore, the overall institutional climate must be engaged in meeting the needs of SGM populations. Moving beyond binary categories and using more accurate, inclusive, and nongendered language on clinic forms and in the electronic medical record is an important step (111). Support of nondiscriminatory policies, inclusive and expansive visitation rights, and engagement in community outreach and collaboration is also essential (3,108). Clinics should have imagery that is representative of the diversity of SGM populations and reflect the communities served. Table 6 summarizes recommendations for the care of SGM populations.

T6
Table 6.:
Recommendations for the care of sexual and gender minority communities

CONCLUSION

SGM communities face numerous challenges both social and health-related that directly affects digestive health. Patients may face bias in multiple aspects of life. A basic understanding of these discriminatory factors is key to dismantling health care bias for all providers and staff. The disparities in digestive health that may exist between SGM communities and the population at large remain unexplored and must be investigated.

CONFLICTS OF INTEREST

Guarantor of the article: Sonali Paul MD, MS.

Specific author contributions: All authors planned, drafted, and edited the entire manuscript and approved the final draft submitted.

Financial support: There was no financial support in the writing of this manuscript. I.C. serves on the Medical Expert Board for Verywell.com. C.S. has salary support from the National Heart, Lung, and Blood Institute (1K01HL151902-01A1), American Heart Association (20CDA35320148), Providence/Boston Center for AIDS Research (P30AI042853-23), and Boston University School of Medicine Department of Medicine Career Investment Award; C.S. also serves on the Board of US Professionals Association for Transgender Health and is a consultant for EverlyWell. S.P. has grant and research support from Target PharmaSolutions, GENFIT, and Intercept Pharmaceuticals, but this work was independent of that support. C.V. has funding from the Cystic Fibrosis Foundation, the Massachusetts General Hospital Equity Innovation Laboratory, which was independent of this support; C.V. also has divisional support for sexual and gender minority care from the Massachusetts General Hospital Division of Gastroenterology.

Potential competing interests: None to report.

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