Dermatology-Related Epidemiologic and Clinical Concerns of Men Who Have Sex With Men, Women Who Have Sex With Women, and Transgender Individuals FREE

From television shows such as Will & Grace,Queer Eye for the Straight Guy, and The L Word to the legalization of same-sex civil unions in Vermont and same-sex marriages in Massachusetts and the focus on these issues in the November 2004 election, gay men and lesbians are assuming an increasingly prominent cultural and political profile in America. Medically, gay men first appeared on the national radar screen in 1981, when physicians in New York, NY, and Los Angeles, Calif, reported cases of Kaposi sarcoma and pneumocystis pneumonia, marking the beginning of the AIDS epidemic.^{1 - 2} Since then, to the extent that they have focused on the health care needs of gay men, dermatologists have focused primarily—and appropriately—on describing and treating the cutaneous manifestations of human immunodeficiency virus (HIV) and AIDS.^{3 - 4}

In this issue of the ARCHIVES, for example, Burnouf et al⁵ report an important case series of patients with HIV-associated facial lipoatrophy treated with autologous fat grafts. Three quarters of the patients treated in the Paris (France)-based study were men who have sex with men (MSM). As Burnouf et al⁵ note, facial lipoatrophy can be a tremendously stigmatizing problem for individuals with HIV and AIDS.^{6 - 7} Autologous fat transfer, described in the article,⁵ is another promising technique, along with the use of other filler materials,^{8 - 11} that can help address this disorder.

Whereas MSM, including gay men, have received the attention of dermatologists in the era of HIV and AIDS, other sexual-minority groups—lesbians, bisexuals, and transgender and intersex individuals—have received scant notice. Sexual minorities, however, have unique needs, including but not limited to HIV and AIDS, of which dermatologists, like other physicians, should be aware. In this review, we describe important issues of terminology, epidemiology, and sensitivity regarding sexual minorities that will enable dermatologists to better care for these patients in their practices. Compared with women who have sex with women (WSW) and transgender patients, MSM have more health concerns relevant specifically to dermatologists on which the medical literature has focused. For this reason, much (but not all) of the disease-specific data in this review relate to MSM.

The terms gay, lesbian, and bisexual refer to an individual’s self-identification. Although these categories may be important and useful culturally, they are less relevant to dermatologists than are patients’ sexual behaviors for 2 reasons. First, sexual behavior, not self-identification, is the important epidemiologic factor in the diseases that dermatologists diagnose and treat. Second, not all self-identified gay men, lesbians, or bisexual individuals are sexually active, and not all individuals who practice same-sex sexual behavior self-identify as gay, lesbian, or bisexual.¹² For these reasons, we focus our discussion of medical concerns on behavioral groups: MSM and WSW. Bisexual MSM and bisexual WSW share many of the health concerns of MSM and WSW, respectively.

Also designating self-identification, transgender is generally used as an umbrella term to include individuals whose appearance and behavior does not conform to cultural norms for their birth sex.¹³ It includes the following categories of individuals:

Our discussion of the dermatologic issues of transgender individuals focuses on transsexuals.

Both HIV and AIDS remain major problems for MSM. Of all the men diagnosed as having HIV infection or AIDS in the United States in 2002, MSM accounted for 68.5%; of all the men with HIV without AIDS, MSM accounted for 50.2%.¹⁶ Overall, 17% of MSM in New York, Los Angeles, Chicago, Ill, and San Francisco, Calif, were estimated to be HIV positive in 1997.¹⁷ The number of newly diagnosed HIV infections in MSM in 29 states with name-based HIV/AIDS surveillance increased 17% from 1999 to 2002, with MSM accounting for 42% of all new infections during this period.¹⁸ Higher and increasing rates of HIV and AIDS have been noted among black, Hispanic, and mixed-race men,¹⁹ who composed 52% of MSM AIDS cases in 1998 compared with 31% in 1989.²⁰ Risk factors for HIV infection in MSM include higher numbers of sex partners, unprotected anal sex, sex while using alcohol or drugs, and injecting drug use.²¹

Cutaneous disorders are common in HIV-infected individuals, with 65% reported to have at least 1 skin manifestation in one study.^{3 ,21} These disorders, including cutaneous effects of antiretroviral medications, have been extensively reviewed elsewhere²² and include the problem of HIV-associated lipoatrophy, as described by Burnouf et al.⁵ Most of these disorders do not differ according to individuals’ sexual behavior. An exception is HIV-associated Kaposi sarcoma, seen 20 times more often in MSM with AIDS compared with male AIDS patients with hemophilia²³ and linked to a high prevalence of human herpesvirus 8 in MSM regardless of HIV status.²⁴

The introduction of protease inhibitors and highly active antiretroviral therapy for HIV and AIDS in 1996 has led to decreased HIV- and AIDS-associated morbidity and mortality among MSM. At the same time, the number of MSM reporting multiple sexual partners and unprotected anal intercourse increased in the late 1990s,²⁵ perhaps due to decreased concern about HIV among MSM in the era of highly active antiretroviral therapy.²⁶ These behaviors may have led to the increased incidences of other sexually transmitted diseases (STDs), including chlamydia and urethral and rectal gonorrhea, in MSM reported since 1995.^{25 - 28} Of therapeutic importance, rates of fluoroquinolone-resistant Neisseria gonorrhoeae isolates in MSM have increased,²⁹ prompting the Centers for Disease Control and Prevention (CDC) to recommend ceftriaxone sodium, cefixime, or spectinomycin hydrochloride rather than a fluoroquinolone for the treatment of gonorrhea in MSM.²⁹ Patients with gonorrhea should receive concomitant empirical treatment for Chlamydia trachomatis unless co-infection can be ruled out.²⁹

On the decline in the late 1980s and early 1990s, primary and secondary syphilis is now also increasing among MSM,^{30 - 32} who account for more than 40% of cases nationwide³³ and 80% or more of cases in some cities, such as New York,³⁰ Seattle, Wash,²⁷ San Francisco,³⁴ and Los Angeles³⁴ (Figure 1). According to CDC surveillance data,³³ the overall syphilis incidence nationwide increased 12.4% from 2001 to 2002; although most cases are in the South, rates are increasing fastest on the West Coast, in the Northeast, and in the Midwest.³³ The increased rates have occurred only among men, however, suggesting that most of the increase can be attributed to MSM.³³ The CDC recently reported increased rates of azithromycin resistance in Treponema pallidum strains isolated from MSM in 2002 and 2003.³⁵ Favored in the past by some public health departments for ease of administration compared with intramuscular penicillin G benzathine, a single dose of oral azithromycin is no longer an acceptable treatment option for syphilis in MSM.³⁵

The seroprevalence of herpes simplex virus (HSV) type 2—the type of HSV that usually causes genital herpes, which in turn may permit more efficient HIV transmission—was also reported to be higher in MSM than in the general population.^{36 - 37} For this reason, studies of the effect of antiviral suppressive therapy in HSV-2–seropositive individuals at risk for HIV infection have been proposed.³⁶

Outbreaks of lymphogranuloma venereum due to C trachomatis infection have been reported among MSM in the Netherlands³⁸ and in Germany.³⁹ In the Netherlands, where usually fewer than 5 cases per year are seen countrywide, 92 MSM with lymphogranuloma venereum have been diagnosed since 2003.³⁸ Only 1 of these 92 patients had the typical clinical features of inguinal adenopathy and buboes; the others had gastrointestinal symptoms, including bloody proctitis with a purulent or mucous anal discharge and constipation.³⁸ The cases in Germany, and some in the Netherlands, were caused by the serovar L strain of C trachomatis, a more invasive strain typically seen in less developed countries.^{39 - 40}

Anal human papillomavirus (HPV) infection has become a topic of increasing interest, although screening for anal HPV has not been universally adopted. Anal squamous cell carcinoma is the fourth most common type of cancer in HIV-infected men, and it is twice as common in HIV-positive MSM as in HIV-negative MSM (Figure 2).⁴¹ Highly active antiretroviral therapy has not been shown to decrease the incidence of anal squamous lesions in MSM.⁴² Anal HPV infection is a risk factor for anal intraepithelial neoplasia and anal squamous cell carcinoma.⁴³ Polymerase chain reaction studies from urban centers in the United States in the early 1990s showed prevalences of anal HPV DNA in 57% to 78% of HIV-negative MSM and in 63% to 93% of HIV-positive MSM.^{44 - 46} In a recent German study of 103 HIV-positive MSM treated with highly active antiretroviral drugs, 89 (86%) had DNA evidence of anal HPV infection; 20 (19%) had histologic evidence of anal intraepithelial neoplasia, which was classified on clinical appearance as bowenoid, erythroplakic, leukoplakic, or verrucous; and none had invasive anal cancer.⁴⁷ Using Papanicolaou screening for cervical cancer as an analogy, some physicians have recommended screening individuals at high risk for anal malignancies, including MSM and HIV-positive individuals, with anal cytology.^{47 - 48} This technique is similar to a Papanicolaou smear, and patients do not need to undergo a preprocedure bowel preparation. Kreuter et al⁴⁷ collected anal Papanicolaou samples by swabbing the perianal and anal area with a Polyester-tipped swab, placing the material collected onto a glass slide, fixing it with ethanol, and staining it with Papanicolaou stain; cytologic samples were interpreted using the same criteria used for cervical Papanicolaou smears.⁴⁷ Anal Papanicolaou smears have been shown to be accurate in detecting the presence of anal intraepithelial neoplasia, which can then be further diagnosed using anoscopy and biopsy.⁴¹ Treatment of invasive anal cancer is necessary. Although there have been reports of successful treatment of anal intraepithelial disease with excision, laser ablation, and imiquimod, studies of the long-term effectiveness of treating these lesions are lacking.⁴⁷ Because of the lack of data on the effectiveness of anal HPV screening, we do not routinely perform anal Papanicolaou smears in MSM or HIV-positive patients at the Hospital of the University of Pennsylvania or the Mazzoni Clinic. We refer patients with perianal condyloma acuminatum to a colorectal surgeon for anoscopic evaluation.

Infection with more than 1 STD is common. Therefore, MSM should be questioned, similar to all other patients, for symptoms suggestive of other STDs, including dysuria, urethral discharge, and the presence of genital and perianal sores and lesions. Positive answers should lead to further examination, testing, and treatment. Testing for other STDs, including gonorrhea, chlamydia, syphilis, and HIV, should also be offered.

It is important, however, for physicians to inquire whether a male patient with an STD engages in same-sex sexual behavior for 2 reasons.⁴⁹ First, the physician will be able to make appropriate recommendations to the patient regarding STD screening because the CDC’s STD screening recommendations are different for MSM than for other populations (Table 1). Second, the physician will be able to inquire about hepatitis vaccination status. According to CDC guidelines, all MSM should be referred for vaccination against hepatitis A and B. Both of these diseases disproportionately affect MSM,^{50 - 51} in whom hepatitis vaccination rates are still low.^{50 ,52}

Outbreaks of community-acquired methicillin-resistant Staphylococcus aureus skin infections, including furuncles, abscesses, paronychia, impetigo, cellulitis, and wound infections, have occurred among groups of MSM in Los Angeles.^{53 - 54} Many of the methicillin-resistant S aureus strains isolated in these groups are resistant to fluoroquinolones.⁵³ Although it has been suggested that these infections may be sexually transmitted,⁵⁴ other outbreaks of community-acquired methicillin-resistant S aureus have been traced to shared common objects (eg, athletic equipment, towels, benches, and personal items).⁵³

Characterized by anorectal pain, bleeding, and changes in bowel habits, proctitis in MSM may be due to infection (Neisseria gonorrhoeae, HSV, C trachomatis, or T pallidum) or to other causes, including trauma or allergies to lubricants.⁵⁵ Receptive anal intercourse can lead to perianal abrasions, fissures, and lacerations.⁵⁵ Rectal abscesses may also occur, requiring surgical intervention.⁵⁵

Finally, MSM who use anabolic corticosteroids for medical reasons (eg, to treat muscle wasting in HIV/AIDS) or for recreational reasons (eg, to look bigger, stronger, or more attractive or to improve athletic performance) may develop corticosteroid acne.⁵⁶ A 2002 study⁵⁶ of gay men attending gyms in central London (England), for example, reported corticosteroid use in the past year in 15% of respondents, of whom 40% reported having acne.

Although risk for STDs for WSW may be lower than that for women who have sex with men, WSW do contract STDs.⁵⁷ Female-to-female transmission of syphilis and HIV has been described,⁵⁸ and genital warts and HSV may also be transmissible between women.^{57 ,59 - 60} In a recent study⁵⁷ of WSW in London that surveyed bisexual women and women with female partners exclusively, histories of genital warts and genital herpes were reported by 1.6% and 1.1% of respondents, respectively. Histories of chlamydia, pelvic inflammatory disease, and gonorrhea infections were reported rarely, by 0.6%, 0.3%, and 0.3% of respondents, respectively.⁵⁷ These infections were reported only in the 82% of women surveyed who reported having also had sex with men.⁵⁷

Compared with women who have sex with either men or women only, women who have sex with both men and women may be more likely to engage in high-risk practices for HIV infection, including sex with an HIV-positive man, multiple male sexual partners, sex with a man who has sex with men, sex with an injecting drug user, trading of sex for drugs or money, and anal sex.⁶¹

High rates of HIV infection in MTF transgender individuals, particularly African Americans, have been reported in San Francisco⁶² and Los Angeles⁶³ ; in Los Angeles, for example, 22% of transgender MTF African Americans who were tested were HIV positive.⁶³

The use of estrogens for feminization has been associated with as much as a 20-fold increased risk for venous thromboembolic events.⁶⁴ Estrogens may also decrease male pattern hair growth and sebum production,⁶⁵ leading to xerosis,⁶⁴ and may improve acne.⁶⁵ To eliminate male pattern hair growth, MTF transgender individuals may use shaving, waxing, plucking, electrolysis, or laser hair removal.⁶⁶

A case of Mycobacterium abscessus cellulitis and abscesses in an MTF transgender individual who received silicone injections in a nonmedical office setting has been reported,⁶⁷ as has a squamous cell carcinoma arising in a neovagina 20 years after sex reassignment surgery.⁶⁸ The cosmetic use of silicone among MTF transgender individuals can result in granuloma formation^{69 - 70} and lymphedema.⁷⁰ We have heard anecdotal reports of the widespread use of silicone in MTF transgender individuals in nonmedical settings, including silicone “pumping parties.” We have also heard anecdotal reports of the prophylactic use of intralesional corticosteroids after silicone injections to prevent granuloma formation.

Masculinizing doses of testosterone in female-to-male transgender individuals cause increased growth of facial and body hair, increased sebum production, worsening of acne, and the development of corticosteroid acne.⁶⁵ Local reactions at sites of intramuscular or transdermal administration may develop.⁷¹ We also recently treated a female-to-male transgender individual for extensive keloids that developed after a bilateral mastectomy procedure.

In 1994, the American Medical Association⁷² adopted as its policy that “the physician's nonjudgmental recognition of sexual orientation and behavior enhances the ability to render optimal patient care in health as well as in illness.” More recently, on April 17, 2005, the American Academy of Dermatology’s board of directors approved changes to the American Academy of Dermatology’s Statement of Principles of Professional Conduct, which now states, “Physicians should work actively to eliminate discrimination in health care, whether based on race, gender, sexual preference, socioeconomic status, ethnicity, religion, or any other social category.”^{73 - 74} Nevertheless, physician bias against gay men, lesbians, bisexuals, and transgender individuals has been well documented.^{75 - 76} This bias may be subtle, manifesting as a physician’s assumption of a patient’s heterosexuality—assuming a wedding ring on a man means that he has a wife, for example, or one on a woman means that she has a husband. Out of concern for real or perceived bias among health care providers, among other reasons, some sexual-minority patients may choose not to access health care,⁷⁷ and when they do they may not divulge their sexual orientation or behavior.⁷⁵

Communicating familiarity and comfort with the dermatologic issues of sexual minorities can help build physician-patient rapport and can lead to better health care for sexual-minority patients. Strategies for demonstrating the acceptance of sexual-minority patients in a dermatology office, based on others’ suggestions^{78 - 80} and our own experiences, are listed in Table 2. The Web sites of the Gay and Lesbian Medical Association (http://www.glma.org), an organization of health care providers, and Boston’s Fenway Community Health Center (http://www.lgbthealthchannel.com), which serves many sexual-minority patients, are also valuable resources for physicians who want to learn more about clinical and sensitivity challenges in taking care of sexual minorities.

Dermatologists who encounter sexual-minority patients whose treatment needs seem to be outside their area of expertise or comfort may want to refer their patients. The Gay and Lesbian Medical Association Web site also maintains a referral list of providers who are willing to see sexual-minority patients. In addition, dermatologists can refer patients to health centers across the country, such as New York’s Callen-Lorde Community Health Center, Fenway Community Health Center, and the Mazzoni Clinic (http://www.glma.org/resources/community_health_centers.shtml), that specifically serve sexual-minority patients.

Correspondence: Kenneth A. Katz, MD, MSc, Department of Dermatology, University of Pennsylvania School of Medicine, 3600 Spruce St, 2 Maloney, Philadelphia, PA 19104 (Kenneth.Katz@post.harvard.edu).

Accepted for Publication: May 19, 2004.

Author Contributions:Study concept and design: Katz. Acquisition of data: Katz and Furnish. Analysis and interpretation of data: Katz. Drafting of the manuscript: Katz and Furnish. Critical revision of the manuscript for important intellectual content: Katz. Administrative, technical, and material support: Furnish. Study supervision: Katz.

Financial Disclosure: None.

Funding/Support: This study was supported by a fellowship funded by a Kirschstein National Research Service Award from the National Institutes of Health, Bethesda, Md.