Health care issues affecting transgender people living with HIV: an opportunity for improvement

Abstract

The high vulnerability of transgender (TG) persons to HIV infection and the difficulties associated with access to health services can lead to delays in the diagnosis and treatment of HIV infection, thus increasing the risk of transmission of HIV by this population. We performed a retrospective study to analyze the main characteristics of TG living with HIV infection in a hospital in Madrid, Spain and to identify issues related to lack of access to the health care system and combination antiretroviral therapy (cART). We analyzed 28 TG, of whom 22 (78.6%) were TG women. Median age was 28 years (interquartile range [IQR]: 29–45), 24 (85.7%) were Latin American (all of them without health insurance), and 12 (42.8%) were sex workers. Accessibility to the health system was more difficult for 22 (78.6%) of foreign-born TG people living with HIV, with a median delay to initiation of cART of six months (IQR: 2–24). These values were greater than those recorded for the control group comprising other people living with HIV (16.9% and one month, respectively). At the first access to health care in our hospital, CD4+ cell count and HIV viral load (VL) were worse in TG patients, with a median baseline CD4+ cell count below 350 cells/µl and a higher median HIV VL, both in naïve patients (28.6%) and in pre-treated patients whose therapy was interrupted owing to access-related issues (46.4%). These data show high vulnerability to HIV infection among TG and highlight that issues associated with access to health care can cause delays in the diagnosis and treatment of HIV infection. Based on our results, we think that the health care system should adapt to the sociodemographic, clinical, and behavioral characteristics of TG people living with HIV and develop specific, targeted preventive programs to address the vulnerability of this group.

Keywords

Transgender HIV access issues antiretroviral therapy

Introduction

The prevalence of HIV infection among transgender (TG) women is estimated to be 19%, increasing to 22% in black TG women.¹ In the USA, there are approximately one million TG people (0.3% of the population), 25–28% of whom are estimated to be living with HIV.^2,3 In Europe, according to data from a decade ago, TG accounted for 0.1–0.5% of the general population. Between 18.4 and 24.5% of these individuals are living with HIV.^4,5 TG represent 0.7–2.9% of the population in southern Asia, the region with the highest prevalence of HIV infection among TG worldwide (12.5–47.3%).^6,7 Available data suggest that although TG women represent a minority of the total number of people newly diagnosed with HIV, they have a 49-fold higher risk of acquiring HIV than the general population.¹ This high prevalence of HIV in TG is associated with the overlap between social, clinical, and structural factors that define specific populations as marginalized.

For more than two decades, Madrid and Barcelona have been considered the most lesbian, gay, bisexual, and transgender (LGBT)-friendly cities in Spain and have thus become an epicenter for TG who are attempting to regularize their civil and social status. Nevertheless, despite considerable efforts by LGBT groups or associations to regularize TG life, and the passing of laws in favor of civil rights for this population, many TG continue to experience stigma, discrimination, social exclusion, and lack of employment opportunities. Consequently, they are economically vulnerable.⁸ In many cases, TG persons are forced to turn to sex work as their only source of income. According to the EPI-HIV study for 2000 and 2009, the prevalence of HIV among TG in Spain was higher (24.5%) than that found previously in other studies and even higher than in countries such as the USA (21.7%) or similar to that recorded in other European countries such as Italy (24.5%). Men who have sex with men (MSM) and TG sex workers give particular cause for concern, since they are at a greater risk for HIV infection (3.0/100 person-years) than female sex workers (0.1/100 person-years).⁹

Moreover, there are some clinical factors including poor adherence to combination antiretroviral therapy (cART) and potential drug-drug interactions, mainly with unmonitored hormonal therapy, which can lead to failure of cART, and therefore, increase the risk of HIV transmission.¹⁰ Finally, TG continue to be stigmatized in terms of the structural and administrative factors arising from social and institutional discrimination. The absence of educational and economic opportunities creates barriers that hamper access by this population to the health care system, especially to cART.^11,12

Updated information on TG people living with HIV (PLHIV) in Europe is very limited.^8,9 Most studies are from South America, Asia,¹³ and the United States,² where low-income people have more difficulties accessing both public and private health care.^11,14

The aim of this study was to analyze the main characteristics of TG PLHIV in a hospital in Madrid, Spain, by addressing issues associated with accessibility to the health care system and cART. We also investigated differences between TG and other PLHIV.

Material and methods

We performed a retrospective study based on data from the medical records of TG PLHIV at a hospital in Madrid, Spain. TG PLHIV were compared with a control group (non-TG PLHIV) also seen for the first time at our hospital.

Selection criteria and variables analyzed

We retrospectively recorded data on all TG and non-TG PLHIV registered in the medical records who were attended for the first time in our clinic between January 2017 and September 2018. We considered TG to be people who have a gender identity that differs from the sex assigned at their birth.

The study variables were classified into three groups: sociodemographic situation (TG gender, age, region of birth, and socioeconomic background including self-reported social class, educational level, and working status), level of accessibility to the health system (health care access paths, legal status), and HIV status (risk factors, viral load [VL], CD4+ lymphocyte count, delayed time to cART, and other sexually transmitted infections [STIs]). Syphilis was diagnosed with serologic tests (treponemal and non-treponemal antibodies), and chlamydia and gonorrhea with pharyngeal, urethral, or rectal culture or polymerase chain reaction (PCR)-based assays.

Primary and secondary outcome measures

We analyzed the main characteristics of TG PLHIV, including the level of accessibility to the health system and cART. In both TG and controls, we analyzed HIV status and the incidence of other STIs as indirect markers of transmission of HIV.

Data collection

Data were obtained from electronic clinical records in December 2018. Participants’ data were stored anonymously in accordance with ethical guidelines. Owing to the retrospective nature of the study, informed consent was not sought. Study data were collected retrospectively from patients’ electronic health records and entered into an anonymous electronic database (REDCap, Research Electronic Data Capture, Vanderbilt University, Nashville, Tennessee, USA).

Statistical analysis

Variables that did not follow a normal distribution were expressed using the median and interquartile range (IQR). Nominal variables were expressed as numbers and percentages. Groups were compared using the Chi square test and binary logistic regression. All analyses were carried out using IBM SPSS Statistics 23.0 (IBM Corp., Armonk, New York, USA).

The study protocol was approved by the Ethics Committee of Hospital Universitario Gregorio Marañón, Madrid, Spain (code MINHUIL-02).

Results

The cohort comprised 93 PLHIV, 28 of whom were TG. Their sociodemographic profile is shown in Table 1. TG women, gender identity as women, accounted for 78.6% of the population, and the median age was 28 years (IQR: 29–45). Latin Americans accounted for 85.7% of patients, and most were from Peru (7; 25%) and Argentina (6; 21.4%). The PLHIV control group mainly included MSM (87.7%), with a median age of 34 years (IQR: 29–49). Only 50% were Latin Americans (p = 0.03).

Table 1.

Baseline sociodemographic profile.

Parameter	TG PLHIVn = 28	Non-TG PLHIVn = 65	p
Demographic data
Age (years); median (IQR)	28 (29–45)	34 (29–39)	p = 0.15
Transgender identity n (%)
Women	22 (78.6)	8 (12.3)
Men	6 (21.4)	57 (87.7)
Region of birth; n (%)			p = 0.03
Latin America	24 (85.7)	33 (50.8)
Peru	7 (25.0)	3 (4.6)
Argentina	6 (21.4)	1 (1.5)
Colombia	3 (10.7)	11 (16.9)
Ecuador	3 (10.7)	2 (3.1)
Venezuela	3 (10.7)	5 (7.7)
Brazil	1 (3.6)	3 (4.6)
El Salvador	1 (3.6)	1 (1.5)
Europe	4 (14.3)	29 (44.6)
Spain	4 (14.3)	25 (38.5)
Socioeconomic background; n (%)
Self-reported social class			p = 0.55
Low	1 (3.6)	19 (29.2)
Medium	4 (14.3)	25 (38.5)
High	1 (3.6)	13 (20.0)
NA	22 (78.6)	8 (12.3)
Educational level			p = 0.001
Primary	7 (25.0)	2 (3.0)
Secondary	3 (10.7)	18 (27.7)
University	1 (3.6)	23 (35.4)
NA	17 (60.7)	22 (33.8)
Working status
Active	18 (64.3)	29 (44.6)	p = 0.085
Sex worker	12 (42.8)	2 (3.0)	p = 0.001
Stylist	4 (14.2)
Night show performer	2 (7.1)
NA	10 (35.7)
Health care access status; n (%)
No health insurance coverage	24 (85.7)	34 (52.3)	p = 0.004
Health care access mode			p = 0.005
NGO	14 (50.0)	9 (13.8)	p = 0.001
STI clinics	6 (21.4)	24 (36.9)
Primary care	3 (10.7)	30 (46.2)
Other patients	4 (14.3)	0 (0.0)
Other	1 (3.6)	2 (3.0)

NA: not available; NGO: non-governmental organization; PLHIV: people living with HIV; STI: sexually transmitted infection; TG: transgender.

In the TG group, 15 patients (53.6%) had undergone surgical treatment to feminize their body and 22 patients (78.6%) had undergone plastic surgery. Thirteen patients (46.4%) received hormone therapy based on antiandrogens or estrogens at some point during their transition process; this treatment was not medically supervised in most cases (84.6%). Only four patients reported currently receiving hormone therapy.

Most patients had no health insurance coverage (85.7% of TG PLHIV versus 52.3% of controls [OR, 5.5; 95% CI, 1.7–17.5; p = 0.004]). TG PLHIV experienced barriers to health care access in 67.6% of cases versus 16.9% in our control group, p = 0.001. Referral to our hospital in the TG group was mainly by non-governmental organizations (NGOs) (14 patients [50%]) and from STI clinics (6 patients [21.4%]), compared with the control group, who were referred in 83.1% of cases from other health care centers (46.2% primary care centers and 36.9% STI clinics [OR, 1.8; 95% CI, 1.2–2.6; p = 0.005]).

This analysis revealed no self-reported differences in social class between the groups (p = 0.55). Only 18 TG patients (64.3%) reported having a financial income and 12 (42.8%) were sex workers.

The main characteristics of PLHIV are summarized in Table 2. Upon arrival at our HIV department, TG cART status was not significantly different from that of the control group (p = 0.2); eight TG PLHIV were treatment-naïve (28.6%) and 20 (71.4%) were treatment-experienced. However, only 13 treatment-experienced patients had an undetectable VL in the TG group; in the remaining seven cases, the detectable VL was due to poor adherence to cART associated with problems of access to health care. There were no significant differences in cART regimens between the groups (non-nucleoside reverse transcriptase inhibitors, p = 0.2; protease inhibitors, p = 0.2; and integrase inhibitors, p = 0.3).

Table 2.

Characteristics of HIV infection and other STIs.

Parameter	TG PLHIV	n = 28	Non-TG PLHIV	n = 65	p
HIV infection
Risk factors; n (%)
Sexual relations		28 (100)		62 (95.4)	p = 0.88
Protected sex with condom; n (%)		2 (7.1)		9 (13.8)	p = 0.84
Months to cART from HIV diagnosis; median (IQR)		6 (2–24)		1 (1–12)	p = 0.04
CD4 and HIV viral load
CD4 at arrival; median (IQR)
CD4 cell count (cells/µl)		342 (237–433)		489 (296–650)	p = 0.01
CD4%		19 (13–22)		24.5 (17–32)	p = 0.3
Nadir CD4; median (IQR)
CD4 cell count (cells/µl)		327 (191–470)		410 (252–567)	p = 0.67
Median HIV viral load; n (%)					p = 0.02
VL <1.6 log₁₀ copies/ml		13 (46.4)		24 (36.9)	p = 0.7
VL >5 log₁₀ copies/ml		6 (21.4)		11 (16.9)	p = 0.6
VL > 5.7 log₁₀ copies/ml		3 (10.7)		1 (1.5)	p = 0.45
cART status n (%)					p = 0.2
Treatment-naïve		8 (28.6)		36 (65.4)	p = 0.001
Treatment-experienced		20 (71.4)		27 (41.5)	p = 0.08
Involuntary cessation of cART		7 (25)		8 (12.3)	p = 0.1
Previous cART; n (%)
Non-nucleoside reverse transcriptase inhibitor		14 (70)		16 (59.2)	p = 0.2
EFV	11 (55)		12 (44.4)
NVP	2 (10)		1 (3.7)
RPV	1 (5)		3 (11.1)
Protease inhibitor		5 (25)		6 (22.2)	p = 0.2
LPV/r	1 (5)		2 (7.4)
FPV/r	2 (10)
DRV/r	2 (10)
ATZ/r			4 (14.8)
Integrase inhibitor		1 (5)		6 (22.2)	P = 0.3
RAL	1 (5)		1 (3.7)
EVG			4 (14.8)
DTG			1 (3.7)
STI and viral hepatitis coinfections; n (%)
STI before HIV diagnosis		7 (25)		22 (33.8)	p = 0.4
Syphilis	6 (21.4)		19 (29.2)
Other	1 (3.6)		8 (12.3)
STI after HIV diagnosis		12 (48.8)		27 (41.5)	p = 0.9
Syphilis	12 (48.8)		23 (35.4)
Chlamydia	1 (3.6)		4 (6.1)
Gonorrhea	1 (3.6)		5 (7.7)
Hepatitis coinfections; n (%)
HBV
HBsAg +		–		5 (77)
HCV
ELISA +		1 (3.6)		2 (3.1)

ATZ: atazanavir/ritonavir; cART: combined antiretroviral therapy; DRV/r: darunavir/ritonavir; DTG: dolutegravir; EFV: efavirenz; ELISA: enzyme-linked immunosorbent assay; EVG: elvitegravir; FPV/r: fosamprenavir/ritonavir; HBsAg: hepatitis B surface antigen; HBV: hepatitis B virus; HCV: hepatitis C virus; LPV/r: lopinavir/ritonavir; NVP: nevirapine; PLHIV: people living with HIV; RAL: raltegravir; RPV: rilpivirine; STI: sexually transmitted infection; TG: transgender; VL: viral load.

The median CD4+ cell count among TG was 342 cells/µl (IQR: 237–433) compared with the control group, who had a higher CD4+ cell count (489 cells/µl [IQR: 296–650 cells/µl], p = 0.01). The median VL was 4.7 log₁₀ copies/ml (IQR: 4.7–5.59 log₁₀ copies/ml) in treatment-naïve TG PLHIV and 5 log₁₀ copies/ml (IQR: 4.1–13.1 log₁₀ copies/ml) in treatment-experienced TG PLHIV who had stopped therapy. In the control group, median VL was lower in treatment-naïve PLHIV (65.4%) (4.5 log₁₀ copies/ml [IQR: 4–5.2 log₁₀ copies/ml]; p = 0.002).

Unprotected sex was reported by over 95% of PLHIV in both groups (p = 0.84). STIs were common among TG before and after diagnosis of HIV infection (7 [25%] and 12 [42.8%], respectively). Primary or secondary syphilis was the most frequent concomitant STI (85.7 and 100% of patients, respectively). In the control group, 33.8% of patients had an STI before being diagnosed with HIV infection, and 41.5% had an STI, mainly syphilis, after the diagnosis.

Discussion

The lack of recent data on TG PLHIV in the two largest cities in Spain, Madrid and Barcelona, and the poor accessibility of TG to the health system and cART, make it necessary to clearly define the current situation of this at-risk population.

In our study, TG PLHIV frequently experienced accessing problems to health care (67.6%) that differed significantly from those of other PLHIV. TG are often subject to social stigma, difficulties arising from public health policies, and considerable administrative barriers.^11,14 In our study, 85.7% of TG PLHIV were affected by these barriers, which hamper access to health care. NGOs played an important role in ensuring access in around 50% of cases, whereas in our control group, regardless of their legal status, access was arranged from health centers in over 80% of cases.

These same barriers were reviewed in a large population-based study of behavioral risk factors,¹⁵ which showed that treatment was more frequently delayed in TG PLHIV than in other non-TG PLHIV and that this delay was sometimes more than five years. In our study, the delay (including foreign-born patients) was six months versus one month, respectively, with delays of more than two years among TG PLHIV. The findings for the TG population differ significantly from those of the control group, for whom access to health care services was earlier and easier.

Delay in treatment has been associated with health-related consequences not only for patients, but also for the community, because HIV infection continues to be transmitted until effective treatment can be developed.¹⁶ Delays in diagnosis and treatment result in a decline in CD4+ T cells and an impaired immune system. The lowest CD4+ T-cell count (<350 cells/ml) was recorded within the TG group with longer delays, thus highlighting the potential risk of developing AIDS and non-AIDS events. These results are consistent with a study based on a cohort of TG PLHIV receiving medical care in the USA.¹⁷ Furthermore, higher HIV VL, combined with the fact that more than 90% of patients engage in unprotected sex (e.g. sex workers), and the presence of STIs, as an indirect marker of transmission, indicate that these PLHIV are at major risk of transmitting HIV infection.⁹

Some of the data collection measures used, such as administrative barriers, referral paths, and delay time, could be considered excessively simple or limited, although we think they are sufficiently objective for assessment of access to health care and can explain the issues we encountered with respect to access. In this sense, although our study was limited by its retrospective design, the small sample size, and the lack of data, we highlight important questions affecting the health of TG and underline the high vulnerability of this group to HIV infection and, thus, their high risk of transmitting HIV.

Control of systemic viral replication through cART is clearly one of the most effective ways to prevent transmission of HIV infection. Therefore, the ‘test and treat’¹⁸ and ‘same-day treatment’ strategies are especially important among TG, not only from a clinical perspective, but also from an epidemiological one. Such approaches would enable better control of HIV infection and should be implemented at the individual, community, and population levels. If these approaches are not undertaken, it will be very difficult to achieve the 2020 WHO population targets for transmission of HIV in all population groups.

In human terms, it is necessary to change health care policies that deny medical coverage in order to improve access to standardized health care for TG. This should include other needs, such as hormone therapy and access to gender reassignment surgery. Not only it is important to ensure that TG have access to health care, but we must also make every attempt to ensure that they continue to receive care. Therefore, we must improve management of this public health issue by eliminating administrative and social barriers and the stigma associated with health care in this population. In our study, we observed that NGOs will continue to play a major role both in the diagnosis of new cases of HIV infection and in facilitating referral to health centers¹⁹ and providing appropriate access to care for all patients. Structured collaboration between administrative institutions, health care centers, and NGOs is mandatory.

Conclusion

Our data show the marked vulnerability of TG to HIV infection and highlight difficulties associated with access to health services, which can lead to delays in the diagnosis and treatment of HIV infection. Therefore, we must find a way to adapt the health care system to the sociodemographic, clinical, and behavioral profile of TG people and develop specific programs to address their vulnerability.

Footnotes

Authors’ contribution

JT: conception and design, interpretation of study data, drafting the manuscript, manuscript review, final approval of the manuscript

JR: drafting the manuscript, manuscript review

PR: manuscript review

GC: manuscript review

MM: manuscript review

BD: data acquisition

VP: manuscript review

JT: manuscript review

MV: drafting the manuscript, manuscript review

Declaration of conflicting interests

The authors declared no potential conflicts of interest with respect to the research, authorship, and/or publication of this article.

Funding

The authors received no financial support for the research, authorship, and/or publication of this article.

ORCID iD

Jesús Troya

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