HIV Care Continuum among cisgender and transgender women sex workers in Greater Kuala Lumpur, Malaysia

Abstract

An estimated 37,000 cisgender and transgender women work as sex workers in Malaysia, a population that has been disproportionately affected by the HIV epidemic. Although Malaysia provides no-cost antiretroviral therapy (ART) to people with HIV, little is known about sex workers’ engagement in the HIV care continuum. We analyzed data from 57 HIV-infected cisgender women (n=33) and transgender women (n=24) sex workers from a respondent-driven sampling study on HIV prevalence among sex workers in Kuala Lumpur, Malaysia. We examined the proportion of women who were newly diagnosed with HIV, had a baseline CD-4 count test, were initiated and retained on antiretroviral treatment (ART). Overall, only 26.3% had ever been HIV tested and almost 60% were newly diagnosed. Only a small proportion of cisgender (15.2%) and transgender (12.5%) women were currently taking ART. Interventions to enhance sex workers’ engagement in the HIV care continuum are urgently needed. Deployment of evidence-based strategies to improve linkage and retention in HIV care should be adapted to address the unique needs of this important key population.

Introduction

Globally, people who sell sex face increased vulnerability to HIV (Kerrigan et al., 2012). Sex work, defined as the exchange of sexual services for money or goods, is illegal in the Southeast Asian country of Malaysia (Overs, 2002). Still, an estimated 37,000 women (about 22,000 cisgender women and 15,000 transgender women) are employed as sex workers in the country (Ministry of Health Malaysia, 2018). Social and structural issues related to migration, poverty and sex trafficking result in hundreds of women and girls being steered into sex work each year, increasing their vulnerability to HIV infection (Baral et al., 2012). While the HIV prevalence in the general adult population is 0.4%, and only 0.2% among women (UNAIDS, 2017), sex workers in Malaysia experience an HIV prevalence nearly thirty-fold higher (11.7%) (Wickersham et al., 2017). Knowledge about HIV transmission and condom use during sex are also found to be low (Wickersham et al., 2017). Transmission through sex, attributed to condomless sex is on the rise, posing an imminent threat of disease transmission in this high-risk population and in the general public (Ngadiman, 2016).

In Malaysia, transgender women sex workers (TWSW) face unique challenges and risks because of their gender identity (Teh, 2008). Cisgender women sex workers (CWSW) are women who identify with the same biological sex they are assigned at birth, while TWSW identify themselves as females, despite being assigned “male” sex at birth (Berg-Weger, 2016). Discrimination against TWSW is deep-rooted in the social and legal structures and transgender people are often subjected to brutality and arrests for cross-dressing (Teh, 2008). Structural, cultural, and biological factors contribute to an increased HIV risk among TWSW and as a result, HIV prevalence is higher (12.4%) among this group than CWSW (11.1%) (Wickersham et al., 2017).

Antiretroviral therapy (ART) effectively reduces morbidity and mortality among people with HIV (PWH), and treatment with ART also curbs onward transmission of HIV (Cohen, McCauley, & Gamble, 2012; Eaton et al., 2012). In Malaysia, ART is provided at no-cost to PWH, however, uptake of ART has remained woefully suboptimal, with only 53.8% of all PWH currently receiving ART (Ngadiman, 2016).

As the United Nations vow to end the AIDS epidemic by 2030, HIV programs globally are gearing towards the 90–90-90 treatment target (identifying 90% of all infected with HIV, linking 90% of all PWH to medical care, and achieving viral suppression (CD4 count <350 cells/μL) for 90% of all receiving care) (Nations, 2016). The HIV care continuum as a framework estimates the proportions of people newly diagnosed with HIV, taking ART, and are virally suppressed. This is a useful tool in informing interventions at each stage of the care continuum. In doing so, the care continuum framework provides insights about the effectiveness, or lack thereof, of HIV programs by identifying gaps at different stages of treatment.

Additionally, early diagnosis and treatment with ART or “Treatment as Prevention” (TasP) is a highly effective method of preventing HIV transmission (Grinsztejn et al., 2014). Therefore, this study aims to understand the HIV care continuum among CWSW and TWSW in Malaysia in order to understand the treatment gaps which can inform HIV programs to redirect focus on areas that require urgent intervention. Additionally, we examine the comorbidities, including sexually transmitted infections (STIs) and social risk factors among sex workers that have HIV that may impact their HIV care.

Method

Study Design and Analytic Sample

Data were drawn from a 2014–2015 sample of 492 CWSW and TWSW recruited using respondent-driven sampling in three regions around Greater Kuala Lumpur. All participants underwent rapid HIV testing and a comprehensive structured questionnaire. Eligibility criteria were: (a) identify as a cisgender or transgender woman, (b) engaged in sex work in the last 90 days; and (c) able to speak Bahasa Malaysia, Tamil or English. The full methods have been previously described elsewhere (Wickersham et al., 2017). The analytic sample for the present study was limited to the 57 participants who had a reactive HIV test result (CWSW=33; TWSW=24).

Measures

HIV testing.

All participants received a rapid 4^th generation HIV-1/2 test by whole-blood fingerstick (Alere Determine HIV-1/2 Antigen/Antibody Combo; Alere, Waltham, Massachusetts, USA). Participants with a reactive HIV test underwent a second rapid HIV-1/2 whole-blood fingerstick test (ACON HIV Ultra Rapid Test Device; ACON Laboratories Inc., San Diego, CA) as a confirmatory test procedure, following World Health Organization guidelines.(WHO, 2015b) Participants with a second reactive HIV test were classified as HIV-infected. Standard HIV pre- and post-test counselling was provided to at the time of testing (WHO, 2015a). All participants received a packet of information on HIV risk reduction and information on community resources for HIV screening. Participants with an HIV-positive test result received additional information on HIV care, including a direct referral to HIV care and information on HIV support services in the community.

Survey measures.

Survey measures included demographic information, history of sex work involvement, history of HIV and sexually transmitted infection (STI) testing, diagnosis, and treatment history. HIV care continuum measures included positive HIV rapid test, prior HIV diagnosis (ever and before the study), prior CD4 cell test, self-reported CD4 count, ever being prescribed ART, ever taking ART, and currently taking ART. Risk behavior included condomless anal and vaginal sex, and drug injection behavior across the lifetime and last 30 days. Comorbidities included alcohol use disorders (AUDs) measured using Alcohol Use Disorders Inventory Test (AUDIT) dichotomized with scores ≥7 indicating hazardous drinking for CWSW and ≥ 8 for TWSW (Saunders, Aasland, Babor, de la Fuente, & Grant, 1993), depression was measured by the CES-D dichotomized with scores ≥11 indicating a major depressive disorder (Irwin, Artin, & Oxman, 1999). HIV knowledge was measured using 17 items. Seventeen statements such as, “Coughing and sneezing do not spread HIV”, “A person can get HIV by sharing a glass of water with someone who has HIV”, and “Someone can get HIV by having anal sex” were coded 0 for incorrect and 1 for correct answers with the possible scores of 0–17.

Ethics

All participants provided written informed consent before enrollment. The study was approved by Yale University.

Informed consent was obtained from all individual participants included in the study.

Data Analysis

After conducting descriptive analyses, we used chi-square tests to compare categorical variables and an independent samples t-test to compare continuous variables with statistical significance set at p<0.05. Post-hoc analyses used adjusted standardized residuals (significant at p<0.05 or z-score>1.96) to determine the contribution to the chi-square test by categorical variables. The HIV care continuum was assessed in terms of the number of CWSW and TWSW: 1) with confirmed HIV by laboratory testing during this study; 2) reporting being previously diagnosed of their HIV status; 3) receiving a CD4 cell test; 4) reporting ever taking ART; and 5) currently taking ART. All analyses were performed using IBM SPSS (version 24.0).

Results

Sample characteristics are presented in Table 1. Participants’ mean age was 38.3 years (SD=9.7), with CWSW being slightly older (M=41.1, SD=9.4) than TWSW (M=34.5, SD=8.8; p<0.01). Most participants were ethnic Malay (63.2%), single (73.7%), and had less than primary-level education (87.5%). Participants average total time involved in sex work was 13.7 years (SD=8.8) and the average age at entry into sex work was 24.3 years (SD=8.4), with TWSW having entered sex work at a significantly younger age (M=18.7, SD=3.4) than CWSW (M=28.3, SD=8.7; p<0.001). The average time since the last HIV test was 40.3 months (SD = 9.2) among those unaware of their infection who had tested before. Among those who had been diagnosed with HIV prior to the study, the mean number of years since diagnosis was 4.5 years (SD = 3.9).

Table 1.

Demographic and psychosocial characteristics of female sex workers in Malaysia

		N (%)
		Total (n = 57)	Cis-gender (33)	Transgender (24)	χ 2 or t	P
Mean Age (SD)		38. 3 (9.7)	41.1 (9.4)	34.5 (8.8)	2.6	<0.01
Ethnicity	Malay	36 (63.2)	22 (38.6)	14 (24.6)	3.8	>0.05
	Indian	15 (26.3)	7 (12.3)	8 (14.0)
	Indonesian	3 (5.3)	2 (3.5)	1 (1.8)
	Chinese	2 (3.5)	0 (0.0)	2 (3.5)
	Indonesian Malay	1 (1.8)	0 (0.0)	1 (1.8)
Language	Bahasa Malaysia	39 (68.4)	24 (42.1)	15 (26.3)	3.7	>0.05
	Tamil	13 (22.8)	5 (8.8)	8 (14.0)
	Chinese	2 (3.5)	2 (2.0)	0 (0.5)
	Bahasa Indonesian	3 (5.3)	2 (3.5)	2 (1.8)
Education	Below Form 5	15 (26.3)	6 (10.5)	9 (15.8)	2.6	>0.05
	Form 5 and above	42 (73.7)	27 (47.4)	15 (26.3)
Relationship	No	42 (73.7)	22 (38.6)	27 (35.1)	1.9	>0.05
	Yes	15 (26.3)	11 (19.3)	4 (7.0)
Unstable housing		14 (24.6)	7 (12.3)	7 (12.3)	0.47	>0.05
First sex work at age	Mean age (SD)	24.3 (8.4)	28.3 (8.7)	18.7 (3.4)	5.03	<0.01
Number of years in sex work	Mean years (SD)	13.7 (8.8)	12.7 (1.6)	15.2 (7.8)	−1.1	>0.05
Ever injected drugs in a lifetime		14 (24.5)	13 (39.4)	1 (4.2)	9.3	<.001
Depression		36 (63.2)	22 (66.7)	14 (58.3)	.415	>0.05

Note.

^*= p≤.05. Adjusted standardized residual appear greater than 1.96.

HIV Care Continuum

The HIV care continuum is presented in Figure 1. Overall, among HIV infected sex workers, 59.6% (n=34) were newly diagnosed, with 50% of TWSW (n = 17) and 51% of CWSW (n = 17) not being aware of their infection. A total of 26.3% (15/57) had never been tested for HIV in their lifetime, which did not differ by gender identity (CWSW=27.3%, 9/33; TWSW=25.0%, 6/24; p>0.05, ns). Among those unaware of their HIV status prior to the study, 44.1% (n=15/34) had never been tested for HIV before.

Figure 1.

HIV care continuum proportions for cisgender (n = 33) and transgender women (n = 24) sex workers.

Among those who were previously diagnosed, only 56.5% (n=13/23) were ever prescribed ART (30.3% CWSW, n=10/23 and 12.5% TWSW, n=3/23, p<0.3) by their health care providers, only 39% (n=9/23) (18.2% CWSW, n=6/23; and 12.5% TWSW, n=3/23) reported ever taking ART, and only 34% (n=8/23) (15.5% CWSW, n=5/23; and 12.5% TWSW, n=3/23) were on the medication. No significant differences were observed between CWSW and TWSW on CD4 cell test, being prescribed ART and currently taking ART.

Among those who were diagnosed with HIV prior to the study, the mean time since last HIV test was 35.5 months (SD=39.7) and only 15.8% had been tested in the last 12 months. HIV testing within the last year was equally low for both CWSW (15.2%, n=5/33) and TWSW (16.7%, n=4/24, p=0.436, ns). Of the 23 participants who had been diagnosed with HIV at the time of the study, close to 70% (n=16) reported receiving a CD4 count test. Among those who had received a CD4 count, 81.3% (n=13) were able to recall the value of their most recent CD4 test. The average CD4 count as recalled by the 13 participants was 429.7 cells per mm³ (SD=255.5, Range: 34–857) with 37.5% (n=6) reporting CD4 count ≤ 350 cells/mL. The average time since last CD4 count test was 11.3 months (SD=20.2).

HIV Risk Behavior, HIV Knowledge and Comorbidities

Proportion of condom use during vaginal sex was low with 31.6% (n=18) compared to 7.0% (n=4) TWSW who reported condomless anal sex in the past 30 days. Nearly one-quarter (n=14) reported having ever injected drugs in lifetime. Injection drug use even once in a lifetime was significantly higher among CWSW 39.4% (n=13) than TWSW 4.2% (n=1) (χ²=9.3, p<0.001). Almost 65% of all sex workers had depression (n = 22), with no significant difference between CWSW (66.7%, n=22) and TWSW (58.3%, n = 14).

Access to and usage of healthcare was low among all participants. The average number of years since the last visit with a healthcare provider was 2.1 years (SD = 1.8) with CWSW (M=2.5, SD=2.2) having a longer gap than TWSW (M=1.5, SD=0.6, p <.05). Only one third (28.6%) reported having had a general physical exam in the past year, including 33.3% of CWSW (n=11) and 21.7% TWSW (n=5) with no significant difference between the two groups. HIV knowledge score was generally low (M=6.9, SD=4.9, Range: 0 −14) with higher knowledge among TWSW (M=8.4, SD=4.1) than CWSW (M=5.9, SD=5.1).

Overall, previous STI testing was low, with only 23.2% (n = 13) reporting having ever being tested. Previous lifetime STI testing was low for syphilis (28.1%), C. trachomatis (19.3%), and N. gonorrhoeae (22.8%) and no differences detected between CWSW and TWSW.

Among all participants, 25.9% (n=14/57) tested positive for Syphilis (16.7% CWSW, n=5/33; 37.5%, n=9/24), 10.7% (6/57) positive for Gonorrhea (16.7% CWSW, n=5/33; 4.3%, n=1/24), and 26.8 % (n=15/57) for Chlamydia (33.3% CWSW, n=11/33; 17.4%, n=4/24).

Discussion

HIV care continuum presents a framework for visualizing engagement in HIV care and identifying gaps. To our knowledge, this is the first study that examines the care continuum among HIV positive cisgender and transgender women sex workers in Malaysia. The findings show significant gaps in every step of the continuum. The first step and the most critical step of the continuum is testing and diagnosis (Kilmarx & Mutasa-Apollo, 2013). Early diagnosis and access to treatment is vital for prolonged life and overall health of infected individuals (Wolitski & Fecik, 2017).

This study, however, found that a quarter of the participants with HIV had never been tested for HIV in their lifetimes. Only about 40% of them were aware of their infection. This is a stark disparity compared to the proportion of PWH aware of their HIV status in the general population, which is above 80% (UNAIDS, 2016). The situation among this key affected population in Malaysia seem distant from the joint UNAIDS and WHO 2020 target of 90–90-90, that is identifying 90% of all HIV infected individuals, delivering ART to 90% of all diagnosed with HIV, and reaching a viral suppression for 90% of everyone on ART (UNAIDS, 2014).

WHO recommends provider-initiated testing at health facilities, and testing frequently (three to six months) for high risk population (WHO, 2015a). However, this study shows that sex workers access healthcare infrequently. The average time since seeing a health care provider was about two years and among those who were unaware of their infection, the average time since the last HIV test was about three years.

Additionally, the frequency of CD4 cell test among those previously diagnosed was an average of 11.9 months, despite the evidence that frequent testing for CD4 cells reduce mortality in resource limited settings (Braitstein et al., 2012). Although this study did not perform viral load testing, self-report of CD4 count test results were concerning, with more than a quarter of HIV infected women reporting low levels of CD4 count.

The next highest attrition in the HIV care continuum in this population was linkage to care. Almost half of the participants aware of their HIV status had not been prescribed ART showing suboptimal access to treatment. Fewer reported ever taking ART and almost all who reported ever taking ART were taking the medication during the study. This drop-off at linkage to and retention in care among sex workers appear bleaker than attrition rates in other developing countries (Lancaster et al., 2016).

Failure to test and diagnose in a timely manner pose an immense threat to the overall health, including HIV treatment of the sex workers and the risk of onward transmission to their clients. A qualitative study of PWH in Malaysia showed social stigma, fear of lack of confidentiality, and inadequate support for PWH as major barriers to screening for HIV (Ahmed et al., 2017). An important and often overlooked barrier to testing, treating and retaining sex workers in HIV care is multi-layered stigma and discrimination faced by cisgender and transgender women sex workers. Malaysia, which has one of the highest populations of transgender women, have deep-rooted stigma manifested through systematic discrimination against this section of the population. For example, cross-dressing is considered a criminal offense punishable under the country’s federal law and the ordinance guided by the Sharia (Islamic) law (Vijay et al., 2018). Additionally, HIV adds another layer of discrimination. A recent study showed that physicians in Malaysia are likely to discriminate against transgender because of HIV-related shame and stigma, and negative attitude towards people with HIV (Tee et al., 2018). To exacerbate the situation, sex work adds further discrimination, including blatant human rights violation that prevent access to health care including HIV care (Decker et al., 2015). FSWs in other Muslim countries in the region, such as Indonesia, experience similar discrepancies in care, where 75% of those with HIV enrolled in a prospective study had started ART, only 45% were retained in care, and fewer of them (23%) achieved viral suppression in six months (Januraga et al., 2018). Hence, it is important to institute rights-based, provider- initiated HIV programs for both transgender and cisgender sex workers, as well as programs to address and reduce stigma and discrimination at individual, social and structural levels in Malaysia.

Evidence based strategies that provide confidential, low cost, easily accessible testing facilities such as community based voluntary counselling and testing (VCT) centers, that meet sex workers where they are, removing barriers to physical accessibility, are urgently required to bridge the gap in HIV testing among this highly vulnerable population. Programs in other Low and Middle Income Countries (LMIC) that facilitate home-based and mobile or community testing also report positive impact on early diagnosis and access to treatment (Scanlon & Vreeman, 2013). In order to scale-up HIV testing among sex workers, alternative approaches to screening, including self-testing which have been highly acceptable in other low-income countries, and mobile testing centers that cater and customize to key populations, should be explored.

Additionally, to reduce time to linkage to HIV care, deployment of either point-of-care CD4 testing or immediate initiation of ART should be rapidly implemented in Malaysia. Although MH ART guidelines state ART should be started immediately regardless of CD4, efforts to reduce the time between screening and initiation of first appointment, initiation of ART, and frequent CD4 count testing needs to be scaled up. Programs that provide simple referral forms, transportation stipends and community navigators show promising results in improving access and adherence to treatment (Nsigaye et al., 2009). Other strategies include system of doctor-based to nurse-based care delivery, decentralization of HIV services from higher level/government facilities to community/mobile clinics, and integration of HIV care into other healthcare delivery programs such as Tuberculosis (TB), and primary care services (Scanlon & Vreeman, 2013). Given the prevalence of psychiatric and physical comorbidities in this population, such as depression and STIs, HIV care may be best delivered when holistically addressing the patient’s health.

Conclusion

Malaysia is a country where the HIV/AIDS epidemic is one of the fastest growing in the region. In 2010, more than 40% of all new infections was attributed to heterosexual transmission. Female sex workers with HIV are the most at risk of comorbidities, mortality and transmitting the infection, and therefore, are need of an urgent and immediate intervention for prevention of transmission through treatment. The study shows a grim picture of care at every step of the HIV care continuum. The most crucial step of identifying the infection through testing and diagnosis is disturbingly low among this at-risk population. Low levels of linkage to care and retention are also concerning and should be targeted for intervention, especially given the efficacy of treatment as prevention. Hence, immediate and urgent attention to strategies at structural, community and individual level must be adopted to improve treatment and care, and curb transmission.

Table 2.

Differences in the HIV care continuum between CWSW and TWSW (n=57)

		Total (n=57)	CWSW (n=33)	TWSW (n=24)	χ 2	P
Previously HIV tested	Yes	42 (73.7)	24 (72.7)	18 (75.0)	0.4	0.50
	No	15 (26.3)	9 (27.3)	6 (25.0)
Previously HIV diagnosed (before study)	Yes	23 (40.4)	16 (48.5)	7 (29.2)	2.2	0.14
	No	34 (59.6)	17 (51.5)	17 (50.0)
Had a CD4 count test	Yes	16 (28.1)	10 (30.3)	6 (25.0)	0.19	0.44
	No	41 (71.9)	23 (69.7)	18 (75.0)
Told to begin ART by provider	Yes	13 (22.8)	10 (30.3)	3 (12.5)	2.5	0.12
	No	44 (77.2)	23 (69.7)	21 (87.5)
Ever taken ART (total n=48, cwsw = 27, twsw = 21)	Yes	14 (29.2)	10 (37.0)	4 (19.0)	1.8	0.14
	No	34 (70.8)	17 (63.0)	17 (81.0)
Currently on ART	Yes	8 (14.0)	5 (15.2)	3 (12.5)	0.8	0.54
	No	49 (86.3)	28 (49.1)	21 (36.8)

ART=antiretroviral therapy