International Journal of Infectious Diseases 22 (2014) 11–15
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International Journal of Infectious Diseases journal homepage: www.elsevier.com/locate/ijid
HIV-related sexual risk behaviors among male-to-female transgender people in Nepal Dharma Nand Bhatta Department of Public Health, Pokhara University, Nobel College, Sinamangal, Kathmandu, Nepal
A R T I C L E I N F O
Article history: Received 7 October 2013 Received in revised form 30 December 2013 Accepted 3 January 2014 Corresponding Editor: Eskild Petersen, Aarhus, Denmark Keywords: HIV risk behavior Male to female Transgender Unprotected sex MtF Nepal
S U M M A R Y
Background: Transgender women are a vulnerable and key risk group for HIV, and most research has shown an increased frequency of HIV infection among this minority population. This study examined the prevalence of HIV-related sexual risk behaviors and the socio-demographic correlates with HIV-related sexual risk behaviors among male-to-female (MtF) transgender persons. Methods: Data were collected from a sample of 232 individuals through venue-based and snowball sampling and face-to-face interviews. Results: The HIV-related sexual risk behaviors among the MtF transgender persons were: sex without using a condom (48.3%; 95% confidence interval (CI) 41.8–54.8), unprotected anal sex (68.1%; 95% CI 62.0–74.2), and unprotected sex with multiple partners (88.4%; 95% CI 84.3–92.5). Statistically significant differences were found for age, income, education, alcohol habit, and sex with more than two partners per day for these three different HIV-related sexual risk behaviors. MtF transgender persons with a secondary or higher level of education were three times (OR 2.93) more likely to have unprotected sex with multiple partners compared to those with a primary level or no education. Conclusions: Age, education, income, frequency of daily sexual contact, and an alcohol habit remain significant with regard to HIV-related sexual risk behavior. There is an urgent need for programs and interventions to reduce risky sexual behaviors in this minority population. ß 2014 The Author. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/bync-nd/3.0/).
1. Introduction Researchers, practitioners, and public health agencies continue to be challenged to identify appropriate methodological and theoretical approaches for the assessment of epidemiological trends and the development of effective interventions, particularly for sexual minorities.1,2 National-level surveillance data are sparse with regard to the incidence and prevalence of HIV among transgender populations in Nepal. Most studies have integrated this population into the ‘men who have sex with men’ (MSM) category in Nepal and in other places.3 Transgender women are at greater risk of HIV infection than other populations. Unprotected sex, drug use, and being an ethnic minority have been found to be associated with HIV status in transgender women.3–5 The previous literature shows that an increased proportion of transgender women are occupied in sex work.3,6 In various countries of Sub-Saharan Africa, transgender persons have a higher HIV prevalence than men.7 A previous systematic
E-mail address: [email protected].
review from Asia found that transgender people are 18 times more likely to be infected with HIV than those in the general population.8 Similarly, a study from North America and Europe showed that transgender women have an elevated rate of HIV infection.9 Due to a lack of nationally representative studies, it is difficult to categorize the burden of HIV infection within this population. A study from India revealed that transgender persons had an increased HIV prevalence compared to the remaining population.10 Nepal has similarities with India regarding its geography and culture. As a result, Nepal may also have this problem. A study from Nepal found an HIV prevalence of 3.8% among urban MSM.11 This result is higher than the overall HIV prevalence in Nepal of 0.3%, and transgender people are categorized as a high-risk group.12,13 Male-to-female (MtF) transgender persons are known locally as ‘Meti’ and ‘chhakka’; these are Nepali words that appear to be used as a way of stigmatizing a man who has female gender characteristics.11,13 In this study, the term ‘MtF transgender’ was used for a person who is biologically a man but self-identifies as a woman; these persons may be either a man or a woman in appearance. A study to investigate the exact HIV-related risk behaviors of transgender persons in Nepal is urgently required.13,14
http://dx.doi.org/10.1016/j.ijid.2014.01.002 1201-9712/ß 2014 The Author. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).
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D.N. Bhatta / International Journal of Infectious Diseases 22 (2014) 11–15
The importance of risk behaviors should be emphasized, particularly as HIV is influencing racial and sexual marginal groups more than ever.15 Most transgender persons engage in risky sexual behaviors that might help to reinforce their female identity and attractiveness.16,17 Previous studies revealed that condom use with regular partners was 14.4% and with irregular partners was 24.1% among transgender persons.18,19 Similarly, in a study from Indonesia on MtF transgender persons, an average condom use of 1.2 was found for the last five sexual acts.18,20 Another study showed that 12–41% of MtF transgender persons used a condom during sex.21 A study from India revealed a low level of condom use among the MtF transgender population.22 Further, a study from Cambodia found that 13% of MtF transgender people engaged in risky sexual behavior.18,23 A study from Thailand found that a myth among transgender people was that the low level of condom use was not the source of the HIV infection.24 Other MtF people from Indonesia believe that they are not at risk of HIV even if they have multiple sex partners without condom use.18,25 A systematic review and meta-analysis based on 39 studies from 15 countries showed the prevalence of HIV to be 19.1% among transgender women, with a prevalence of 17.7% in low and middle income countries and 21.6% in higher income countries.26 Moreover, unprotected sexual intercourse frequently takes place under the influence of substance use.3 Low condom use, casual sex, multiple partners, low socioeconomic status, addiction to drugs and alcohol, and street sex were found to be associated with HIV risk among sex workers.3,27,28 Previous studies have found that the heavy use of alcohol and drugs are related to unprotected sexual intercourse.3,29 2. Methods A cross-sectional survey was conducted between October 2011 and March 2012 among 232 MtF transgender persons. No document was available showing the exact geographical and population distribution of MtF transgender persons in Nepal. The information was obtained from the national-level non-governmental organization Blue Diamond Society; this organization works for sexual health, human rights, and the well-being of sexual and gender minorities, especially LGBTI (lesbian, gay, bisexual, transgender and inter-sex persons). Twenty-six districts were listed from the working districts of this organization. Finally, 15 districts were selected from that list (Kanchanpur, Kailali, Bardiya, Banke, Surkhet, Dang, Rupandehi, Chitwan, Kaski, Parsa, Rautahat, Saptari, Kathmandu, Bhaktapur, Lalitpur). These districts represent different geographical areas of Nepal and thus provided a diverse sample of transgender persons and the possibility of comparing different epidemiological trends. An interviewer administered a questionnaire to collect information on demographic characteristics, risk behaviors, and substance use. Recruitment took place at the local non-governmental organization and at other community contact points where transgender people are found. The institutional ethics review board approved the study and all respondents completed an informed consent procedure. Eligibility was screened and determined by trained research staff with verbal information. The following criteria were necessary for eligibility: (1) biologically male at birth; (2) selfidentified as a woman; (3) aged 16 years or older. A total 245 people were screened for recruitment into this study; eight did not agree to participate and five did not meet the eligibility criteria. The study used a snowball/chain referral and venue-based sampling method to recruit participants. Research staff were posted at different non-governmental organization (Blue Diamond Society) venues to recruit respondents, and at the same time
snowball/chain referral sampling was used, in which recruited respondents referred an eligible peer.30 2.1. Data collection and measures The interview instrument was developed in both English and Nepali, and face-to-face interviews were conducted using structured questionnaires; a pilot was tested among the target population. Researchers were trained with regards to ethical and sensitive issues. Participants involved in the study were fully informed about the nature of the study, its objectives, and confidentiality of the data. Each participant’s written consent was obtained after assuring confidentiality. The interview was carried out in a secret place without the presence of a third person. The researcher did not provide any financial recompense to respondents. Confidentiality of information was assured by removing individual identifiers from the completed questionnaires. Data collection took around 60 min. Socio-demographic measures recorded included age, education, income, and employment status. HIV-related sexual risk behavior among MtF was used as the dependent variable in this study. In this study, all the sexual partners were male and it could be either a committed relationship or not. Respondents reported sexual behavior with three variables, as follows: (1) Have you practiced unprotected anal sex with all types of partners (both committed and not committed sexual relationship) during the past 6 months? (2) Have you engaged in unprotected sex with multiple sex partners (having more than one sex partner considered as multiple partners) during the past 6 months? (3) Have you had sex with any partner not using a condom during the past 6 months? All the variables were dichotomized and coded as ‘no’ = 0 and ‘yes’ = 1. Those MtF persons who had practiced at least one of the three acts were considered to have an HIV-related sexual risk behavior. With regard to substance use, this measure was focused only on whether they had had sex under the influence of alcohol in the past 6 months. The variable was dichotomized and coded as ‘no sex under the influence of alcohol’ = 0 and ‘sex under the influence of alcohol’ = 1. Similarly, the variable of a smoking habit in the past 6 months after involvement in sex work was dichotomized and coded as ‘no’ = 0 and ‘yes’ = 1. 2.2. Data analysis The data were cleaned and cross-checked daily before and after data entry for completeness and accuracy. To estimate the prevalence of the study variables of interest (e.g., condom use, alcohol use), SPSS version 16 software was used (SPSS Inc., Chicago, IL, USA). Both descriptive and inferential statistics were applied. The Chi-square test was used to determine significant differences between demographic variables and HIV-related sexual risk behaviors. The variables were examined in the multivariate analysis (binary logistic regression) in order to identify the factors associated with the likelihood of having an HIV-related sexual risk behavior. When sampling is associated with potential independent variables in a multivariable model, those variables should be incorporated, but it is not essential to load observations.1 Thus, the multivariate results shown here were derived from unweighted estimations, with each variable known to be associated with participation in the sample included in the model. 3. Results The demographic characteristics of the study population are shown in Table 1. The median age of the participants was 25 years. Most of the respondents (56.5%) were aged 25 years and above.
D.N. Bhatta / International Journal of Infectious Diseases 22 (2014) 11–15 Table 1 Demographic characteristics of the transgender persons (n = 232) Result
Characteristics Age Median years Minimum–maximum years 25 years, n (%) 24 years, n (%) Education, n (%) Secondary or higher level Primary level or no education Employment, n (%) Formal employment Informal or no employment Income per month Median NPR 5001 NPR, n (%) 5000 NPR, n (%) Interested in giving birth to a child, n (%) Interested in marriage, n (%) Daily sexual contact per person, n (%) 1 person 2–3 persons 4 persons
25 16–55 131 (56.5) 101 (43.5) 133 (57.3) 99 (42.7)
13
Table 2 Prevalence estimates for reported sexual risk behavior among transgender persons (n = 232) Characteristics
Prevalence % (95% CI)
Alcohol in last 6 months Smoking in last 6 months Sex without using a condom in last 6 months Unprotected sex with multiple partners in last 6 months Unprotected anal sex in last 6 months Unprotected oral sex in last 6 months Other sex in last 6 months
68.5 58.2 48.3 88.4
(62.6–74.4) (51.9–64.5) (41.8–54.8) (84.3–92.5)
68.1 (62.0–74.2) 51.5 (45.0–58.0) 6.1 (3.0–9.2)
124 (53.4) 108 (46.6) 10 000 172 (74.1) 60 (25.9) 113 (48.7) 152 (65.5) 156 (67.2) 56 (24.1) 20 (8.6)
More than half (57.3%) of the total sample had a secondary or higher level of education. The percentage of unemployed participants was also high (46.6%), and income levels were fairly low, with 25.9% of the respondents earning 5000 NPR per month (1 USD = 87 NPR). Nearly half (48.7%) of the MtF transgender persons were interested in giving birth to a child. Two-thirds (65.5%) of the respondents were interested in marriage. Nearly a third of the respondents had sexual contact with more than one person per day. All of the respondents in this study were unmarried. Table 2 shows the prevalence of HIV-related sexual risk behaviors and substance use. Heavy alcohol use was highly prevalent in the transgender population (68.5%; 95% confidence interval (CI) 62.6–74.4%) as was a smoking habit (58.2%; 95% CI 51.9–64.5%), although this was relatively lower than alcohol. A pattern of sexual risk behavior emerged in this sample, showing
that approximately half of respondents (48.3%; 95% CI 41.8–54.8%) engaged in sex without using condom. The prevalence of multiple sex partners was found to be extremely high (88.4%; 95% CI 84.3– 92.5%) among the MtF transgender persons. The prevalence of unprotected anal sexual intercourse was higher than oral sexual intercourse (anal sex: 68.1%; 95% CI 62.0–74.2%; oral sex: 51.5%; 95% CI 45.0–58.0%). The prevalences of HIV risk behaviors with regard to selected demographic characteristics are shown in Table 3. The prevalence of HIV risk behavior varied significantly by age group; it was relatively higher among the participants aged 25 years and above. Sex without using a condom and unprotected anal sex were found to differ significantly by age. When compared among educational groups, the highest prevalence was found among participants who had a secondary or higher level of education. Unprotected sex with multiple partners differed significantly by education level. The prevalence of HIV risk behavior varied dramatically by income group, with the lowest income group having the lowest prevalence. Unprotected sex with multiple partners was found to differ significantly by income. Sex without using a condom was found to differ significantly by employment status. Finally, HIV-related sexual risk behavior was higher among those MtF transgender persons who had an alcohol habit. Unprotected sex with multiple partners was significantly associated with an alcohol habit. Interestingly, a similar result was found for smoking habit. Similarly, sex without using a condom,
Table 3 Estimated HIV-related sexual risk behavior prevalence among male-to-female transgender persons by socio-demographic variables and substance use (n = 232) Characteristics
Age 25 years 24 years Education Secondary or higher level Primary level or no education Income per month 5001 NPR 5000 NPR Employment Formal employment Informal or no employment Alcohol habit Yes No Smoking habit Yes No Daily sexual contact per person 1 person 2–3 persons 4 persons
Sex without condom use (n = 232)
Unprotected anal sex (n = 232)
Unprotected sex with multiple partners (n = 232)
Yes, %
Yes, %
Yes, %
p-Value (Chi-square) 0.029
49.1 50.9
0.029 58.3 41.7
0.203 61.6 38.4
0.597
0.038
0.063
0.526
0.143 51.7 48.3
0.530 69.9 30.1
0.121 63.4 36.6
0.019 76.6 23.4
57.7 42.3
70.5 29.5
0.022 54.6 45.4
73.1 26.9
46.4 53.6
0.180
0.411
0.374
0.000 74.1 25.9
0.728 59.0 41.0
0.022
0.005 61.5 38.5
0.008 70.5 18.6 10.9
p-Value (Chi-square)
58.0 42.0
57.7 42.3
76.8 23.2
60.7 32.1 7.1
p-Value (Chi-square)
0.011 63.9 26.3 9.8
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D.N. Bhatta / International Journal of Infectious Diseases 22 (2014) 11–15
Table 4 Logistic regression for HIV-related sexual risk behavior among male-to-female transgender persons (n = 232) Characteristics
Age 25 years 24 years, Ref. Education Secondary or higher level Primary level or no education, Ref. Income per month 5001 NPR 5000 NPR, Ref. Employment Formal employment Informal or no employment, Ref. Alcohol habit Yes No, Ref. Smoking habit Yes No, Ref. Daily sexual contact per persons 1 person, Ref. 2–3 persons 4 persons
Unprotected anal sex (n = 232)
Sex without condom use (n = 232) OR
SE
1.65
(0.30)
0.66
B
OR
SE
0.50
0.99
(0.31)
(0.29)
0.42
0.96
0.94
(0.34)
0.06
1.59
(0.29)
1.34
Unprotected sex with multiple partners (n = 232) B
OR
SE
B
0.01
0.82
(0.47)
0.19
(0.31)
0.04
2.93a
(0.53)
1.08
1.15
(0.36)
0.14
0.67
(0.48)
0.40
0.47
0.59
(0.31)
0.53
1.35
(0.49)
0.30
(0.39)
0.30
0.66
(0.41)
0.41
0.13a
(0.65)
2.03
0.51
(0.36)
0.68
1.04
(0.38)
0.04
1.65
(0.64)
0.50
1.30 2.68
(0.52) (0.56)
0.26 0.99
0.39 0.18a
(0.68) (0.69)
0.95 1.72
0.00 0.00
(3.93) (3.93)
18.64 17.47
OR, odds ratio; Ref., reference; SE, standard error. a p < 0.05.
unprotected anal sex, and unprotected sex with multiple partners were found to differ significantly by per-person daily sexual contact (Table 3). The results of the logistic regression for HIV-related sexual risk behavior in this transgender population are shown in Table 4. The coefficients describe changes in the estimated odds of engaging in unprotected sexual intercourse associated with changes in the variable in question. MtF transgender persons with a secondary or higher level of education were three times more likely to have unprotected sex with multiple partners than those with a primary level or no education. Most of the variables had higher odds with different sexual risk behaviors, but these were not statistically significant. 4. Discussion This study characterized the HIV-related sexual risk behavior among MtF transgender persons coming from 15 different districts across the country of Nepal. An appropriate methodology was applied to improve the reliability and validity of the study findings. Based on the lack of knowledge in the literature, this study scrutinized the sexual health needs and sexual behavior among MtF transgender persons in Nepal, as well as discussing the risk and influencing factors that are linked with HIV-related sexual risk behaviors among MtF transgender persons. The sampling and recruitment method worked effectively. Exact populations of transgender people in Nepal are unknown. However, the sample represented different geographical areas. No major problems were encountered during the recruitment process. The researcher also found no evidence of coercive peer recruitment. Unemployment and poverty were common among the transgender persons, as in other populations in Nepal. Nearly half of the respondents had no formal employment and a fourth of the participants indicated that they had a low income status, which is less than two dollars per day. The study also found that nearly a third of participants had sexual intercourse with more than one sex partner per day, which indicates a great risk for HIV and
sexually transmitted diseases. A previous study has highlighted that the MtF population engages with a higher number of sexual associates.13 The findings regarding substance use suggest that alcohol consumption is widespread in the transgender population. This may be considered a serious public health problem, given that more than two-thirds of the participants had an alcohol drinking habit. Similarly, nearly three-fifths of the participants had a smoking habit. Unprotected sex with multiple partners was found to differ significantly by alcohol and smoking habits. Previous studies have found alcohol to be associated with HIV risk among sex workers and those having unprotected sexual intercourse.3,27–29 However, there is no previous evidence for the association between HIVrelated sexual risk behavior and smoking. Nearly half of the participants engaged in unsafe sex and did not use a condom with their sex partners. Previous studies have revealed irregular and lowlevel condom use among MtF populations.13,18–21 However, the great majority of the participants had multiple sex partners. Anal sex appears to be the most common sexual behavior among the MtF transgender persons. The results showed no distinctive variations in HIV risk behavior among the age groups. Sex without using a condom and unprotected anal sex were found to differ significantly by age group. However, HIV risk behavior was found to be more common among the more educated participants. Educated respondents were three times more likely to have unprotected sex with multiple partners than the less educated and this was statistically significant. Previous studies have found the level of education to be positively correlated with unprotected sex.1 Having very limited comparable data, the researcher proposes an explanation. Transgender persons with a higher education level may find it easier to build a network with varied sexual associates than less educated persons and may thus be further expected to engage in more unprotected sexual acts. They might be unaware that they are themselves at risk either because of the self-confidence that education may bring or because they are unaware or do not care to see their sexual partners as being at risk of HIV. Unprotected sex with multiple partners was found to be significantly associated
D.N. Bhatta / International Journal of Infectious Diseases 22 (2014) 11–15
with income. Risky sexual intercourse might be encouraged with the influence of money and somewhat higher in the highest income group than in the lowest income group. It is difficult to make comparisons across studies, not only because of the procedural dissimilarities, but also because there have been so few or no studies and they have not been concurrent. Sexual intercourse under the influence of alcohol and drugs appears to be common, and somewhat higher with an alcohol habit than with a smoking habit.31 A previous study has found a higher level of substance use among transgender women.32 A statistically significant difference was found between HIVrelated sexual risk behaviors and sexual contact with persons per day. A third of the respondents had a daily sexual risk behavior with two or more persons. Unprotected anal intercourse was reported for 52.9% of participants. This is higher than the rate found in a previous study.31 This finding suggests that the rate of unprotected sexual intercourse among MtF transgender populations may have increased. This study had limitations that should be noted. First, the researcher could not ascertain causality of the association between the different variables. Second, the data were obtained by interviewer-administered questionnaire, including details of HIV-related sexual risk behaviors; face-to-face interviews may have resulted in a reporting bias. The sample came from different geographical areas, and generalizations to other transgender populations are strapping. This study opened up new lines of inquiry regarding this vulnerable minority group. In fact, a researcher might be examining diverse, though linked, public health problems necessitating different approaches. Likewise, the structural factors related to HIV, for instance age, education, income, and employment, may function in different ways among the transgender population. Studies within ethnic and sexual minority groups are essential to further explore the role of these structural factors. Additional empirical evidence is needed to gain a firm understanding of the different sampling approaches. In conclusion, age, education, income, frequency of daily sexual contact, and alcohol habit remain significant with regard to HIVrelated sexual risk behavior. There is an urgent need for programs and interventions to reduce risky sexual behaviors in this minority population.
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Contents lists available at ScienceDirect
International Journal of Infectious Diseases journal homepage: www.elsevier.com/locate/ijid
HIV-related sexual risk behaviors among male-to-female transgender people in Nepal Dharma Nand Bhatta Department of Public Health, Pokhara University, Nobel College, Sinamangal, Kathmandu, Nepal
A R T I C L E I N F O
Article history: Received 7 October 2013 Received in revised form 30 December 2013 Accepted 3 January 2014 Corresponding Editor: Eskild Petersen, Aarhus, Denmark Keywords: HIV risk behavior Male to female Transgender Unprotected sex MtF Nepal
S U M M A R Y
Background: Transgender women are a vulnerable and key risk group for HIV, and most research has shown an increased frequency of HIV infection among this minority population. This study examined the prevalence of HIV-related sexual risk behaviors and the socio-demographic correlates with HIV-related sexual risk behaviors among male-to-female (MtF) transgender persons. Methods: Data were collected from a sample of 232 individuals through venue-based and snowball sampling and face-to-face interviews. Results: The HIV-related sexual risk behaviors among the MtF transgender persons were: sex without using a condom (48.3%; 95% confidence interval (CI) 41.8–54.8), unprotected anal sex (68.1%; 95% CI 62.0–74.2), and unprotected sex with multiple partners (88.4%; 95% CI 84.3–92.5). Statistically significant differences were found for age, income, education, alcohol habit, and sex with more than two partners per day for these three different HIV-related sexual risk behaviors. MtF transgender persons with a secondary or higher level of education were three times (OR 2.93) more likely to have unprotected sex with multiple partners compared to those with a primary level or no education. Conclusions: Age, education, income, frequency of daily sexual contact, and an alcohol habit remain significant with regard to HIV-related sexual risk behavior. There is an urgent need for programs and interventions to reduce risky sexual behaviors in this minority population. ß 2014 The Author. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/bync-nd/3.0/).
1. Introduction Researchers, practitioners, and public health agencies continue to be challenged to identify appropriate methodological and theoretical approaches for the assessment of epidemiological trends and the development of effective interventions, particularly for sexual minorities.1,2 National-level surveillance data are sparse with regard to the incidence and prevalence of HIV among transgender populations in Nepal. Most studies have integrated this population into the ‘men who have sex with men’ (MSM) category in Nepal and in other places.3 Transgender women are at greater risk of HIV infection than other populations. Unprotected sex, drug use, and being an ethnic minority have been found to be associated with HIV status in transgender women.3–5 The previous literature shows that an increased proportion of transgender women are occupied in sex work.3,6 In various countries of Sub-Saharan Africa, transgender persons have a higher HIV prevalence than men.7 A previous systematic
E-mail address: [email protected].
review from Asia found that transgender people are 18 times more likely to be infected with HIV than those in the general population.8 Similarly, a study from North America and Europe showed that transgender women have an elevated rate of HIV infection.9 Due to a lack of nationally representative studies, it is difficult to categorize the burden of HIV infection within this population. A study from India revealed that transgender persons had an increased HIV prevalence compared to the remaining population.10 Nepal has similarities with India regarding its geography and culture. As a result, Nepal may also have this problem. A study from Nepal found an HIV prevalence of 3.8% among urban MSM.11 This result is higher than the overall HIV prevalence in Nepal of 0.3%, and transgender people are categorized as a high-risk group.12,13 Male-to-female (MtF) transgender persons are known locally as ‘Meti’ and ‘chhakka’; these are Nepali words that appear to be used as a way of stigmatizing a man who has female gender characteristics.11,13 In this study, the term ‘MtF transgender’ was used for a person who is biologically a man but self-identifies as a woman; these persons may be either a man or a woman in appearance. A study to investigate the exact HIV-related risk behaviors of transgender persons in Nepal is urgently required.13,14
http://dx.doi.org/10.1016/j.ijid.2014.01.002 1201-9712/ß 2014 The Author. Published by Elsevier Ltd on behalf of International Society for Infectious Diseases. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/3.0/).
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The importance of risk behaviors should be emphasized, particularly as HIV is influencing racial and sexual marginal groups more than ever.15 Most transgender persons engage in risky sexual behaviors that might help to reinforce their female identity and attractiveness.16,17 Previous studies revealed that condom use with regular partners was 14.4% and with irregular partners was 24.1% among transgender persons.18,19 Similarly, in a study from Indonesia on MtF transgender persons, an average condom use of 1.2 was found for the last five sexual acts.18,20 Another study showed that 12–41% of MtF transgender persons used a condom during sex.21 A study from India revealed a low level of condom use among the MtF transgender population.22 Further, a study from Cambodia found that 13% of MtF transgender people engaged in risky sexual behavior.18,23 A study from Thailand found that a myth among transgender people was that the low level of condom use was not the source of the HIV infection.24 Other MtF people from Indonesia believe that they are not at risk of HIV even if they have multiple sex partners without condom use.18,25 A systematic review and meta-analysis based on 39 studies from 15 countries showed the prevalence of HIV to be 19.1% among transgender women, with a prevalence of 17.7% in low and middle income countries and 21.6% in higher income countries.26 Moreover, unprotected sexual intercourse frequently takes place under the influence of substance use.3 Low condom use, casual sex, multiple partners, low socioeconomic status, addiction to drugs and alcohol, and street sex were found to be associated with HIV risk among sex workers.3,27,28 Previous studies have found that the heavy use of alcohol and drugs are related to unprotected sexual intercourse.3,29 2. Methods A cross-sectional survey was conducted between October 2011 and March 2012 among 232 MtF transgender persons. No document was available showing the exact geographical and population distribution of MtF transgender persons in Nepal. The information was obtained from the national-level non-governmental organization Blue Diamond Society; this organization works for sexual health, human rights, and the well-being of sexual and gender minorities, especially LGBTI (lesbian, gay, bisexual, transgender and inter-sex persons). Twenty-six districts were listed from the working districts of this organization. Finally, 15 districts were selected from that list (Kanchanpur, Kailali, Bardiya, Banke, Surkhet, Dang, Rupandehi, Chitwan, Kaski, Parsa, Rautahat, Saptari, Kathmandu, Bhaktapur, Lalitpur). These districts represent different geographical areas of Nepal and thus provided a diverse sample of transgender persons and the possibility of comparing different epidemiological trends. An interviewer administered a questionnaire to collect information on demographic characteristics, risk behaviors, and substance use. Recruitment took place at the local non-governmental organization and at other community contact points where transgender people are found. The institutional ethics review board approved the study and all respondents completed an informed consent procedure. Eligibility was screened and determined by trained research staff with verbal information. The following criteria were necessary for eligibility: (1) biologically male at birth; (2) selfidentified as a woman; (3) aged 16 years or older. A total 245 people were screened for recruitment into this study; eight did not agree to participate and five did not meet the eligibility criteria. The study used a snowball/chain referral and venue-based sampling method to recruit participants. Research staff were posted at different non-governmental organization (Blue Diamond Society) venues to recruit respondents, and at the same time
snowball/chain referral sampling was used, in which recruited respondents referred an eligible peer.30 2.1. Data collection and measures The interview instrument was developed in both English and Nepali, and face-to-face interviews were conducted using structured questionnaires; a pilot was tested among the target population. Researchers were trained with regards to ethical and sensitive issues. Participants involved in the study were fully informed about the nature of the study, its objectives, and confidentiality of the data. Each participant’s written consent was obtained after assuring confidentiality. The interview was carried out in a secret place without the presence of a third person. The researcher did not provide any financial recompense to respondents. Confidentiality of information was assured by removing individual identifiers from the completed questionnaires. Data collection took around 60 min. Socio-demographic measures recorded included age, education, income, and employment status. HIV-related sexual risk behavior among MtF was used as the dependent variable in this study. In this study, all the sexual partners were male and it could be either a committed relationship or not. Respondents reported sexual behavior with three variables, as follows: (1) Have you practiced unprotected anal sex with all types of partners (both committed and not committed sexual relationship) during the past 6 months? (2) Have you engaged in unprotected sex with multiple sex partners (having more than one sex partner considered as multiple partners) during the past 6 months? (3) Have you had sex with any partner not using a condom during the past 6 months? All the variables were dichotomized and coded as ‘no’ = 0 and ‘yes’ = 1. Those MtF persons who had practiced at least one of the three acts were considered to have an HIV-related sexual risk behavior. With regard to substance use, this measure was focused only on whether they had had sex under the influence of alcohol in the past 6 months. The variable was dichotomized and coded as ‘no sex under the influence of alcohol’ = 0 and ‘sex under the influence of alcohol’ = 1. Similarly, the variable of a smoking habit in the past 6 months after involvement in sex work was dichotomized and coded as ‘no’ = 0 and ‘yes’ = 1. 2.2. Data analysis The data were cleaned and cross-checked daily before and after data entry for completeness and accuracy. To estimate the prevalence of the study variables of interest (e.g., condom use, alcohol use), SPSS version 16 software was used (SPSS Inc., Chicago, IL, USA). Both descriptive and inferential statistics were applied. The Chi-square test was used to determine significant differences between demographic variables and HIV-related sexual risk behaviors. The variables were examined in the multivariate analysis (binary logistic regression) in order to identify the factors associated with the likelihood of having an HIV-related sexual risk behavior. When sampling is associated with potential independent variables in a multivariable model, those variables should be incorporated, but it is not essential to load observations.1 Thus, the multivariate results shown here were derived from unweighted estimations, with each variable known to be associated with participation in the sample included in the model. 3. Results The demographic characteristics of the study population are shown in Table 1. The median age of the participants was 25 years. Most of the respondents (56.5%) were aged 25 years and above.
D.N. Bhatta / International Journal of Infectious Diseases 22 (2014) 11–15 Table 1 Demographic characteristics of the transgender persons (n = 232) Result
Characteristics Age Median years Minimum–maximum years 25 years, n (%) 24 years, n (%) Education, n (%) Secondary or higher level Primary level or no education Employment, n (%) Formal employment Informal or no employment Income per month Median NPR 5001 NPR, n (%) 5000 NPR, n (%) Interested in giving birth to a child, n (%) Interested in marriage, n (%) Daily sexual contact per person, n (%) 1 person 2–3 persons 4 persons
25 16–55 131 (56.5) 101 (43.5) 133 (57.3) 99 (42.7)
13
Table 2 Prevalence estimates for reported sexual risk behavior among transgender persons (n = 232) Characteristics
Prevalence % (95% CI)
Alcohol in last 6 months Smoking in last 6 months Sex without using a condom in last 6 months Unprotected sex with multiple partners in last 6 months Unprotected anal sex in last 6 months Unprotected oral sex in last 6 months Other sex in last 6 months
68.5 58.2 48.3 88.4
(62.6–74.4) (51.9–64.5) (41.8–54.8) (84.3–92.5)
68.1 (62.0–74.2) 51.5 (45.0–58.0) 6.1 (3.0–9.2)
124 (53.4) 108 (46.6) 10 000 172 (74.1) 60 (25.9) 113 (48.7) 152 (65.5) 156 (67.2) 56 (24.1) 20 (8.6)
More than half (57.3%) of the total sample had a secondary or higher level of education. The percentage of unemployed participants was also high (46.6%), and income levels were fairly low, with 25.9% of the respondents earning 5000 NPR per month (1 USD = 87 NPR). Nearly half (48.7%) of the MtF transgender persons were interested in giving birth to a child. Two-thirds (65.5%) of the respondents were interested in marriage. Nearly a third of the respondents had sexual contact with more than one person per day. All of the respondents in this study were unmarried. Table 2 shows the prevalence of HIV-related sexual risk behaviors and substance use. Heavy alcohol use was highly prevalent in the transgender population (68.5%; 95% confidence interval (CI) 62.6–74.4%) as was a smoking habit (58.2%; 95% CI 51.9–64.5%), although this was relatively lower than alcohol. A pattern of sexual risk behavior emerged in this sample, showing
that approximately half of respondents (48.3%; 95% CI 41.8–54.8%) engaged in sex without using condom. The prevalence of multiple sex partners was found to be extremely high (88.4%; 95% CI 84.3– 92.5%) among the MtF transgender persons. The prevalence of unprotected anal sexual intercourse was higher than oral sexual intercourse (anal sex: 68.1%; 95% CI 62.0–74.2%; oral sex: 51.5%; 95% CI 45.0–58.0%). The prevalences of HIV risk behaviors with regard to selected demographic characteristics are shown in Table 3. The prevalence of HIV risk behavior varied significantly by age group; it was relatively higher among the participants aged 25 years and above. Sex without using a condom and unprotected anal sex were found to differ significantly by age. When compared among educational groups, the highest prevalence was found among participants who had a secondary or higher level of education. Unprotected sex with multiple partners differed significantly by education level. The prevalence of HIV risk behavior varied dramatically by income group, with the lowest income group having the lowest prevalence. Unprotected sex with multiple partners was found to differ significantly by income. Sex without using a condom was found to differ significantly by employment status. Finally, HIV-related sexual risk behavior was higher among those MtF transgender persons who had an alcohol habit. Unprotected sex with multiple partners was significantly associated with an alcohol habit. Interestingly, a similar result was found for smoking habit. Similarly, sex without using a condom,
Table 3 Estimated HIV-related sexual risk behavior prevalence among male-to-female transgender persons by socio-demographic variables and substance use (n = 232) Characteristics
Age 25 years 24 years Education Secondary or higher level Primary level or no education Income per month 5001 NPR 5000 NPR Employment Formal employment Informal or no employment Alcohol habit Yes No Smoking habit Yes No Daily sexual contact per person 1 person 2–3 persons 4 persons
Sex without condom use (n = 232)
Unprotected anal sex (n = 232)
Unprotected sex with multiple partners (n = 232)
Yes, %
Yes, %
Yes, %
p-Value (Chi-square) 0.029
49.1 50.9
0.029 58.3 41.7
0.203 61.6 38.4
0.597
0.038
0.063
0.526
0.143 51.7 48.3
0.530 69.9 30.1
0.121 63.4 36.6
0.019 76.6 23.4
57.7 42.3
70.5 29.5
0.022 54.6 45.4
73.1 26.9
46.4 53.6
0.180
0.411
0.374
0.000 74.1 25.9
0.728 59.0 41.0
0.022
0.005 61.5 38.5
0.008 70.5 18.6 10.9
p-Value (Chi-square)
58.0 42.0
57.7 42.3
76.8 23.2
60.7 32.1 7.1
p-Value (Chi-square)
0.011 63.9 26.3 9.8
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D.N. Bhatta / International Journal of Infectious Diseases 22 (2014) 11–15
Table 4 Logistic regression for HIV-related sexual risk behavior among male-to-female transgender persons (n = 232) Characteristics
Age 25 years 24 years, Ref. Education Secondary or higher level Primary level or no education, Ref. Income per month 5001 NPR 5000 NPR, Ref. Employment Formal employment Informal or no employment, Ref. Alcohol habit Yes No, Ref. Smoking habit Yes No, Ref. Daily sexual contact per persons 1 person, Ref. 2–3 persons 4 persons
Unprotected anal sex (n = 232)
Sex without condom use (n = 232) OR
SE
1.65
(0.30)
0.66
B
OR
SE
0.50
0.99
(0.31)
(0.29)
0.42
0.96
0.94
(0.34)
0.06
1.59
(0.29)
1.34
Unprotected sex with multiple partners (n = 232) B
OR
SE
B
0.01
0.82
(0.47)
0.19
(0.31)
0.04
2.93a
(0.53)
1.08
1.15
(0.36)
0.14
0.67
(0.48)
0.40
0.47
0.59
(0.31)
0.53
1.35
(0.49)
0.30
(0.39)
0.30
0.66
(0.41)
0.41
0.13a
(0.65)
2.03
0.51
(0.36)
0.68
1.04
(0.38)
0.04
1.65
(0.64)
0.50
1.30 2.68
(0.52) (0.56)
0.26 0.99
0.39 0.18a
(0.68) (0.69)
0.95 1.72
0.00 0.00
(3.93) (3.93)
18.64 17.47
OR, odds ratio; Ref., reference; SE, standard error. a p < 0.05.
unprotected anal sex, and unprotected sex with multiple partners were found to differ significantly by per-person daily sexual contact (Table 3). The results of the logistic regression for HIV-related sexual risk behavior in this transgender population are shown in Table 4. The coefficients describe changes in the estimated odds of engaging in unprotected sexual intercourse associated with changes in the variable in question. MtF transgender persons with a secondary or higher level of education were three times more likely to have unprotected sex with multiple partners than those with a primary level or no education. Most of the variables had higher odds with different sexual risk behaviors, but these were not statistically significant. 4. Discussion This study characterized the HIV-related sexual risk behavior among MtF transgender persons coming from 15 different districts across the country of Nepal. An appropriate methodology was applied to improve the reliability and validity of the study findings. Based on the lack of knowledge in the literature, this study scrutinized the sexual health needs and sexual behavior among MtF transgender persons in Nepal, as well as discussing the risk and influencing factors that are linked with HIV-related sexual risk behaviors among MtF transgender persons. The sampling and recruitment method worked effectively. Exact populations of transgender people in Nepal are unknown. However, the sample represented different geographical areas. No major problems were encountered during the recruitment process. The researcher also found no evidence of coercive peer recruitment. Unemployment and poverty were common among the transgender persons, as in other populations in Nepal. Nearly half of the respondents had no formal employment and a fourth of the participants indicated that they had a low income status, which is less than two dollars per day. The study also found that nearly a third of participants had sexual intercourse with more than one sex partner per day, which indicates a great risk for HIV and
sexually transmitted diseases. A previous study has highlighted that the MtF population engages with a higher number of sexual associates.13 The findings regarding substance use suggest that alcohol consumption is widespread in the transgender population. This may be considered a serious public health problem, given that more than two-thirds of the participants had an alcohol drinking habit. Similarly, nearly three-fifths of the participants had a smoking habit. Unprotected sex with multiple partners was found to differ significantly by alcohol and smoking habits. Previous studies have found alcohol to be associated with HIV risk among sex workers and those having unprotected sexual intercourse.3,27–29 However, there is no previous evidence for the association between HIVrelated sexual risk behavior and smoking. Nearly half of the participants engaged in unsafe sex and did not use a condom with their sex partners. Previous studies have revealed irregular and lowlevel condom use among MtF populations.13,18–21 However, the great majority of the participants had multiple sex partners. Anal sex appears to be the most common sexual behavior among the MtF transgender persons. The results showed no distinctive variations in HIV risk behavior among the age groups. Sex without using a condom and unprotected anal sex were found to differ significantly by age group. However, HIV risk behavior was found to be more common among the more educated participants. Educated respondents were three times more likely to have unprotected sex with multiple partners than the less educated and this was statistically significant. Previous studies have found the level of education to be positively correlated with unprotected sex.1 Having very limited comparable data, the researcher proposes an explanation. Transgender persons with a higher education level may find it easier to build a network with varied sexual associates than less educated persons and may thus be further expected to engage in more unprotected sexual acts. They might be unaware that they are themselves at risk either because of the self-confidence that education may bring or because they are unaware or do not care to see their sexual partners as being at risk of HIV. Unprotected sex with multiple partners was found to be significantly associated
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with income. Risky sexual intercourse might be encouraged with the influence of money and somewhat higher in the highest income group than in the lowest income group. It is difficult to make comparisons across studies, not only because of the procedural dissimilarities, but also because there have been so few or no studies and they have not been concurrent. Sexual intercourse under the influence of alcohol and drugs appears to be common, and somewhat higher with an alcohol habit than with a smoking habit.31 A previous study has found a higher level of substance use among transgender women.32 A statistically significant difference was found between HIVrelated sexual risk behaviors and sexual contact with persons per day. A third of the respondents had a daily sexual risk behavior with two or more persons. Unprotected anal intercourse was reported for 52.9% of participants. This is higher than the rate found in a previous study.31 This finding suggests that the rate of unprotected sexual intercourse among MtF transgender populations may have increased. This study had limitations that should be noted. First, the researcher could not ascertain causality of the association between the different variables. Second, the data were obtained by interviewer-administered questionnaire, including details of HIV-related sexual risk behaviors; face-to-face interviews may have resulted in a reporting bias. The sample came from different geographical areas, and generalizations to other transgender populations are strapping. This study opened up new lines of inquiry regarding this vulnerable minority group. In fact, a researcher might be examining diverse, though linked, public health problems necessitating different approaches. Likewise, the structural factors related to HIV, for instance age, education, income, and employment, may function in different ways among the transgender population. Studies within ethnic and sexual minority groups are essential to further explore the role of these structural factors. Additional empirical evidence is needed to gain a firm understanding of the different sampling approaches. In conclusion, age, education, income, frequency of daily sexual contact, and alcohol habit remain significant with regard to HIVrelated sexual risk behavior. There is an urgent need for programs and interventions to reduce risky sexual behaviors in this minority population.
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