Characteristics of HIV/sexually transmitted infections among men who have sex with men and women in Bangkok,Thailand

Abstract

Background

Men who have sex with men (MSM) are a key HIV target population in Thailand. An important subgroup is men who have sex with men and women (MSMW) as they can sexually transmit infections between individuals with different gender identities. This study compared the sexually transmitted infection risk behavior of different types of men in Thailand.

Methods

We retrospectively reviewed the medical records of 839 consecutive male patients who visited an STI clinic in Bangkok, Thailand, between 2014 and 2020.

Results

Men who have sex with women only (MSWO) predominated (58.0%), followed by men who have sex with men only (MSMO, 32.2%) and MSMW (9.8%). MSMW and MSMO shared similar sexual risk behaviors, such as significantly higher median numbers of sex partners (10 and 8, respectively) than MSWO (5; Kruskal–Wallis, p < 0.001). MSMW had the highest prevalence of concurrent sexual partnerships (91.4%), significantly different from MSWO (61.2%) and MSMO (76.7%; chi-squared, p < 0.001). HIV and syphilis prevalence was significantly higher for MSMO (48.9% and 51.1%) and MSMW (42.7% and 48.8%) than MSWO (12.3% and 20.9%; chi-squared, p < 0.001).

Conclusions

MSMW exhibited similar sexual risk behavior and high HIV/STI prevalence comparable to MSMO.

Keywords

HIV men who have sex with men men who have sex with men and women bisexual sexually transmitted infections syphilis

Introduction

In 2019, a total of 36.8 million people were living with HIV worldwide, and Sub-Saharan Africa was the area that had the highest burden.¹ In Asia and the Pacific region, an estimated 6 million people were living with HIV (PLHIV) in 2019.² Thailand reported an adult PLHIV rate of 1.1%, which was higher than that of neighboring countries in Asia, such as Myanmar (0.81%), Cambodia (0.5%), Indonesia (0.41%), India (0.3%), Vietnam (0.4%), and China (<0.1%).^2–4

The negative impact of HIV infection is not limited to each individual’s health but also impacts their families, communities, and a country’s economic growth.⁵ In Thailand, the cost of HIV/AIDS represented 1.5% of the current health expenditure, which was 298.5 million US dollars per year.⁶ Other sexually transmitted infections (STIs) also substantially impact the economic burden worldwide, especially syphilis, a re-emerging global health issue.^7–9

The Thai government has prioritized HIV infection since 1992, consequently a remarkable reduction in HIV infection has been observed.^10,11 The incidence of PLHIV has markedly decreased over the past decade.¹² In 2010, Thailand had approximately 580,000 PLHIV, with an estimated 16,000 people becoming newly HIV positive. In 2019, Thailand had 470,000 PLHIV, with an estimated 5400 newly HIV positive.^3,12

One of the key HIV subgroups in Thailand are men who have sex with men (MSM).³ Approximately 40% of new adult Thai PLHIV occur in this group, especially young men. Additionally, 12%–15% of Thai MSM have been estimated to be living with HIV.³ MSM are heterogeneous. For example, some MSM also have female partners; this sexual behavior has been termed “men who have sex with men and women” (MSMW). MSMW can sexually transmit infections between individuals with different gender identities. MSMW are an important but often overlooked MSM subgroup.¹³ The estimated pooled prevalence of MSMW among Asian MSM was 32.8%.¹⁴ MSMW have sex with women for many reasons. Apart from individual sexual orientation, the grounds include fear of stigmatization or being socially perceived as having decreased masculinity, and sociocultural pressures to have a wife or children. MSMW were less likely to disclose their sexual identity to their family, friends, and even their doctor than men who have sex with women only (MSWO) or men who have sex with men only (MSMO).¹⁵ Therefore, MSMW may have been inadequately reached by HIV prevention programs, which are mainly targeted toward MSMO.¹⁴

There have been few studies on the sexual behavior risks and the prevalence of HIV/STIs in MSMW in Thailand.^16,17 This study set out to compare the characteristics, sexual high-risk behavior, and prevalence rates of HIV/STIs of MSMW, MSMO, and MSWO in patients who visited an STI clinic during 2014–2020 in Bangkok, Thailand.

Methods

The study was granted ethical approval by the Siriraj Institutional Review Board. Medical records of male patients who visited the STI clinic of the Department of Dermatology, Siriraj Hospital, Bangkok, Thailand, were retrospectively reviewed. Most of the clinic’s clients were male, as females would typically be referred to the gynecology clinic at the hospital. Demographic data, sexual risk behaviors, and history of sexually transmitted infections were routinely recorded for all patients entering the STI clinic. Details of these items were extracted from case records. Male patients were categorized into 3 groups based on their sexual orientation: MSWO, MSMO, and MSMW. Men who attended the clinic multiple times during the study period were analyzed only on the first visit to our clinic.

The statistical analyses were undertaken using PASW Statistics for Windows (version 18; SPSS Inc., Chicago, IL, USA). Categorical variables are presented as numbers or numbers with percentages, while continuous variables are shown as the means with standard deviations or medians with ranges. Pearson’s chi-squared test was used to compare the categorical data of the groups. Fisher’s exact test was used instead when more than 20% of cells had an expected value of < 5.¹⁸ To compare the quantitative variables of the groups, one-way ANOVA and the Kruskal–Wallis test were used. Normally distributed data were analyzed with ANOVA, while non-normally distributed data were analyzed with the Kruskal–Wallis test. The Bonferroni correction for multiple comparisons based on 2-sided tests was used to adjust for all pairwise comparisons within a row. A p value of ≤0.05 indicated statistical significance.

Results

In all, 839 male patients attended the clinic and were included in the analysis. The majority of participants were single (69.1%), highly educated (55.2%), and self-employed (40.6%; Table 1). MSWO was the largest group (58.0%), followed by MSMO (32.2%) and MSMW (9.8%). The median participant age was 29 years, with MSMO the youngest (25 years). MSMO were more likely to have a bachelor’s degree or higher education than other groups. Regarding occupation, MSMO had the highest percentage in the health care worker group and the student group, whereas MSMW had the highest percentage in the office worker group and the police officer/soldier group.

Table 1.

Demographic data of all included patients and subcategory groups of MSWO, MSMO, and MSMW.

	All(n = 839)		MSWO (n = 487)		MSMO (n = 270)		MSMW(n = 82)		p Value
Demographics
Age (years), median, IQR	29	23, 40	32	25, 47	25	22, 31	33	27, 40.8	<0.001^1,3
Marital status, n (%) (n = 831)									<0.001^1,2,3
Single	574	69.1	252	52.0	260	98.4	62	75.6
Married	257	30.9	233	48.0	4	1.6	20	24.4
Education, n (%) (n = 820)									<0.001¹
Less than bachelor’s degree	367	44.8	253	53.2	80	30.4	34	42.0
Bachelor’s degree or higher	453	55.2	223	46.8	183	69.6	47	58.0
Occupation, n (%)									<0.001^1,2,3
Self-employed	341	40.6	215	44.1	100	37.0	26	31.7
Office worker	190	22.6	102	20.9	61	22.6	27	32.9
Student	138	16.4	57	11.7	74	27.4	7	8.5
Unemployed	86	10.3	63	12.9	15	5.6	8	9.8
Healthcare worker	26	3.1	11	2.3	14	5.2	1	1.2
Police officer/soldier	58	6.9	39	8.0	6	2.2	13	15.9

¹significant between MSWO and MSMO.

²significant between MSWO and MSMW.

³significant between MSMO and MSMW; “Other” includes chancroid, lymphogranuloma venereum, and molluscum contagiosum.

Statistical significance in this table was calculated by using Kruskal–Wallis (Age) and Pearson’s chi-squared test with Bonferroni correction for multiple comparisons based on 2-sided tests (marital status, education, and occupation).

Sexual behaviors and prevalence of HIV/STIs are shown in Table 2. MSMW had the highest median number of lifetime sex partners (10), which was significantly different from MSWO (5) but was not different from MSMO (8). They also had the highest prevalence of concurrent sexual partnerships (91.4%), which was significantly different from the findings for MSWO (61.2%) and MSMO (76.7%). Moreover, MSMW had the highest percentage of sex-worker contact during the preceding 5 years (29.3%), significantly different from MSMO (9.6%). On the other hand, MSMW reported the highest percentage of condom use on every occasion (26.3%), but there was no significant difference relative to MSMO (21.4%). Overall, the men in all groups reported very low injection drug use.

Table 2.

Sexual behavior, and prevalence of HIV/STIs in MSWO, MSMO, and MSMW.

	All (n = 839)		MSWO (n = 487)		MSMO (n = 270)		MSMW (n = 82)		p Value
Sexual behavior
Age of first sexual intercourse (years), mean, SD (n = 774)	18.3	3.6	18.3	3.7	18.3	3.5	18.5	3.3	0.877
Number of sex partners, median, IQR (n = 774)	6	3, 13	5	3, 10	8	4, 20	10	5, 26.5	<0.001^1,2
History of oral sex, n (%) (n = 822)	392	47.7	142	30.0	207	77.5	43	53.1	<0.001^1,2,3
History of concurrent sexual partnerships, n (%) (n = 835)	578	69.2	297	61.2	207	76.7	74	91.4	<0.001^1,2,3
Frequency of condom use during sexual intercourse, n (%) (n = 801)									<0.001^1,2
Every time	125	15.6	51	10.8	54	21.4	20	26.3
Often	580	72.4	346	73.2	187	74.2	47	61.9
Never	96	12.0	76	16.0	11	4.4	9	11.8
Sex worker contact in 5 years, n (%) (n=836)	157	18.8	107	22.3	26	9.6	24	29.3	<0.001^1,3
PLHIV sex partner, n (%) (n = 807)	36	4.5	11	2.3	17	6.6	8	10.4	0.001^1,2
Person who injects drugs, n (%) (n = 838)	21	2.5	7	1.4	13	4.8	1	1.2	0.013¹
Sexually transmitted infections
	n	%	n	%	n	%	n	%	p Value
HIV	227	27.1	60	12.3	132	48.9	35	42.7	<0.001^1,2
Syphilis	280	33.4	102	20.9	138	51.1	40	48.8	<0.001^1,2
Condyloma acuminate	308	36.7	195	40.0	92	34.1	21	25.6	0.024²
GU and NGU	158	18.8	113	23.2	30	11.1	15	18.3	<0.001¹
Genital herpes	71	8.5	60	12.3	6	2.2	5	6.1	<0.001¹
Other	22	2.6	17	3.5	4	1.5	1	1.2	0.178

¹significant between MSWO and MSMO.

²significant between MSWO and MSMW.

³significant between MSMO and MSMW; “Other” includes chancroid, lymphogranuloma venereum, and molluscum contagiosum.

GU, gonococcal urethritis; HIV, human immunodeficiency virus; NGU, non-gonococcal urethritis; PLHIV, people living with human immunodeficiency virus.

Statistical significance in this table was calculated using one-way ANOVA (age of first sexual intercourse); Kruskal–Wallis (number of sex partners); Pearson’s chi-squared test with Bonferroni correction for multiple comparisons based on 2-sided tests (history of oral sex, history of concurrent sexual partnerships, frequency of condom use during sexual intercourse, sex worker contact in 5 years, PLHIV sex partner, person who injects drugs); and Fisher’s exact test/Pearson’s chi-squared test (sexually transmitted infections).

The HIV prevalence in this study was 27.1%. The rates of MSMO (48.9%) and MSMW (42.7%) living with HIV were significantly higher than that of MSWO (12.3%). Syphilis was significantly more common among MSMO (51.1%) and MSMW (48.8%) than MSWO (20.9%). Condyloma acuminata, gonococcal urethritis (GU), non-gonococcal urethritis (NGU), and genital herpes were more common among MSWO.

Co-infections between HIV and other STIs are detailed in Table 3. Most co-infections of PLHIV occurred with syphilis and were also significantly more common in MSMO (60.6%) and MSMW (57.1%) than MSWO (28.3%). Condyloma acuminata and genital herpes were more common among PLHIV in MSWO.

Table 3.

Co-infection of other STIs with HIV in MSWO, MSMO, MSMW.

	Total PLHIV (n = 227)		PLHIV in MSWO (n = 60)		PLHIV in MSMO (n = 132)		PLHIV in MSMW (n = 35)		p Value
	n	%	n	%	n	%	n	%	p Value
Syphilis	117	51.5	17	28.3	80	60.6	20	57.1	<0.001^1,2
Condyloma acuminata	80	35.2	26	43.3	43	32.6	11	31.4	0.308
GU and NGU	12	5.3	5	8.3	4	3.0	3	8.6	0.201
Genital herpes	15	6.6	11	18.3	3	2.3	1	2.9	<0.001¹
Other	3	1.3	1	1.7	2	1.5	0	0.0	N/A

¹significant between MSWO and MSMO.

²significant between MSWO and MSMW.

“Other” includes chancroid, lymphogranuloma venereum, and molluscum contagiosum.

GU, gonococcal urethritis; NGU, non-gonococcal urethritis; PLHIV, people living with human immunodeficiency virus; Statistical significance in this table was calculated using Pearson’s chi-squared test (condyloma acuminata, GU and NGU) with Bonerroni correction for multiple comparisons based on 2-sided tests (syphilis); and Fisher’s exact test (genital herpes).

The factors that might be associated with HIV infection were analyzed, and the results are detailed in Table 4. MSMO and MSMW, younger age, single status, a history of oral sex, concurrent sexual partnership, and PLHIV sex partners were associated with HIV infection.

Table 4.

Factors associated with HIV infection.

Factors	Total (n = 839)
Factors	HIV (+) (n = 227)		HIV (−) (n = 612)		p Value
Age (years), median, IQR	28	23, 36	30	23, 41	0.029*
Sexual orientation, n (%)					<0.001^1,2
MSWO (n = 487)	60	12.3	427	87.7
MSMO (n = 270)	132	48.9	138	51.1
MSMW (n = 82)	35	42.7	47	57.3
Marital status, n (%)					<0.001*
Single (n = 579)	188	32.5	391	67.5
Married (n = 257)	39	15.2	218	84.8
Education, n (%)					0.397
Under Bachelor’s degree (n = 367)	93	25.3	274	74.7
Bachelor’s degree or higher (n = 454)	127	28.0	327	72.0
Occupation, n (%)					0.763
Self-employed (n = 341)	95	27.9	246	72.1
Office worker (n = 190)	54	28.4	136	71.6
Student (n = 138)	31	22.5	107	77.5
Unemployed (n = 86)	24	27.9	62	72.1
Police/soldier (n = 58)	14	24.1	44	75.9
Health care worker (n = 27)	9	33.3	18	66.7
Age of first sexual intercourse (years), mean, SD.	18.1	3.3	18.4	3.7	0.450
Number of sex partners, median, IQR	8	4, 20	6	3, 11	0.061
History of oral sex, n (%)					<0.001*
Yes (n = 392)	132	33.7	260	66.3
No (n = 429)	91	21.2	338	78.8
History of concurrent sexual partnerships, n (%)					0.006*
Yes (n = 578)	172	29.8	406	70.2
No (n = 257)	53	20.6	204	79.4
Frequency of condom use during sexual intercourse, n (%)					0.293
Every time (n = 125)	40	32.0	85	68.0
Often (n = 580)	154	26.6	426	73.4
Never (n = 96)	22	22.9	74	77.1
Sex worker contact in 5 years, n (%)					0.135
Yes (n = 157)	35	22.3	122	77.7
No (n = 678)	191	28.2	487	71.8
PLHIV sex partner, n (%)					<0.001*
Yes (n = 36)	20	55.6	16	44.4
No (n = 770)	195	25.3	575	74.7
Person who inject drugs, n (%)					0.508
Yes (n = 21)	7	33.3	14	66.7
No (n = 816)	219	26.8	597	73.2

^*significant at P < 0.05

¹significant between MSWO and MSMO.

²significant between MSWO and MSMW.

PLHIV, people living with human immunodeficiency virus.

Statistical significance in this table was calculated using Kruskal–Wallis (age, number of sex partner); One-way ANOVA (age of first sexual intercourse); Pearson’s chi-squared test (marital status, education, occupation, history of oral sex, history of concurrent sexual partnerships, frequency of condom use during sexual intercourse, sex worker contact in 5 years, PLHIV sex partner, person who injects drugs) with Bonferroni correction for multiple comparisons based on 2-sided tests (sexual orientation).

Discussion

The data for the 7-year study period supported the previous findings in the literature that HIV infection in Thailand continued to be common among MSM.³ Regarding the MSM subgroups, MSMW and MSMO had comparable HIV-positive rates (42.7% and 48.9%, respectively). As to characteristics and risk, the MSMW demonstrated high sexual risk behavior: a large number of sex partners, concurrent sexual partnerships, and a history of sex-worker contact during the preceding 5 years.

MSMW from various countries shared some similar characteristics regarding condom usage. Compared with MSMO, previous studies in the US and Australia revealed that MSMW were less likely to have condomless sex and less likely to have been diagnosed with HIV/STIs.^15,19 In India, MSMW were also less likely to use condoms inconsistently, but the prevalence of HIV/STIs was not different from MSMO.²⁰ Previous studies from Thailand revealed a higher rate of consistent condom use and a lower prevalence of PLHIV by Thai MSMW than by MSMO.^16,17 Our study revealed that MSMW had a slightly higher rate of condom usage at every sexual intercourse and had comparable rates of HIV and syphilis infection, compared with MSMO.

One key point was that 24.4% of the MSMW in our study were married. Married couples typically have condomless sex.²¹ A previous report from West Africa revealed that inconsistent condom usage with wife/girlfriend was reported in 57% of MSMW.²² Since MSMW have sex with both genders, there is the possibility that they will transmit HIV and other STIs from a male partner to a female partner or vice versa.²³ Another issue is that MSMW were found to be less likely to have HIV laboratory testing and thus more likely to be unaware of an HIV infection.²⁴ Therefore, there is a clear need to focus HIV/STI prevention efforts on MSMW.

A small proportion (36/807, 4.5%) of our participants reported having sex with a PLHIV partner. Of those 36 patients, 20 were PLHIV, and 16 were not. Of the remaining 771 patients with no history of having sex with a PLHIV partner, 195 were PLHIV. Our results revealed the disparity in the HIV status of the partners in HIV serodiscordant couples and serodiscordant sexual encounters. HIV transmission rates within serodiscordant couples have been highly reported (3.7–19.0/100 person-years).²⁵ Further investigation should specify details of serodiscordant relationships between subtypes of MSM, including viral load and detectability data.

To enhance HIV prevention, Thailand promotes the usage of pre-exposure prophylaxis (PrEP) antiretroviral drugs. They were made available on a self-pay basis via a PrEP program that commenced in 2014. However, access was subsequently broadened with their inclusion in the national Universal Health Coverage scheme in 2019.^26,27 In 2018, studies still found an increasing trend in HIV positivity in young Thai men, especially among MSM.²⁸ Consequently, MSM should be the key target group for the provision of information about the PrEP program. Although the present research did not have data available on the number of patients who received PrEP, our estimation was a likely low rate of PrEP utilization in this cohort for 2 reasons. First, the antiretroviral drugs used in our hospital had to be prescribed by an infectious disease specialist. Most of our STI patients denied ever consulting such a specialist because of the long waiting times involved. The second reason is generally low awareness of the importance of PrEP. Our patients were mainly focused on receiving treatment for their presenting STI complaint, and many were lost to follow-up (22.7%–44.2% from our previous studies).^29–31 Given their mindset, lack of understanding of PrEP, and apparent reluctance to receive prolonged therapy, there is a need for further education and increased PrEP resources for the overall MSM community.

Over the past two decades, the prevalence of several STIs—especially syphilis—has risen in Thailand.³² A 2008–2012 study at our clinic revealed that the overall prevalence of syphilis was 15.5%, with MSM representing 18.2% of those cases.³⁰ In marked contrast, the current investigation found a much higher prevalence of syphilis (33.4%), with MSM accounting for 63.6% of the cases (MSMO, 49.3%; MSMW, 14.3%).

Between 2007 and 2011, the prevalence of condyloma acuminata at our clinic was 14.3%, with 22.6% of the affected individuals being MSM.³¹ The present work showed that the disease prevalence had risen noticeably to 36.7%; moreover, 29.9% of the cases were in MSMO, and 6.8% were in MSMW. The overall prevalence and proportion of MSM with condyloma acuminata also increased. The very low vaccination coverage among Thai males might explain the rising rate of the human papillomavirus.³³

In a previous study at our clinic from 2007 to 2014, the prevalence of GU plus NGU was 16.4%. Additionally, 12.2% of those cases were in MSM.²⁹ Our current work showed the prevalence of GU plus NGU to be 18.8%, with 28.5% of the patients being MSM (MSMO, 19.0%; MSMW, 9.5%). Even though condyloma acuminata and GU/NGU remained more common among MSWO than MSM during the last 2 decades, the proportion of MSM with these diseases notably increased. Whether this rising proportion occurred because of a higher rate of infection among MSM or a fall in the rate among MSWO, the data highlight that MSM should be the primary target group for the prevention of syphilis and other STIs.

Overall, the prevalence of several STIs rose relative to the findings of previous studies at our clinic. ^29–31 Although MSMW had the smallest proportions for each type of STI, the HIV/STI infection rates of MSMW were similar to those of MSMO. Encouraging the usage of condoms along with PrEP should therefore be emphasized in MSMW.

Our work has some limitations. One is that it was conducted at an STI clinic at a tertiary-care hospital. The clinic served patients who had symptoms of a suspected STI. Our study showed a higher prevalence of HIV and syphilis in MSM than another Thai study where their clinic also screened for HIV/STIs in asymptomatic patients.³⁴ The prevalence rates of HIV and syphilis in MSM from that study were 16.7% and 24%, respectively. Co-infection of HIV and syphilis in MSM was only 8.3%.³⁴ Future studies incorporating asymptomatic routine HIV/STI screening in Thai MSMW should be performed to characterize better the prevalence of HIV/STIs in this group. Another limitation was the lack of data related to PrEP utilization. Attitudes regarding PrEP and the history of its usage in Thai MSM should be further investigated. In addition, sexual behavior data were retrieved from medical records. There might be measurement errors in sexual risk questions, such as the age of first sexual intercourse, the number of sex partners, or frequency of condom use during sexual intercourse.

Even though the proportion of Thai MSMW was far less common than that of MSMO, they exhibited similar high sexual risk behavior and had high HIV/STI prevalence. The overall prevalence of being HIV-positive remained high among MSM. The proportions of MSM with syphilis, condyloma acuminata, or GU/NGU are growing. HIV/STI prevention efforts should be intensified. Expanding access to HIV prevention should be done by getting more providers (such as trained health care workers) to prescribe PrEP, improving PrEP education by increasing patient awareness of the HIV transmission risk, and decreasing stigmatizing beliefs about PrEP utilization. These strategies should be prioritized to MSM, with specific attention given to both MSMO and MSMW.

Footnotes

Acknowledgements

The authors thank Mr Suthipol Udompunthurak for his assistance with the statistical analysis. The authors are also indebted to Mr David Park for the English-language editing of this paper.

Declaration of conflicting interests

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

Funding

The author(s) received no financial support for the research, authorship, and/or publication of this article.

ORCID iDs

Chayada Chaiyabutr

Yanisorn Nanchaipruek

References

Global regional . And national sex-specific burden and control of the HIV epidemic, 1990-2019, for 204 countries and territories: the Global Burden of Diseases Study 2019. Lancet HIV 2021; 8(10): e633–e651.

Riono

Challacombe

. HIV in Indonesia and in neighbouring countries and its social impact. Oral Dis 2020; 26(Suppl 1): 28–33.

Global

Avert

. Information and education on HIV and AIDS [cited 2021 April, 24]. Available at: https://www.avert.org/professionals/hiv-around-world/asia-pacific/thailand#footnote15_qi33ppw

Avert. HIV and AIDS IN CHINA [cited 2022 March, 19.]. Available at: https://www.avert.org/professionals/hiv-around-world/asia-pacific/china

Roy

. The effects of HIV/AIDS on economic growth and human capitals: A panel study evidence from Asian countries. AIDS Care 2014; 26(12): 1568–1575.

Viriyathorn

Sachdev

Wanwong

, et al. The Impact of HIV Spending on Health Outcomes in Thailand. World J AIDS; 2021(11): 85–100.

Peeling

Mabey

Kamb

, et al. Syphilis Nat Rev Dis Primers 2017; 3: 17073.

Zou

Liao

Liu

, et al. The Annual Economic Burden of Syphilis: An Estimation of Direct, Productivity, and Intangible Costs for Syphilis in Guangdong Initiative for Comprehensive Control of Syphilis Sites. Sex Transm Dis 2017; 44(11): 671–677.

Pultorak

Wong

Rabins

, et al. Economic Burden of Sexually Transmitted Infections: Incidence and Direct Medical Cost of Chlamydia, Gonorrhea, and Syphilis Among Illinois Adolescents and Young Adults. Sex Transm Dis 2005-2006; 36(10): 629–636.

10.

Wong

Macikunas

Manduric

, et al. Reaching the Hard to Reach in Thailand: Eliminating Mother-To-Child HIV Transmission. Health Syst Reform 2020; 6(1): 1–7.

11.

Siraprapasiri

Ongwangdee

Benjarattanaporn

, et al. The impact of Thailand’s public health response to the HIV epidemic 1984-2015: understanding the ingredients of success. J Virus Erad 2016; 2(Suppl 4): 7–14.

12.

The United Nations . UNAIDS DATA 2020 [cited 2022 January, 12]. Available at: https://www.unaids.org/sites/default/files/media_asset/2020_aids-data-book_en.pdf

13.

Sathane

Horth

Young

, et al. Risk Factors Associated with HIV Among Men Who Have Sex Only with Men and Men Who Have Sex with Both Men and Women in Three Urban Areas in Mozambique. AIDS Behav 2016; 20(10): 2296–2308.

14.

Bowring

Veronese

Doyle

, et al. HIV and Sexual Risk Among Men Who Have Sex With Men and Women in Asia: A Systematic Review and Meta-Analysis. AIDS Behav 2016; 20(10): 2243–2265.

15.

Shadaker

Magee

Paz-Bailey

, et al. Characteristics and Risk Behaviors of Men Who Have Sex With Men and Women Compared With Men Who Have Sex With Men-20 US Cities, 2011 and 2014. J Acquir Immune Defic Syndr 2017; 75(Suppl 3Suppl 3): S281–s287.

16.

Chariyalertsak

Kosachunhanan

Saokhieo

, et al. HIV incidence, risk factors, and motivation for biomedical intervention among gay, bisexual men, and transgender persons in Northern Thailand. PLoS One 2011; 6(9): e24295.

17.

Varangrat

Wimonsate

, et al. Sexual behavior and risk factors for HIV infection among homosexual and bisexual men in Thailand. AIDS Behav 2009; 13(2): 318–327.

18.

Kim

H-Y

. Statistical notes for clinical researchers: Chi-squared test and Fisher’s exact test. Restor Dent Endod 2017; 42(2): 152–155.

19.

Martín-Sánchez

Case

Fairley

, et al. Trends and differences in sexual practices and sexually transmitted infections in men who have sex with men only (MSMO) and men who have sex with men and women (MSMW): a repeated cross-sectional study in Melbourne, Australia. BMJ Open 2020; 10(11): e037608.

20.

Ramakrishnan

Ramanathan

Chakrapani

, et al. Comparison of Sexual Risk, HIV/STI Prevalence and Intervention Exposure Among Men Who Have Sex with Men and Women (MSMW) and Men Who Have Sex with Men Only (MSMO) in India: Implications for HIV Prevention. AIDS Behav 2015; 19(12): 2255–2269.

21.

Bauni

Jarabi

. The Low Acceptability and Use of Condoms Within Marriage: Evidence From Nakuru District, Kenya. Afr Popul Stud 2003; 18: 51–55.

22.

Fiorentino

Eubanks

Coulaud

, et al. Homonegativity, sexual violence and condom use with women in men who have sex with men and women in West Africa. Aids 2021; 35(4): 681–687.

23.

Dodge

Banik

Bowling

, et al. Sexual Relationships, Behaviors, and Experiences among Bisexual Men in Mumbai, India. Int J Sex Health 2016; 28(1): 70–84.

24.

McCree

Oster

Jeffries

WLt

, et al. HIV acquisition and transmission among men who have sex with men and women: What we know and how to prevent it. Prev Med 2017; 100: 132–134.

25.

Zheng

Jiang

, et al. Population HIV transmission risk for serodiscordant couples in Guangxi, Southern China: A cohort study. Medicine 2018; 97(36): e12077.

26.

Kritsanavarin

Bloss

Manopaiboon

, et al. HIV incidence among men who have sex with men and transgender women in four provinces in Thailand. Int J STD AIDS 2020; 31(12): 1154–1160.

27.

Pattanasin

van Griensven

Mock

, et al. Recent declines in HIV infections at Silom Community Clinic Bangkok, Thailand corresponding to HIV prevention scale up: An open cohort assessment 2005-2018. Int J Infect Dis 2020; 99: 131–137.

28.

Jose

JEd

Sakboonyarat

Mungthin

, et al. Rising prevalence of HIV infection and associated risk factors among young Thai Men in 2018. Scientific Rep 2021; 11(1): 7796.

29.

Leeyaphan

Jiamton

Chanyachailert

, et al. Treatment outcomes and loss to follow-up rate of male patients with gonococcal and nongonococcal urethritis who attended the sexually transmitted disease clinic: An 8-year retrospective study. Indian J Sex Transm Dis AIDS 2017; 38(1): 37–42.

30.

Leeyaphan

Jiamton

Prasertworonun

, et al. Clinical and epidemiological characteristics of patients with syphilis: 5 year-case study from Thailand. J Med Assoc Thai 2014; 97(9): 963–968.

31.

Jiamton

Leeyaphan

Maneeprasopchoke

, et al. Prevalence and clinical manifestations of male patients with anogenital warts attending a sexually transmitted disease clinic prior hpv vaccine recommendation. Southeast Asian J Trop Med Public Health 2014; 45(6): 1337–1343.

32.

AIDS committee National . Thailand AIDS Reoponse Progress Report 2017. [cited 2021 April, 25]. https://hivhub.ddc.moph.go.th/Download/Report/APR/2017/GARP2017%20eng%20Final.pdf

33.

Chanprasertpinyo

Rerkswattavorn

. Human papillomavirus (HPV) vaccine status and knowledge of students at a university in rural Thailand. Heliyon 2020; 6(8): e04625.

34.

Pattanasin

Griensven

Mock

, et al. AIDS Care. In: HIV and syphilis prevalence among transgender women and men who have sex with men. Bangkok: Silom Community Clinic, Thailand, 2017-2019, pp. 1–9.