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Journal of General - Procedural Dermatology & Venereology Journal of General - Procedural Dermatology & Venereology Indonesia

Indonesia

Volume 2

Number 2 Vol. 2, No. 2 (Dec 2017) Article 3

12-31-2017

Seroprevalence of syphilis and herpes simplex virus type 2 and its Seroprevalence of syphilis and herpes simplex virus type 2 and its association with sexual behaviour factors (a cross-sectional study association with sexual behaviour factors (a cross-sectional study among men who have sex with men in Manado, Indonesia)

among men who have sex with men in Manado, Indonesia)

Nurdjanah J. Niode

Department of Dermatology and Venereology, Faculty of Medicine, University of Sam Ratulangi/RD Kandou Hospital, Manado, Indonesia.

Hendra Minarto

Andravita F. Mitaart

Grace M. Kapantow

Renate T. Kandou

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Part of the Dermatology Commons, Integumentary System Commons, and the Skin and Connective Tissue Diseases Commons

Recommended Citation Recommended Citation

Niode, Nurdjanah J.; Minarto, Hendra; Mitaart, Andravita F.; Kapantow, Grace M.; and Kandou, Renate T.

(2017) "Seroprevalence of syphilis and herpes simplex virus type 2 and its association with sexual behaviour factors (a cross-sectional study among men who have sex with men in Manado, Indonesia),"

Journal of General - Procedural Dermatology & Venereology Indonesia: Vol. 2: No. 2, Article 3.

DOI: 10.19100/jdvi.v2i2.53

Available at: https://scholarhub.ui.ac.id/jdvi/vol2/iss2/3

This Article is brought to you for free and open access by UI Scholars Hub. It has been accepted for inclusion in Journal of General - Procedural Dermatology & Venereology Indonesia by an authorized editor of UI Scholars Hub.

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Original article

Seroprevalence of syphilis and herpes simplex virus type 2 and its association with sexual behavior factors

(a cross-sectional study among men who have sex with men in Manado, Indonesia)

Nurdjannah J. Niode, Hendra Minarto, Andravita F. Mitaart,

Grace M. Kapantow, Renate T. Kandou

E-mail: [email protected]

Abstract

Aims: This study investigated the seroprevalence and sexual risk behavior factors associated with syphilis and herpes simplex virus type 2 (HSV-2) among men who have sex with men (MSM), in Manado, Indonesia.

Methods: Serum samples and questionnaires regarding their socio-demographic and sexual behavior were collected from 60 MSM in Manado. Samples were screened for anti-HSV-2 IgG for herpes, the Venereal Disease Research Laboratory (VDRL) and the Treponema Pallidum Haemagglutination (TPHA) test for

syphilis. A cross sectional method was used in this study.

Results: Of 60 MSM (median age was 20 years), 35% had homosexual orientation and 65% had bisexual orientation. First sexual intercourse of most participants (48.3%) within 16 to 18 years old. In the last 12 months, most participants (55%) had only one male sex partner. There were 63.3% and 16.7% participants performed oral and anal intercourse. About 23.3% participants used condom consistently, but only 35.7% used compatible lubricant. Seropositivity of VDRL and TPHA was detected in 5% participants and anti-HSV-2 IgG in 23.3% participants. The positive serology test for syphilis was associated with sexual intercourse mode (p=

0.001). Significant association was found between anti-HSV-2 IgG seropositivity and condom-use behavior (p=0,028).

Conclusions: The study demonstrated 5% and 23.3% positivity of serology test for syphilis and anti-HSV-2 IgG respectively. Seropositivity of syphilis was correlated with oral and anal intercourse while HSV-2 with no condom-use behavior among MSM in Manado, Indonesia.

Keywords: syphilis, herpes simplex virus type 2, men who have sex with men, sexual behavior, Manado

Background

Sexually transmitted infections (STIs) are a major public health issue causing huge health, social, and economic burden on families and communities worldwide.¹Men who have sex with men (MSM) are considered as a high-risk group for STIs. They are disproportionately affected by STIs and Human immunodeficiency virus (HIV) infection.²The risk for infection remains high among them and it can be associated with the epidemic of STIs and HIV infection, stigma and discrimination, high-risk practices such as promiscuity, unprotected sex or inconsistent condom-use, and sex at juvenile age.³

Genital ulcers due to syphilis and Herpes simplex virus type 2 (HSV-2) need more attention since both infections are associated with an increased risk of acquiring HIV in addition to cause significant morbidity.⁴ Asymptomatic cases in syphilis and HSV-2 may become important co-factor for spreading infection.⁵ High prevalence of syphilis was found among MSM population globally.

Increasing number of new cases were reported in many parts of the world, especially among HIV- infected MSM.⁶Concurrently, there has been an important increase in the prevalence of viral infections around the world, including HSV-2. It is

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known now that HSV-2 is the main cause of genital ulcers in developing countries.¹ High HSV-2 seroprevalence has been well documented among MSM population in developed countries. On the other hand, HSV-2 seroprevalence data from developing countries has been generated primarily focusing on non-MSM risk groups, such as female sex workers and STI clinic attendees. Specifically, data is limited regarding the seroprevalence of HSV-2 among MSM communities.⁷In Indonesia, syphilis prevalence in MSM increased from 4% to 13% during year 2007-2011.⁸ Prevalence of HSV- 2 infections among MSM in Jakarta was 23,7%

(2012).⁹

Identification of asymptomatic case in the vulnerable group is important to control the spread of infection.¹⁰ The non-treponema Venereal Disease Research Laboratory (VDRL) test and the Treponema Pallidum Haemagglutination (TPHA) test are often used to screen asymptomatic cases.

Both tests are effective and efficient with high sensitivity and specificity against Treponema pallidum.¹¹ Serologic HSV type-specific glycoprotein G (IgG) test can be used to detect asymptomatic case of genital herpes. The sensitivities of these glycoprotein G type-specific tests for the detection of HSV-2 antibody vary from 80-98%.¹²

Manado, the capital of North Sulawesi, is located on the northern tip of Sulawesi island. The city had 423.357 people in population per 2014. It is the second largest city in Sulawesi Island. Beside tourism, it also acts as a hub city in the Asia Pacific region.¹³To our knowledge, there is no data available on seropositivity of syphilis and HSV-2 nor articulating the association of these two pathogens with sexual risk behavior factors among MSM in Manado. We conducted a cross sectional study in Manado to determine the seropositivity of syphilis and HSV-2 among MSM and to establish the associated sexual risk behavior factors.

Methods

Study population

A total of 60 MSM in Manado, Indonesia were enrolled in this study from March to April 2015.

Inclusion criteria was men 18 years old or more who reported engaging in sex with men in the previous year. Exclusion criteria were as follows (1) refused to be part of the study, (2) past history of receiving blood transfusion, (3) past history of intravenous drug abuse.

Recruitment was performed in collaboration with The Disease Control and Environmental Health

Department, Manado Health Authorities. Their outreach workers had given education and health promotion to MSM and had established rapport with them. Participants were approached via their peer leader, who then contacted other participants in their workplaces or at social venues including coffee houses and parks to participate in the study.

This study was carried out at a primary health centre in Karame subdistrict, Manado. Written informed consent was provided for the participants prior to data collection. All participants completed the questionnaire in private interview rooms. The information collected in the standardized questionnaire included socio-demographic characteristics; sexual orientation, age at first sexual intercourse, number of male sex partner(s), condom use during sexual intercourse with male partner(s), and water-based lubricant use with condom during anal intercourse. After obtaining the procedures, participants were asked to provide a blood sample.

Specimen collection

Venous blood samples were collected from each individual. These blood samples were centrifuged to produce serum. Each serum was collected into a 3 cc screw top plastic tube. They were kept in storage box (4^oC) before transported to the main laboratory.

Laboratory methods

Syphilis test was performed using two serological assays: the VDRL test (Akurat Intan Madya VDRL test®) and the TPHA test (Akurat Intan Madya TPHA test®). Using both assays, active syphilis was defined with reactive VDRL test and reactive TPHA test. Enzyme-linked immunosorbent assay (ELISA) test was performed to detect Immunoglobulin G (IgG) class antibodies against HSV-2 by using ELISA analyser (Euro Immune Analyser®). HSV- 2 seropositivity was defined by a positive ELISA with index ratio > 1.1, borderline with index ratio 0.8 - 1.1and negative with index ratio < 0.8.

Treatment

The results were available around 3 days after recruitment. Participants with positive results of serologic test for syphilis and anti-HSV-2 IgG were counselled. Then offered free treatment for syphilis (benzathine penicillin G 2.4 million units, intramuscularly once weekly for three consecutive weeks or doxycycline 100 mg twice daily orally for 30 days in case of participant has penicillin allergy) and encouraged to inform all partners to undergo examinations at the nearest health center if possible.

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Data analysis

Bivariate analyses were used to asses the association of MSM sexual behavior variables with syphilis and HSV-2 (P<0.05). The ethic approval was granted by the Human Research Ethics Committee of Kandou General Hospital, Faculty of Medicine, University of Sam Ratulangi, Manado and permission from Manado health authorities.

Results

Sociodemographic data

A total of 60 eligible participants completed the survey. Data on socio-demographic characteristic of subjects in this study can be seen in table 1. The age of participants was ranged from 18 to 63 years with median age of 20 years. Fifty-one point seven percent of participants were under 21 years of age.

More than 60% of respondents had senior high school education. Seventy-five percent of participants were single, 23.3% were married, and only 1 participant (1.7%) was divorced. Nearly 42%

of the participants were unemployed and 58.3%

had various occupations such as motorcycle taxi driver (16.7%), merchant (13.3%), clerk (10.0%), driver (6.7%), labor (5.0%), teacher (3.3%), and hairdresser (3.3%).

Tables

Sexual behavior

Data on sexual behavior characteristic of subjects can be seen in table 2. Of the 60 men, 35% had homosexual orientation and 65% had bisexual orientation. Most of participants (48.3%) reported that they were in 16 to 18 years of age when started their first sexual intercourse.

Fifty-five percent of participants had only one male sex partners in last 12 months. Only one participant had 10 male sex partners in last 12 months (1.7%).

There were 43.3% participants who had 2 to 9 male sex partners in last 12 months. More than 60%

exclusively engaged in oral intercourse, 16.7%

exclusively engaged in anal intercourse, and 20%

engaged in both oral and anal intercourse. About 23.3% participants reported always using condoms during sexual intercourse with male partner(s), while 21.7% reported sometimes; 55% reported never using condoms. Of 14 participants who consistently used condom during intercourse, there was only 35.7% men who used compatible lubricant for the correct functioning of condoms, while 64.3% reported did not use lubricant.

Table 1. Socio-demographic characteristics of 60 men who have sex with men (MSM) in Manado, in 2015

Characteristic Number % Age group (years)

< 21 21 – 30 > 30

31 13 16

51.7 21.7 26.6 Educational level

Junior high school or lower

Senior high school College or higher

17 38 5

28.3 63.3 8.3 Marital status

Single Married Divorced

45 14 1

75.0 23.3 1.7

Occupation

Unemployed 25 41.7

Motorcycle

taxi driver 10 16.7

Merchant 8 13.3

Clerk 6 10.0

Driver 4 6.7

Labor 3 5.0

Teacher 2 3.3

Hairdresser 2 3.3

Prevalence of syphilis and HSV-2 serology Table 3 showed the seroprevalence of syphilis and HSV-2. Serologic test for syphilis (VDRL and TPHA) was detected in 5% of MSM, while anti- HSV-2 IgG was detected in 23.3%.

Sexual behavior factors associated with syphilis and HSV type 2 serology

Results of sexual behavior association (p<0.05) with syphilis serology are shown in table 4. No significant association was found among sexual orientation, age at the first sexual intercourse, number of male sex partners in the last 12 months, condom use during sexual intercourse, and water- based lubricant use with condom during anal intercourse with the positivity of syphilis serology.

The positive serology test of syphilis was associated with sexual practices with male

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partner(s) (p= 0.001), MSM with positive serology test performed both oral and anal sex.

Table 2. Sexual behavior characteristics of 60 men who have sex with men in Manado, in 2015

Characteristic Number % Sexual orientation

Homosexual

Bisexual 21

39 35

65 Age at first sexual

intercourse <12 12 – 15 16 – 18 >18

1 24 29 6

1.7 40 48.3 10 Number of male sex

partners in the last 12 months

1 2 – 9 ≥ 10

33 26 1

55 43.3 1.7 Sexual practices with

male partner(s)

Oral sex 38 63.3

Anal sex 10 16.7

Oral and anal

sex 12 20 Condom-use during

sexual intercourse with male partner(s)

Never 33 55

Always 14 23.3

Sometimes Water-based lubricant use with condom

during anal

intercourse^*

13 21.7

Yes

No 5/14

9/14 35.7

64.3

*of 14 participants who used condom consistently during intercourse

Table 3. Prevalence of syphilis and herpes simplex type 2 serology among 60 men who have sex with men in Manado, in 2015

Test Results N %

VDRL and TPHA

Reactive 3 5

Non reactive Anti-HSV-2 IgG Positive Borderline Negative

57 14 4 42

95 23.3

6.7 70

Table 4 also showed 4 and 10 MSM with positive anti-HSV-2 IgG were homosexual and bisexual respectively. Most cases were found in MSM who had their first sexual intercourse at aged 12-15 years old and 16-18 years old. There was a higher number of positive IgG test in MSM who had less than 10 sexual partners in the last 12 months compared to those who had more than 10 sexual partners. Participants who engaged oral sex had higher number of IgG positive serology test.

Significant association was found between condom use behavior with positive anti-HSV-2 IgG serology test (p=0,028). Positive HSV-2 IgG was also found in MSM who never used water-based lubricants.

Discussion

To our knowledge, this is the first report of syphilis and HSV-2 seroprevalence and the association of these two pathogens with sexual risk behavior factors among MSM in Manado, North Sulawesi Province. This study showed the seropositivity of VDRL-TPHA and anti-HSV-2 IgG among MSM in Manado. There was no previous data available in Manado so that the comparison of this result could not be done. In Bangkok, study by Ananworanich et al¹⁴ in 2005 showed similar positive syphilis serology result of 5% among MSM. On the other side, study by Pisani et al¹⁵ in 2005 in Jakarta showed lower rate of 1.1% and 2.0% among MSM and male sex workers (MSW) respectively. Wang et al¹⁶ in Guangxi China in 2014 showed the increasing of syphilis prevalence from 5.1% in 2008 to 8.4% in 2012. Differences in findings from these studies may not be comparable as there were differences in the study methods. The participants of our study were all MSM, while in study by Pisani, the subjects were differentiated into MSM and MSW. Study by Wang was able to show yearly data comparison during his 5-year study, in contrary to our study which was only

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conducted during March to April 2015. Our finding on positive anti-HSV-2 IgG rate of 23.3% was similar to Lubis et al⁸ in 2012 in Jakarta with 23.7%

positive rate and Hill C. et al¹⁷ in 2003 in the United Kingdom with 22.75%.

Although the majority of participants were bisexual, there was no significant association among seropositivity of syphilis and HSV-2 and they sexual orientation. This might be due to participants who have bisexual orientation engage in only insertive intercourse with female partner while the link between receptive intercourse and STIs included syphilis and herpes prevalence is well established.¹⁸

Despite there was no association between the seropositivity of these STIs and the age of first sexual intercourse, subjects who had positive result of both VDRL-TPHA and anti-HSV-2 IgG showed their first sexual intercourse in young age.

The early initiation of sexual intercourse has been correlated to the increased risk of STIs, high-risk sexual partners, and sexual practices under the influence of alcohol or drugs. Early age of sexual debut is one of the risk factor of HSV-2. Similar to this STI, young age is also the risk factor of syphilis.^19,20

Promiscuity increased the risk of STIs transmission. Positive syphilis serology was found among subjects who had more than one sexual partners, while positive anti-HSV-2 IgG was found both in subjects who had only one partner and more than one partner. The finding however was not significant statistically. In theory, the more sexual partners, the higher the risk of being infected, but in reality even when only exposed to one sex partner, if that partner is infected then transmission of the disease may occur.

Significant relationship was observed between mode of sexual intercourse and positive syphilis serology (p=0.001). Positive syphilis serology of VDRL and TPHA were found among MSM who had both oral and anal sex. Meanwhile anti-HSV-2 IgG positivity was most among MSM engaged oral sex, anal sex, and both of it respectively. The major transmission of syphilis comprised of unprotected anal and oral intercourse.²¹ The most frequently transmission of HSV infections occurs through close contact with an infected person who is shedding virus at several sites such as mucosal surface, in genital secretions, and oral secretions.²² According to the literature, vulnerable thin lining of rectum was subject to tear, allowing micro lesion to develop, thus serving as port d entrée for infection.

Large surface area of rectum and colon facilitated

higher microbial penetration. Oral sex was another preferred type of sexual intercourse among MSM.

Despite having lower risk of transmission for STI, oral sex with in-mouth ejaculation may increase the risk of transmission. ²¹

MSM who both never use a condom and use condom inconsistently showed reactive syphilis serology. A similar result was found among MSM with incompatible lubricant (such as oil-based lubricant) use. These finding however were insignificant. In contrast, no condom-use was significantly associated with positive anti-HSV-2 IgG (p=0.028). Condom played a major role in the prevention of STI and HIV transmission. World Health Organization (WHO) strongly recommended the use of condom consistently during anal intercourse among MSM to prevent STI and HIV transmission.^2,6 While water-based lubricant use is a key for the correct functioning of condoms during anal sex.²In Indonesia, prevention of sexual transmission was conducted through condom promotion and STIs services provision.

The promotion of condom-use has reached the vulnerable population included MSM. There were more than 15.000 unit of condom outlets throughout Indonesia with more than 20 million condoms distributed each year for free as well as commercial.²³Condom-use must be asserted with compatible lubricant. Lubricant improve the effectiveness of condoms in penetrative sex, and anal sex particularly. It can reduce the risk of condom tear, malfunction, and the inconvenience during sexual intercourse. Generous amount of lubricant use was suggested during anal intercourse. Water-based lubricant does not deteriorate latex condom, in contrary, oil-based lubricant will damage it.^2,6

Conclusions

This study demonstrated 5% and 23.3% positivity of serology test for syphilis and anti-HSV-2 IgG respectively. Seropositivity of syphilis was correlated with oral and anal intercourse while HSV-2 with no condom-use behavior among MSM in Manado, Indonesia.

(This paper had been presented as a poster in Regional Conference of Dermatology, Singapore, April 2016)

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Table 4. Associations of sexual behavior with serology test of syphilis and Herpes Simplex Type 2 among 60 men who have sex with men in Manado, in 2015

Characteristics VDRL and TPHA P anti-HSV-2 IgG P

Reactive Non

reactive Borderline Negative Positive Sexual orientation

Homosexual Bisexual

1

2 20

37 0.722^# 0

4

17 25

4 10

0,113^Č

Age at first sexual intercourse

<12 12 – 15 16 – 18 >18

0 1 2 0

1 23 27 6

0.222^$

0 0 3 1

1 17 20 4

0 7 6 1

0,450^$

Number of male sex partners in the last 12 months

1 2 – 9 ≥ 10

0 3 0

33 23 1

0.054^$ 2 2 0

25 17 0

6 7 1

0,087^$

Sexual practices with male partner(s)

Oral sex Anal sex

Oral and anal sex

0 0 3

38 10

9 0,001^Č

3 1 0

26 6 10

9 3 2

0,374^Č

Condom-use during sexual intercourse with male partner(s)

Never Always Sometimes

1 0 2

32 14 3

0,069^Č 4

0 0

18 13 11

11 1 2

0,028^Č

Water-based lubricant use on condom during anal intercourse^*

Yes No

0

3 5

6 0,231^# 0

0

4 9

0 1

0,643^#

*= of 14 participants who used condom consistently during intercourse

$= Spearman’s correlation test, Č= X²test

#= Fisher exact test

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