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Sexually Transmitted Infection Services as a Component of HIV Care: Findings of a Demonstration Project Among HIV-Infected Women in Thailand

Sirivongrangson, Pachara MD*; Bollen, Liesbeth J. M. MD, PhD†§; Chaovavanich, Achara MD; Suksripanich, Orapin; Jirarojwat, Naiyana*; Virapat, Pongsri; Charoenwatanachokchai, Angkana MD*; Lokpichat, Somchai*; Pobkeeree, Vallerut; Chantharojwong, Nartlada; Supawitkul, Somsak; Tappero, Jordan W. MD, MPH†§; Levine, William C. MD, MSc†§

JAIDS Journal of Acquired Immune Deficiency Syndromes: April 15th, 2006 - Volume 41 - Issue 5 - p 671-674
doi: 10.1097/
Epidemiology and Social Science

Objectives: As Thailand scales up its antiretroviral treatment program, the role of sexually transmitted infection (STI) services to prevent HIV'transmission has not been addressed. We provided STI services for HIV-infected women as a component of HIV care and assessed STI prevalence and risk behaviors.

Methods: HIV-infected women attending an infectious disease clinic and an STI clinic in Bangkok were screened for the presence of genital ulcers by visual inspection, for gonorrhea and chlamydial infection by polymerase chain reaction, for trichomoniasis by wet mount, and for syphilis by serology. Women were asked about sexual risk behavior and use of antiretroviral treatment. Risk-reduction counseling, condoms, and STI treatment were provided.

Results: Two-hundred ten HIV-infected women at an infectious disease clinic (n = 150) and an STI clinic (n = 60) received STI services from July 2003 through February 2004. The prevalence for any STI was 8.0% at the infectious disease clinic and 30.0% at the STI clinic (P < 0.01). Of the 116 (55.2%) sexually active women, 42 (36.2%) reported sex without a condom during the last 3 months. Women receiving antiretroviral treatment reported condom use during last sex more often compared with those not receiving antiretroviral treatment (82.2% vs. 58.8%; P = 0.03).

Conclusion: STIs and sexual risk behavior were common among these HIV-infected women, and STI services for HIV-infected persons have been expanded to more clinics in Thailand. Further analysis of HIV transmission risk is necessary for developing a national strategy for prevention of HIV transmission among HIV-infected persons.

From the *Sexually Transmitted Infection (STI) Division, Bureau of AIDS, Tuberculosis (TB), and STIs, Thai Ministry of Public Health (MOPH), Bangkok, Thailand; §Thailand MOPH-US (CDC) Collaboration, Nonthaburi, Thailand; ‡Bamrasnaradura Institute, MOPH, Nonthaburi, Thailand; and †Global AIDS Program, CDC, Atlanta, GA.

Received for publication June 1, 2005: accepted October 21, 2005.

Presented in part at the XV International AIDS Conference, July 11-16, 2004, Bangkok, Thailand [abstract ThPeC7390].

Supported through a cooperative agreement between the Thai MOPH and the US CDC Global AIDS Program and, in part, by an appointment to the Research Participation Program at the CDC, National Center for HIV, STD, and TB Prevention, administered by the Oak Ridge Institute for Science and Education through an interagency agreement between the US Department of Energy and the CDC.

Reprints: Liesbeth J. M. Bollen, Thailand MOPH-CDC Collaboration, P.O. Box 139, Nonthaburi 11000, Thailand (e-mail:

In recent years, the Thai Ministry of Public Health (MOPH) has been greatly expanding access to antiretroviral treatment. Although antiretroviral treatment may decrease the risk of HIV transmission by reducing HIV shedding in genital secretions, sexual activity and risk behavior might increase.1,2 Therefore, antiretroviral programs have been encouraged to include HIV transmission prevention as an integral component.3-5 Few data on HIV transmission risk are available from resource-limited settings, where it is likely to be challenging to integrate risk reduction counseling into HIV care.

Sexually transmitted infections (STIs) have been associated with HIV infectiousness6 and may substantially increase HIV transmission. It has been estimated that a quarter of HIV transmissions from persons who are dually infected with HIV and STI to HIV-uninfected persons may be averted through STI treatment, independent of behavior change.7 Routine screening for STIs is recommended for sexually active HIV-infected persons by the US Centers for Disease Control and Prevention (CDC) to decrease HIV transmission.8 In Thailand, few HIV-infected women are currently receiving STI services as part of their HIV care.

We provided enhanced STI services for HIV-infected women at two clinics in Bangkok as a component of routine HIV care. In addition, the prevalence of different STIs and risk behaviors was assessed to explore the need for continuing and expanding these services.

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Project Design

HIV-infected women seeking care at 2 clinics of the Thai MOPH (an infectious disease clinic at Bamrasnaradura Institute in Nonthaburi and an STI clinic in central Bangkok at Bangrak Hospital) were offered improved STI services. Both clinics offer health care under the Royal Thai Government's universal health care program. The project started in July 2003, and data were collected through February 2004 to evaluate the program. A standardized data form was used to collect information on sexual behavior and STI symptoms. Women consenting to STI services underwent a gynecologic examination, were screened for the presence of genital ulcers by visual inspection, and samples were obtained for STI testing. STI treatment was conducted according to the guidelines of the STI Division of the Thai MOPH and was provided free of charge, along with condoms. Women attending the STI clinic received an HIV test to confirm their HIV status and were offered a CD4 cell test as part of this demonstration project. Eligible women were referred for opportunistic infection prophylaxis and antiretroviral treatment according to the national guidelines for HIV care (CD4 cell count less than 200 cells/mm3 or clinical AIDS).9

This project was approved by the Thai MOPH and the US CDC as a programmatic activity that did not require institutional review board approval.

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Laboratory Evaluation

First-void urine was collected for the detection of Chlamydia trachomatis and Neisseria gonorrhoeae by polymerase chain reaction Amplicor analysis (Roche Diagnostic System, Basel, Switzerland). Vaginal swab specimens were collected for saline wet preparations for the detection of Trichomonas vaginalis by light microscopy. Serum samples were tested for syphilis using Venereal Disease Research Laboratory (VDRL) Slide Test as a screening test. The Treponema pallidum hemagglutination assay (TPHA; Fuji-rebio, Japan) was performed as a confirmatory test.

HIV infection status was confirmed by Murex HIV1-2 enzyme-linked immunosorbent assay (ELISA; Murex Biotech, Dartford, UK). CD4 cell testing was performed using a FACScan flow cytometer (Becton Dickinson Immunocytometry Systems, San Jose, CA).

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Data Analysis

For purposes of analysis, women were considered to have an STI if they had clinician-confirmed genital ulcers or positive test results indicating chlamydial infection, gonorrhea, trichomoniasis, or syphilis.

Data were analyzed using Epi Info 2000, version 3.2 (February 4, 2004). P values were assessed by the χ2 test, and values of less than 0.05 were considered statistically significant. Significant factors from univariate analyses were subsequently included in multivariate models using logistic regression.

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From July 2003 through February 2004, 272 consecutive HIV-infected women were offered STI services. More HIV-infected women attended the infectious disease clinic (n = 210) than the STI clinic (n = 62). Time constraints or menstruation was a common reason why some women declined to be screened. A total of 210 women (77.2%) consented to screening, 150 at the infectious disease clinic and 60 at the STI clinic. Women entered the project at the infectious disease clinic when they made a visit for their HIV care. Women entered the project at the STI clinic when they sought care for STI-related symptoms (n = 19), for follow-up of a previous visit (n = 8), for a routine checkup if they were engaged in sex work (n = 11), or because they had heard about the project (n = 22). All women were confirmed to be HIV-positive. Table 1 shows characteristics of the HIV-infected women by clinic site.



Among the 210 women, 30 (14.3%) had 1 or more STIs, including genital ulcer (n =12), chlamydial infection (n = 7), gonorrhea (n = 4), trichomoniasis (n = 1) and syphilis (n = 9). The STI prevalence was lower among women at the infectious disease clinic than at the STI clinic (8.0% vs. 30.0%; P < 0.01) and was not related to age (Table 2). A higher proportion of women with CD4 cell counts lower than 200 cells/mm3 had genital ulcers compared with women with CD4 cell counts of 200 cells/mm3 or higher (11.1% vs. 1.7%; P = 0.004).



Only history of sex work remained a statistically significant risk factor for STIs in multivariate analysis (P = 0.02), after controlling for the variables listed in Table 2. After excluding the 35 women with a history of sex work from the model, women attending the STI clinic (n = 35) and those with CD4 cell counts lower than 200 cells/mm3 (n = 76) remained at higher risk for STIs compared with women attending the infectious disease clinic and those with CD4 cell counts higher than 200 cells/mm3 (22.9% vs. 6.5%; P = 0.004 and 15.8% vs. 5.1%; P = 0.02, respectively).

A total of 116 (55.2%) women reported that they had been sexually active in the last 3 months, of whom 42 (36.2%) had not used a condom during sex at least once during that period. One hundred thirteen (97.4%) women had a steady sex partner. Of these women, 64 (56.6%) reported that they knew the HIV status of their sex partner, of whom 20 (31.3%) reported him to be HIV-negative. Bivariate analysis of factors associated with condom use during last sex with a steady sex partner showed that antiretroviral treatment was significantly associated with increased condom use (Table 3). This association remained significant after controlling for clinic site (P = 0.03).



CD4 cell testing was provided for all 60 women attending the STI clinic and was the first CD4 cell test ever for 48 (80.0%) of these women. Of the 60 women, 26 (43.3%) had CD4 cell counts lower than 200 cells/mm3; 17 had not previously been prescribed prophylaxis for opportunistic infections, and 21 were not receiving antiretroviral treatment. Referral for HIV care resulted in the start of opportunistic infection prophylaxis and antiretroviral treatment in all 26 eligible HIV-infected women.

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Public health experts unanimously emphasize the importance of preventing HIV transmission while scaling up access to antiretroviral treatment. These prevention efforts should include screening and treatment of STIs, distribution of free condoms, risk-reduction counseling, assistance to HIV-infected persons in notifying partners of their HIV infection, and partner HIV testing.3

Almost 10% of women attending the infectious disease clinic had an STI, and it seems appropriate to screen these women as part of their initial HIV evaluation, with intervals depending on risk factors. As expected, STIs were common among HIV-infected women attending the STI clinic in our project, confirming the need for screening these women regularly with sensitive diagnostic tests. Although few clinics may have the capacity and resources to screen women for gonorrhea and chlamydial infections using sensitive tests, screening for the presence of genital ulcers by visual inspection should be possible in all clinics.

We observed a correlation between CD4 cell counts and genital ulcers, suggesting that these may have been opportunistic infections with herpes simplex virus type 2. Recent studies have shown herpes simplex virus type 2 to be the predominant cause of genital ulcers in Thailand, particularly among HIV-infected people.10 In addition, a recent review discussed the role of herpes simplex infection in HIV transmission and the possibility of decreasing HIV infectiousness by acyclovir treatment.11 Acyclovir treatment should be considered for HIV-infected persons with genital ulcers in Thailand to improve quality of care and to prevent herpes simplex virus type 2 and HIV transmission.

Unprotected sex was common among the HIV-infected women at these clinics as well as among women who did not know the HIV status of their partner or reported him to be HIV-negative. This emphasizes the need for strengthening prevention of HIV transmission among couples. In addition, a high proportion of women did not know the HIV status of their partner, indicating the importance of promoting partner HIV testing in Thailand.

This cross-sectional assessment showed that women receiving antiretroviral treatment reported more condom use than those not on treatment. It is possible that persons with less risk behavior seek HIV care more often than those with more risk behavior or that counseling messages during HIV care may have resulted in less risk behavior. In contrast, antiretroviral treatment may actually increase risk behavior as has been observed in the United States among men who have sex with men; men receiving antiretroviral treatment were more likely to develop an STI compared with those not receiving treatment.12 In contrast, the use of antiretroviral treatment was associated with a decreased prevalence of self-reported sexual risk behavior in a study among persons attending HIV clinics in California.13 Nevertheless, the occurrence of STIs and risk behavior among persons receiving antiretroviral treatment should be monitored to evaluate the impact of treatment on risk for HIV transmission.

Based on findings from this project, the Thai MOPH has expanded STI services for HIV-infected men and women to additional facilities. Data on STIs and risk behaviors are to be routinely collected in the context of antiretroviral treatment and used to plan a national strategy for prevention of HIV transmission among HIV-infected persons.

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HIV infection; sexually transmitted infections; prevention; Thailand

© 2006 Lippincott Williams & Wilkins, Inc.