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Epidemiology
Maximising the potential of voluntary counselling and testing for HIV: sexually transmitted infections and HIV epidemiology in a population testing for HIV and its implications for practice
  1. Hsiu Wu1,
  2. Pei-Ying Wu2,
  3. Shu-Ying Li1,
  4. Sui-Yuan Chang3,4,
  5. Wen-Chun Liu2,
  6. Cheng-Hsin Wu2,
  7. Yi-Cheng Lo2,
  8. Chia-Yin Hsieh2,
  9. Hsin-Yun Sun2,
  10. Chien-Ching Hung2
  1. 1Centers for Disease Control, Taipei, Taiwan
  2. 2Department of Internal Medicine, National Taiwan University Hospital and National Taiwan University College of Medicine, Taipei, Taiwan
  3. 3Department of Laboratory Medicine, National Taiwan University Hospital and National Taiwan University College of Medicine, Taipei, Taiwan
  4. 4Department of Clinical Laboratory Sciences and Medical Biotechnology, National Taiwan University College of Medicine, Taipei, Taiwan
  1. Correspondence to Dr Chien-Ching Hung, Department of Internal Medicine, National Taiwan University Hospital, 7 Chung-Shan South Road, Taipei, Taiwan; hcc0401{at}ntu.edu.tw

Abstract

Objectives This study aimed to describe the epidemiology of HIV infection and sexually transmitted infections (STIs) among persons who attended voluntary counselling and testing (VCT) service for HIV and to assess whether the VCT programme reached the right population at risk in Taiwan.

Methods From 2006 to 2010, questionnaire interview, integrated pretesting and post-testing counselling, followed by serological tests for HIV, Treponema pallidum and Entamoeba histolytica were performed for all VCT clients; additional tests for Chlamydia trachomatis and Neisseria gonorrhoeae using PCR assays of urine specimens were provided when the assays became available in two periods.

Results During the study period, 10 198 VCT attendances occurred in 6863 clients, in whom 1685 (24.6%) had re-attendances. Male clients, men who have sex with men and clients with one-night stand and casual sexual partners were more likely to re-attend VCT service in the next 12 months. The overall STI prevalence was 3.5% for HIV infection, 2.2% syphilis, 1.0% amoebiasis, 4.7% chlamydia and 0.7% gonorrhoea. In logistic regression model, men who have sex with men were consistently independently associated with HIV infection, syphilis and amoebiasis. Among the repeaters, the incidence rate of HIV infection and syphilis was 3.4 and 1.6 per 100 person-years of follow-up, respectively. In Cox regression analysis, clients who used illicit non-injection recreational drugs and who practiced unprotected anal sex were at significantly higher risk of acquiring HIV infection and syphilis.

Conclusions With higher rates of re-attendances and STIs, the VCT programme reached the population most at risk for HIV and STIs compared with other screening programmes in Taiwan. The potential of VCT programme can be maximised in the prevention and control of HIV infection and STIs by providing tests for more STIs and counselling to avoid use of recreational drugs and to promote safe sex.

  • Sexually transmitted infection
  • epidemiology
  • HIV
  • syphilis
  • amoebiasis
  • chlamydia
  • gonorrhoea
  • voluntary counselling and testing
  • Taiwan
  • antibiotic resistance
  • Chlamydia trachomatis
  • Neisseria gonorrhoea
  • molecular epidemiology
  • diagnosis
  • hepatitis B
  • HIV
  • HIV clinical care

https://doi.org/10.1136/sextrans-2011-050354

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    Introduction

    Sexually transmitted infections (STIs) are important public health issues due to their complications and interdependence with HIV infection.1 ,2 Monitoring of prevalences of STIs and HIV infection and investigation of risk factors are crucial for the evaluation of the programmes that are implemented for prevention and control of STIs and HIV infection. In Taiwan, several free-of-charge screening programmes have been implemented for prevention and control of HIV infection. Anonymous voluntary counselling and testing (VCT) for HIV that was mostly performed in medical facilities was implemented in 1990 (HIV prevalence, 2.6% of 20 397 tests performed in 2010). HIV testing was provided to pregnant women attending antenatal care in an opt-out approach (HIV prevalence, 0.02% of 190 000 tests performed in 2010) and to patients with STIs (HIV prevalence, 0.48% of 41 633 tests in 2010). HIV testing was mandatory for blood donors (HIV prevalence, 0.05% of 1 681 570 tests in 2011), draftees (HIV prevalence, 0.06% of 126 614 tests in 2011) and injection drug users (IDUs) and non-IDUs in prisons or correctional facilities and IDUs enrolled in harm reduction programme (HIV prevalence, 0.07% of 107 086 tests in 2011).3

    HIV infection, syphilis, amoebiasis and gonorrhoea are reportable diseases in Taiwan.4 According to Taiwan Centers for Disease Control (CDC), 20 057 cases of HIV infection were diagnosed in Taiwanese from 1984 to 2010, with an estimated HIV prevalence of 0.17% among persons aged between 20 and 49 years.4 After control of the outbreak of HIV infection among IDUs that occurred between 2003 and 2007, men who have sex with men (MSM) have re-emerged as the most common risk factor for HIV infection in Taiwan.4 The proportion of MSM has increased to at least 71% of HIV infections detected in 2010.4 In 2010, 6482 cases of syphilis (diagnosed by elevated titres of rapid plasma reagin (RPR) or Venereal Disease Research Laboratory and positivity for Treponema pallidum haemagglutination (TPHA)) were reported to Taiwan CDC (annual incidence, 28.01 per 100 000 population).4 Between 2006 and 2009, a total of 408 cases of amoebiasis were confirmed in Taiwanese, in which 82 (20.1%) occurred in HIV-infected patients. The annual incidence of gonorrhoea was estimated 9.79 per 100 000 population, which increased after 2005, primarily in men.4 In this study, we aimed to describe the epidemiology of HIV infection and STIs among the VCT clients and to assess whether the VCT programme reached the right population at risk and its actual and potential role for diagnosis of HIV infection and STIs.

    Methods

    Procedure of VCT for HIV and STIs

    From 2006 to 2010, an anonymous self-administered questionnaire interview that is designed by Taiwan CDC was performed at the National Taiwan University Hospital, the largest hospital designated for HIV care, to obtain information on demographics, sexual practices, risk behaviours for HIV infection and STIs, history of STI, number of sexual partners, HIV serostatus of sexual partners, condom use and use of illicit injection drug and non-injection recreational drugs (questionnaire available as supplementary material). After completion of interview and a 30-min session of integrated pretesting and post-testing counselling, the clients provided 8–10 ml of blood specimens for serological tests for HIV infection, syphilis and amoebiasis. With availability of PCR assays from October 2008 to February 2009 and from March 2010 to December 2010, VCT clients were encouraged to provide a 10-ml first-catch urine specimen for the detection of Chlamydia trachomatis and Neisseria gonorrhoeae. Condoms and lubricant were distributed at the end of counselling session. The clients, each with a unique code for identification, would be informed of the results by cell phone when post-testing counselling was repeated on the phone. For those who tested positive for any of the five tests, they would be linked to clinical care for confirmation and treatment and follow-up and were encouraged to identify partners for referral for VCT service. For those who were negative for any of the tests, they would be encouraged to re-attend VCT service for follow-up. The study was approved by the research ethics committee of the hospital, and subjects gave written informed consent using identification codes for testing of amoebiasis, syphilis, gonorrhoea and chlamydia.

    Laboratory investigations

    Anti-HIV antibody was tested using particle agglutination and was confirmed with western blot. Reverse-transcription PCR assay was used for indeterminate western blot. Assays for RPR and TPHA were simultaneously performed for diagnosis of syphilis that was defined as a RPR titre ≧4 and positivity for TPHA. The incidence rates of syphilis and HIV infection were estimated by the occurrences of seroconversion for RPR and anti-HIV antibody, respectively, among repeaters with initial seronegative results. The indirect haemagglutination assay was used to detect anti-Entamoeba histolytica antibodies. Detection of C trachomatis and N gonorrhoeae were performed with the use of a multiplex real-time PCR assay on an automated system (test kits available as supplementary material for anti-HIV particle agglutination, Western blot, reverse-transcription PCR, RPR, anti- E. histolytica antibodies and multiplex real-time PCR assay).5

    Statistical analysis

    χ2 Test and Student t test were used to analyse categorical and continuous variables, respectively. Variables with p value <0.05 in univariate analysis were entered into a multiple logistic regression to calculate the OR and 95% CI. We estimated the re-attendance rate for different risk groups within the first year of the first visit. Survival analyses were used to describe the time of clients adhering to VCT service, and incidence rates and risk factors for acquiring HIV infection and syphilis among repeaters. Kaplan–Meier curves, log-rank tests and Cox-regression models were used to describe and test differences among risk groups in survival analysis. All p values were two-tailed. Analyses were performed using Statistical Package for the Social Sciences (SPSS) statistics V.17.0 software.

    Results

    From 1 April 2006 to 31 December 2010, 10 198 attendances of VCT service occurred in 6863 clients, in whom 1685 (24.6%) attended VCT service more than once. Of the 10 198 attendances, 8105 (79.5%) occurred in VCT clients who received three serological tests (HIV infection, syphilis and amoebiasis) and 2093 (20.5%) in clients who received all five tests. Of the 6863 clients, 5818 (84.8%) were male. Clients who were MSM accounted for 5924 (58.1%) of the attendances and heterosexual and IDU clients 4268 (41.9%).

    The prevalence of at least one of the three STIs tested (HIV infection, syphilis and amoebiasis) was 6.1% (494/8105), which was 10.7% (224/2093) when all five tests were included. The STIs detected included 361 (3.5%) cases of HIV infections, 228 (2.2%) syphilis, 104 (1.0%) amoebiasis, 98 (4.7%) chlamydia and 14 (0.7%) gonorrhoea (table 1). Clients with at least one STI other than HIV infection had a significantly higher prevalence of HIV infection than those without any other STIs (14.7% vs 3.0%, p<0.01).

    View this table:
    Table 1

    Results of univariate analysis to identify associated factors with HIV infection and other sexually transmitted infections

    Within the first year of the first visit, the re-attendance rate was 36.5% (916/2512) for MSM, 16.2% (579/2662) for heterosexuals and 6.7% (1/15) for IDUs. The median time between the first VCT attendance and the first re-attendance was 149 days (IQR, 91–284 days). In Cox regression analysis, clients who were male (HR 1.69, 95% CI 1.31 to 2.19) and MSM (HR 1.94, 95% CI 1.66 to 2.26) and who had one-night stand (HR 1.19, 95% CI 1.02 to 1.40) and casual sexual partners (HR 1.34, 95% CI 1.15 to 1.56) were more likely to re-attend our VCT service. The 1-year re-attendance rate among clients who reported unprotected anal sex and non-injection recreational drug use were 37.0% and 32.5%, respectively.

    In multivariate analysis (table 2), HIV infection was associated with older age (OR 1.04), MSM (OR 11.54), use of non-injection recreational drugs (OR 4.19), syphilis (OR 4.79) and amoebiasis (OR 3.53). Among the 1685 repeaters, 66 clients acquired HIV infection during 1930.7 person-years of follow-up (PYFU), resulting in an incidence rate of 3.4 per 100 PYFU. Of 66 incident cases of HIV infection, six occurred within 90 days after first testing. The median time from first VCT attendance to HIV infection was 429 days (IQR, 415). In Cox regression analysis, clients who used illicit non-injection recreational drugs (HR 3.84, 95% CI 2.11 to 6.97) and who practiced unprotected anal sex (HR 2.69, 95% CI 1.34 to 5.41) were at a higher risk of acquiring HIV infection during the follow-up.

    View this table:
    Table 2

    Results of multivariate analysis to identify associated factors with HIV infection and other sexually transmitted infections*

    Syphilis was associated with MSM (OR 5.84), one-night stand (OR 1.89) and a history of STIs (OR 5.79) and HIV infection (OR 4.77) (table 2). After excluding 41 clients with syphilis at baseline, 30 developed syphilis during 1851.0 PYFU, resulting in an incidence rate of 1.6 per 100 PYFU. In Cox regression analysis, clients who used illicit non-injection recreational drug (HR 5.01, 95% CI 1.90 to 13.20) and practiced unprotected anal sex (HR 5.84, 95% CI 1.34 to 25.42) were at a higher risk of acquiring syphilis during the follow-up.

    Of the 104 clients with amoebiasis, 38 submitted stool specimens for specific E histolytica antigen assays, in which 35 were tested positive. In multivariate analysis (table 2), amoebiasis were associated with older age (OR 1.08), MSM (OR 8.31), oral-anal sex practices (OR 2.46), HIV infection (OR 3.63) and syphilis (OR 2.77). Higher education achievement than college or university was a protective factor for HIV infection and amoebiasis.

    Of the 2093 urine specimens examined, 98 (4.7%) and 14 (0.7%) were positive for C trachomatis and N gonorrhoeae, respectively (table 1). There was no difference between heterosexual males and MSM in the prevalence of chlamydia and gonorrhoea. While female clients were more likely to have chlamydia than male clients, chlamydia and gonorrhoea were closely associated with each other and with urethral symptoms (table 2).

    Discussion

    In this study, we found that the prevalences and incidences of STIs among VCT clients were significantly higher than those observed in the other screening programmes among the general population or other risk groups in Taiwan. The prevalence was 6.1% for at least one of the three STIs that included HIV infection, syphilis and amoebiasis in this study and was 10.7% when tests for gonorrhoea and chlamydia were added. Risk factors identified for incident HIV infections and syphilis, especially among MSM, are of important clinical and public health implications in Taiwan, where MSM has re-emerged as the leading risk group for HIV transmission.4

    There are several limitations of this study, and interpretation of our data should be cautious. First, since the testing was anonymous, we may not be able to precisely recognise the repeaters solely based on the identification code that is provided by the clients. Second, the information on previous treatments for STIs was not recorded in the questionnaire. Since RPR and indirect haemagglutination titres will not normalise soon after treatment, the prevalences of syphilis and amoebiasis may be overestimated by serological diagnosis. Third, compared with the assays using combination of antibody and antigen for HIV, screening assays that only detect anti-HIV antibody have a longer window period and may miss more patients with acute HIV infections.6 Fourth, the present study did not investigate the prevalence of other STIs, such as infections with human papillomavirus, herpes simplex viruses and hepatitis viruses. Fifth, only 20% of the clients underwent PCR assays to detect C trachomatis and N gonorrhoeae. Sixth, we did not perform rectal or throat swab for detection of C trachomatis and N gonorrhoeae, we may have underestimated the prevalences of these two infections when only urine specimens were tested.7 Last, the clients in this study consisted of a high proportion of MSM (58.1%) and clients with higher educational achievement. The results may not be generalisable to the general population or IDUs.

    Compared with other screening programmes for HIV, VCT programme that is associated with medical facilities is unique in that accessibility to testing and counselling for HIV infection and STIs and linkage to clinical care can be improved in this setting where the procedures are conducted anonymously.8 In our study, 25% of the clients re-attended the VCT service, with clients at higher risk for HIV infection and syphilis having a higher re-attendance rate; furthermore, the prevalence and incidence of HIV infection were significantly higher than those of other screening programmes.3 These findings suggest that our VCT programme has reached the population most at risk for HIV and STIs rather than those low-risk clients who worried well. Nevertheless, the total number of VCT attendances nationwide remains relatively small, and improvement of accessibility and operational research to understand the barriers to VCT attendances and re-attendances are warranted.8

    In addition to HIV infection and syphilis, our VCT programme also provides tests for amoebiasis, chlamydia and gonorrhoea. Our findings demonstrated that clients with HIV infection, syphilis and amoebiasis shared similar risky behaviours and a significant interdependence existed among these STIs. To maximise the potential of VCT programme in the prevention and control of HIV infection in Taiwan, more studies are needed to identify STIs other than syphilis and amoebiasis that are closely associated with HIV infection to be included in the VCT programme9–11; and to assess whether such a model can be extended to the other VCT sites in Taiwan.

    In this study, we found that use of illicit recreational drugs and practice of unprotected anal sex were the risk factors for acquiring HIV infection and syphilis among the repeaters. However, the 1-year re-attendance rate among the clients recognised to be at the highest risk for HIV infection was <40%. To further improve effectiveness of VCT programme for HIV, counselling during a VCT visit that provides information, communication and education against the use of recreational drugs and unprotected anal sex cannot be overemphasised and strategies to promote re-attendances and follow-up for those with risky behaviours need to be explored.8

    In conclusion, with higher rates of re-attendances and STIs, the VCT programme reached the population most at risk for HIV and STIs compared with other screening programmes in Taiwan. The potential of VCT programme can be maximised in the prevention and control of HIV infection and STIs by providing tests for more STIs and counselling to avoid use of recreational drugs and to promote safe sex.

    Key messages

    • With higher rates of re-attendances and STIs, VCT programme reached the population most at risk for HIV and STIs compared with other screening programmes in Taiwan.

    • VCT clients who are MSM had significantly higher risks for HIV infection, syphilis and amoebiasis.

    • Among the repeaters, use of non-injection recreational drugs and unprotected anal sex were risk factors for incidence HIV infection and syphilis.

    • Strategies are needed to maximise the potential of VCT programme in Taiwan by providing effective counselling and tests for more STIs and to increase re-attendances among the clients at high risk for HIV transmission.

    Acknowledgments

    We thank the VCT clients for participating in this survey.

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    Supplementary materials

    • Supplementary Data

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    Footnotes

    • Preliminary analyses of these data were presented as P2062 at the 21st European Congress of Clinical Microbiology and Infectious Diseases and the 27th International Congress of Chemotherapy, Milan, Italy, 7–10 May 2011.

    • HW and P-YW contributed equally to this work.

    • Funding This work was supported by the Taiwan Centers for Disease Control (grant numbers AIDS-97-1002 and EU099059).

    • Competing interests None.

    • Ethics approval Ethics approval was provided by the research ethics committee of the National Taiwan University Hospital (approved registered number: 200904084R).

    • Provenance and peer review Not commissioned; externally peer reviewed.