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The European Journal of Public Health Advance Access originally published online on March 31, 2008
The European Journal of Public Health 2008 18(4):376-379; doi:10.1093/eurpub/ckm120
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© The Author 2008. Published by Oxford University Press on behalf of the European Public Health Association. All rights reserved.

Infectious Diseases

Low HIV-testing rates and awareness of HIV infection among high-risk heterosexual STI clinic attendees in The Netherlands

Akke K. Van der Bij1, Nicole H. T. M. Dukers1,2,3, Roel A. Coutinho1,2,3,4 and Han S. A. Fennema5

1 Department of Research, Cluster Infectious Diseases, Health Service of Amsterdam, Amsterdam, The Netherlands
2 Department of internal medicine, Academic Medical Center/University of Amsterdam, Amsterdam, The Netherlands
3 Center for Infection and Immunity Amsterdam, Academic Medical Center/University of Amsterdam, Amsterdam, The Netherlands
4 Center for Infectious Disease Control, National Institute for Public Health and the Environment, Bilthoven, The Netherlands
5 STI outpatient clinic, Cluster Infectious Diseases, Health Service of Amsterdam, Amsterdam, The Netherlands

Correspondence: Nicole H. T. M. Dukers-Muijrers, Department of Infectious Diseases, South Limburg Public Health Service, PO Box 2022, 6160 Geleen, The Netherlands, tel: 31 458506246, fax: 31 455742801, e-mail: nicole.dukers{at}ggdzl.nl

Received February 27, 2007, accepted November 19, 2007


    Abstract
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 
Objectives: Since 1999, HIV testing is routinely offered to all attendees of the sexually transmitted infections (STI) outpatient clinic in Amsterdam, the Netherlands. This study evaluates whether this more active HIV-testing policy increased uptake of HIV testing and awareness of an HIV-positive serostatus among heterosexual attendees. Methods: In addition to routine data collected at each STI consultation, data from half-yearly HIV surveys were used from 1994 to 2004. During each survey period, 1000 consecutive attendees are enrolled voluntary and anonymously for HIV testing and are interviewed on previous HIV testing and outcome. Trends in and predictors for uptake of HIV testing as offered during routine STI consultation were analysed by logistic regression. Trends in awareness of an HIV-positive serostatus as obtained from the anonymous HIV surveys were likewise analysed. Results: The percentage of heterosexual attendees opting for an HIV test during consultation increased from 13% in 1996 to 56% in 2004. However, the proportion of individuals aware of their HIV infection did not change over time and only a minority (19%) of the 108 attendees found HIV-positive in the anonymous surveys were aware of their HIV infection. Persons being or visiting a commercial sex worker, having a non-Dutch ethnicity, lacking health insurance and having an STI diagnosed were less likely to opt for an HIV test. Conclusions: Although heterosexual attendees increased their uptake of HIV testing during STI consultation over time, uptake of testing by attendees at risk for HIV infection, such as those infected with an STI, remained low. As a result, the percentage of persons aware of their HIV infection remained low, posing a risk for their individual health and for ongoing HIV transmission. Current testing strategies, therefore, misses the group that most needs testing. Based on these results, ‘opt-out’ HIV testing is now the standard procedure at the Amsterdam STI clinic.

Keywords: awareness, heterosexuals, HIV, HIV testing, trends


    Introduction
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 
In the Netherlands, a more active HIV-testing strategy was adopted only after the availability of highly active antiretroviral therapy (HAART). Previously, HIV testing was not promoted or even discouraged. This policy changed due to HAART since it strongly improved the prognosis and quality of life of persons infected with HIV.1 Moreover, it has been suggested that early treatment improves treatment response.2 In addition, awareness of HIV infection can moderate risky behaviour and therapy may also reduce HIV transmission.3 Timely awareness of HIV infection is therefore important for both the individual and for public health.

Since 2000, the absolute number of HIV diagnoses in heterosexuals rose to the same level as in men who have sex with men (MSM) in the Netherlands, increasing from around 160 new diagnoses in 1996 to 373 in 2004; representing 40% of all diagnoses in 2004.4 In the UK, recent increases in new HIV diagnoses have also largely been driven by heterosexually acquired infections.5,6 In 1995, only 32% of the diagnoses were among heterosexuals and 56% among MSM. In 2004, these numbers changed to 59% and 30%, respectively.6 Most of these infections were acquired abroad in high prevalence areas, such as Sub-Saharan Africa. In the Netherlands, heterosexuals originating from Sub-Saharan Africa contribute substantially to the new number of HIV diagnoses as well. Although heterosexuals contribute increasingly to new HIV diagnoses in industrialized countries, they often receive a late-stage HIV diagnosis7,8 that negates early treatment. This study evaluates if uptake of HIV testing and, more importantly, awareness of an HIV-positive serostatus among heterosexual attendees of a sexually transmitted infection (STI) clinic increased over time, reflecting effectiveness of increased promotion of HIV testing in the Netherlands.


    Materials and Methods
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 
To evaluate the uptake of voluntary HIV testing and factors associated with testing during STI consultation, we included data on all heterosexual attendees (i.e. defined as having sex exclusively with someone of the opposite sex in the past six months) visiting the STI outpatient clinic of the Public Health Service of Amsterdam for the first time or seeking care for a new possible STI episode or related symptoms from 1994 to 2004. The STI clinic offers free-of-charge examination and treatment for STI (i.e. syphilis, chlamydia and gonorrhoea for all attendees and trichomoniasis for women only). Since 1999, the clinic routinely offers voluntary HIV testing and pre-test counselling to all attendees (i.e. the option of an HIV test is discussed routinely with all attendees by all health care workers). Attendees were tested for HIV after giving written consent. Non-Dutch speaking attendees were informed in English language or if possible in their native language. Before 1999, HIV testing was not routinely offered, but the clinic provided free-of-charge HIV counselling and testing on request (i.e. the option of an HIV test was only discussed and given when an attendee actively asked for an HIV test).

To assess the level of awareness of an HIV-positive serostatus, we used data collected in half-yearly cross-sectional anonymous HIV prevalence surveys at the same clinic from 1994 to 2004.9 During each survey period, a representative sample of approximately 1000 consecutive attendees are enrolled and interviewed by a public health nurse on HIV risk behaviours (i.e. drug use, commercial sexual contact, recent sexual contact and previous STI) and knowledge of HIV serostatus (i.e. ever tested and last test result) after consent. Attendees are considered eligible for these surveys when they visit the clinic for evaluation of a possible new STI episode. The interviews are followed by routine physical examination including STI and possibly voluntary (i.e. non-anonymous) HIV testing. Additional blood is taken for anonymous HIV antibodies testing using commercially available enzyme-linked immunosorbent assay, with positive results confirmed by western blot. Participants in the anonymous HIV prevalence survey do not receive their HIV test results, unless they opt for a voluntary HIV test during STI consultation.

Trends in voluntary HIV testing (i.e. number of tests by number of visits) and awareness of HIV-positive serostatus were analysed by univariate logistic regression, with calendar year as a continuous variable. Interaction between ethnicity as defined by the attendee him/herselves, STI and HIV-testing rates before and after 1999 was evaluated to see if the uptake of voluntary HIV testing differed among different risk groups after introduction of routinely offered HIV testing in 1999. Associations between opting for a voluntary HIV test during routine STI consultation in 2004 and factors such as gender, age, ethnicity, drug use, being or visiting a commercial sex worker (CSW) and STI diagnoses were analysed by multivariate logistic regression. Backward selection was used to obtain a multivariate model that included only statistically significant variables. Significance for individual parameters was tested using the Wald test. Estimates and standard errors were corrected for intra-individual correlation between visits of the same person by using generalized estimating equations (GEE), assuming an exchangeable correlation matrix. A P-value <0.05 was considered statistically significant.


    Results
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 
The annual number of new consultations at the STI clinic increased from 11 178 in 1994 to 20 897 in 2004. Of the 11-year total, heterosexual men and women contributed to 144 466 of these consultations (82%); 40% of the heterosexual attendees frequented the clinic more than once in the study period. Of the heterosexual attendees, 48% were male; their median age was 28 years (Interquartile Range (IR): 23–35 years). The majority (60%) were of Dutch origin. Other ethnicity groups were Surinamese or Dutch Antillean (12%), Sub-Saharan African (4%), South-American (4%), North African (3%), Turkish (3%), Eastern European (3%); 12% originated from Asia, North America or Australia. The demographics of the population changed over time: the proportion of women and the proportion of persons with a Dutch ethnicity increased over the years from 48%, 50% respectively in 1994 to 53%, 69% in 2004. The proportion of persons aged younger than 30 years also increased, whereas the proportion of persons aged over 30 years decreased from 53% to 36%. The number of persons reporting drug use also decreased from 8% in 1994 to 4% in 2003 and less than 1% in 2004.

The percentage of heterosexual attendees opting for a voluntary non-anonymous HIV test during consultation increased in the past 11 years from around 10% in 1996 to 56% in 2004 [figure 1, odds ratio (OR): 1.39 per year, 95% confidence interval (CI): 1.38–1.40]. Overall, there was a significant increase in HIV-testing rates when comparing the period before and after 1999 (OR: 5.7, 95% CI: 5.6–5.9). Additionally, there was a significant interaction effect between time period and ethnicity or STI (both P < 0.001). The increase in HIV-testing rates when comparing the period before and after 1999, was more pronounced among persons with a non-Dutch ethnicity than in persons with a Dutch ethnicity (table 1 and figure 2), or in persons with a chlamydia or gonorrhoea infection diagnosed than in persons with no STI diagnosed (table 1 and figure 2). However, for persons with a gonorrhoea infection the percentage opting for a voluntary HIV test remained substantially lower than in persons without an STI. Using data from 2004, multivariate logistic analysis showed that persons less likely to opt for a voluntary HIV test, were persons lacking health insurance, persons with a North-African or Turkish ethnicity and persons with a chlamydia or gonorrhoea infection (table 2).


Figure 1
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Figure 1 Voluntary non-anonymous HIV testing during STI consultation (n = 144 466), number of HIV-positives, and percentage being aware of their HIV infection in anonymous HIV surveys (n = 17 093) among heterosexual attendees, STI clinic Amsterdam, 1994–2004

 

Figure 2
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Figure 2 Voluntary non-anonymous HIV testing during STI consultation (n = 144 466), among heterosexual attendees, STI clinic Amsterdam, 1994–2004 by ethnicity and STI

 
Of the 17 093 heterosexual attendees participating in the anonymous HIV prevalence surveys, 108 were found HIV-positive from 1994 to 2004. Of these 108, the majority were female (57%); 19% were of Dutch ethnicity, 24% Sub-Saharan African, 13% Surinamese/Dutch Antillean and 11% South American; 42% lacked health insurance and 19% were CSW. Of these 108, only a minority (n = 20, 19%) were aware of their HIV infection at the time of STI consultation. The absolute number of persons not aware of their HIV infection was 54 before 1999, and 34 after 1999. However, the proportion of individuals aware of their HIV infection did not change over time (figure 1, P = 0.6).


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Table 1 Increase in voluntary HIV-testing rates during STI consultation (n = 144 466) among heterosexual attendees, STI clinic Amsterdam, before and after 1999 by ethnicity and STI, univariate logistic regression analysis

 

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Table 2 Factors associated with opting for a voluntary HIV test among heterosexual attendees (n = 16 011), STI clinic Amsterdam, in 2004, multivariate logistic regression analysis

 

    Discussion
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 
Although heterosexual attendees increased their uptake of voluntary non-anonymous HIV testing during STI consultation over time, the percentage of persons aware of their HIV infection remained low. The absolute number of persons not aware of their infection decreased over time, a result biased by the decrease in the HIV prevalence in our clinic population resulting in less persons testing HIV-positive in the anonymous HIV surveys. The decreasing HIV prevalence is probably due to the substantial increase in attendees of Dutch ethnicity, being at lower risk of HIV infection than persons with a non-Dutch ethnicity.9

Small numbers of HIV-positive persons found in the half-yearly surveys might limit this study. However, the fact remains that persons at risk for an HIV infection such as those infected with an STI9,10 were less likely to be tested, posing a risk for their health and for ongoing HIV transmission. Although both attendees at lower risk as well as attendees at high risk for HIV infection, such as those with a non-Dutch ethnicity or those infected with an STI,9,10 increased their uptake of voluntary non-anonymous HIV testing, the uptake of testing by attendees with a gonorrhoea infection remained low. Current testing strategies, therefore, misses the group that most needs testing. Our findings combined with the fact that heterosexuals largely account for the recent increase in new HIV diagnoses, both internationally and nationally,4,5 calls for further strategies to target high-risk heterosexuals and thereby reduce undiagnosed prevalent HIV infection.

Further uptake of HIV testing can be achieved by performing ‘opt-out’ testing for persons seeking STI screening, especially for those at high risk. By ‘opt-out’ testing all attendees receive an HIV test, unless they specifically state that they do not want to be tested. In the Netherlands, this is the standard approach for HIV screening among pregnant women to reduce mother-to-child HIV transmission. After its implementation in Amsterdam, the proportion of women that refused to be tested for HIV declined substantially.11 International studies also show effectiveness of opt-out testing in increasing HIV-testing rates,12,13 and in 2006 the United States Centers for Disease Control and Prevention revised its HIV screening recommendations to advocate routine voluntary HIV screening as a normal part of medical practice.14 Goals of the new recommendations include earlier HIV diagnoses, reducing stigma associated with risk-based testing, facilitating care and treatment for HIV-positive patients, and reducing high-risk sexual behaviours and HIV transmission by those previously unaware of their HIV status. Since 2007 ‘opt-out’ testing is now the standard procedure for all visitors of the Amsterdam STI clinic.


    Acknowledgements
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 
The authors would like to express their gratitude to the Public Health Nurses of the STI Outpatient Clinic, Amsterdam for all data collection; to all personnel of the Public Health Laboratory of the Health Service of Amsterdam for performing the laboratory diagnostics; to R. Geskus for critically reading the manuscript, and to L. Phillips for editing this manuscript.

Conflict of interest: None declared.


Key points

  • Heterosexual STI clinic attendees increased their uptake of voluntary HIV testing.
  • Heterosexual attendees at risk of HIV infection, such as those infected with gonorrhoea, were substantially less likely to be tested for HIV.
  • HIV testing at STI clinics should be performed by ‘opt-out’ testing strategies, especially in groups at high risk for HIV infection, to reduce undiagnosed infection.

 


    References
 Top
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 Acknowledgements
 References
 
1 Palella FJJ, Delaney KM, Moorman AC, et al. Declining morbidity and mortality among patients with advanced human immunodeficiency virus infection. HIV Outpatient Study Investigators. N Engl J Med (1998) 338:853–60.[Abstract/Free Full Text]

2 Holmberg SD, Palella FJ, Lichtenstein KA, et al. The case for earlier treatment of HIV infection. Clin Infect Dis (2004) 39:1699–704.[CrossRef][Web of Science][Medline]

3 Vernazza PL, Eron JJ, Fiscus SA, et al. Sexual transmission of HIV: infectiousness and prevention. AIDS (1999) 13:155–66.[CrossRef][Web of Science][Medline]

4 Laar MJW van de, Boer IM, Koedijk FDH, et al. HIV and sexually transmitted infections in the Netherlands in 2004. An update: November 2005. (2005) Bilthoven, the Netherlands: National Institute for Public Health and the Environment. Report No.: 441100022.

5 Brown AE, Sadler KE, Tomkins SE, et al. Recent trends in HIV and other STIs in the United Kingdom: data to the end of 2002. Sex Transm Infect (2004) 80:159–66.[Abstract/Free Full Text]

6 The UK Collaborative Group for HIV and STI surveillance. Mapping the issues. HIV and other sexually transmitted infections in the United Kingdom: 2005. (2005) London, UK: Health Protection Agency of Infections.

7 Centres for Disease Control. Late versus early testing of HIV – 16 sites, United States, 2000-2003. MMWR (2003) 52:581–6.[Medline]

8 Longo B, Pezzotti P, Boros S, et al. Increasing proportion of late testers among AIDS cases in Italy, 1996-2002. AIDS Care (2005) 17:834–41.[Web of Science][Medline]

9 Fennema JS, van Ameijden EJ, Coutinho RA, et al. HIV surveillance among sexually transmitted disease clinic attenders in Amsterdam, 1991-1996. AIDS (1998) 12:931–8.[CrossRef][Web of Science][Medline]

10 Bos JM, Fennema JS, Postma MJ. Cost-effectiveness of HIV screening of patients attending clinics for sexually transmitted diseases in Amsterdam. AIDS (2001) 15:2031–6.[CrossRef][Web of Science][Medline]

11 Mulder-Folkerts DK, van den Hoek JA, van der Bij AK, et al. Less refusal to participate in HIV screening among pregnant women in the Amsterdam region since the introduction of standard HIV screening using the opting-out method [In dutch]. Ned Tijdschr Geneeskd (2004) 148:2035–7.[Medline]

12 Yudin MH, Moravac C, Shah RR. Influence of an "opt-out" test strategy and patient factors on human immunodeficiency virus screening in pregnancy. Obstet Gynecol (2007) 110:81–6.[CrossRef][Web of Science][Medline]

13 Stanley B, Fraser J, Cox NH. Uptake of HIV screening in genitourinary medicine after change to "opt-out" consent. Br Med J (2003) 326:1174.[Free Full Text]

14 Branson BM, Handsfield HH, Lampe MA, et al. Revised recommendations for HIV testing of adults, adolescents, and pregnant women in health-care settings. MMWR Recomm Rep (2006) 55:1–17.[Medline]


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