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Sexually Transmitted Infections in Western Europe Among HIV-Positive Men Who Have Sex With Men

Dougan, Sarah MA, MSc*; Evans, Barry G. DM, FFPH; Elford, Jonathan MSc, PhD*

doi: 10.1097/01.olq.0000260919.34598.5b

Background: Since 1996, there has been a resurgence in sexually transmitted infections (STIs) among men who have sex with men (MSM) in Western Europe. This has coincided with a significant decrease in HIV-associated mortality following the introduction of highly active antiretroviral therapies (HAART) and a corresponding increase in the number of MSM living with HIV. Levels of unprotected anal intercourse have also increased. In this article, we use STI surveillance data from a number of Western European countries to better understand the contribution of HIV-positive MSM to the recent increase in STIs.

Methods: Published literature, surveillance reports, and ad hoc publications relating to HIV prevalence trends and STIs among HIV-positive MSM in Western Europe were reviewed.

Results: Post-HAART, HIV prevalence among community samples of MSM ranged from 5% to 18%. HIV prevalence among MSM diagnosed with an STI was substantially higher. On average, HIV prevalence among MSM diagnosed with syphilis in 11 countries was 42% (range 14%–59%). Most HIV-positive MSM with syphilis were aware of their HIV status. In England and Wales, 32% of MSM with gonorrhea were HIV-positive in 2004. Outbreaks of lymphogranuloma venereum have been documented in 9 countries; HIV-positive MSM accounted for 75% of cases on average (range 0%–92%). Cases of sexually transmitted hepatitis C have been predominantly identified among HIV-positive MSM in Rotterdam, Paris, Amsterdam, and the United Kingdom.

Conclusions: In Western Europe, STIs have been disproportionately diagnosed among HIV-positive MSM post-HAART. Improved survival coupled with serosorting among HIV-positive MSM appears to explain the high prevalence of HIV among MSM with STIs. STI transmission among HIV-positive men will have contributed substantially to increasing STI trends seen among MSM in Western Europe, since 1996. These findings highlight the need for routine STI testing among HIV-positive MSM as well as safer sex messages highlighting the implications of STI coinfection.

A review of the literature found that since the introduction of highly active antiretroviral therapies, STIs have been disproportionately diagnosed among HIV positive men who have sex with men in Western Europe.

From *City University, Institute of Health Sciences, St. Bartholomew School of Nursing and Midwifery, London, United Kingdom; and †Health Protection Agency Centre for Infections, London, United Kingdom

The authors extend their thanks to Drs. Eline op de Coul, Femke Koedijk, Michael Boclow, and Anthony Nardone for providing, or clarifying, data that are presented in this manuscript. The authors thank the reviewers for their insightful comments.

Contribution of authors: SD conceived the idea for the article with input from JE. SD undertook the literature review and wrote the first draft. JE and BE commented on subsequent drafts. All authors read and approved the final draft. SD is currently registered for a PhD at City University, London.

Correspondence: Sarah Dougan, City University, Institute of Health Sciences, 24 Chiswell Street, London EC1Y 4TY, United Kingdom. E-mail:

Received for publication September 5, 2006, and accepted February 2, 2007.

THE INCIDENCE OF SEXUALLY transmitted infections (STIs) among men who have sex with men (MSM) in Western Europe began to decline in the late 1970s and continued falling during the early 1980s, mainly because of the behavioral change in response to HIV/AIDS.1 STI incidence among MSM remained relatively low until the introduction of highly active antiretroviral therapies (HAART) for the treatment of HIV in 1996.2 Over the last 8 years, however, a resurgence in STIs among MSM has been reported in many Western European countries.2,3

Increased levels of unprotected anal intercourse among MSM were documented from 1996 onwards in the United Kingdom, France, Germany, and Switzerland, although there is some evidence that levels may have now stabilized in some cities.4–10 However, although some MSM are reporting unprotected sex, they are also adopting HIV risk reduction strategies, such as “serosorting,” where sexual partners are chosen on the basis of HIV serostatus.11 But even though effective serosorting (which requires serostatus to be accurately known and communicated) will prevent HIV transmission, the risk of STI transmission remains.

The widespread use of HAART has dramatically changed the epidemiology of HIV among MSM, with significant decreases in HIV-associated morbidity and mortality from 1996 onwards.12–14 As a consequence, there is now an increasing number of MSM living with diagnosed, asymptomatic HIV infection who are sexually active.12,15

For the first time, we examine HIV prevalence among MSM with STIs across Western Europe, and compare and contrast outbreaks in different countries. Understanding STI epidemiology among known HIV-positive MSM is important for 3 reasons. First, to inform “positive prevention” which focuses on the sexual health of HIV-positive men and the prevention of STI as well as HIV transmission. Second, to inform the need for STI testing of HIV-positive MSM during routine HIV care. Finally, for the interpretation of epidemiologic data on STIs, specifically the use of STI trends as a proxy marker for HIV incidence.

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We reviewed the published literature, surveillance reports and ad hoc publications relating to trends in HIV prevalence and STIs among HIV-positive MSM in Western Europe in the post-HAART era (1996–June 2006). We focused on diagnoses of gonorrhea, syphilis, lymphogranuloma venereum (LGV), and sexually transmitted hepatitis C because of epidemiologic synergies with HIV,16,17 their historical use as markers of unsafe sex and their recent (re-)emergence among MSM. We limited publications to those where data on both HIV status and STI diagnoses were collected for the same individuals. Where surveillance data have been published more than once, we present the most recent data.

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HIV Prevalence

HIV prevalence estimates were obtained from behavioral studies of MSM in community settings where oral fluids had been taken for unlinked anonymous testing or self-reported HIV prevalence data had been collected.

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Enhanced surveillance systems have been set up to monitor syphilis and LGV in many Western European countries.18 These collect information on sexual orientation and HIV status. Similarly, this information has been gathered during clinical studies investigating sexually transmitted hepatitis C infection. Unfortunately, there are not many enhanced surveillance systems collecting data on gonorrhea and for the most part in routine systems, sexual orientation and HIV status are either not collected or not well reported.

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HIV Prevalence

In Western Europe, HIV prevalence among community surveys of MSM conducted between 2000 and 2004 ranged from 5% to 18% (Table 1).4,8,12,19–23



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Syphilis Outbreaks

Post-HAART, the first syphilis outbreak among MSM was reported in Hamburg in 1997.24 Increasing trends have been observed since then across Western Europe, with a recent decline in some countries.15,25,26 The largest reported outbreaks have been in London, Paris, and Dublin.26–28

HIV prevalence varied widely among MSM diagnosed with syphilis (14%–59%) by country and within countries, with an average of 42% across the region (Table 2).24,27–39 Despite this variation, HIV-positive MSM were disproportionately diagnosed with syphilis.





In London, HIV-positive MSM with syphilis were older than HIV negative MSM [49% (272/556) aged 35–44 years vs. 33% (158/483)] (P < 0.001) and they had an altered presentation, being more likely to present with secondary syphilis rather than primary or early latent syphilis.27,37 Similar observations were made in other cities.40 Where calculated, syphilis incidence rates were higher among HIV-positive MSM. At a Dublin sexual health clinic, the crude incidence rate of syphilis in HIV-positive MSM was 10 times greater than in HIV negative MSM, peaking at 7280 per 100,000 in 2001, and then falling to 1553 per 100,000 in 2002.26 Incidence rates among HIV-positive MSM in Germany also exceeded 1000 per 100,000.24

There was evidence of a temporal decline in HIV prevalence among MSM with syphilis in some settings. In Hamburg, the proportion of syphilis cases among HIV-positive MSM decreased from 80% in 1997–1998 to 40%–50% in later years41 and similarly, in the Ile de France region from 72% in 2000 to 47% in 2003.28 Conversely, there were no observed decreases in other French regions28 or in Denmark.30

The majority of HIV-positive MSM diagnosed with syphilis were already aware of their HIV status (Table 2).27–29,32,33,35,38 At a Paris hospital (2000–2002), HIV-positive MSM had been HIV diagnosed for a median of 8.8 years (range 0–19) before syphilis diagnosis.40 Two-thirds (48/71) were receiving HAART.40 In Germany, the proportion of reported syphilis reinfections was significantly higher among HIV-positive MSM.24

Across Western Europe, a significant proportion of MSM with syphilis reported unprotected oral intercourse (Table 2), with no difference by HIV status.25–27,37,42 In Rotterdam, as elsewhere, MSM frequently reported using condoms for anal intercourse but not with oral contacts.33,34

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Trends in Gonorrhea

Since the late 1990s, increases in diagnoses and rates of gonorrhea have been observed across the region, although recently there has been evidence of a levelling off and even a decline in some countries.2,3,43

In Denmark (1994–1999), gonorrhea incidence was 6 times higher among known HIV-positive MSM (P < 0.001).44 A study in a Parisian clinic showed that at least one-third (30/92) of MSM diagnosed with gonorrhea between January 1999 and May 2001 were HIV-positive; more than half the MSM reported oral sex as the sole risk factor.45 In Sweden, 5.4% (4/74) of gonorrhea cases were in HIV-positive MSM in 2000.46 By comparison, at sentinel sites in England and Wales, 32% (123/381) of MSM with gonorrhea were HIV-positive in 2004.15

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Reemergence of LGV

The first outbreak of LGV (serovar L2) among MSM was reported in Rotterdam in 2003.47 Since then, LGV outbreaks among MSM have been documented in 9 Western European countries; the largest in the United Kingdom and France (Table 3)48–59 (Eline op de Coul and Femke Koedijk, personal communication). Again, HIV-positive MSM were disproportionately affected, accounting for 75% of all reported cases on average (range 0%–92%). The LGV outbreaks have shared similar characteristics to the syphilis outbreaks: most cases were among older, white MSM who had probably acquired infection in Europe.48,59 In Rotterdam and in the United Kingdom, LGV infection has been associated with concurrent STIs, particularly sexually transmitted hepatitis C (as shown in Eline op de Coul and Femke Koedijk, personal communication and Ref. 57).



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Sexually Transmitted Hepatitis C

Active case finding has identified sexually transmitted hepatitis C among HIV-positive MSM in Rotterdam, Paris, Amsterdam, and the United Kingdom.60–66

More than 225 HIV-positive MSM had been diagnosed with sexually transmitted hepatitis C in London and Brighton by February 2006.65 Significant risk factors were a high number of sexual partners, unprotected anal intercourse, mucosally traumatic practices (e.g., fisting), group sex, and use of ‘club' drugs.65 In Rotterdam, investigation of LGV cases and contacts of an index patient identified 17 HIV-positive MSM with sexually transmitted hepatitis C; 4 had confirmed LGV.60 Twenty-nine cases of acute hepatitis C among HIV-positive MSM were identified in Paris between March 2001 and October 2004.61,62 Twelve (41%) of the MSM had an STI coinfection.61 Median time between HIV and hepatitis C diagnosis was 6.5 years; 76% (22) of MSM were clinically asymptomatic; and 86%25 of the MSM were on HAART.61

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STIs have been disproportionately acquired by HIV-positive MSM across Western Europe in the post-HAART era. Although HIV prevalence among MSM in community settings ranged from 5% to 18%, in contrast it averaged 75% among MSM diagnosed with LGV, 42% among those with syphilis, and in England and Wales, 32% among those with gonorrhea. The majority of HIV-positive MSM diagnosed with STIs were already aware of their HIV-positive status and in some instances, had been on HAART for several years. Nearly all MSM diagnosed with sexually transmitted hepatitis C have been HIV-positive, but there has been active case finding among HIV-positive MSM. However, the incidence of sexually transmitted hepatitis C among HIV negative MSM is low.67 In Western Europe since the introduction of HAART, transmission among HIV-positive MSM has accounted almost entirely for the outbreaks of LGV and established cases of sexually transmitted hepatitis C; it has also contributed significantly to the syphilis outbreaks and, probably, the increase in gonorrhea too.

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Strengths and Limitations

The main limitation of the analyses is the heterogeneity of the studies and surveillance systems from which these data are derived. In their review of European STI surveillance, Lowndes and Fenton found differences at all levels, including case definitions, coverage, STI screening, partner notification, and treatment practices.18 All of these will impact on the reported number of STI diagnoses.2,18 Similarly, the HIV prevalence figures from community studies of MSM vary in their sampling techniques and measurement of HIV status. Self-reported HIV status may be inaccurate because some men will not be aware of their positive status. In addition, although community based studies give more realistic measures of HIV prevalence among MSM when compared with sexual health clinic attendees, HIV prevalence may still be overestimated.68 Despite these limitations, however, this is the first time that data on a range of STIs among known HIV-positive MSM have been systematically collated in Western Europe, with enhanced STI surveillance systems providing valuable information.

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Serosorting and Survival

Improved survival and reduced morbidity coupled with unprotected MSM who, like themselves are also HIV-positive (i.e., serosorting) would explain the very high prevalence of HIV among MSM diagnosed with STIs. In the early 1990s, it was estimated that every 20 AIDS deaths per 100,000 adult men were associated with a decline of about 7%–12% in syphilis incidence rates.69 Since the introduction of HAART however, sexual networks of HIV-positive MSM have grown substantially.10,11 The Internet in particular, has facilitated serosorting among HIV-positive MSM.70,71 Evidence also points toward acquisition of multiple STIs and in Germany at least, high levels of syphilis reinfection among some HIV-positive MSM. This has led some researchers to refer to ‘the core of the core'—a network of HIV-positive MSM where there is intense circulation of STIs making a disproportionate contribution to overall STI diagnoses.72

Presently, LGV and sexually transmitted hepatitis C transmission are circulating almost exclusively among HIV-positive MSM. In contrast, both HIV-positive and negative men are being diagnosed with syphilis and gonorrhea. There are likely to be several explanations for these differences including differences in transmission probabilities and epidemiologic synergies with HIV16,17; sexual partnerships and sexual networks including serosorting and time since introduction of the STIs to the network; differential sexual behaviors; differences in testing and case finding; and the differential impact of public health interventions.73,74 Equally, these factors may explain variations in HIV prevalence among MSM with syphilis in different settings. The number of HIV-positive MSM may also play a role in this. Where population size is limited, dissortative sexual mixing is more likely to occur—in this case, serodiscordant partnerships.75 Taken together, the epidemiologic and behavioral data highlight a role for “positive prevention”, i.e., prevention that focuses on the sexual health of HIV-positive MSM in ‘high-risk' sexual networks as well as on the transmission of STIs and HIV to uninfected MSM.

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Impact on HIV Transmission

The resurgence in STIs among MSM led to concerns about a corresponding increase in HIV incidence because historically HIV incidence had broadly mirrored STI incidence among MSM in Western Europe.1,76 Disproportionate circulation of STIs among known HIV-positive MSM would however, change the relationship between HIV and STI incidence. In addition, use of syphilis as a proxy marker is complicated by the significant proportion of cases among MSM acquired through unprotected oral sex, which has a much lower risk of HIV transmission than unprotected anal intercourse.77

The relationship between STI incidence and HIV incidence is difficult to assess because of ecological fallacy; most studies do not measure trends in HIV and STI incidence in the same individuals. In the Amsterdam cohort study however, STI incidence has been increasing among all MSM but strikingly there has only been an increase in HIV incidence among older (34+ years), but not younger men.78 A similar observation has been made in San Francisco.79 Taken in concert, this evidence indicates that STI incidence may no longer be a suitable proxy for HIV incidence among MSM and that care should be taken when interpreting these epidemiologic trends.

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Comparisons With the United States

The United States has also been experiencing a resurgence in STIs among MSM.80–85 Syphilis has increased since the introduction of HAART,79 with HIV-positive MSM being disproportionately affected.86,87 In 2004, gonorrhea positivity in 9 US cities was higher among HIV-positive MSM than among those who were HIV negative or of unknown status [e.g., urethral gonorrhea: 17% (range 12%–25%) vs. 10% (range 6%–12%)].80 A case of LGV has also been confirmed.88 Furthermore, matching of STD and AIDS databases in San Francisco has shown that people on HAART are more likely to develop an STI.89

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Conclusion and Recommendations

STIs have been disproportionately diagnosed among HIV-positive MSM in the post-HAART era in Western Europe. Although HIV prevalence among MSM with STIs varied by infection and by setting, the majority of HIV-positive MSM diagnosed with STIs were already aware of their positive HIV status.

These findings highlight the need for routine testing for STIs among known HIV-positive MSM in Western Europe. For example, in the United States, routine laboratory screening for common STIs for all MSM (HIV-positive, negative and of unknown status) is recommended on an annual basis for those who are sexually active.90 Routine screening for HIV would help to diagnose more HIV-infected MSM; our findings indicate that in some settings, a large proportion of HIV-positive MSM with STIs were unaware of their HIV status.

Safe sex messages have typically focused on HIV prevention but with a growing population of sexually active HIV-positive MSM, messages need to also highlight the consequences of STI infection. The consequences include their impact on HIV treatment response, coinfection affecting the natural history of HIV infection, and increased transmissibility of HIV infection.91–93 Safe sex messages also need to underline the risks associated with sexual practices other than unprotected anal intercourse with a partner of unknown or discordant HIV status. In epidemiologic terms, the disproportionate circulation of STIs among HIV-positive MSM means that changes in STI incidence may no longer reflect corresponding changes in HIV incidence among MSM.

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