Dougan, Sarah MA, MSc*; Evans, Barry G. DM, FFPH†; Elford, Jonathan MSc, PhD*
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.
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.
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.
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.
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
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
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
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).
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
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.
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.
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.
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.
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
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.
1. Nicoll A, Hughes G, Donnelly M, et al. Assessing the impact of national anti-HIV sexual health campaigns: Trends in the transmission of HIV and other sexually transmitted infections in England. Sex Transm Infect 2001; 77:242–247.
2. Fenton KA, Lowndes CM. Recent trends in the epidemiology of sexually transmitted infections in the European Union. Sex Transm Infect 2004; 80:255–263.
3. Nicoll A, Hamers FF. Are trends in HIV, gonorrhea and syphilis worsening in Western Europe? BMJ 2002; 324:1324–1327.
4. Dodds JP, Mercey DE, Parry JV, et al. Increasing risk behavior and high levels of undiagnosed HIV infection in a community sample of homosexual men. Sex Transm Infect 2004; 80:236–240.
5. Elford J, Bolding G, Davis M, et al. Trends in sexual behavior among London homosexual men 1998–2003: Implications for HIV prevention and sexual health promotion. Sex Transm Infect 2004; 80:451–454.
6. Dubois-Arber F, Moreau-Gruet F, Jeannin A. Men having sex with men and HIV/AIDS prevention in Switzerland: 1987–2000. Euro Surveill 2002; 7:16–18.
7. Stolte G, Dukers NH, de Wit JB, et al. A summary report from Amsterdam: Increase in sexually transmitted diseases and risky sexual behavior among homosexual men in relation to the introduction of new anti-HIV drugs. Euro Surveill 2002; 7:19–22.
8. Bochow M. Gay Men, AIDS and Safer Sex: New Developments. Berlin: Deutsche AIDS-Hilfe e.V, 2001, (in German).
9. Adam P, Hauet E, Caron C. Increase in Risk-Taking and Sexually Transmitted Infections Among Gay Men. Results of the Gay Press Survey, 2000. Paris: L'Institut de Veille Sanitaire, 2000, (in French).
10. Elford J, Bolding G, Sherr L, et al. High risk sexual behavior among London gay men: No longer increasing. AIDS 2005; 19:2171–2174.
11. Elford J. Changing patterns of sexual behavior in the era of highly active antiretroviral therapy. Curr Opin Infect Dis 2006; 19:26–32.
12. EuroHIV. HIV/AIDS Surveillance in Europe. End-year Report 2005. Saint-Maurice: Institut de Veille Sanitaire, 2006. No. 72.
13. Aalen OO, Farewell VT, De Angelis D, et al. New therapy explains the fall in AIDS incidence with a substantial rise in number of persons on treatment expected. AIDS 1999; 13:103–108.
14. CASCADE Collaboration. Survival after introduction of HAART in people with known duration of HIV infection. Lancet 2000; 355:1158–1159.
15. The UK Collaborative Group for HIV and STI Surveillance. Mapping the Issues. HIV and Other Sexually Transmitted Infections in the United Kingdom, 2005. London: Health Protection Agency Centre for Infections, 2005.
16. Fleming DT, Wasserheit JN. From epidemiological synergy to public health policy and practice: The contribution of other sexually transmitted diseases to sexual transmission of HIV infection. Sex Transm Infect 1999; 75:3–17.
17. Rottingen JA, Cameron DW, Garnett GP. A systematic review of the epidemiologic interactions between classic sexually transmitted diseases and HIV: How much is really known? Sex Transm Dis 2001; 28:579–597.
18. Lowndes CM, Fenton KA; European Surveillance of STI's Network. Surveillance systems for STIs in the European Union: Facing a changing epidemiology. Sex Transm Infect 2004; 80:264–271.
19. Velter A, Bouyssou-Michel A, Arnaud A, et al. Premier Resultants De l'Enquête Presse Gay 2004. Saint-Maurice: Institut de Veille Sanitaire, 2005.
20. Carroll D, Foley B, Hickson F, et al. Vital Statistics Ireland. Findings from the all-Ireland Gay Men's Sex Survey, 2000. Dublin: Gay Men's Health Network, 2002.
21. Folch C, Casabona J, Munoz R, et al. Trends in the prevalence of HIV infection and risk behaviors in homo- and bisexual men. Gac Sanit 2005; 19:294–301.
22. Balthasar H, Jeannin A, Dubois-Arber F. VIH/SIDA: Augmentation des expositions au risqué d'infection par le VIH chez les hommes ayant des rapports sexuels avec des hommes: Premier résultants de Gay Survey 04. Bull BAG 2005; 48:891–895.
23. Bolding G, Davis M, Sherr L, et al. Use of gay internet sites and views about online health promotion among men who have sex with men. AIDS Care 2004; 16:993–1001.
24. Marcus U, Hamouda O. Syphilis in Germany, 2004: Diagnoses increasing, particularly in smaller cities and rural areas. Euro Surveill 2005; 10:28/07/2005.
25. Defraye A, Sasse A. STI surveillance by a sentinel network of physicians in Belgium. Acta Clin Belg 2005; 60:69–73.
26. Hopkins S, Lyons F, Coleman C, et al. Resurgence of infectious syphilis in Ireland: An epidemiologic study. Sex Transm Dis 2004; 31:317–321.
27. Simms I, Fenton KA, Ashton M, et al. The re-emergence of syphilis in the United Kingdom: The new epidemic phases. Sex Transm Dis 2005; 32:220–226.
28. Couturier E, Michel A, Janier M, et al. Syphilis surveillance in France 2000–2003. Euro Surveill 2004; 9:8–10.
29. Sasse A, Defraye A, Ducoffre G. Recent syphilis trends in Belgium and enhancement of STI surveillance systems. Euro Surveill 2004; 9:6–8.
30. Cowan S. Syphilis in Denmark-outbreak among MSM in Copenhagan 2003–2004. Euro Surveill 2004; 9:25–27.
31. Health Protection Surveillance Centre and Health Services Executive. Enhanced Syphilis Surveillance in Ireland, Q1-2000 to Q2-2005. Dublin: The Health Protection Surveillance Centre, 2005.
32. Cusini M, Ghislanzoni M, Bernardi C, et al. Syphilis outbreak in Milan, Italy. Sex Transm Infect 2004; 80:154.
33. van de Laar M, van Veeke M, Götz H, et al. Continued transmission of syphilis in Rotterdam, The Netherlands. Euro Surveill 2003; 7:25/09/2003.
34. Blystad H, Nilsen Ö, Berglund T, et al. Syphilis outbreak in Norway and Sweden among men who have sex with men 1998–2002. Euro Surveill 2003; 7:12/06/2003.
35. Mayans MV, Benicio SC, Armengol P, et al. Outbreaks of infectious syphilis and other STIs in men who have sex with men in Barcelona, 2002–2003. Euro Surveill 2004; 10:28/10/2004.
36. Payne L, Berglund T, Henriksson L, et al. Re-emergence of syphilis in Sweden: Results from a surveillance study for 2004. Euro Surveill 2005; 10:10/11/2005.
37. Righarts A, Simms I, Wallace L, et al. Syphilis surveillance and epidemiology in the UK. Euro Surveill 2004; 9:21–25.
38. Wallace L, Winter A, Goldberg D. Increase in reported syphilis infections in Scotland in 2004. Euro Surveill 2005; 10:28/07/ 2005.
39. Irvine N, Doherty L. Sexually transmitted infections on the rise in Northern Ireland. Euro Surveill 2005; 10:03/02/2005.
40. Abraham B, Marih L, Thevenet S, et al. Outbreak of syphilis among HIV-infected patients: Descriptive data from a parisian hospital. Sex Transm Dis 2005; 32:718–719.
41. Bremer V, Marcus U, Hofmann A, et al. Building a sentinel surveillance system for sexually transmitted infections in Germany, 2003. Sex Transm Infect 2005; 81:173–179.
42. Lynch A, Smyth B. Syphilis outbreak in Northern Ireland. Euro Surveill 2003; 6:12/06/2003.
43. Macdonald N, Dougan S, McGarrigle CA, et al. Recent trends in diagnoses of HIV and other sexually transmitted infections in England and Wales amongst men who have sex with men. Sex Transm Infect 2004; 80:492–497.
44. Johansen JD, Smith E. Gonorrhea in Denmark: High incidence among HIV-infected men who have sex with men. Acta Derm Venereol 2002; 47:279–287.
45. Janier M, Lassau F, Casin I, et al. Pharyngeal gonorrhea: The forgotten reservoir. Sex Transm Infect 2003; 79:345.
46. Halsos AM, Edgardh K. An outbreak of syphilis in Olso. Int J STD AIDS 2002; 31:370–372.
47. Nieuwenhuis RF, Ossewaarde JM, van der Meijden WI, et al. Unusual presentation of early lymphogranuloma venereum in an HIV-1 infected patient: Effective treatment with Ig azithromycin. Sex Transm Infect 2003; 79:453–455.
48. Vandenbruaene M, Ostyn B, Crucitti T, et al. Lymphogranuloma venereum outbreak in men who have sex with men (MSM) in Belgium, January 2004 to July 2005. Euro Surveill 2005; 10:29/09/2005.
49. Institut de Veille Sanitaire. Surveillance des Infections Sexuellement Transmissibles. Actualitiés épidémiologiques sur le VIH, le SIDA et les IST, 2005.
50. Van de Laar MJ, Fenton KA, Ison C. Update on the European lymphogranuloma venereum epidemic among men who have sex with men. Euro Surveill 2005; 10:02/06/2005.
51. Plettenberg A, von Krosigk A, Stoehr A, et al. Four cases of lymphogranuloma venereum in Hamburg, 2003. Euro Surveill 2004; 8:22/07/2004.
52. Health Protection Surveillance Centre. Sexually Transmitted Infections 2004: Annual Summary Report. Dublin: Health Protection Surveillance Centre; 2005.
53. op de Coul ELM, de Boer IM, Koedijk FDH, et al. HIV and STIs increasing in the Netherlands according to latest surveillance data. Euro Surveill 2006; 11:16/02/2006.
54. Gebhardt M, Goldenberger D. Lymphogranuloma venereum (LGV) serotype L2 in Switzerland, 2003–2005. Euro Surveill 2005; 10:22/12/2005.
55. Berglund T, Bratt G, Herrmann B, et al. Two cases of lymphogranuloma venereum (LGV) in homosexual men in Stockholm. Euro Surveill 2005; 10:03/03/2005.
56. Vall Mayans M, Sanz Colomo B, Ossewaarde JM. First case of LGV confirmed in Barcelona. Euro Surveill 2005; 10:03/02/2005.
57. Health Protection Agency. Lymphogranuloma venereum in the United Kingdom: An update. Commun Dis Rep CDR Wkly [serial online] 2006; 16(24).
58. Herida M, Sednaoui P, Couturier E, et al. Rectal lymphogranuloma venereum, France. Emerg Infect Dis 2005; 11:505–506.
59. Nieuwenhuis RF, Ossewaarde JM, Götz HM, et al. Resurgence of lymphogranuloma venereum in Western Europe: An outbreak of Chlamydia trachomatis serovar L2 proctitis in the Netherlands among men who have sex with men. Clin Infect Dis 2004; 39:996–1003.
60. Götz HM, van Doornum G, Niesters GM, et al. A cluster of acute hepatitis C virus infection among men who have sex with men—Results from contact tracing and public health implications. AIDS 2005; 19:969–974.
61. Gambotti L; The Acute Hepatitis C Collaborating Group. Acute hepatitis C infection in HIV positive men who have sex with men in Paris, France, 2001–2004. Euro Surveill 2005; 10:115–117.
62. Ghosn J, Pierre-François S, Thibault V, et al. Acute hepatitis C in HIV-infected men who have sex with men. HIV Med 2004; 5:303–306.
63. Rauch A, Rickenbach M, Weber R, et al. Unsafe sex and increased incidence of hepatitis C virus infection among HIV-infected men who have sex with men: The Swiss HIV cohort study. Clin Infect Dis 2005; 41:395–402.
64. Browne R, Asboe D, Gilleece Y, et al. Increased numbers of acute hepatitis C infections in HIV positive homosexual men: Is sexual transmission feeding the increase? Sex Transm Infect 2004; 80:326–327.
65. Danta M, Brown D, Dusheiko G, et al. Evidence for sexual transmission of HCV in recent epidemic in HIV-infected men in the UK. Abstract 86, presented at 13th Conference on Retroviruses and Opportunistic Infections, Denver, 2006.
66. Coutinho R, Thijs van de Laar. Rise in HCV incidence in HIV-infected men who have sex with men in Amsterdam: Sexual transmission of difficult to treat genotypes 1 and 4. Abstract 87, presented at 13th Conference on Retroviruses and Opportunistic Infections, Denver, 2006.
67. Alary M, Joly JR, Vincelette J, et al. Lack of evidence of sexual transmission of hepatitis C virus in a prospective cohort study of men who have sex with men. Am J Public Health 2005; 95:502–505.
68. Dodds JP, Mercer CH, Mercey DE, et al. Men who have sex with men: A comparison of a probability sample survey and a community based study. Sex Transm Infect 2006; 82:86–87.
69. Chesson HW, Dee TS, Aral SO. AIDS mortality may have contributed to the decline in syphilis rates in the United States in the 1990s. Sex Transm Dis 2003; 30:419–424.
70. Davis M, Hart G, Bolding G, et al. Sex and the internet: Gay men, risk reduction and identity. Cult Health Sex 2006; 8:161–174.
71. Bolding G, Davis M, Hart G, et al. Gay men who look for sex on the internet: Is there more HIV/STI risk with online partners? AIDS 2005; 19:961–968.
72. Mercer CH, Imrie J, Davis M, et al. ‘The core within the core': Ultra-high risk sexual behavior and STI/HIV transmission risk in a UK sample of HIV-positive men who have sex with men (MSM). Abstract MP-105, presented at 16th Biennial meeting of the International Society for Sex Transm Dis Research (ISSTDR), Amsterdam, 2005.
73. Fenton KA, Imrie J. Increasing rates of sexually transmitted diseases in homosexual men in Western Europe and the United States: Why? Infect Dis Clin North Am 2005; 19:311–331.
74. Aral SO, Padian NS, Holmes KK. Advances in multilevel approaches to understanding the epidemiology and prevention of sexually transmitted infections and HIV: An overview. J Infect Dis 2005; 191 (Suppl 1):S1–S6.
75. Doherty IA, Padian NS, Marlow C, et al. Determinants and consequences of sexual networks as they affect the spread of sexually transmitted infections. J Infect Dis 2005; 191 (Suppl 1):S42–S54.
76. Dukers HTM, Spaargaren J, Geskus RB, et al. HIV incidence on the increase among homosexual men attending an Amsterdam sexually transmitted disease clinic: Using a novel approach for detecting recent infections. AIDS 2002; 16:F19–F24.
77. Page-Shafer K, Shiboski CH, Osmond DH, et al. Risk of HIV infection attributable to oral sex among men who have sex with men and in the population of men who have sex with men. AIDS 2002; 16:2350–2352.
78. Van der Bij AK, Stolte IG, Coutinho RA, et al. Increase in sexually transmitted infections, but not HIV, among young homosexual men in Amsterdam: Are STIs still reliable markers for HIV transmission? Sex Transm Infect 2005; 81:34–37.
79. Truong HH, Kellogg T, Klausner JD, et al. Increases in sexually transmitted infections and sexual risk behavior without a concurrent increase in HIV incidence among men who have sex with men in San Francisco: A suggestion for HIV serosorting? Sex Transm Infect 2006; 82:461–466.
80. Centers for Disease Control and Prevention. Sexually transmitted disease surveillance, 2004. Atlanta (GA): US Department of Health and Human Services, 2004.
81. Centers for Disease Control and Prevention. Resurgent bacterial sexually transmitted disease among men who have sex with men—King County, Washington, 1997–1999. MMWR Morb Mortal Wkly Rep 1999; 48:773–777.
82. Centers for Disease Control and Prevention. Outbreak of syphilis among men who have sex with men—Southern California, 2000. MMWR Morb Mortal Wkly Rep 2001; 50:117–120.
83. Fox KK, del Rio C, Holmes KK, et al. Gonorrhea in the HIV era: A reversal in trends among men who have sex with men. Am J Public Health 2001; 91:959–964.
84. Centers for Disease Control and Prevention. Primary and secondary syphilis among men who have sex with men—New York City, 2001. MMWR Morb Mortal Wkly Rep 2002; 51:853–856.
85. Kim AA, Kent CK, Klausner JD. Risk factors for rectal gonococcal infection amidst resurgence in HIV transmission. Sex Transm Dis 2003; 30:813–817.
86. Buchacz K, Greenberg A, Onorato I, et al. Syphilis epidemics and human immunodeficiency virus (HIV) incidence among men who have sex with men in the United States: Implications for HIV prevention. Sex Transm Dis 2005; 32:S73–S79.
87. Chesson HW, Heffelfinger JD, Voigt RF, et al. Estimates of primary and secondary syphilis rates in persons with HIV in the United States, 2002. Sex Transm Dis 2005; 32:265–269.
88. Van de Laar MJW, Götz HM, O de Zwart, et al. Lymphogranuloma Venereum among men who have sex with men—Netherlands, 2003–2004. MMWR Morb Mortal Wkly Rep 2004; 53:985–988.
89. Scheer S, Chu PL, Katz MH, et al. Effect of highly active antiretroviral therapy on diagnoses of sexually transmitted diseases in people with AIDS. Lancet 2001; 357:432–435.
90. Workowski KA, Berman SM. Sexually transmitted treatment guidelines, 2006. MMWR Morb Mortal Wkly Rep 2006; 55(RR11): 1–94.
91. Walter T, Lebouche B, Miailhes P, et al. Symptomatic relapse of neurologic syphilis after benzathine penicillin G therapy for primary or secondary syphilis in HIV-infected patients. Clin Infect Dis 2006; 43:787–790.
92. Cohen MS, Hoffman IF, Royce RA, et al. Reduction of concentration of HIV-1 in semen after treatment of urethritis: Implications for prevention of sexual transmission of HIV-1. AIDSCAP Malawi Research Group. Lancet 1997; 349:1868–1873.
93. Kofoed K, Gerstoft J, Mathiesen LR, et al. Syphilis and human immunodeficiency virus (HIV)-1 coinfection: Influence on CD4 T-cell count, HIV-1 viral load, and treatment response. Sex Transm Dis 2006; 33:143–148.