Sexually Transmitted Diseases:
High Prevalence of Sexually Transmitted Infections in HIV-Infected Men During Routine Outpatient Visits in the Netherlands
Heiligenberg, Marlies MD*†; Rijnders, Bart MD, PhD‡; Schim van der Loeff, Maarten F. MD, PhD*†; de Vries, Henry J. C. MD, PhD*§¶; van der Meijden, Willem I. MD∥; Geerlings, Suzanne E. MD, PhD†; Fennema, Han S. A. MD, PhD*; Prins, Maria PhD*†; Prins, Jan M. MD, PhD†
From the *Department of Research, Cluster of Infectious Diseases, Health Service Amsterdam, Amsterdam, the Netherlands; †Division of Infectious Diseases, Tropical Medicine and AIDS, Department of Internal Medicine, Center for Infection and Immunity Amsterdam (CINIMA), Academic Medical Centre, Amsterdam, the Netherlands; ‡Division of Infectious Diseases, Department of Internal Medicine, Erasmus Medical Centre, Rotterdam, the Netherlands; §Department of Dermatology, Academic Medical Centre, Amsterdam, the Netherlands; ¶Centre for Infectious Diseases Control, National Institute for Public Health and the Environment (Rijksinstituut voor Volksgezondheid en Milieu, RIVM), Bilthoven, the Netherlands; and ∥Department of Dermatology, Erasmus Medical Centre, Rotterdam, the Netherlands
The authors thank all the participants and HIV physicians and HIV nurses of the Departments of Internal Medicine of the Erasmus MC in Rotterdam (especially Danny Brok) and the AMC in Amsterdam, for help with inclusion of patients. The authors also thank the colleagues of the Public Health Laboratory (Health Service Amsterdam), and the Microbiology Laboratories of the Erasmus MC and the AMC, especially Arjen Speksnijder, Karin Adams, and Douwe Abma for CT, LGV, and NG testing; Hans Zaaijer for providing HBV and HCV test results; Anita Buskermolen for syphilis testing; Suzanne Jurriaans and Margreet Bakker for their help with retrieving serum samples from participants; and Ronald Geskus for critical reading.
Supported by funds from the National Institute for Public Health and the Environment, Centre for Infectious Diseases Control, the Netherlands and by grant 7115 0001 from ZonMw, the Netherlands Organisation for Health Research and Development.
Presented previously at NCHIV, Amsterdam, 2009 and CROI, San Francisco, 2010.
The funding agencies had no role in the study design, data collection, data analysis, data interpretation, or the writing of the article.
Correspondence: Marlies Heiligenberg, MD, Public Health Service of Amsterdam, Nieuwe Achtergracht 100, 1018 WT, Amsterdam, the Netherlands. E-mail: email@example.com.
Supplemental Digital Content is available for this article. A direct URL citation appears in the printed text, and a link to the digital file is provided in the HTML text of this article on the journal's Web site (http://www.stdjournal.com).
Received for publication February 21, 2011, and accepted August 4, 2011.
Background: In the Netherlands, no guidelines exist for routine sexually transmitted infection (STI) screening of human immunodeficiency virus (HIV)-infected men having sex with men (MSM). We assessed prevalence and factors associated with asymptomatic STI.
Methods: MSM visiting HIV outpatient clinics of academic hospitals were tested for Chlamydia trachomatis (CT), Neisseria gonorrhoeae (NG), syphilis, and hepatitis B and C infection. Prevalence and risk factors were studied using logistic regression.
Results: In total, 659 MSM were included between 2007 and 2008. STI were found in 16.0% of patients, mostly anal CT and syphilis. One new hepatitis B and 3 new hepatitis C infections were identified. In multivariate analyses, any STI (syphilis, CT, or NG) was associated with patient's age below 40 years (odds ratio [OR]: 2.5, 95% confidence interval [CI]: 1.3–5.0), having had sex with 2 or more sexual partners (OR 2.1, 95% CI: 1.2–3.5), the use of the same sexual toys with a sexual partner (OR 2.2, 95% CI: 1.0–4.9), and enema use before sex (OR: 2.3, 95% 1.2–4.2). Syphilis was independently associated with fisting with gloves versus no fisting (OR: 4.9, 95% CI: 1.7–13.7) and with rimming (OR: 5.0, 95% CI: 1.7–15.0). CT or NG were associated with age below 45 years (age 40–44 years: OR: 2.4, 95% CI: 1.1–5.3; age <40 years: OR: 2.4, 95% CI: 1.1–5.4), enema use before sex (OR: 2.4, 95% CI: 1.3–4.4) and drug use during sex (OR: 2.4, 95% CI: 1.4–4.0).
Conclusions: High-risk sexual behavior was very common, and 16% of HIV-infected MSM in HIV care had an asymptomatic STI, mostly anal CT and syphilis. Development of STI screening guidelines is recommended.
Due to the introduction of combination antiretroviral therapy (cART), morbidity and mortality among human immunodeficiency virus (HIV) infected people has dramatically decreased, resulting in a near-normal life expectancy in high-income countries.1 This has led to an increasing number of HIV-infected men and women who are sexually active.
In recent years, the incidence of sexually transmitted infections (STIs) among men having sex with men (MSM) has increased,2–4 especially among HIV-infected MSM.2 This has been attributed to a decrease in safe sex practices.5–7 National surveillance at STI clinics in the Netherlands shows that prevalences of Chlamydia trachomatis (CT) and Neisseria gonorrhoeae (NG) infections and syphilis were higher among HIV-infected MSM than among HIV-negative MSM.8 The prevalence of CT and NG in HIV-infected MSM in primary HIV care in Western countries ranged from 0.25% for CT and 3.1% for NG to 14% for both CT and NG,9–11 and the prevalence of syphilis ranged from 1.8% to 6.4%.10,11 In Amsterdam, we found a syphilis incidence of 6.2/100 person-years in HIV-infected MSM in HIV care.12 In addition, outbreaks of lymphogranuloma venereum (LGV) and hepatitis C have been described in HIV-infected MSM.13,14
STI increases the transmission of HIV.15–18 HIV-infected MSM and their partners could benefit from prevention, early detection, and treatment of STI. In addition, certain STIs such as viral hepatitis and syphilis are difficult to treat and/or may have a less favorable outcome among HIV-infected patients.
Data on STI prevalence among the growing population of HIV-infected individuals are mostly limited to data collected at STI clinics. As individuals have a reason to attend those clinics (e.g., risk behavior or STI-related complaints), HIV-infected MSM seen at the HIV treatment centers in the Netherlands are more likely to be representative of the total population of HIV-infected MSM. Therefore, linkage of HIV treatment and STI screening could improve care for HIV-infected MSM.19,20
In the Netherlands, as in most European countries, no guidelines exist for routine STI screening of HIV-infected MSM, and STI and HIV care are currently not integrated. In this article, we report the results of routine STI screening in HIV-infected MSM visiting the HIV outpatient clinics of 2 large university hospitals in the Netherlands. Objectives of this study were to estimate the prevalence of STI during routine visits in this group, to determine the prevalence of high-risk sexual behavior, and to determine which factors are associated with the presence of STI.
MATERIALS AND METHODS
Study Population and Sampling Procedure
From October 2007 through June 2008, we enrolled HIV-infected patients who were scheduled for a regular visit at the HIV outpatient clinic of 2 university hospitals in the Netherlands: the Academic Medical Centre (AMC) in Amsterdam and the Erasmus Medical Centre (Erasmus MC) in Rotterdam. Eligible patients were all HIV-infected MSM (≥18 years of age) who could read Dutch or English. Patients who spontaneously reported STI symptoms were excluded and referred to the STI clinic because we only wanted to include those patients who at present would not have been screened for STI. Patients were also excluded if they had terminal illness, were in detention, had severe psychiatric problems, or changed antiretroviral therapy at that visit. Patients were asked to participate regardless of reported sexual activity in the previous 6 months. Participants gave written informed consent before inclusion in the study. The medical ethics committees of both hospitals approved the study.
Patients were asked to self-complete a written questionnaire including questions about STI testing and STI treatment in the past 6 months, current STI-related symptoms, number of sexual partners during the past 6 months and number of lifetime sexual partners, type of sexual relationships (i.e., steady, casual, or group sex), HIV status of sexual partners, sexual techniques used (e.g., fisting, anal sex, rimming [oral-anal contact]), condom use, enema use, bleeding during sex, and use of recreational drugs during sex.
In addition to the regular blood draw for standard HIV care, serum was collected for syphilis, hepatitis B (HBV), and hepatitis C (HCV) testing. If the patient had provided a blood sample <4 months ago, and the regular care did not require a new blood sample, the last stored sample was used for testing. Participants gave informed consent for this. Serum was routinely stored at −80°C. If a patient was already known to be HBsAg positive or immune for HBV after vaccination or infection, HBV serology was not done. Likewise, if a patient was already known to have antibodies against HCV, anti-HCV was not tested.
NG and CT screening was performed in urine samples, in anal swabs, and in pharyngeal swabs. In Amsterdam, urine and anal swabs for CT and NG testing (Aptima Urine Specimen Collection Kit and Aptima Vaginal Swab Specimen Collection Kit, Gen-probe Aptima Assay, Tigris, San Diego, CA) were self-collected, after verbal and written instruction. Pharyngeal swab (Aptima Unisex Swab Specimen Collection Kit for endocervical and Male Urethral Swab Specimens), collected by the nurse, was screened for oral NG. The Gen-probe Aptima Assay (Tigris, San Diego, CA) was used. In Rotterdam, urine (Becton Dickinson's [BD] ProbeTec ET system collection kit for urethral specimen collection, Sparks, MD) was self-collected after verbal instruction. A research-assistant collected the anal and pharyngeal swabs (BD ProbeTec ET system). The ProbeTec assay was used (BD, Sparks, MD).
CT-positive anal mucosal swabs were checked for LGV by serovar L typing as described earlier.21
In case of a newly diagnosed syphilis, or a positive CT or NG screening result, participants were referred to an STI clinic for diagnosis and treatment.
Assays for Syphilis, HBV, and HCV
Serum was tested for syphilis antibodies with Treponema pallidum hemagglutination assay and rapid plasma reagin (RPR) in Amsterdam and with Treponema screening assay and Venereal Disease Research Laboratory (VDRL) in Rotterdam. The diagnostic criterion for a new early or late syphilis was positive syphilis serology (Treponema pallidum hemagglutination assay in Amsterdam, Treponema screening assay in Rotterdam) in previously syphilis seronegative patients, or a 4-fold or more increase in RPR (in Amsterdam) or VDRL (in Rotterdam) titers in patients with a history of treated syphilis infections. A <4-fold increase in RPR or VDRL in previously syphilis seropositive patients was regarded as a past or adequately treated syphilis infection.
HBV and HCV serology was performed in Amsterdam, using AxSYM automated enzyme immunoassays (Abbott Laboratories, Chicago, IL) and in Rotterdam, using Architect assays (Abbott). Conventional rules for the diagnosis of past or present HBV infection were followed; HCV infection was diagnosed based on a positive enzyme-linked immunosorbent assay for anti-HCV followed by a positive HCV polymerase chain reaction test.
Numerical variables are summarized as medians with interquartile ranges (IQR) or categorical variables with percentages. Four age categories were created based on quartiles of the age distribution. HIV RNA levels and CD4 counts were only used in the analysis if they were measured within 90 days before or after the date of participation. Differences between the 2 HIV clinics regarding numerical variables or diagnoses were analyzed using the Mann-Whitney rank-sum test or the χ2 test, respectively. Logistic regression was used to assess associations between reported sexual behavior and the following outcomes: any STI (syphilis, CT, or NG), syphilis, and CT or NG. Univariable and multivariable odds ratios (ORs), and 95% confidence intervals (95% CIs) were calculated.
All variables with an overall P value <0.10 in univariable analyses were included in multivariable analyses, after which manual backward selection was performed. A variable was retained in the model if it was itself significantly associated with the outcome (P < 0.05) or if removal of the variable led to a considerable (larger than 10%) change in the OR of 1 or more of the other variables in the model. The correlations between variables that were associated with the outcome variable at P < 0.10 were examined with Spearman ρ. No variables were found with correlations coefficients above 0.8. Analyses were performed using STATA 9.2 (STATA Intercooled, College Station, TX).
In Amsterdam, 430 of 1007 HIV-infected MSM registered at the AMC HIV outpatient clinic participated (42.7%), and in Rotterdam, 229 of 577 (41.1%). Not all patients who visited the outpatient clinic in the inclusion period were invited to participate due to logistical restrictions. MSM who participated were older, had more often an undetectable plasma HIV RNA, and were more often on cART (all P ≤ 0.001) compared with those who did not participate. There was no significant difference in CD4 count or years on cART. Of the 659 men who participated in this study, 616 (93.5%) completed the questionnaire. Nine pharyngeal swabs, 22 anal swabs, and 33 urine samples were not tested or test results were missing. The most common reasons for missing CT or NG test results were the patient's inability to produce enough urine during the visit and technical problems such as handling error of the specimen.
Characteristics and Sexual Behavior of the Participants
Patient demographics are summarized in Table 1. The median age of the total population was 46 (IQR: 41–53) years. There was no difference in age between participants in Amsterdam and Rotterdam. In Amsterdam, 79.7% of participants were on cART compared with 68.6% in Rotterdam (P = 0.002), and, probably as a result, in Amsterdam more participants had a plasma HIV-RNA <150 copies/mL and a CD4 count ≥200 cells/mm3 compared with those in Rotterdam. In Table 2, information about STI complaints, sexual history, and sexual behavior is summarized. Although patients who spontaneously reported symptoms of STI were excluded, 84 (14.0%) MSM answered positive to a question in the questionnaire specifically enquiring about symptoms of STI. Of the 183 (29.9%) MSM who had been tested for STI in the previous 6 months, 16 (2.7%) were diagnosed with an STI, mostly rectal CT, urethral NG, or syphilis.
The median number of sexual partners in the last 6 months was 2 (IQR: 1–6). The most often reported sexual technique was oral sex (82.0%), followed by anal sex (70.6%), rimming (53.8%), and fingering (55.5%); 40.5% reported recreational drug use during sex. The use of sexual toys, the use of enemas before sex, and fisting were less often reported, that is, between 10% and 20%. Almost 10% of patients reported anal blood loss or anal blood loss of their sexual partner(s) during or after sex. In all, 100 men (17.0%) reported that they had not had sex in the previous 6 months.
Condom use differed significantly by the HIV-status of the sex partner: 22.6% of HIV-infected MSM reported unprotected anal sex with HIV-negative partners and 24.8% reported unprotected anal sex with partners with an unknown HIV-status. This is in sharp contrast with the percentage of men (62.3%) who reported unprotected anal sex with an HIV-infected sexual partner.
CT and NG
In Table 3, CT and NG prevalences are shown. Overall prevalence of CT was 8.6% and NG, 5.2%. There were no significant differences between Amsterdam and Rotterdam regarding the proportion of patients with CT or NG diagnoses. Anorectal LGV was diagnosed in 3 men (0.5%). Anal infections were more frequent than urethral infections (9.3% vs. 1.6%). Of the patients with non-oral CT or NG infections, 86.8% had an anal infection. Of those who reported not having had sex in the last 6 months, 8 men (8%) were diagnosed with CT (n = 4) or NG (n = 4).
HBV, HCV, and Syphilis
Ninety-one men (14.0%) were still susceptible for HBV infection and 619 men (95.4%) were susceptible for HCV infection (Table 3). One new HBV infection and 3 new HCV infections were identified. When we tested stored serum of these patients, we found that 2 patients appeared to be HCV infected between June 2006 and January 2007; the infection date of the third patient was unknown but dated from before January 2007.
One-third of the participants were known to have a positive syphilis serology, based on a past or adequately treated infection. New syphilis infections, based on serologic evidence, were found in 33 men (5.0%). Of those who reported not to have had sex in the last 6 months, 2 men (2%) were diagnosed with a new syphilis. HBV, HCV, and syphilis prevalence did not differ between the 2 HIV clinics.
Associations Between Demographics, Sexual Behavior and STI
We performed univariable (see Table, Supplemental Digital Content 1, http://links.lww.com/OLQ/A27), which shows univariate associations between demographic characteristics, sexual behavior, and any STI, syphilis, and CT/NG) and multivariable analyses to assess associations between sexual behavior and any STI (syphilis, CT, or NG) and separately syphilis, and CT or NG. The results of multivariable analyses are shown in Table 4.
Four factors remained significantly associated with any STI in multivariable analysis: age <40 years (OR: 2.5, 95% CI: 1.3–5.0), having had sex with 2 or more sexual partners in the last 6 months (OR: 2.1, 95% CI: 1.2–3.5), the use of the same sexual toys with a sexual partner (OR: 2.2, 95% CI: 1.0–4.9), and enema use before sex (OR: 2.3, 95% CI: 1.2–4.2).
Three factors remained significantly associated with CT or NG in multivariable analysis: younger age (age <40 years: OR: 2.4, 95% CI: 1.1–5.4; age 40–44 years: OR: 2.4, 95% CI: 1.1–5.3), enema use before sex (OR: 2.4, 95% CI: 1.3–4.4), and drug use during sex (OR: 2.4 95% CI: 1.4–4.0).
Two factors remained significantly associated with syphilis in multivariable analysis: fisting always with gloves (OR: 4.9, 95% CI: 1.7–13.7) and rimming (OR: 5.0, 95% CI: 1.7–15.0).
Because HIV-RNA data were lacking for a substantial subset of the participants, we performed the multivariable analysis reported above without including plasma HIV-RNA. We performed an extra analysis to examine whether plasma HIV-RNA was associated with any STI, including only the 436 participants with a known HIV-RNA; plasma HIV- RNA load ≥150 copies/mL was significantly associated with presence of any STI (OR: 2.1, 95% CI: 1.1–3.8).
Based on the variables independently associated with CT or NG infection, we made models to explore whether targeted screening based on the variables associated with CT or NG was possible. Restricting CT and NG testing to those <45 years of age, and/or using enemas before sex, and/or using drugs during sex in the last 6 months, we would have to screen 63.8% of all patients to find 91% of all CT and NG infections.
The most important findings of this study are that (1) high-risk sexual behavior in HIV-infected MSM in HIV care is very common and (2) the prevalence of STI during routine visits in HIV-infected MSM not spontaneously reporting symptoms is very high, that is, 16.0%, mostly syphilis and anal CT or NG. The prevalence of STI is even higher when we exclude men who did not have sex in the last 6 months, that is, 17.2%. However, from the 100 men who reported not to have had sex in the last 6 months, 10 (10.0%) were diagnosed with an STI. This means that STI screening should not be limited to those men who report to have been sexually active in the last 6 months. As shown before,22 patients had no problems with the self-collection of urine and anal swabs, and all procedures fitted in a standard consultation.
In our study, only 14% of participants were still susceptible for HBV, mainly due to vaccination nonresponse. Only 1 new HBV infection and 3 new HCV infections were found. Currently, 10 to 20 new HCV infections are detected yearly at the AMC. Testing for HCV is usually triggered by elevated liver enzymes found during regular clinic visits, and routine testing for HCV appears to be of limited added value. Indeed, in retrospect 2 of the 3 newly diagnosed HCV infections in this study were preceded by a new liver enzyme elevation and could have been diagnosed in this way.
We performed this study not only to assess the prevalence of STIs, but also to determine which risk factors are associated with these STIs. Patient's age below 40 years, having had sex with 2 or more sexual partners, the use of the same sexual toys with a sexual partner, and enema use before sex were associated with any STI.
Testing for NG/CT using a Nucleic Acid Amplification Technique (NAAT) is expensive, that is, around 50 euro. Therefore, based on the associations found in multivariable analyses, we examined what percentage of CT and NG would be found if we used targeted screening based on the items strongest associated with CT and NG, such as younger age, use of enemas, and the use of recreational drugs before sex. Still nearly two-third of the men would have to be screened. Therefore, the value of these screening questions is low.
Several strengths and weaknesses of the current study should be taken into consideration when interpreting these results. First, we tested patients scheduled for a regular visit in a routine setting, regardless of reported sexual activities in the last 6 months. Second, another strength of this study is that it provides data on various sexual techniques other than unsafe anal sex. This and the relatively large sample size made it possible to analyze the associations between detailed risk behaviors and STIs. A potential limitation of our study is that we have used a specimen collection kit for vaginal swabs to collect anal swabs, and that we have used the specimen collection kit for an endocervical and male urethral swab to collect pharyngeal swabs. The use of the kits for other than the intended sites is not approved by the Food and Drug Administration; nevertheless, it was shown that in a high prevalence group such as MSM, NAAT assays such as Aptima Combo 2 and ProbeTec have superior sensitivity compared with culture.23 The anal swab was self-collected in Amsterdam, whereas in Rotterdam, the research assistant took the anal swab. As the sensitivity and specificity of self-collected anal swabs is good,22,24 we believe this did not influence the test results. As several months may elapse before HCV antibodies become positive, we may have missed acute HCV infections, as we screened for HCV antibodies and only used an HCV polymerase chain reaction test when HCV antibodies were detected.25 Next, if the patient had provided a blood sample <4 months ago, and the regular care did not require a new blood sample, the last stored sample was used for testing. This means that we could have missed recent infections. Another limitation is that we did not specify insertive or receptive sex (anal sex, rimming, and/or fisting), because we were interested in unsafe versus safe sex and its association with STI in HIV-infected MSM. Therefore, we can not specify associations between insertive or receptive sex and STI. Participating patients were older, were more often on cART, and had a lower HIV-RNA viral load than nonparticipants. It is difficult to predict how this has influenced the results. Finally, we have no further details on actual drug use, as we did not ask about frequency, technique of drug use, or types of drugs used.
The prevalence of STI (syphilis, CT, or NG) found in our study (16.0%) is similar to the prevalence of 13.7% found in another study performed in an HIV clinic in Los Angeles, CA in 2008.10 The prevalence of syphilis in our study (5.0%) is similar to the 6.3% prevalence found in HIV-infected MSM under primary HIV care in Boston, MA,11 and is in line with a previous study performed in Amsterdam.12 The finding that 10.0% of MSM who reported not to have had sex in the last 6 months were diagnosed with an STI is in accordance with a recent study in HIV-infected men that showed that 11% of CT and NG cases would have been missed when only those patients acknowledging risk behavior during the prior month were screened.26
The prevalence of unsafe anal sex in the last 6 months (205/434, 47.2%) was higher than that found in other studies that reported the prevalence of unsafe anal sex in HIV-infected MSM in primary HIV care.10,27,28 Also, we found that if the sexual partner was HIV-negative, 22.6% of HIV-infected MSM reported unsafe anal sex. The high prevalence of unsafe anal sex in HIV-infected MSM fuels the spread of STI in this group. Unprotected anal sex can lead to HIV transmission, especially when a coinfection with STI is present. Therefore, transmission of HIV and STI from (STI coinfected) HIV-infected MSM to HIV-negative MSM in the Netherlands is likely.
The use of drugs during sex was associated with CT or NG. Similar findings were reported in other studies analyzing STIs in MSM.11,29,30 Drug use is associated with increased sexual risk behavior in MSM, especially with unprotected anal intercourse.31–33 We showed that rimming and fisting were associated with syphilis. These sexual techniques have been associated with CT, NG, and HCV in the past.34–36
The association between younger age and CT and NG has been found before.11 One other study found an association between the use of dildos and anal CT.37 However, in that study, no distinction was made between sharing and not sharing dildos with partners. MSM reporting receptive anal intercourse and fisting often take anal enemas before having sex for reasons of hygiene.38 Anal enemas have been shown to be associated with sexual transmission of HIV, LGV, HBV, and HCV in MSM39–42 and were associated with STIs in our study. The biologic and behavioral effects of anal enemas on the transmission of STI warrant further study.
In conclusion, STI during routine visits are common among HIV-infected MSM. Our study results suggest that routine screening is appropriate and should not be limited to those who report being sexually active or practicing high-risk sexual techniques. Because most STI found were either syphilis or anal CT/NG, we recommend screening for syphilis and for anal CT and NG and the development of guidelines about STI screening in HIV outpatient clinics.
1.Antiretroviral Therapy Cohort Collaboration. Life expectancy of individuals on combination antiretroviral therapy in high-income countries: A collaborative analysis of 14 cohort studies. Lancet 2008; 372:293–299.
2.Dougan S, Evans BG, Elford J. Sexually transmitted infections in Western Europe among HIV-positive men who have sex with men. Sex Transm Dis 2007; 34:783–790.
3.Fenton KA, Lowndes CM. Recent trends in the epidemiology of sexually transmitted infections in the European Union. Sex Transm Infect 2004; 80:255–263.
4.Nicoll A, Hamers FF. Are trends in HIV, gonorrhoea, and syphilis worsening in Western Europe? BMJ 2002; 324:1324–1327.
5.Stolte G, Dukers NH, de Wit JB, et al. A summary report from Amsterdam: Increase in sexually transmitted diseases and risky sexual behaviour among homosexual men in relation to the introduction of new anti-HIV drugs. Euro Surveill 2002; 7:19–22.
6.van Kesteren NM, Hospers HJ, Kok G. Sexual risk behavior among HIV-positive men who have sex with men: A literature review. Patient Educ Couns 2007; 65:5–20.
7.Ostrow DE, Fox KJ, Chmiel JS, et al. Attitudes towards highly active antiretroviral therapy are associated with sexual risk taking among HIV-infected and uninfected homosexual men. AIDS 2002; 16:775–780.
8.Vriend HJ, Koedijk FDH, van den Broek IVF, et al. Sexually transmitted infections, including HIV, in the Netherlands in 2009. National Institute for Public Health and the Environment. RIVM report 210261007; 2010. http://www.rivm.nl/bibliotheek/rapporten/210261007.html
. Accessed March 23, 2011.
9.Phipps W, Stanley H, Kohn R, et al. Syphilis, chlamydia, and gonorrhea screening in HIV-infected patients in primary care, San Francisco, California, 2003. AIDS Patient Care STDS 2005; 19:495–498.
10.Rieg G, Lewis RJ, Miller LG, et al. Asymptomatic sexually transmitted infections in HIV-infected men who have sex with men: prevalence, incidence, predictors, and screening strategies. AIDS Patient Care STDS 2008; 22:947–954.
11.Mayer KH, O'Cleirigh C, Skeer M, et al. Which HIV-infected men who have sex with men in care are engaging in risky sex and acquiring sexually transmitted infections: Findings from a Boston community health centre. Sex Transm Infect 2010; 86:66–70.
12.Branger J, van der Meer JT, van Ketel RJ, et al. High incidence of asymptomatic syphilis in HIV-infected MSM justifies routine screening. Sex Transm Dis 2009; 36:84–85.
13.Urbanus AT, van de Laar TJ, Stolte IG, et al. Hepatitis C virus infections among HIV-infected men who have sex with men: An expanding epidemic. AIDS 2009; 23:F1–F7.
14.Ward H, Miller RF. Lymphogranuloma venereum: Here to stay? Sex Transm Infect 2009; 85:157.
15.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.
16.Freeman EE, Weiss HA, Glynn JR, et al. Herpes simplex virus 2 infection increases HIV acquisition in men and women: Systematic review and meta-analysis of longitudinal studies. AIDS 2006; 20:73–83.
17.Jin F, Prestage GP, Imrie J, et al. Anal sexually transmitted infections and risk of HIV infection in homosexual men. J Acquir Immun Defic Syndr 2010; 53:144–149.
18.Rottingen JA, Cameron DW, Garnett GP. A systematic review of the epidemiologic interactions between classic sexually transmitted diseases and HIV: How much really is known? Sex Transm Dis 2001; 28:579–597.
19.Brickley DB, Almers L, Kennedy CE, et al. Sexual and reproductive health services for people living with HIV: A systematic review. AIDS Care 2011; 23:303–314.
20.Kennedy CE, Spaulding AB, Brickley DB, et al. Linking sexual and reproductive health and HIV interventions: A systematic review. J Int AIDS Soc 2010; 13:26.
21.Morre SA, Spaargaren J, Fennema JS, et al. Molecular diagnosis of lymphogranuloma venereum: PCR-based restriction fragment length polymorphism and real-time PCR. J Clin Microbiol 2005; 43:5412–5413.
22.van der Helm JJ, Hoebe CJ, van Rooijen MS, et al. High performance and acceptability of self-collected rectal swabs for diagnosis of Chlamydia trachomatis
and Neisseria gonorrhoeae
in men who have sex with men and women. Sex Transm Dis 2009; 36:493–497.
23.Ota KV, Tamari IE, Smieja M, et al. Detection of Neisseria gonorrhoeae
and Chlamydia trachomatis
in pharyngeal and rectal specimens using the BD Probetec ET system, the Gen-Probe Aptima Combo 2 assay and culture. Sex Transm Infect 2009; 85:182–186.
24.Moncada J, Schachter J, Liska S, et al. Evaluation of self-collected glans and rectal swabs from men who have sex with men for detection of Chlamydia trachomatis
and Neisseria gonorrhoeae
by use of nucleic acid amplification tests. J Clin Microbiol 2009; 47:1657–1662.
25.Thomson EC, Nastouli E, Main J, et al. Delayed anti-HCV antibody response in HIV-positive men acutely infected with HCV. AIDS 2009; 23:89–93.
26.Cachay ER, Sitapati A, Caperna J, et al. Denial of risk behavior does not exclude asymptomatic anorectal sexually transmitted infection in HIV-infected men. PLoS One 2009; 4:e8504.
27.Morin SF, Steward WT, Charlebois ED, et al. Predicting HIV transmission risk among HIV-infected men who have sex with men: Findings from the healthy living project. J Acquir Immun Defic Syndr 2005; 40:226–235.
28.Crepaz N, Marks G, Liau A, et al. Prevalence of unprotected anal intercourse among HIV-diagnosed MSM in the United States: A meta-analysis. AIDS 2009; 23:1617–1629.
29.Tabet SR, Krone MR, Paradise MA, et al. Incidence of HIV and sexually transmitted diseases (STD) in a cohort of HIV-negative men who have sex with men (MSM). AIDS 1998; 12:2041–2048.
30.Kim AA, Kent CK, Klausner JD. Risk factors for rectal gonococcal infection amidst resurgence in HIV transmission. Sex Transm Dis 2003; 30:813–817.
31.Rusch M, Lampinen TM, Schilder A, et al. Unprotected anal intercourse associated with recreational drug use among young men who have sex with men depends on partner type and intercourse role. Sex Transm Dis 2004; 31:492–498.
32.Colfax G, Vittinghoff E, Husnik MJ, et al. Substance use and sexual risk: a participant- and episode-level analysis among a cohort of men who have sex with men. Am J Epidemiol 2004; 159:1002–1012.
33.Koblin BA, Murrill C, Camacho M, et al. Amphetamine use and sexual risk among men who have sex with men: results from the National HIV Behavioral Surveillance study—New York City. Subst Use Misuse 2007; 42:1613–1628.
34.Templeton DJ, Jin F, McNally LP, et al. Prevalence, incidence and risk factors for pharyngeal gonorrhoea in a community-based HIV-negative cohort of homosexual men in Sydney, Australia. Sex Transm Infect 2010; 86:90–96.
35.Turner JM, Rider AT, Imrie J, et al. Behavioural predictors of subsequent hepatitis C diagnosis in a UK clinic sample of HIV positive men who have sex with men. Sex Transm Infect 2006; 82:298–300.
36.Jin F, Prestage GP, Mao L, et al. Incidence and risk factors for urethral and anal gonorrhoea and chlamydia in a cohort of HIV-negative homosexual men: The Health in Men Study. Sex Transm Infect 2007; 83:113–119.
37.Jin F, Prestage GP, Zablotska I, et al. High rates of sexually transmitted infections in HIV positive homosexual men: Data from two community based cohorts. Sex Transm Infect 2007; 83:397–399.
38.Carballo-Dieguez A, Bauermeister JA, et al. The use of rectal douches among HIV-uninfected and infected men who have unprotected receptive anal intercourse: Implications for rectal microbicides. AIDS Behav 2008; 12:860–866.
39.Rietmeijer CA, Penley KA, Cohn DL, et al. Factors influencing the risk of infection with human immunodeficiency virus in homosexual men, Denver 1982–1985. Sex Transm Dis 1989; 16:95–102.
40.de Vries HJ, van der Bij AK, Fennema JS, et al. Lymphogranuloma venereum proctitis in men who have sex with men is associated with anal enema use and high-risk behavior. Sex Transm Dis 2008; 35:203–208.
41.Schreeder MT, Thompson SE, Hadler SC, et al. Hepatitis B in homosexual men: Prevalence of infection and factors related to transmission. J Infect Dis 1982; 146:7–15.
42.Ndimbie OK, Kingsley LA, Nedjar S, et al. Hepatitis C virus infection in a male homosexual cohort: Risk factor analysis. Genitourin Med 1996; 72:213–216.
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