Because sexually transmitted infections (STIs) increase HIV transmission [1–3], HIV-infected patients and their partners benefit from early detection of STI. A study at two university HIV clinics in the Netherlands found that 16% of HIV-infected men who have sex with men (MSM) had asymptomatic STI , indicating that MSM would benefit from regular STI screening. However, its value for HIV-infected heterosexual men and women is unclear. Among such patients in the USA, the prevalence of Chlamydia trachomatis and Neisseria gonorrhoeae, tested in HIV clinics, varied between 0% and 5% [5–7]. The prevalence among these patients in other high-income countries has not been investigated recently.
In 2007 and 2008, we studied heterosexual patients who attended the HIV outpatient clinic of the Academic Medical Center (AMC) in Amsterdam for a routine visit. The study was approved by the AMC medical ethics committee and written informed consent was obtained. Whether or not they were sexually active, patients were eligible if they were aged 18 years and older, could understand Dutch, English or French and had not spontaneously reported STI symptoms at their routine visit. In case of spontaneously reported STI-related symptoms, patients were not included and referred to the STI outpatient clinic for further care. Men who indicated three or more male sexual partners in their lifetime were considered MSM and excluded. Patients were interviewed by a trained interviewer about demographics and both sexual behaviour in the preceding 6 months and lifetime. Oral, vaginal, and anal self-swabs were obtained [8,9], as were serum and urine samples. If a patient's blood had been sampled less than 4 months previously, and routine care did not require new sampling, the stored blood was used for serological testing.
C. trachomatis and N. gonorrhoeae were tested by Nucleic Acid Amplification Test (Gen-probe Aptima Assay, Tigris, San Diego, California, USA). Serologic testing for hepatitis B (HBV) and hepatitis C (HCV) was performed using Axsym automated enzyme immune assays (Abbott Laboratories, Chicago, Illinois, USA). Conventional rules for diagnosis of HBV or HCV infection were applied. HBV serology was not done for patients already known to be HBsAg-positive or HBV immune after vaccination or infection. Anti-HCV was not tested in patients known to have antibodies against HCV. Patients were screened for syphilis with Treponema pallidum haemagglutination assay (TPHA) and Rapid Plasma Reagin (RPR). Diagnostic criteria for recent syphilis infection was a positive TPHA with a recently found positive RPR or a more than four-fold increase in RPR titre compared with the last measurement. Analyses were performed using STATA, version 11 (Stata Corp, College Station, Texas, USA).
Of 895 HIV-infected heterosexual patients registered at the AMC HIV outpatient clinic, 245 participated (27.4%). Not all patients who visited the outpatient clinic in the inclusion period were invited to participate due to logistical restrictions. There were no significant differences in age, sex, ethnicity, transmission route, plasma HIV RNA, CD4 cell count, combination antiretroviral therapy (cART) use or duration of cART use between participants and those who did not participate.
The median age of the total population was 41 years, range 18–82 years (Table 1). All were tested for STI and 201 (82%) patients were interviewed, although some were unable or unwilling to answer all questions. Forty-nine percent were married or living with a partner.
Only four of all asymptomatic patients (1.6%) were diagnosed with an STI: two women had cervical C. trachomatis, one man had urethral C. trachomatis, and a woman with a history of injecting drug use and syphilis had a new syphilis infection [negative RPR in 2006 and new positive RPR (1 : 36) in 2008]. We diagnosed no new HBV infections. We diagnosed one HCV infection in a man who was an injecting drug user. As he reported no sex with men, this HCV infection was not classified as sexually acquired.
Table 1 describes the sexual behaviour of interviewed participants over the preceding 6 months. In the 44 participants who were not interviewed, we only found one STI (C. trachomatis). Therefore, there does not seem to be a reservoir of STI in those who were not interviewed. High-risk behaviour was low; unprotected vaginal and anal sex with a casual partner were reported by 3.2% and 1.7%, respectively. Recreational drug use just before or during sex was 8.4%. No sex at all was reported by 34.4%. Overall, 55.9% had one sexual partner; in 88.9% of cases this was a steady partner. Because we were interested in asymptomatic infections, we excluded patients who spontaneously reported STI symptoms at their routine visit. When questioning them about genital itching, redness, or pain, 34 (18.3%) of the 186 who responded to this question reported one or more symptoms; all 34 tested negative for C. trachomatis, N. gonorrhoeae, and syphilis.
Our most important finding is that the prevalence of asymptomatic STI is very low (1.6%) in this group of HIV-infected heterosexuals. It contrasts sharply with the 16% prevalence found in a study of HIV-infected MSM performed in the same setting , and with the moderate prevalence of C. trachomatis and N. gonorrhoeae found among HIV-infected women in a study done in the USA (Louisiana): 5.9% and 3.0%, respectively . However, in line with our findings, studies in 1999 and 2000 in the USA found a low prevalence of C. trachomatis (1.7%) , and C. trachomatis and N. gonorrhoeae (together 0.5%)  in HIV-infected men and women in HIV clinics. Our diagnosis of one new syphilis infection accords with other studies finding no syphilis  or a very low prevalence  in HIV-infected heterosexuals. Younger age is a risk factor for acquiring C. trachomatis [11,12], so age differences among studies can hinder comparisons. The finding of low prevalence in our population may be explained by the low level of high-risk sexual behaviour in interviewed participants.
Recently, HCV has emerged as an STI among HIV-infected MSM . However, the HCV infection diagnosed in this study was most likely transmitted through needle sharing, and this suggests that HIV-infected heterosexuals are still not at risk of sexually acquired HCV.
Although it has previously been suggested  that STI screening among HIV-infected heterosexuals should be considered, our study results suggest that STI screening during routine visits of asymptomatic heterosexual patients in clinics with comparable patient groups is currently not needed.
We would like to thank all study participants. In addition, we thank the HIV physicians and nurses of the Department of Internal Medicine of the AMC in Amsterdam for their help with inclusion of patients. We thank the colleagues of the Public Health Laboratory (Health Service of Amsterdam) and the Microbiology Laboratory of the AMC, especially Karin Adams, Douwe Abma, Hans Zaaijer, Anita Buskermolen, Suzanne Jurriaans and Margreet Bakker. We also thank Lucy Phillips for editorial review and Ronald Geskus for critical review of the manuscript.
J.P. is the guarantor of this study. J.P. and M.P. were responsible for study conceptualisation. J.P., M.P., H.d-V, S.G., M.H. and M.S. designed the study. M.H. and M.S. were responsible for data management and analysis. M.H., M.S. and J.P. wrote the article. All authors assisted in revising the manuscript. All authors have seen and approved the final version of the manuscript.
Conflicts of interest
There are no conflicts of interest.
This study was funded by grant 7115 0001 from ZonMw, the Netherlands Organisation for Health Research and Development. The funding agency had no role in the study design, data collection, data analysis, data interpretation, or writing of the article.
The protocol was approved by the medical ethics committee of the AMC, and all participants gave written informed consent.
1. 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
2. Jin F, Prestage GP, Imrie J, Kippax SC, Donovan B, Templeton DJ, et al. Anal sexually transmitted infections and risk of HIV infection in homosexual men
. J Acquir Immune Defic Syndr
3. 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
4. Heiligenberg M, Rijnders B, Schim van der Loeff MF, de Vries HJC, Speksnijder AGCL, Geerlings SE, et al. High prevalence of sexually transmitted infections in HIV-infected men during routine outpatient visits in the Netherlands. Sex Transm Dis
5. Absalon J, Della-Latta P, Wu F, El-Sadr WM. Sexual behaviors and condom use of HIV-infected men and women of color attending a treatment and care clinic
. J Natl Med Assoc
6. Klausner JD, Stanley H, Stansell J. STD screening among HIV-infected patients in care, San Francisco
. AIDS Patient Care STDS
7. Gatski M, Martin DH, Clark RA, Harville E, Schmidt N, Kissinger P. Co-occurrence of trichomonas vaginalis and bacterial vaginosis among HIV-positive women
. Sex Transm Dis
8. van der Helm JJ, Hoebe CJ, van Rooijen MS, Brouwers EE, Fennema HS, Thiesbrummel HF, 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
9. Moncada J, Schachter J, Liska S, Shayevich C, Klausner JD. 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
10. Phipps W, Stanley H, Kohn R, Stansell J, Klausner JD. Syphilis, chlamydia, and gonorrhea screening in HIV-infected patients in primary care, San Francisco, California
. AIDS Patient Care STDS
11. Arno JN, Katz BP, McBride R, Carty GA, Batteiger BE, Caine VA, et al. Age and clinical immunity to infections with Chlamydia trachomatis
. Sex Transm Dis
12. Datta SD, Sternberg M, Johnson RE, Berman S, Papp JR, McQuillan G, et al. Gonorrhea and chlamydia in the United States among persons 14 to 39 years of age 1999 to 2002
. Ann Intern Med
13. van de Laar TJ, Matthews GV, Prins M, Danta M. Acute hepatitis C in HIV-infected men who have sex with men: an emerging sexually transmitted infection
© 2012 Lippincott Williams & Wilkins, Inc.
14. Farley TA, Cohen DA, Wu SY, Besch CL. The value of screening for sexually transmitted diseases in an HIV clinic
. J Acquir Immune Defic Syndr