The Recent Increase of Syphilis Cases in Lyon University Hospitals Is Mainly Observed in HIV-Infected Patients: Descriptive Data From a Laboratory-Based Surveillance System

To the Editor: A recent increase of the incidence of syphilis has been observed in North America 1 and in Europe. 2 As this agent shares the sexual route of transmission with HIV, a rise of infection of HIV might also be expected. In France, most of the results have been reported from Paris 3 and data from other centers are lacking. The objective of this study is to report the recent increase of syphilis cases diagnosed in Lyon University hospitals and to describe the patient characteristics, with an emphasis on those co-infected with HIV. The patients from an area of about 2.5 millions inhabitants were referred to the Lyon University Hospital, the second largest teaching medical center in France, for diagnosis and care of syphilis. All biologic tests for syphilis diagnosis were done in a single university laboratory and the tests were requested mostly by patients receiving care in the university hospital. The patients who were already followed for HIV infection and who had given their informed consent were registered in the French Hospital database. 4 The laboratory database was linked to the HIV database using anonymous cross-checked linkage. All the diagnostic tests for syphilis have been performed in the same university laboratory for >10 years. We found no case of syphilis in 1998, 1 case in 1999, and no case in 2000. A sexually transmitted disease research laboratory test (bioMérieux, Marcy l'Etoile, France), and a Treponema pallidum hemagglutination test (Biokit, Barcelona, Spain) were used for initial screening. In case of positive result, fluorescent treponemal antibody absorption tests (bioMérieux) (IgG and IgM) and a solid-phase hemadsorption assay for IgM detection (SPHA) were done. A diagnosis of recent infection or reinfection was based on the detection of fluorescent treponemal antibody IgM and solid-phase hemadsorption assay IgM. According to the request of the physicians, hepatitis B surface antigen (HBsAg) (Bio-Rad, Marnes-La-Coquette, France), HIV antibodies (bioMérieux), and hepatitis C virus antibodies (Bio-Rad or Janssen Ortho, Inc., Toronto, Canada) were performed. All these tests used an enzyme-linked immunosorbent assay technique. HIV RNA level was measured with the versant HIV-RNA 3. 0. according to the manufacturer's technique (Bayer, Puteaux, France). A total of 2342, 2727, 2036, 2419, and 3421 syphilis screening tests were performed in 1998, 1999, 2000, 2001, and 2002, respectively. The first case of syphilis was identified in September 2001, and the cumulative number reached 28 cases on October 31, 2002. Most of the patients were men (92.9%), the median age was 34 years (range 23–89) and the men who had sex with men (MSM) accounted for 42.9% of cases (Table 1).TABLE 1: Characteristics of HIV-Infected Patients with Acute Syphilis in Lyon, FranceA total of 18 patients (64.3%) were HIV antibody positive. The median delay between the first positive HIV serology performed in the laboratory and acute syphilis was 38.7 months (range 0.2–106.3). At the time of syphilis diagnosis, the median HIV RNA level in the serum was 6719 copies/mL (range <50–325,809), 3 of 16 patients (19%) had <50 copies of HIV-RNA/mL, and the median CD4/mm3 was 416 (range 296–840). Among the 16 HIV-positive individuals followed in the Lyon HIV hospital database, 2 patients had AIDS, 9 patients were known to receive antiretroviral therapy at the time of syphilis, and 1 within 6 months of acute syphilis. Antibodies against hepatitis C virus were positive for 2 patients of 18. HBsAg was detected in 2 individuals of 19. Two patients (7.1%) were infected by syphilis, HIV, and hepatitis C virus, and 1 was infected by syphilis, HIV, and hepatitis B virus. None of the tested patients had concomitant syphilis, HIV, hepatitis C and B virus infection. We report an increase of acute syphilis, with 28 cases in Lyon University hospitals between September 2001 and October 2002, whereas no case had been observed the previous years. Syphilis occurred in HIV-infected patients for nearly 65% of cases and most of these patients were MSM. The HIV French Hospital database shows that they were also regularly followed. This issue is important for the dynamic of both epidemics because these individuals remain susceptible to sexually transmitted agents and a potential source of HIV for their partners. The 10 patients who received antiretroviral therapy within the 6 months before syphilis diagnosis might have developed HIV-resistant variants that they could have transmitted at the time they became infected with syphilis. However, a relatively low level of viral load (<104 copies/mL) observed in 56% of patients may have reduced the rate of transmission. 5 Since 1998, an increase of unsafe sex and sexually transmitted infections in HIV-positive individuals has been reported and specifically for MSM. 6 The use of highly active antiretroviral therapy (HAART) and the knowledge of one's undetectable HIV viral load or high CD4 count might be falsely reassuring factors for the risk of transmission. 7 Indeed, even while undetectable in the blood, HIV RNA has been found in the semen, 8 suggesting a possible transmission of the virus. Thus it should be interesting in a further investigation to determine whether HIV-infected individuals receiving HAART are overexposed to syphilis compared with those who are not treated. Our findings raise the following provocative but key question: In what population does HIV circulate? In other words, it seems important to know whether patients with HIV had risky behaviors with partners who were HIV infected. In the second case, we can expect a fast spreading of HIV in uninfected populations. Both infections can affect each other in a number of ways. The risk of HIV transmission is increased in case of genital ulceration 9 and the natural course of syphilis may be more malignant, more difficult to treat in HIV-positive persons. 10 A positive point of this study is that all the tests for syphilis serology were performed in the same laboratory over the past 10 years, limiting the detection bias. A selection bias toward patients with more severe disease or patients expecting more anonymous care cannot be excluded. Finally, another finding of this study is that some patients diagnosed with syphilis and HIV have poorly controlled HIV infection. Justifiably, scientists and public health specialists have been pressing for innovative sexually transmitted infection/HIV prevention campaigns and screening activities. 11 Our findings, which echo other reports, highlight the fact that even 20 years after recognition of the first case of AIDS, strong public health messages focused on populations with persistent behaviors at risk for HIV transmission remain crucial. Marine Giard, MD Philippe Chevallier Queyron, MD Jacques Ritter, MD Dominique Peyramond, MD Christian Trépo, MD Patrick Miailhes, MD Christian Chidiac, MD Jean-Louis Touraine, MD Jean-Michel Livrozet, MD André Boibieux, MD Jacques Fabry, MD Robert Allard, MD, MSc Philippe Vanhems, MD, PhD

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