• View in gallery

    Number of new cases of recent syphilis per year among patients followed for human immunodeficiency virus infection in Martinique according to gender and sexual orientation. This figure appears in color at www.ajtmh.org.

  • View in gallery

    Number of new cases of recent syphilis per year among patients followed for human immunodeficiency virus infection in Martinique according to the professional status. This figure appears in color at www.ajtmh.org.

  • 1.

    Pugliese P, Cuzin L, Cabié A, Poizot-Martin I, Allavena C, Duvivier C, El Guedj M, de la Tribonnière X, Valantin MA, Dellamonica PNadis Group, 2009. A large French prospective cohort of HIV-infected patients: the Nadis Cohort. HIV Med 10: 504511.

    • Search Google Scholar
    • Export Citation
  • 2.

    Fenton KA, Breban R, Vardavas R, Okano JT, Martin T, Aral S, Blower S, 2008. Infectious syphilis in high-income settings in the 21st century. Lancet Infect Dis 8: 244253.

    • Search Google Scholar
    • Export Citation
  • 3.

    Cabié A, Rollin B, Pierre-François S, Abel S, Desbois N, Richard P, Hochedez P, Théodose R, Quist D, Hélénon R, Derancourt C, Cavelier A, Liautaud B, 2010. Reemergence of syphilis in Martinique, 2001–2008. Emerg Infect Dis 16: 106109.

    • Search Google Scholar
    • Export Citation
  • 4.

    Figueroa JP, Brathwaite A, Ward E, DuCasse M, Tscharf I, Nembhard O, Williams E, 1995. The HIV/AIDS epidemic in Jamaica. AIDS 9: 761768.

  • 5.

    Chow EPF, Wilson DP, Zhang L, 2011. HIV and syphilis co-infection increasing among men who have sex with men in China: a systematic review and meta-analysis. PLoS One 6: e22768.

    • Search Google Scholar
    • Export Citation
  • 6.

    Kahn RH, Heffelfinger JD, Berman SM, 2002. Syphilis outbreaks among men who have sex with men: a public health trend of concern. Sex Transm Dis 29: 285287.

    • Search Google Scholar
    • Export Citation
  • 7.

    Zoni AC, González MA, Sjögren HW, 2013. Syphilis in the most at-risk populations in Latin America and the Caribbean: a systematic review. Int J Infect Dis 17: e84e92.

    • Search Google Scholar
    • Export Citation
  • 8.

    Wolitski RJ, Valdiserri RO, Denning PH, Levine WC, 2001. Are we headed for a resurgence of the HIV epidemic among men who have sex with men? Am J Public Health 91: 883888.

    • Search Google Scholar
    • Export Citation
  • 9.

    Centers for Disease Control (CDC), 1984. Syphilis: United States, 1983. Morb Mortal Wkly Rep 33: 433436.

  • 10.

    Stall RD, Hays RB, Waldo CR, Ekstrand M, McFarland W, 2000. The Gay '90s: a review of research in the 1990s on sexual behavior and HIV risk among men who have sex with men. AIDS 14 (Suppl 3): S101S114.

    • Search Google Scholar
    • Export Citation
  • 11.

    Kravcik S, Victor G, Houston S, Sutherland D, Garber GE, Hawley-Foss N, Angel JB, Cameron DW, 1998. Effect of antiretroviral therapy and viral load on the perceived risk of HIV transmission and the need for safer sexual practices. J Acquir Immune Defic Syndr Hum Retrovirol 19: 124129.

    • Search Google Scholar
    • Export Citation
  • 12.

    Strauss BB, Greene GJ, Phillips G, Bhatia R, Madkins K, Parsons JT, Mustanski B, 2016. Exploring patterns of awareness and use of HIV pre-exposure prophylaxis among young men who have sex with men. AIDS Behav 21: 12881298.

    • Search Google Scholar
    • Export Citation
  • 13.

    Centers for Disease Control and Prevention (CDC), 2003. Internet use and early syphilis infection among men who have sex with men: San Francisco, California, 1999–2003. Morb Mortal Wkly Rep 52: 12291232.

    • Search Google Scholar
    • Export Citation
  • 14.

    Morlat P, 2013. Prise en charge médicale des personnes vivant avec le VIH. Recommandations du groupe d'experts. Rapport 2013. Available at: http://www.sante.gouv.fr/rapport-2013-sur-la-prise-en-charge-medicale-des-personnes-vivant-avec-le-vih.html. Accessed September 20, 2016.

    • Search Google Scholar
    • Export Citation
  • 15.

    Fleming DT, Wasserheit JN, 1999. 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 75: 317.

    • Search Google Scholar
    • Export Citation
  • 16.

    Roberts CP, Klausner JD, 2016. Global challenges in human immunodeficiency virus and syphilis co-infection among men who have sex with men. Expert Rev Anti Infect Ther 14: 10371046.

    • Search Google Scholar
    • Export Citation
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New Surge of Syphilis among Patients Living with Human Immunodeficiency Virus in Martinique in 2015

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  • 1 Service de Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire de Martinique, Fort de France, France
  • | 2 Service de Médecine Gériatrique, Hôpital de Champmaillot, Centre Hospitalier Universitaire de Dijon, Dijon, France
  • | 3 Service de Parasitologie, Mycologie, Centre Hospitalier Universitaire de Martinique, Fort de France, France
  • | 4 INSERM CIC1425, Centre Hospitalier Universitaire de Martinique, Fort de France, France

A syphilis outbreak began in Martinique, French Antilles, in 2004, initially among men who had sex with men (MSM) and who were living with human immunodeficiency virus (HIV). The outbreak subsequently affected all groups at risk, leading to a first epidemic peak in 2008. After an initial decrease, the outbreak started growing again in 2014 among patients living with HIV with unprecedented incidence among MSM. Herein, we describe the change in medical and social parameters of the outbreak since 2005.

INTRODUCTION

As in other western countries, a syphilis outbreak began in Martinique, French Antilles, in 2004, and concerned initially men who had sex with men (MSM) and who were living with human immunodeficiency virus (HIV). The outbreak spread rapidly in the other groups at risk, including crack cocaine users and persons leaving in precarious conditions. After an initial decrease in incidence, the outbreak started growing again in 2014 among patients living with HIV (PLHIV) and primarily concerns MSM.

Unpublished data of the French sexually transmitted infections (STIs) surveillance network highlight an increase in STIs, including syphilis, since 2012 among MSM, with a progression of high-risk sexual behavior in this population. In France, one-third of patients with a new diagnosis of recent syphilis were coinfected with HIV. In 2013, the incidence of HIV in Martinique was estimated at 26 per 100,000 person-years; among these persons, 35% were MSM.

MATERIALS AND METHODS

All PLHIV followed in the French University Hospital of Martinique between January 1, 2005 and December 31, 2015, with a new diagnosis of recent syphilis (primary, secondary, or early latent syphilis), were included. Both treponemal (Treponema pallidum hemagglutination assay) and nontreponemal tests (Venereal Disease Research Laboratory tests) were performed together at least annually in all PLHIV followed. All positive and discordant results were verified by using fluorescent treponemal antibody absorption. Characteristics of patients with a diagnosis made between January 1, 2005 and June 30, 2010 (first period), were compared with those diagnosed between July 1, 2010 and the December 31, 2015 (second period). Demographic and clinicobiological data were prospectively collected via the standardized electronic medical record Nadis®.1 We determined the medical and social parameters of patients affected by this outbreak, including demographical, immunovirological, socioprofessional data, and declared sexual orientation. Syphilis reinfections were defined as two or more distinct episodes of recent syphilis reported by the patient or the medical records.

RESULTS

Among a cohort of 1,047 PLHIV followed in Martinique in 2015, 201 recent cases of syphilis were diagnosed between January 1, 2005 and December 31, 2015 (Table 1). Median age of patients was 40.6 years. Mean annual incidence in the whole outbreak was 2.1%. The outbreak was characterized by a first epidemic peak in 2008 (first epidemic peak) and a new surge in 2015 (second epidemic peak) with respective annual incidences of 4.3 and 3.8%. Annual incidence among MSM living with HIV was evaluated at 6.6% in 2009 and 10.6% in 2015.

Table 1

Demographic data (number of patients) and incidence of recent syphilis among patients followed for HIV infection in Martinique per year, 2005–2015

Year20052006200720082009201020112012201320142015
PLHIV (total)6597247607878168518929479629911,047
Women245267279291314333343362368365378
Heterosexual men259274293295299313332355346364377
MSM155183188198203205217230248262292
Recent syphilisTotalNumber1211133410111815122540
Incidence (%)1.81.51.74.31.21.321.61.22.53.8
MSMNumber77713661311102031
Incidence (%)4.53.83.76.63.02.96.04.84.07.610.6

HIV = human immunodeficiency virus; MSM = men who have sex with men; PLHIV = patients living with HIV.

The main medical characteristics of patients are presented in Table 2: Age, immunovirological parameters (CD4 count, HIV viral load), and syphilis recurrence rates did not significantly differ between 2008 and 2015.

Table 2

Main characteristics of patients with recent syphilis among patients followed for HIV infection in Martinique: comparison between the first (2008) and the second (2015) epidemic peak

2005–2015 (N = 201)2008 (N = 34)2015 (N = 40)P value*
Age (years)40.1 (31.6–46.6)42.4 (36.6–48.6)40.5 (29.1–48.5)0.2
Women23 (11.4%)10 (31.5%)2 (5%)0.009
MSM127 (63.2%)13 (38.2%)31 (77.5%)< 0.001
Non-MSM men51 (25.4%)11 (32.4%)7 (17.5%)0.1
Viral hepatitis25 (12.4%)6 (17.6%)2 (5%)0.1
Immunovirological parameters
 Nadir CD4 (/mm3)294 (132–400)296 (119–379)270 (170–478)0.5
 CD4 (/mm3)584 (478–721)558 (471–703)621 (531–733)0.8
 HIV viral load (UI/mL)20 (20–444)20 (20–13,000)20 (20–594)0.4
HIV diagnosis (vs. syphilis):
 Before152 (75.6%)25 (73.5%)36 (90%)0.07
 Concurrent38 (18.9%)7 (20.6%)4 (10%)
 After11 (5.5%)2 (5.9%)0
Previous syphilis74 (36.8%)10 (29.4%)14 (35%)0.6

HIV = human immunodeficiency virus; MSM = men who have sex with men.

Comparison between 2009 and 2015 (Student's test for quantitative values, χ2 or Fisher's test for qualitative values).

As shown in Figures 1 and 2, the population affected in the epidemic peaks of 2008 differed from that in 2015.

Figure 1.
Figure 1.

Number of new cases of recent syphilis per year among patients followed for human immunodeficiency virus infection in Martinique according to gender and sexual orientation. This figure appears in color at www.ajtmh.org.

Citation: The American Journal of Tropical Medicine and Hygiene 97, 3; 10.4269/ajtmh.16-0760

Figure 2.
Figure 2.

Number of new cases of recent syphilis per year among patients followed for human immunodeficiency virus infection in Martinique according to the professional status. This figure appears in color at www.ajtmh.org.

Citation: The American Journal of Tropical Medicine and Hygiene 97, 3; 10.4269/ajtmh.16-0760

In 2015, recent syphilis was diagnosed in 36 men, including 31 MSM and two women. In 2008, recent syphilis was diagnosed in 23 men, including 13 MSM and 11 women. The outbreak affected proportionally more MSM during the second peak than during the whole study period (77.5% versus 62.2%, P = 0.03), whereas in the first peak MSM were less affected than during the whole study period (38% versus 63.2%, P = 0.006).

Socioprofessional status also differed between the two epidemic peaks: 12 patients were unemployed in 2015 (37.5%) versus 25 in 2008 (73.5%) and 93 (46.3%) considering the whole period of the study. Unlike the second peak of 2015, during the first peak, the outbreak affected proportionally more unemployed patients than during the whole period of the study (P = 0.003).

Concerning the educational level, recent syphilis was diagnosed among 25 patients without a bachelor's degree in 2008 (73.5%), 26 in 2015 (65%), and 111 (55.2%) considering the whole period of the study. Unlike the second peak of 2015, the first peak of 2008 affected proportionally more patients with a lower educational level compared with the whole period of the study (P = 0.04).

DISCUSSION

In 2000, a syphilis outbreak started in western countries, including France.2 This outbreak appeared in Martinique in 2004 among MSM living with HIV. Four years later, it shifted to other groups at risk, including heterosexuals, leading to a first epidemic peak in 2008.3 This shift was similar to that reported previously for HIV infection.4

The incidence of recent syphilis among PLHIV in Martinique more than tripled in 2015 compared with 2013. This highlights a clear surge of new cases during the past 2 years. However, the sociodemographic characteristics of infected patients have changed: although almost three-quarters of patients in the first epidemic peak were unemployed and/or had a low educational level, the proportion of patients in these categories was significantly lower in the 2015 peak. This sociodemographic switch may be related to the shift from one group at risk (PLHIV living in precarious conditions, crack-cocaine users, and sex workers) to another (MSM) with a higher mean socioprofessional level. In contrast, MSM were a minority during the 2008 epidemic peak, but the majority in 2015, confirming the upsurge during the two last years. However, these findings, which concern PLHIV, may not be generalizable to other populations affected by the syphilis epidemic and who are not infected with HIV. This outbreak of syphilis among MSM in Martinique is not isolated. Indeed, similar outbreaks have previously been reported throughout the world at different times.59 The acquired immunodeficiency syndrome epidemic has resulted in behavioral changes with a decrease in syphilis among MSM in the 90s.10 The current surge of syphilis is consistent with reports of increased high-risk sexual practices among MSM,8 in part related to a decreased perceived risk of HIV transmission, due to highly active antiretroviral therapy11 and preexposure prophylaxis development.12 As already described,13 the increasing use of social media to meet sex partners could also have facilitated the rapid expansion of syphilis among MSM in Martinique. The high incidence of recent syphilis among patients already followed for an HIV infection, especially since 2010, reflects the lack of condom use and the failure of prevention policies in this population. Unfortunately, data on sexual practices were not collected in this study, and we do not know if this new surge is associated with a progression of high-risk sexual behavior. Another limitation to the study is the lack of a multivariate analysis, due to the small number of patients, to control for confounders in the characteristics of the population.

Syphilis is the most common coinfection in newly diagnosed PLHIV in France14 and is associated with more frequent complications among PLHIV.2 As syphilis increases the risk of HIV infection15 and because MSM are at the highest risk of HIV infection,16 the control of this outbreak is a priority. Monitoring syphilis incidence among PLHIV is also an excellent indicator of sexual risk-taking among high-risk populations, including MSM. This study offers the opportunity to establish the sociodemographic shift of this new surge in a relatively isolated population of 400,000 people living in Martinique, and to sound the alarm on sexual risk-taking among the MSM population.

CONCLUSION

These data reveal a growing outbreak of syphilis since 2014 among PLHIV in Martinique. Contrary to the first epidemic peak of 2008, this new outbreak concerns mainly MSM. A strengthening of targeted preventive policies to prevent high-risk sexual practices is urgently required.

Acknowledgment:

We are grateful to Philip Bastable for assistance with language.

REFERENCES

  • 1.

    Pugliese P, Cuzin L, Cabié A, Poizot-Martin I, Allavena C, Duvivier C, El Guedj M, de la Tribonnière X, Valantin MA, Dellamonica PNadis Group, 2009. A large French prospective cohort of HIV-infected patients: the Nadis Cohort. HIV Med 10: 504511.

    • Search Google Scholar
    • Export Citation
  • 2.

    Fenton KA, Breban R, Vardavas R, Okano JT, Martin T, Aral S, Blower S, 2008. Infectious syphilis in high-income settings in the 21st century. Lancet Infect Dis 8: 244253.

    • Search Google Scholar
    • Export Citation
  • 3.

    Cabié A, Rollin B, Pierre-François S, Abel S, Desbois N, Richard P, Hochedez P, Théodose R, Quist D, Hélénon R, Derancourt C, Cavelier A, Liautaud B, 2010. Reemergence of syphilis in Martinique, 2001–2008. Emerg Infect Dis 16: 106109.

    • Search Google Scholar
    • Export Citation
  • 4.

    Figueroa JP, Brathwaite A, Ward E, DuCasse M, Tscharf I, Nembhard O, Williams E, 1995. The HIV/AIDS epidemic in Jamaica. AIDS 9: 761768.

  • 5.

    Chow EPF, Wilson DP, Zhang L, 2011. HIV and syphilis co-infection increasing among men who have sex with men in China: a systematic review and meta-analysis. PLoS One 6: e22768.

    • Search Google Scholar
    • Export Citation
  • 6.

    Kahn RH, Heffelfinger JD, Berman SM, 2002. Syphilis outbreaks among men who have sex with men: a public health trend of concern. Sex Transm Dis 29: 285287.

    • Search Google Scholar
    • Export Citation
  • 7.

    Zoni AC, González MA, Sjögren HW, 2013. Syphilis in the most at-risk populations in Latin America and the Caribbean: a systematic review. Int J Infect Dis 17: e84e92.

    • Search Google Scholar
    • Export Citation
  • 8.

    Wolitski RJ, Valdiserri RO, Denning PH, Levine WC, 2001. Are we headed for a resurgence of the HIV epidemic among men who have sex with men? Am J Public Health 91: 883888.

    • Search Google Scholar
    • Export Citation
  • 9.

    Centers for Disease Control (CDC), 1984. Syphilis: United States, 1983. Morb Mortal Wkly Rep 33: 433436.

  • 10.

    Stall RD, Hays RB, Waldo CR, Ekstrand M, McFarland W, 2000. The Gay '90s: a review of research in the 1990s on sexual behavior and HIV risk among men who have sex with men. AIDS 14 (Suppl 3): S101S114.

    • Search Google Scholar
    • Export Citation
  • 11.

    Kravcik S, Victor G, Houston S, Sutherland D, Garber GE, Hawley-Foss N, Angel JB, Cameron DW, 1998. Effect of antiretroviral therapy and viral load on the perceived risk of HIV transmission and the need for safer sexual practices. J Acquir Immune Defic Syndr Hum Retrovirol 19: 124129.

    • Search Google Scholar
    • Export Citation
  • 12.

    Strauss BB, Greene GJ, Phillips G, Bhatia R, Madkins K, Parsons JT, Mustanski B, 2016. Exploring patterns of awareness and use of HIV pre-exposure prophylaxis among young men who have sex with men. AIDS Behav 21: 12881298.

    • Search Google Scholar
    • Export Citation
  • 13.

    Centers for Disease Control and Prevention (CDC), 2003. Internet use and early syphilis infection among men who have sex with men: San Francisco, California, 1999–2003. Morb Mortal Wkly Rep 52: 12291232.

    • Search Google Scholar
    • Export Citation
  • 14.

    Morlat P, 2013. Prise en charge médicale des personnes vivant avec le VIH. Recommandations du groupe d'experts. Rapport 2013. Available at: http://www.sante.gouv.fr/rapport-2013-sur-la-prise-en-charge-medicale-des-personnes-vivant-avec-le-vih.html. Accessed September 20, 2016.

    • Search Google Scholar
    • Export Citation
  • 15.

    Fleming DT, Wasserheit JN, 1999. 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 75: 317.

    • Search Google Scholar
    • Export Citation
  • 16.

    Roberts CP, Klausner JD, 2016. Global challenges in human immunodeficiency virus and syphilis co-infection among men who have sex with men. Expert Rev Anti Infect Ther 14: 10371046.

    • Search Google Scholar
    • Export Citation

Author Notes

Address correspondence to Alain Putot, Service de Médecine Gériatrique, Hôpital de Champmaillot, Centre Hospitalier Universitaire de Dijon, 2 rue Jules Violle, Dijon 21079, France. E-mail: alain.putot@chu-dijon.fr

Financial support: This work was funded by Centre Hospitalier Universitaire de Martinique, France.

Authors' addresses: Alain Putot, Service de Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire de Martinique, Fort de France, France, and Service de Médecine Gériatrique, Hôpital de Champmaillot, Centre Hospitalier Universitaire de Dijon, Dijon, France, E-mail: alain.putot@chu-dijon.fr. Benoît Rozé, Sandrine Pierre-François, Mathilde Pircher, Rosalie Vilain, Patrick Hochedez, Karine Guitteaud, Ingrid Laudarin, and Sylvie Abel, Service de Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire de Martinique, Fort de France, France, E-mails: benoit.roze@chu-fortdefrance.fr, sandrine.pierre-francois@chu-fortdefrance.fr, mathilde.pircher@chu-fortdefrance.fr, rosalie.vilain@chu-fortdefrance.fr, patrick.hochedez@chu-fortdefrance.fr, karine.guitteaud@chu-fortdefrance.fr, ingrid.laudarin@chu-fortdefance.fr, and sylvie.abel@chu-fortdefrance.fr. Charline Miossec and Nicole Desbois, Service de Parasitologie, Mycologie, Centre Hospitalier Universitaire de Martinique, Fort de France, France, E-mails: charline.miossec@chu-fortdefrance.fr and nicole.desbois@chu-fortdefrance.fr. André Cabié, INSERM CIC1425, Centre Hospitalier Universitaire de Martinique, Fort de France, France, and Service de Maladies Infectieuses et Tropicales, Centre Hospitalier Universitaire de Martinique, Fort de France, France, E-mail: andre.cabie@chu-fortdefrance.fr.

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