Sexually Transmitted Diseases:
Infectious Syphilis Among Adolescent and Young Adult Men: Implications for Human Immunodeficiency Virus Transmission and Public Health Interventions
Brewer, Toye H. MD*†; Schillinger, Julie MD, MSc†‡; Lewis, Felicia M. T. MD†§; Blank, Susan MD, MPH†‡; Pathela, Preeti PhD‡; Jordahl, Lori MBA-HA¶; Schmitt, Karla MPH, PhD*; Peterman, Thomas A. MD, MSc†
From the *Bureau of STD Prevention, State of Florida Department of Health, Tallahassee, FL; †Field Epidemiology Unit, Division of STD Prevention, Centers for Disease Control and Prevention, Atlanta, GA; ‡Bureau of STD Control, New York City Department of Health and Mental Hygiene, New York, NY; §STD Control Program, Philadelphia Department of Public Health, Philadelphia, PA; and ¶STD Prevention and Control Program, Miami-Dade County Health Department, Miami, FL
The authors thank Stacy Shiver, Greta L. Anschuetz, MPH, Adrian Cooksey, MPH, Marsha Mullings, MPH, and Consuelo Beck-Sague, MD for support in the development of this manuscript.
Correspondence: Toye H. Brewer, MD, STD Program, Miami Dade County Health Department, 1350 NW 14th St, Miami, FL 33125. E-mail: email@example.com.
Received for publication June 23, 2010, and accepted September 28, 2010.
Background: In 2008, an increase in syphilis among young black men was noted in New York City (NYC), Miami-Fort Lauderdale, and Philadelphia. To explore this trend, we examined infectious syphilis cases from 2000 to 2008 among adolescent and young adult men in these areas.
Methods: Descriptive analysis of male infectious syphilis cases reported to public health authorities in NYC, FL, and Philadelphia.
Results: From 2000 to 2008, infectious syphilis cases among males increased in NYC (107–1027 cases), Miami-Fort Lauderdale (109–374), and Philadelphia (41–142). This increase was largely attributable to cases among men who have sex with men. Rates among black adolescent males (15–19 years) increased in NYC ([2.6–43.0]/100,000), Miami-Fort Lauderdale ([5.5–48.1]/100,000), and Philadelphia (]8.3–40.3]/100,000). Among males with infectious syphilis in 2008 in NYC, 9.1% of blacks and 6.6% of Hispanics were adolescents compared with 1.6% of whites (P < 0.001). In Miami-Fort Lauderdale, 12.2% of black males were adolescents compared to 2.0% of whites (P < 0.01) and 2.7% of Hispanics (P < 0.01). Black males dominated all age groups in Philadelphia, but were more likely to be <25 years of age than whites (P = 0.02). Human immunodeficiency virus coinfection rates were 14.8% among adolescent males in NYC, 15.4% in Philadelphia, and 25.0% in Miami-Fort Lauderdale.
Conclusions: Very young black males have emerged as a risk group for syphilis in these 3 areas, as have young Hispanic males in NYC. Many are men who have sex with men and some are already human immunodeficiency virus-infected. Targeted risk reduction interventions for these populations are critical.
The current US syphilis epidemic, which began in about 2000, was initially characterized by a predominance of older white and Hispanic men who have sex with men (MSM), who were often human immunodeficiency virus (HIV) coinfected.1,2 Adolescents, primarily heterosexual blacks, accounted for 10% to 12% of infectious (primary and secondary) syphilis cases during the early 1990s3 but only 4.4% of all cases in 2004.4 We noticed increases in infectious syphilis cases among very young black MSM in our areas, New York City (NYC), Miami-Fort Lauderdale, and Philadelphia since 2005. These increases are particularly concerning due to the strong association of syphilis with HIV transmission. Syphilis increases the efficiency of HIV transmission 3- to 5-fold5 and was associated with HIV-infection among black and Hispanic adolescents in NYC during the last epidemic.6
MSM are the group most affected by HIV in the United States. Black and to a lesser extent Hispanic MSM tend to acquire HIV-infection at younger ages than their white counterparts.7,8 Therefore, syphilis increases in young MSM require public health interventions not only to control syphilis transmission but also to reinforce, or initiate, HIV prevention activities. In order to gain insight into this problem, we quantified and examined patterns of increases in infectious syphilis among black, Hispanic, and whites 15 to 19 years of age, 20 to 24 years of age, and over 25 years of age in each of our 3 jurisdictions.
We used surveillance data from NYC, Philadelphia (Philadelphia County), and the metropolitan statistical area of Miami-Fort Lauderdale (Miami-Dade and Broward Counties) to examine age-related trends in infectious syphilis. Each jurisdiction collects standardized data required for completion of Centers for Disease Control and Prevention (CDC) surveillance forms. Infectious syphilis data from 2000 to 2008 from each jurisdiction were analyzed by age group (15–19, 20–24, >25 years), gender, sexual behavior, and HIV status. We limited our analysis to cases of infectious syphilis (primary and secondary),4 because they most accurately reflect incident infections and other stages of syphilis are frequently misclassified.9 As increasing rates among males was the remarkable finding, cases among women were not included in the analysis except for the computation of male-to-female ratios.
Age groups were compared and trends examined, including the number and proportion of cases in each age group, racial/ethnic composition, sexual behavior, and HIV status. MSM were men who self-reported sex with men or were named by sex partners of the same gender. Data on HIV serostatus were self-reported unless a positive test result was obtained in the health department sexually transmitted disease (STD) clinic database or, in the case of Florida, cross-linked with the HIV surveillance database. Only HIV-positive results are reported here, as only NYC data clearly differentiated between unknown and negative results. Data on HIV status for Philadelphia were limited to 2007–2008.
Data were analyzed using Open-Epi (version 2.3, www.openepi.com) statistical calculators for bivariate analyses and for calculation of risk ratios and 95% confidence intervals (CI). Chi square tests of independence for frequencies were used to test for differences between groups over time (2000 vs. 2008) and by race. All statistical tests were 2 tailed and results were considered statistically significant when P ≤ 0.05. Rates per 100,000 were calculated using US census data for 2000 and 2008 US Government intercensal estimates for Miami-Fort Lauderdale and Philadelphia, and 2000 census and 2007 intercensal estimates for NYC.
Overall Infectious Syphilis Trends
NYC, Miami-Fort Lauderdale, and Philadelphia all experienced increases in infectious syphilis cases among males from 2000 to 2008. Increase in infectious syphilis cases was from 107 to 1027 (nearly 10-fold) in NYC, from 109 to 374 cases (over 3-fold) in Miami-Fort Lauderdale, and from 41 to 142 (over 3-fold) in Philadelphia. Cases among males greatly exceeded those among females, reflecting the increased percentage of cases among MSM, with subsequent increases in the male-to-female ratio of syphilis cases. Male-to-female ratio increased from approximately 10:1 to 28:1 in NYC. Miami-Fort Lauderdale, which had the highest proportion of female cases, had a ratio increase from 3:1 to 6:1, and in Philadelphia the ratio increased most dramatically from 2:1 to 18:1. HIV coinfection increased from 12.1% to 25.4% in NYC, and from 22.9% to 45.4% in Miami-Fort Lauderdale.
Ages 15 to 19
From 2000 to 2008, all 3 areas had increases in the number of infectious syphilis cases among adolescent males 15 to 19 years of age, with an apparent jump in cases around 2006 (Fig. 1). In each area, increases in infectious syphilis cases among 15 to 19 years old males were greater than those among cases overall; cases in this age group increased 18-fold in NYC, 8-fold in Miami-Fort Lauderdale, and over 6-fold in Philadelphia (Table 1). In 2008, in each area, most adolescent male cases were MSM and 14% to 25% of adolescent male cases were coinfected with HIV (Table 1). In NYC, 9.1% of all black male cases and 6.6% of all Hispanic male cases were in the adolescent age group compared with 1.6% of white male cases (RR: 5.7, 95% CI: 4.4, 8.3 for blacks and RR: 4.1, 95% CI: 1.4, 12.2 for Hispanics). In Miami-Fort Lauderdale, black, but not Hispanic males, were significantly more likely to be in the adolescent age group than white males; 12.2% of black males were in the adolescent age group compared to 2.0% of whites (RR: 6.0; 95% CI: 1.4, 25.3) and 2.7% of Hispanics (RR: 4.6; 95% CI: 1.4, 15.1). In Philadelphia, blacks were more likely to be in the adolescent age group than whites (10.5% vs. 4%) but the difference was not statistically significant, perhaps due to the smaller number of cases.
Ages 20 to 24
Similar trends were observed among 20 to 24 years old men in each area over the same time period (Table 1). Cases among males in this age group increased 12-fold in NYC, 8-fold in Miami-Fort Lauderdale, and 9-fold in Philadelphia. Again, the majority of male cases were MSM. Reported HIV coinfection rates were higher in the 20 to 24 years old age group than among adolescents (Table 1). In NYC in 2008, 17.4% of black and 17.9% of Hispanic males with infectious syphilis were in this age group compared with 5.2% of white males (RR: 3.4, 95% CI: 1.9, 6.0 for blacks; RR: 3.3; 95% CI: 1.8, 6.0 for Hispanics). Similarly, in Miami-Fort Lauderdale black, but not Hispanic, males were more likely to be in this age group (23% of black cases vs. 5.1% of white cases [RR: 4.5; 95% CI: 1.8–11.2] and 8.9% of Hispanics [RR: 3.0; 95% CI: 1.4, 7.0]). In Philadelphia, blacks were more likely to be in this age group compared to whites (22.8% vs. 4.0%), although this difference was not statistically significant.
Age 25 and Greater
In each of these 3 metropolitan areas, there were large increases in infectious syphilis among men 25 or more years of age (Table 1). Although the number of cases was much larger, the proportional increases were not as high as among younger age groups. Again, a majority of cases were identified as MSM and HIV coinfection rates were higher than among other age groups (Table 1). In 2008 in NYC, 93.2% of white males diagnosed with infectious syphilis were in this age group compared with 73.5% of blacks (RR: 1.44; 95% CI: 1.27, 1.63) and 76.5% of Hispanics (RR: 1.21; 95% CI: 1.12, 1.31). In Miami-Fort Lauderdale, 92.9% of white males and 89.3% of Hispanics diagnosed with infectious syphilis were in this age group compared with 64.6% of blacks (RR: 1.44, 95% CI: 1.26, 1.64 for whites; RR: 1.37, 95% CI: 1.19, 1.57 for Hispanics). In Philadelphia, 92.0% of white males were in this age group compared with 66.7% of black males (RR: 1.38; 95% CI: 1.16, 1.65). Due to the small number of Hispanic cases in Philadelphia, we did not calculate risk ratios for this group.
Although the number of cases in each age group varied considerably by metropolitan area in 2008, rates, by age group, were remarkably similar for blacks (Table 2). Rates among whites, by age group, were also very similar in NYC and Miami-Fort Lauderdale, while they were considerably lower in Philadelphia. While infectious syphilis rates among black males were higher than among white males in each of the 3 age groups in 2008, the difference was most striking among adolescents and young adults.
Since 2006, adolescent and young adult black men have emerged as a risk group for syphilis in NYC, Philadelphia, and Miami-Fort Lauderdale, with rates that have increased rapidly. Blacks were disproportionately affected in all 3 metropolitan areas. Young Hispanic males were also affected in NYC, but not in Miami-Fort Lauderdale. Although most young men were identified as MSM, the actual percentage of cases among MSM is likely to be higher because some young men (particularly nonwhites) are unwilling to self identify as MSM.10,11
Among the young men with infectious syphilis in this analysis, reported HIV coinfection was high. However, the proportion of men with infectious syphilis who were HIV coinfected was likely underestimated as some men were not tested at the time of syphilis diagnosis and some men who were HIV-infected may not have reported their serostatus. Other men with early syphilis may have had acute HIV infection that would not be detectable with an antibody test,12 and thus they may have believed they were HIV-negative. Black MSM and, to a lesser extent, Hispanic MSM generally acquire HIV infection at a younger age than white MSM and have a higher seroprevalence of HIV.7,8 Although blacks are a minority group in the US population, twice as many black MSM aged 13 to 24 years were diagnosed with HIV-infection from 2000 to 2006 compared with white MSM in the same age group.7 Although there is no evidence to suggest that black MSM have higher risk sexual behaviors,13,14 this may be partly related to the structure of their sexual networks. For example, black MSM are more likely to have significantly older sex partners compared with other MSM, increasing the risk of HIV transmission from older to younger men.15–17 Evidence also suggests that higher rates of STDs among black MSM are facilitating HIV transmission13,18 and that black MSM are often unaware of their HIV serostatus and, therefore, are at greater risk of infecting partners.13,14 Therefore, reaching young black MSM as early as possible with prevention messages is critical. However, this task is particularly difficult because these young men may not realize (or admit) that they are MSM. A sexually transmitted infection may be the only thing that brings these young men in contact to health care; therefore, it is especially important that providers take a nonjudgmental sexual history, which includes ascertaining the sex of sexual partners. This may be the first opportunity for these young men to openly discuss their sexuality with a healthcare provider.
HIV prevention counseling and HIV testing are of critical importance for young MSM diagnosed with syphilis or any other sexually transmitted infections, providing what for many may be their only opportunity for risk reduction counseling.19 Risk reduction counseling for persons previously known to have been HIV-infected should be offered and those with newly diagnosed HIV infection should be linked to care. Those who are HIV-negative need to have follow-up testing to rule out seroconversion, particularly if diagnosed with primary syphilis. Due to the high risk of seroconversion, persons with primary syphilis who test negative for HIV should be retested after 3 months if negative serology is not followed by HIV polymerase chain reaction testing to rule out acute infection.20,21 They also should be counseled to reduce risk behaviors in order to prevent subsequent HIV-infection.22–24
Few risk-reduction interventions have been tailored to young black and Hispanic MSM, although they should be an urgent research priority.22,24 Currently, 2 prevention interventions targeting black MSM are offered in the CDC's Diffusion of Effective Behavioral Interventions.25 Many Voices, Many Men was a randomized controlled intervention for black MSM who demonstrated decreased unprotected anal intercourse with casual partners and increased HIV testing in the intervention arm.26 The second intervention, d-up: Defend Yourself was successfully adapted for black MSM after having been shown to decrease risk behaviors among other MSM groups.27 Neither of these interventions is specifically addressed to youth under 18 years of age.
Even with the existence of evidence-based interventions, only a small fraction of at-risk MSM is being reached with prevention messages28,29 outside of HIV pre- and post-test counseling scenarios.19 In the 2003 to 2005 cycle of the CDC-sponsored National HIV Behavioral Risk Surveillance, only 15% of MSM reported receiving individual level risk reduction interventions while 8% reported receiving group level interventions.29 For Miami-Dade County, the percentage of men receiving such services showed little change from the 2005 to the 2008 cycle—from 13% reporting individual and 6% reporting group interventions in 200529 to 13% and 5% respectively in 2008.19 Unfortunately, if current trends continue the deterioration of sexual health of MSM in the United States28 will continue, with black MSM bearing a disproportionate burden of disease.
This study has the limitations of likely underestimating the HIV seroprevalence and proportion of male cases identified as MSM. Data on heterosexual activities among MSM were not available. Additionally, data on race/ethnicity were missing in some cases. There were also some variations in data collection methods between STD control programs in the 3 jurisdictions; however, these were minor. We studied the NYC, Philadelphia, and Miami-Fort Lauderdale syphilis epidemics as these are the areas where we work. These results therefore may not represent the experience of other East Coast areas. However, while we are not aware of specific studies examining infectious syphilis trends in young MSM by race in other local areas, the findings of increased syphilis among young black MSM are supported by national data.30
The MSM syphilis epidemic is increasingly diverse and involves MSM of different age and racial/ethnic groups with their own subcultures. New, targeted prevention messages for young black and Hispanic MSM are essential. In order to facilitate effective counseling and interventions, syphilis trends among youth in areas with ongoing syphilis epidemics trends should be stratified by race/ethnicity and monitored. Types of hangouts, methods of sex partner selection and recruitment, and comfort level with public health agencies attempting to perform contact investigation is likely to vary among different age groups, racial/ethnic groups, and persons of different sexual orientation. Understanding these differences is critically important to meet the prevention needs of this population.
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