The High Risk of an HIV Diagnosis Following a Diagnosis of Syphilis: A Population-level Analysis of New York City Men
The High Risk of an HIV Diagnosis Following a Diagnosis of Syphilis: A Population-level Analysis of New York City Men
Preeti Pathela () 2
Sarah L. Braunstein 1
Susan Blank 0 2
Colin Shepard 1
Julia A. Schillinger 0 2
0 Division of STD Prevention, Centers for Disease Control and Prevention , Atlanta , Georgia
1 Bureau of HIV/AIDS Prevention and Control, New York City Department of Health and Mental Hygiene , New York
2 Bureau of Sexually Transmitted Disease Control
Background. Epidemiologic studies have shown that syphilis is associated with risk for human immunodeficiency virus (HIV) infection. We used population-level syphilis and HIV data to quantify HIV incidence among men following primary or secondary (P&S) syphilis diagnoses and identify the highest-risk subgroups for intensified prevention, such as pre-exposure prophylaxis with antiretroviral medications. Methods. Male cases reported to the New York City HIV/AIDS and Sexually Transmitted Disease (STD) surveillance registries were matched using a deterministic algorithm. We measured HIV incidence following P&S syphilis diagnosed between 2000 and June 2010 and identified risk factors for HIV infection using Cox proportional hazards models. Results. Of 2805 men with syphilis contributing 11 714 person-years of follow-up, 423 (15.1%) acquired HIV; annual incidence was 3.61% (95% confidence interval [CI], 3.27%, 3.97%). HIV incidence was high among: men who have sex with men (MSM) (5.56%, 95% CI, 5.02%-6.13%); males with secondary compared with primary syphilis (4.10% vs 2.64%, P < .0001); and males diagnosed with another bacterial STD after syphilis (7.89%, 95% CI, 6.62%-9.24%). Conclusions. HIV incidence among men diagnosed with syphilis is high; one in 20 MSM were diagnosed with HIV within a year. Our data have implications for syphilis and HIV screening and may be useful for further targeting HIVnegative populations for pre-exposure prophylaxis.
syphilis; HIV incidence
Human immunodeficiency virus (HIV) infection
disproportionately affects men in the industrialized
world, primarily gay men and other men who have
sex with men (MSM) . In 2012 in New York City
(NYC), 79% of 3141 new HIV/AIDS diagnoses were
among men, and 69% of new male diagnoses were
among MSM . NYC surveillance data also indicate
a large burden of sexually transmitted diseases (STD)
among men, with 96%–98% of primary and secondary
(P&S) syphilis cases each year being male, and >80% of
male cases being among MSM . Significant overlap in
subpopulations of NYC men affected by HIV and P&S
syphilis, and large increases in disease rates over time
have been reported . Syphilis may be associated
with a high risk for subsequent HIV infection because:
(1) syphilis lesions are efficient portals of entry for the
HIV virus; (2) HIV can be found in syphilis lesions; and
(3) there are high rates of HIV co-infection among
MSM with syphilis  (eg, 64% of NYC MSM
diagnosed with P&S syphilis in 2013 reported being
HIVinfected ), and with especially high HIV prevalence
in certain sexual networks, a person who is exposed to a
partner with syphilis is likely exposed to HIV during the
same sexual encounter.
To prevent the spread of HIV, it is necessary to
identify persons for prevention interventions such as
pre-exposure prophylaxis (PrEP), the daily use of oral
emtricitabine-tenofovir to prevent HIV acquisition. Recent studies
examining predictors of HIV acquisition in large prospective
cohorts, HIV vaccine efficacy trials, and clinic-based samples
have found very high incidence rates among MSM engaging
in unprotected receptive anal intercourse with HIV-positive/
serostatus unknown partners or MSM with rectal bacterial
STD [6–9], groups that have been incorporated in the US Public
Health Service clinical practice guidelines for PrEP .
Given the epidemiologic link between syphilis and HIV,
HIV-uninfected men who have had syphilis may be expected
to have an elevated HIV risk. This has been demonstrated in
recent analyses of surveillance data from Florida and prospective
cohort data from the Pre-exposure Prophylaxis Initiative
(iPrEX) study [11, 12]. We used population-level syphilis and
HIV surveillance data to quantify HIV incidence in order to
identify subgroups in need of intensified prevention efforts,
such as PrEP, using the universe of men with P&S syphilis in
NYC over a 10-year period.
Disease Surveillance Registries
The NYC HIV/AIDS surveillance registry contains information
on NYC residents diagnosed with AIDS since 1981 and HIV
infection or disease since 2000. Healthcare providers are required
by law to report all new diagnoses of HIV and AIDS and all new
HIV-related illnesses. Laboratories are required to report all
positive Western blot and other diagnostic test results, HIV
viral loads, CD4 counts, and viral nucleotide sequences results.
A cumulative total of 216 164 HIV/AIDS cases were reported to
the HIV/AIDS registry through 31 March 2011. The vital status
of cases in the registry is routinely updated .
The NYC STD surveillance registry contains information on
NYC residents diagnosed and reported with the following
notifiable STD: syphilis, gonorrhea, chlamydia, lymphogranuloma
venereum (LGV), chancroid, granuloma inguinale, and
neonatal herpes. Diagnosing healthcare providers are legally required
to report all new cases. Clinical laboratories are required to
report positive laboratory tests for the 7 STD, as well as negative
confirmatory syphilis tests. A total of 618 597 diagnoses of STD
among 431 685 unique persons were reported to the STD
registry between 1 January 2000 and 30 June 2010.
We conducted a match of male cases in the STD registry
(reported 1 January 2000–30 June 2010) with male cases in the
HIV/AIDS registry (reported through 31 March 2011) using
deterministic record linkage. Persons in the registries were
matched based on 36 combinations of patient information
(eg, name, birth date, social security number). Records that
matched based on the strictest criteria of 7 combinations were
accepted without further review. Records that matched on
another set of 17 combinations were considered probable matches
and manually reviewed by 2 trained staff, with inter-reviewer
discrepancies settled by a third staff member; manual reviews
required matches on gender and incorporated other patient
demographic variables available in the disease registries (eg,
race, ethnicity, address). Records that linked on the remaining
12 combinations or did not link on any were not acceptable
matches, and those persons were considered as STD cases
without HIV infection. Afterward, all persons with a death
date before 1 January 2000 were removed from the matched
Our outcome of interest was incident HIV infection, measured
as an HIV diagnosis reported to the HIV/AIDS registry,
following syphilis reported to the STD registry between 1 January
2000 and 30 June 2010. Accordingly, we excluded men from
our analytic cohort if they had an HIV diagnosis date before
2000 in the matched dataset. Given that 95% of individuals
seroconvert 2–8 weeks after HIV infection, we also excluded men
whose HIV diagnosis dates were <60 days after their syphilis
diagnosis dates to minimize the possibility of including those who
acquired syphilis and HIV at the same time. For men with
multiple P&S syphilis infections, follow-up for HIV started at the
time of diagnosis of their last (most recent) infection. We
conducted Kaplan–Meier survival analysis to account for varying
times to HIV diagnosis. For men diagnosed with HIV,
HIVfree time-at-risk was calculated as the interval between syphilis
diagnosis date and HIV diagnosis date; those without a new
HIV diagnosis during the analytic period were presumed HIV
uninfected and censored on 31 March 2011, or death date for
deaths before 1 April 2011.
We calculated HIV incidence estimates for subgroups defined
by age, race/ethnicity, transmission risk, stage of syphilis (
primary vs secondary), other bacterial STD, year of syphilis
diagnosis, and syphilis diagnostic setting (STD clinic provider vs
other providers). Age was assigned as the age at time of syphilis
diagnosis. Transmission risk was assigned using the Centers for
Disease Control and Prevention (CDC) transmission risk
categories, and categorized as: (1) sex with men (MSM), including
MSM reporting a history of injection drug use (IDU); (2)
heterosexual contact/sex with women (MSW); (3) IDU; and (4)
other or unknown risk. Risk category assignments were based
on information in the HIV registry, or sex of partners gleaned
during syphilis case interviews and recorded in the STD
registry. Other bacterial STD was classified as: (1) “none (syphilis
only)” when the patient had no diagnoses of chlamydia,
gonorrhea, or LGV reported to the STD registry at or after the time of
syphilis diagnosis, (2) “concurrent with syphilis” if there were
Characteristic Total Age
Number of P&S
Percent of P&S
Syphilis Cases (%)
Number of Newly
Diagnosed HIV Cases
Annual HIV 95% CI
Incidence (%) (HIV Incidence)
Person-years at Risk 11714.18 646.12
diagnoses of any of those 3 infections with specimen collection
dates matching the collection date associated with the syphilis
diagnosis, or (3) “syphilis and subsequent STD” if there were
any of the 3 diagnoses after the syphilis diagnosis.
Univariate and multivariate Cox proportional hazards models
were used to analyze contributions of risk factors to HIV
diagnosis. For the models, age at syphilis diagnosis was grouped as “<35
years” vs “≥35 years.” Other bacterial infection was collapsed
into: (1) none, vs (2) concurrent with, or subsequent to syphilis.
Analyses were performed using SAS 9.1 (SAS Institutes, Cary,
North Carolina), conducted using de-identified records collected
for surveillance purposes and not involving human subjects, and
were not subject to review by the NYC Department of Health and
Mental Hygiene Institutional Review Board .
Between 1 January 2000 and 30 June 2010, 6053 men with P&S
syphilis were reported to the STD registry. Of those, 3081 (51%)
had an HIV diagnosis date before 1 January 2000 recorded in
the HIV registry and an additional 167 were reported with
HIV <60 days after their syphilis diagnosis. The remaining
2805 men lacking evidence of prior or concurrent HIV infection
comprised our analytic cohort. Of them, 111 (4%) had more
than 1 P&S syphilis diagnosis. The median age was 33 years
(range, 14–86), and approximately one-quarter were
nonHispanic white, one-quarter Hispanic, and one-third
nonHispanic black. Two-thirds of men were classified as MSM,
13.3% as MSW, and 19.5% with IDU, unknown, or other risk
(Table 1). Over two-thirds of the cohort (1946/2805) had
secondary syphilis diagnoses. Overall, 82.4% of men were reported
with only P&S syphilis during the analytic period, whereas 3.7%
had a concurrent, and 14.0% a subsequent bacterial STD
diagnosis (Table 2).
The 2805 men with syphilis contributed 11 714 person-years
of follow-up time (mean: 4.2 years). A total of 423 men (15.1%)
were newly diagnosed with HIV during the analytic period, and
median time to HIV diagnosis was 1.6 years (range: 60 days–8.6
years). The annual HIV incidence for all men diagnosed with
P&S syphilis was 3.61%. Risk of being diagnosed with HIV
did not change appreciably with age, although older men
(≥50 years) had lower annual incidence (1.15%) than men
aged 13 through 44 years (range 2.85%–5.42%). HIV incidence
was similar across the major race/ethnicity groups (range
3.79%–4.70%), and lower among men of other/unknown
races (1.32%). Incidence was substantially higher for MSM
(5.56%) compared to MSW (1.20%) and men with other, IDU,
and unknown risk (0.46%) (Table 1). Men diagnosed with
Characteristic Syphilis stage Primary
Number of P&S Percent of P&S
Syphilis Cases Syphilis Cases (%)
Number of Newly
secondary syphilis had more than 1.5 times the annual HIV
incidence of those diagnosed with primary syphilis (4.10% vs
2.64%). HIV incidence among men with bacterial STD
diagnosed after the syphilis diagnosis (7.89%) was more than
twice the incidence among those with only syphilis (2.89%) or
with concurrent infections (3.44%). HIV risk did not differ
appreciably by year of syphilis diagnosis or syphilis diagnosing
provider (Table 2).
The multivariate model showed that among men with
syphilis, race/ethnicity, MSM risk transmission category, secondary
syphilis, and other bacterial STD were independently associated
with a new HIV diagnosis (Table 3). In the adjusted model:
non-Hispanic white, non-Hispanic black, and Hispanic men
each had similar HIV risk, twice that of men with other or
unknown races/ethnicities; MSM had a 9-fold risk of HIV
infection compared to men with other, unknown, or IDU risk
(adjusted hazard ratio [aHR] 8.88; 95% confidence interval
[CI], 5.20–15.18); men with secondary syphilis diagnoses had
higher risk compared to men with primary syphilis (aHR
1.37; 95% CI, 1.10–1.72); and men with concurrent or
subsequent STD had a 2-fold risk compared to those with only
syphilis (aHR 2.03; 95% CI, 1.65–2.50).
We found that men in NYC who have been diagnosed with P&S
syphilis are at high risk for HIV, with more than 1 in 30
diagnosed with HIV within a year of syphilis infection. Annual HIV
incidence in NYC (3.6%) exceeded that found in a similar
analysis from Florida (2.3%) . It has been estimated that at an
annual HIV incidence rate of 2.4%, 41% of men who are
HIV-negative at age 18 will be seropositive by age 40 .
The HIV incidence we measured among NYC men who had
had P&S syphilis portends an eventual HIV prevalence of
even greater magnitude. Estimates such as ours point to the
need for more effective primary HIV prevention efforts
among all men with P&S syphilis and especially for MSM
and men with syphilis followed by other bacterial STD.
Immunodeficiency Virus Diagnosis Among Men With Primary
Other, IDU, or 1
Other bacterial infections
None (syphilis 1
STDb concurrent 2.46
Multivariate HR 1.13 1
Abbreviations: CI, confidence interval; HR, hazard ratio; IDU, injection drug
users; MSM, men who have sex with men; MSW, men who have sex with
women; STD, sexually transmitted disease.
a Includes Native American/Alaskan Native, Asian, Hawaiian/Pacific Islander,
and men of multiple, other, and unknown races.
b STD include chlamydia, lymphogranuloma venereum, and gonorrhea.
We were surprised to find little variation in annual HIV
incidence rates among men with syphilis by race/ethnicity, or by age.
A study of HIV incidence rates among men in Florida showed
black–white rate ratios of 5.5 for MSM and 16 for MSW ,
and we have previously reported extremely high case rates of
both new HIV and P&S syphilis diagnoses among black and
young MSM and MSW in NYC . Furthermore, epidemiologic
studies have consistently identified black race/ethnicity as an
independent risk factor for HIV seroconversion [16, 17]. The
relatively uniform risk of HIV following syphilis infections across
groups defined by race/ethnicity and by age in this analysis
suggests that men who acquire syphilis are involved in the
highestrisk partnerships or sexual networks and/or have risk behaviors
that are more influential with regard to HIV risk than
demographic factors otherwise associated with HIV acquisition.
As expected, MSM had the highest HIV incidence (5.4%), but
our measure exceeded overall incidence estimates from many
other studies (2%–3% [9, 14, 16]) and instead approximated
rates reported for subpopulations at the highest risk for HIV,
such as young black MSM who have participated in the HIV
Prevention Trials Network 061 Study  or the National HIV
Behavioral Surveillance System . Also, and not surprisingly,
indicators of ongoing risky behaviors, such as STD diagnoses
subsequent to P&S syphilis infection and secondary rather
than primary syphilis diagnoses, were associated with a greater
risk for incident HIV. Bacterial STD diagnoses almost certainly
indicate a lack of consistent/correct condom use, a shared risk
factor for the sexual transmission of HIV. A diagnosis of
syphilis during its secondary stage may result when initial infection
is introduced in the anorectum, where transient and painless
chancres can go unnoticed and not diagnosed as primary
lesions. The occurrence of anorectal lesions suggests condomless
receptive anal sex, a practice that very well could continue after
treatment for syphilis and has been associated with a higher risk
for HIV .
A new syphilis diagnosis in an HIV-negative man offers a key
opportunity for PrEP initiation. A recent study by Buchbinder
and colleagues to identify MSM populations that would benefit
the most from PrEP showed a population attributable fraction
(PAF) for syphilis of approximately 10%; of 11 other
HIVassociated risks that were examined, only condomless receptive
anal intercourse and reporting more than 5 recent sex partners
had higher PAFs . The investigators estimated that
approximately 30 persons with prior syphilis infection would need to
be on PrEP for a year to prevent 1 HIV infection. In June 2014,
New York Governor Andrew Cuomo announced the state’s
successful negotiations with pharmaceutical companies that
represent 70% of the HIV antiretroviral market to reduce costs of the
medications, thereby expanding access to PrEP. Currently CDC
recommends PrEP for MSM with recent ( past 6 months)
histories of bacterial STD . Our data, however, show that a
substantial proportion of individuals who acquire HIV are
diagnosed well after their syphilis diagnoses, and we suggest
that all men in NYC with a new P&S syphilis diagnosis be
considered for this prevention strategy, even if that diagnosis
occurred more than 6 months ago.
The risk of HIV acquisition following syphilis infection
among MSM, men with subsequent STD, and men with
secondary syphilis indicates the importance of frequent STD and
HIV screening. The CDC recommends that all sexually active
MSM who are HIV-negative or not tested within the previous
year be screened for HIV at least annually . Given the
substantial HIV risk that we measured, healthcare providers should
conduct more frequent HIV screening for their HIV-negative
patients who have had syphilis, perhaps as often as every 3–6
months. During our study period, approximately one-third of
P&S syphilis cases were diagnosed and reported from public STD
clinics. With US healthcare reform, patients may increasingly
access primary care clinicians for STD care, and it is important,
high HIV incidence we have shown has implications for
ongoeven in the PrEP era, for providers diagnosing STD to continue
ing HIV transmission. Although HIV acquisition among men
to counsel patients on the effectiveness of condoms in
preventwith syphilis may not drive substantial increases in HIV
inciing HIV transmission. It is also critical for providers to take
dence among the general population, it can certainly greatly
incomprehensive sexual histories and routinely screen for STD
crease the probability of HIV infection in selected sexual
that disproportionately affect MSM and often are
asymptomatnetworks. Consideration of promising HIV prevention
strateic, such as syphilis and extragenital (rectal and oral) chlamydia
and gonorrhea. Because it can be difficult to clinically
distingies (eg, PrEP) and maximizing use of existing effective
interventions (eg, frequent repeat HIV testing) will be necessary to
guish between the chancres of primary syphilis and other
ulcerreduce the rate of HIV in this group.
ative diseases, all patients who have genital, anal, or perianal
ulcers should be evaluated with a serologic test for syphilis;
the US Food and Drug Administration’s recent waiver for a
rapid screening test for syphilis will enable screening in a greater
variety of healthcare settings and should contribute to a higher
rate of detection .
Our study has limitations. First, both our exposure and
outcome of interest were diagnosed infections. Men without
additional STD reports due to lack of testing after syphilis or
migration out of NYC were presumed STD-free. True HIV
incidence may have been underestimated if men did not have an HIV
test during the follow-up period, or if men were diagnosed with
HIV outside of NYC and not reported to the NYC HIV registry.
Second, we cannot be sure that men who were diagnosed with
HIV after syphilis actually acquired HIV after syphilis;
determining the timing of HIV acquisition would require data from
laboratory-based tests to distinguish recent from established
infections [22, 23], which were only incorporated in routine
surveillance starting in 2005 and increasingly complete in the later
years of this study. We could have overestimated risk if men
who were diagnosed with syphilis were already HIV-infected at
that time but were not tested until later; these men were not at
risk of acquiring HIV and should not have been included in
follow-up. Third, estimates of HIV risk among syphilis cases with
concurrent or subsequent STD may have been affected by the
under-ascertainment of certain STD. A lack of availability and/
or use of extragenital tests for chlamydia and gonorrhea results
in missed diagnoses and underreported STD. By counting the
most recent P&S syphilis infection in our analysis, we did not
assess the association between repeat syphilis infections (observed
for 4% of our cohort) and incident HIV. Estimates of HIV risk
among syphilis cases with other STD may also have been affected
by better ascertainment of HIV infection if they were more likely
to have been tested for HIV at the time of STD diagnosis. Finally,
underreporting is a possibility even with electronic laboratory
reporting; any unreported HIV diagnoses, or missing syphilis
reports among men in the cohort that could have shortened the
follow-up period would have led to underestimating true HIV
After years of relatively stable rates, P&S syphilis infections
among men in the United States are on the rise . Substantial
HIV prevalence among men with P&S syphilis coupled with the
Disclaimer. The findings and conclusions in this paper are those of the
authors and do not necessarily represent the views of the Centers for Disease
Control and Prevention.
Potential conflicts of interest. All authors: No reported conflicts.
All authors have submitted the ICMJE Form for Disclosure of Potential
Conflicts of Interest. Conflicts that the editors consider relevant to the
content of the manuscript have been disclosed.
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