Epidemiology of infectious syphilis in Ottawa. Recurring themes revisited.

Abstract

To describe the epidemiology of an outbreak of infectious syphilis in Ottawa.
A retrospective chart review of infectious syphilis cases in Ottawa from 2001-2006.
Rates of syphilis have risen more than tenfold. The epidemic was centered in men, with the majority of cases (83.5%) occurring among men who have sex with men (MSM). These individuals differed from the general MSM population residing in Ottawa in their being older, more likely to be HIV positive, and more sexually promiscuous. Inconsistent condom use by MSM engaged in either oral or anal sex was pervasive. Thirty-seven percent of MSM reported sexual encounters with men from Montreal and Toronto. Visceral manifestations of syphilis, including neurosyphilis, were more common in persons co-infected with HIV. As a result, this subgroup was more likely to have received an extended antibiotic treatment regimen. There was a substantial delay between serological diagnosis and treatment. Less than half of treated cases returned for a six-month evaluation.
Multiple sexual partners, unprotected oral sex, and increased age among MSM were the predominant risk factors contributing to this syphilis epidemic. Co-infection with HIV modified the clinical presentation of syphilis, necessitating a more intensive diagnostic and therapeutic approach. The interconnection of urban sexual networks has likely contributed to the dynamics of local syphilis transmission and suggests that effective interventions will require a coordinated national approach.

Full text

Page 1

Epidemiology of Infectious
Syphilis in Ottawa
Recurring Themes Revisited
Aviva Leber, MD
Paul MacPherson, MD, PhD
B. Craig Lee, MD
ABSTRACT
Objectives: To describe the epidemiology of an outbreak of infectious syphilis in Ottawa.
Methods: A retrospective chart review of infectious syphilis cases in Ottawa from 2001-
2006.
Results: Rates of syphilis have risen more than tenfold. The epidemic was centered in men,
with the majority of cases (83.5%) occurring among men who have sex with men (MSM).
These individuals differed from the general MSM population residing in Ottawa in their
being older, more likely to be HIV positive, and more sexually promiscuous. Inconsistent
condom use by MSM engaged in either oral or anal sex was pervasive. Thirty-seven
percent of MSM reported sexual encounters with men from Montreal and Toronto.
Visceral manifestations of syphilis, including neurosyphilis, were more common in persons
co-infected with HIV. As a result, this subgroup was more likely to have received an
extended antibiotic treatment regimen. There was a substantial delay between serological
diagnosis and treatment. Less than half of treated cases returned for a six-month
evaluation.
Conclusions: Multiple sexual partners, unprotected oral sex, and increased age among
MSM were the predominant risk factors contributing to this syphilis epidemic. Co-infection
with HIV modified the clinical presentation of syphilis, necessitating a more intensive
diagnostic and therapeutic approach. The interconnection of urban sexual networks has
likely contributed to the dynamics of local syphilis transmission and suggests that effective
interventions will require a coordinated national approach.
Key words: Syphilis; epidemiology; HIV
T
vividly illustrated the dynamics of the
host-pathogen relationship. These periodic
fluctuations in syphilis rates2have been
attributed to host perturbations, such as
changes in population-wide immunity3
and in sexual practices, as evidence of
alterations in the virulence of the
pathogen, Treponema pallidum, have been
lacking. A similar epidemiological pattern
has been observed in Canada, in which the
incidence of syphilis declined throughout
the late 1990s, with rates as low as
0.4 cases/100,000 in 1997,4before recent
presaging outbreaks in Calgary and
Vancouver.4,5
The re-emergence of syphilis has impor-
tant implications for HIV infection.
Syphilitic chancres significantly increase
HIV sexual transmission, including during
‘low risk’ sexual acts such as oral sex.5In
addition, the increasing number of syphilis
infections, with its short incubation time
and early detection relative to HIV, may
represent a harbinger of rising HIV infec-
tions.6Similar speculations attend the rise
in gonococcal infections.7-9
Conventional antibiotic treatment for
HIV co-infected individuals is controver-
sial with support for both traditional and
augmented regimens.10-15As the presence
of HIV infection modifies the clinical
expression of syphilis, an expanded diag-
nostic approach has been advocated, such
as the adoption of lumbar puncture to
exclude neurosyphilis in HIV co-infected
patients.16
In this study, we sought to identify fea-
tures contributing to the recent upsurge in
infectious syphilis in Ottawa between
2001 and 2006. Our results indicate that
potential therapeutic interventions rely
upon an understanding of local and
regional transmission dynamics operating
in tandem.
he oscillations in the incidence of
infectious syphilis since the late
1950s1in the United States have
METHODS
A retrospective chart review was conduct-
ed of syphilis cases occurring between
January 2001 and June 2006 in the
Ottawa-Carleton region, a metropolitan
centre with a population of approximately
one million. Patient records were analyzed
at the Ottawa Sexual Health Center
(SHC), a public health clinic, and at the
La traduction du résumé se trouve à la fin de l’article.
Department of Medicine, University of Ottawa, Ottawa, ON
Correspondence and reprint requests: Dr. B. Craig Lee, Department of Medicine, University of
Ottawa, 501 Smyth Road, Ottawa, ON K1H 8L6, Tel: 613-737-8899, ext. 72296, Fax: 613-737-
8009, E-mail: clee@uottawa.ca
Acknowledgements: The authors thank the staff at the Sexual Health Center in Ottawa, in particular
Dr. Mary Gordon and Orhan Hassan for helping to coordinate data collection.
SEPTEMBER – OCTOBER 2008 CANADIAN JOURNAL OF PUBLIC HEALTH 401

Page 2

Infectious Diseases Clinic at the Ottawa
Hospital General Campus. Cases were
defined as individuals with a clinical pic-
ture consistent with either primary, sec-
ondary or early latent syphilis17and posi-
tive serological tests for syphilis, or
seropositive individuals identified through
contact tracing. HIV status was assigned
based on a reactive serological immuno-
assay, self-reporting or documentation of
antiretroviral treatment. Demographic
characteristics were collected from ques-
tionnaires routinely used at the SHC, and
from medical transcriptions and contact
tracing reports.
Treatment start dates and treatment reg-
imens were recorded directly from chart
records. Treatment success was defined as a
fourfold decrease in serum RPR (rapid
plasma reagin) titers six months after treat-
ment.18Re-infection was diagnosed as the
presence of new clinical signs, new epi-
demiological contact tracing and any RPR
titer rise. In such cases, re-infection was
recorded as a new infection.
RESULTS
One hundred and two cases of infectious
syphilis were reviewed. The rate of infec-
tion in the Ottawa-Carleton region
increased from 0.6 cases/100,000 in 2001
to 2.8 cases/100,000 in 2003 and remained
steady thereafter. The male to female ratio
was 19:1. The majority of infected men
(83.5%) were MSM or bisexual.
Heterosexual transmission accounted for
18.6% of cases. All but four cases resided in
Ottawa. Three quarters of individuals were
born in Canada and the country of origin
of the remainder was diverse. Two thirds of
the cases were between the ages of 31 and
50 years with three quarters of the MSM
population in this age group (Figure 1).
Concurrent HIV infection was present
in 44 (43.1%) cases with the highest pro-
portion found in MSM compared to that
in the heterosexual cohort (48% versus
21%, respectively)(Figure 2). However, the
HIV status was unknown in 42% of het-
erosexuals and 16% of MSM. MSM
reported a higher annual number of sexual
partners than heterosexual cases (Figure 3)
and the number of sexual partners per year
in MSM increased with age over 30 years.
Oral-genital contact was the predominant
form of sexual practise in MSM (Figure 4).
Approximately one half of epidemiologi-
cally linked sexual partners resided outside
of Ottawa (data not shown).
Secondary syphilis was the predominant
clinical expression of disease as 57 (59%) of
cases presented with this clinical manifesta-
tion (Figure 5). HIV co-infected patients
were more likely to exhibit visceral signs of
secondary syphilis including hepatitis,
meningitis and retinitis, compared to HIV-
negative individuals. A chancre was present
in all of the 29 cases of primary syphilis
irrespective of the HIV status.
The elapsed time between the dates of
serological confirmation and the initiation
of treatment were recorded for 87 of the
102 cases. The length of time between
diagnosis and treatment did not correlate
with the stage of syphilis. Patients present-
ing to the Infectious Diseases Clinic at the
Ottawa Hospital were more likely to
receive treatment at the initial assessment.
Benzathine penicillin G was the sole
antibiotic administered to 33 (89%) HIV
uninfected patients and to 17 (40%)
patients concurrently infected with HIV.
With the exception of 5 cases (4 HIV co-
infected and 1 HIV negative) who received
a combination of benzathine penicillin G
and doxycycline, the use of doxycycline
SYPHILIS EPIDEMIOLOGY
402 REVUE CANADIENNE DE SANTÉ PUBLIQUEVOLUME 99, NO. 5
Figure 1.
Distribution of cases by age in years
Figure 2.
HIV status of cases of infectious syphilis
0
10
20
30
40
Number of cases
<2021-3031-40
Age
41-50 51+
Bisexual
Heterosexual
MSM
0
10
20
30
40
50
Number of
cases
HIV+HIV- Unknown
Bisexual
Heterosexual
MSM
HIV status
Figure 3.
Number of sexual partners per year of patients with infectious syphilis
0
5
1 0
1 5
2 0
2 5
3 0
3 5
Number of cases
0 to 5 6 to 1011 to 20 greater than
20
unknown
Bisexual
Heterosexual
MSM
Number of sexual partners

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was confined to penicillin-allergic patients
(3 HIV negative and 9 HIV co-infected
cases). Of the 37 HIV-negative individu-
als, 27 (81%) were treated with one dose
of intramuscular benzathine penicillin G
2.4 million units and 3 with a 14-day
course of oral doxycycline 100 mg bid. In
contrast, only 6 (14%) HIV-positive
patients received either regimen. Of the 42
HIV-positive individuals, 20 (48%) were
treated with an extended regimen of either
three weekly intramuscular injections of
benzathine penicillin G (total of 7.2 mil-
lion units) or with a prolonged 28-day
course of oral doxycycline 100 mg bid.
The majority (65%) of these 20 individu-
als presented with secondary syphilis.
Lumbar puncture was performed in 19
neurologically asymptomatic patients with
HIV infection with a serum RPR titer
≥1:32, or a CD4 cell count <350 cells/μL
irrespective of titer.19,20Twelve (63%) of
these patients were diagnosed with neu-
rosyphilis,20reflected by either a positive
CSF VDRL titer or CSF pleocytosis. All
were treated with a minimum two-week
course of either intravenous penicillin G
4 million units Q4H or ceftriaxone 2 gm
daily. Seven individuals received an addi-
tional three weekly intramuscular injec-
tions of benzathine penicillin G. Overall,
27% of HIV-positive cases were diagnosed
with neurosyphilis.20
Successful treatment of syphilis was
defined as a fourfold decrease in RPR titers
six months post-therapy,18,21therefore this
analysis was confined to patients who com-
pleted the six-month serological evalua-
tion. Only 49 of the 102 cases met this cri-
terion. The extent of follow-up did not dif-
fer in the HIV-positive and HIV-negative
groups. Twenty-eight (67%) of the 42
HIV-positive patients completed follow-
up. Twenty-three (78%) of these individu-
als received either an extended therapy reg-
imen or an intravenous β-lactam antibiot-
ic, and only three cases (13%) failed treat-
ment, including one person who received
intravenous penicillin. Similarly, only one
HIV co-infected patient receiving conven-
tional regimens did not achieve serological
success. Two of the treatment failures were
felt to be due to unrecognized CNS infec-
tion. Less than half of HIV-negative indi-
viduals had 6-month follow-ups. The
majority (71%) received conventional ther-
apies and five patients failed treatment.
One HIV-negative individual was deemed
serofast, defined as a case whose titers did
not decline irrespective of treatment and
symptomatic resolution, and consequently
this result were not included. The small
number of patients returning for the six-
month evaluation precluded a meaningful
assessment regarding whether treatment
failure was associated with a specific anti-
biotic regimen.
DISCUSSION
The rate of infectious syphilis in Ottawa
has risen sharply, increasing greater than
tenfold from 0.2 cases/100,000 between
1997-99 (Ottawa Public Health, data not
published) to 2.8 cases/100,000 in the
interval from 2003-06. As in previous
studies,1,22a disproportionate number of
these cases were male. Although cases of
infectious syphilis treated outside of these
two clinics were not included in the analy-
sis, the magnitude of the epidemic was
likely captured in our study as the SHC
tracks all reactive serologic tests for syphilis
in the Ottawa-Carleton region.
The median age of men in this study
was 40 years, which is 2.5 years older than
the median age of men in Ottawa,23indi-
cating that an older age group is primarily
affected by this epidemic.1,24The shift in
age demographics may be explained by the
unique risk factors present in these men.
Qualitative research revealed that older
men are less likely to insist on condom use
due to fear of rejection from younger sexu-
al partners.25Older MSM also have a high-
er incidence of isolation and depression
which is associated with risky sexual prac-
tices.25Our findings support these observa-
tions as MSM over 30 years of age had a
higher number of sexual partners and a
higher incidence of unprotected anal sex.
The MSM community is less defined by
geographic borders, as infected men are
known to travel between cities to meet sex-
ual partners.7,25-27Movement between
Montreal, Toronto, and Ottawa was com-
mon within the Ottawa MSM population.
The parallel increase in the number of
cases of infectious syphilis in Quebec28and
SYPHILIS EPIDEMIOLOGY
SEPTEMBER – OCTOBER 2008CANADIAN JOURNAL OF PUBLIC HEALTH 403
Figure 4.
Sexual practices of cases of infectious syphilis
0
10
20
30
40
50
60
Number of cases
consistent
condom use
inconsistent
condom use
consistent
condom use
inconsistent
condom use
consistent
condom use
inconsistent
condom use
Anal Sex
Sexual practices
Bisexual
Heterosexual
MSM
Oral Sex Vaginal Sex
Figure 5.
Syphilis stage at presentation and HIV status
0
20
40
60
Number of cases
Early LatentSecondary Primary
Syphilis stage
Unknown
HIV negative
HIV positive

Page 4

Toronto (T. Wong, personal communica-
tion) suggests that increased interconnec-
tivity of an underlying network of sexual
contacts in these three cities has con-
tributed to the dynamics of both local and
regional syphilis transmission.
Such a synchronization of syphilis rates
across wide geographical areas has been
attributed to progressive recruitment of a
non-immune susceptible population inter-
acting with an infected core group.29Data
from the Ontario Men’s Survey30supports
the existence of such a group of highly sex-
ually active individuals as the behaviour of
the MSM diagnosed with syphilis are clear-
ly distinct from the general MSM popula-
tion. Similarly, the conduct of men with
syphilis in our study exhibited a stronger
history of previous sexually transmitted
infections in which the prevalence of HIV
and other STIs was ten- and twofold more
prevalent, respectively (data not pub-
lished). In addition, MSM infected with
syphilis were more sexually promiscuous,
with only 21.3% reporting fewer than
5 partners in the past year compared to 56%
of the general Ottawa MSM population.
The low prevalence of condom use was
notable. Within the heterosexual popula-
tion, vaginal sex was the sole source of
transmission reported in two thirds of cases
and only about 10% of individuals used
condoms consistently. Among MSM, the
high prevalence of unprotected oral sex,
largely regarded as an HIV-safe alternative
to anal sex, is recognized as an independent
mode of syphilis transmission6and is likely
a contributor to spread in the Ottawa epi-
demic. Indeed, over one third of MSM
with syphilis reported consistent use of
condoms with anal sex, indicating that
these cases were infected likely by oral sex.
The overall high rate of unprotected sex
correlates with previous reports that also
demonstrate an increasing prevalence of
unsafe sexual
MSM,22,25,26,31attributed to faith in anti-
retroviral therapies and to mental fatigue
arising from years of protected sex to
reduce the risk of HIV.32,33
The optimal treatment of syphilis in
HIV-infected patients is controversial.11-16
In our study, the majority of HIV-positive
cases attained serologic treatment success. A
high proportion of the HIV co-infected
patients underwent lumbar puncture to
exclude neurosyphilis.19,20Two of the treat-
practices among
ment failures in the HIV-positive group
were attributed to unrecognized CNS infec-
tion, in agreement with prior studies15,16
which demonstrated neurosyphilis relapses
in HIV-positive patients previously treated
with benzathine penicillin G injections.
Our results support the selective perfor-
mance of lumbar puncture in HIV concor-
dant patients exhibiting laboratory features
suggestive of asymptomatic neurosyphilis.19
Of note, one third (5 of 14) of HIV-
negative patients failed treatment with intra-
muscular long-acting penicillin G for rea-
sons that are unclear, emphasizing the
importance of extended clinical and serological
monitoring.34However, such extended follow-
up occurred in less than 50% of cases, a
finding that has been previously associated
in perpetuating syphilis transmission.9
A significant delay between serological
diagnosis and treatment has also likely con-
tributed to maintaining the pool of infect-
ed individuals and sustaining the syphilis
outbreak. Several individuals with classic
secondary syphilitic rashes were repeatedly
misdiagnosed and required skin biopsies
for the correct etiology.
This study has several limitations. The
low patient compliance with follow-up
syphilis serology and the undetermined
HIV status in a significant number of cases
restrict judgements regarding the effica-
ciousness of a particular therapeutic regi-
men and clinical outcome. A selection bias
may have occurred as individuals using the
SHC may have chosen this clinic for its
testing anonymity and therefore represent
an unbalanced number of ‘high risk’ indi-
viduals. Second, patients seen at the
Infectious Diseases Clinic may have creat-
ed a treatment bias towards augmented
regimens. Finally, self-reported sexual
behaviours are subject to recall and social
desirability biases.
In conclusion, the syphilis epidemic in
Ottawa is centered in the MSM popula-
tion in which the dynamics of transmission
appear to reside in a core group of infected
individuals. The mobility of this popula-
tion subset emphasizes the necessity for a
coordinated nuanced regional-based inter-
vention program. Unsafe sexual behaviours
and the delay in recognition and treatment
of infected patients underscores the need
for continual education of health care pro-
fessionals and of individuals engaged in
high-risk sexual practices.
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Received: September 18, 2007
Accepted: April 3, 2008
SYPHILIS EPIDEMIOLOGY
SEPTEMBER – OCTOBER 2008CANADIAN JOURNAL OF PUBLIC HEALTH 405
RÉSUMÉ
Objectifs : Décrire l’épidémiologie d’une flambée de syphilis infectieuse à Ottawa.
Méthode : Examen d’un graphique rétrospectif des cas de syphilis infectieuse survenus à Ottawa de
2001 à 2006.
Résultats : Les taux de syphilis ont plus que décuplé. L’épidémie était concentrée dans la
population masculine, la majorité des cas (83,5 %) s’étant produits chez des hommes ayant des
relations sexuelles avec des hommes (HRSH). Ces sujets différaient de la population générale des
HRSH vivant à Ottawa du fait de leur âge (ils étaient plus vieux), de leur probabilité accrue d’être
séropositifs pour le VIH et de leur plus grande promiscuité sexuelle. L’irrégularité dans le port du
condom par les HRSH pratiquant le sexe oral ou anal était omniprésente. Trente-sept p. cent des
HRSH ont déclaré avoir eu des rapports sexuels avec des hommes de Montréal et de Toronto. Les
manifestations viscérales de la syphilis, y compris la neurosyphilis, étaient plus courantes chez les
sujets co-infectés par le VIH. Par conséquent, ce sous-groupe était plus susceptible d’avoir suivi une
antibiothérapie prolongée. Nous avons observé un délai important entre le sérodiagnostic et le
traitement. Moins de la moitié des cas traités se sont soumis à une nouvelle évaluation après six
mois.
Conclusion : Les partenaires sexuels multiples, les rapports sexuels oraux non protégés et le
vieillissement de la population des HRSH étaient les principaux facteurs de risque ayant contribué à
l’épidémie de syphilis. La co-infection par le VIH a modifié le tableau clinique de la syphilis et
nécessité une approche diagnostique et thérapeutique plus intensive. L’interconnexion des réseaux
sexuels des villes a sans doute contribué à la dynamique de la transmission locale de la syphilis, ce
qui donne à penser que des interventions efficaces exigent une approche coordonnée à l’échelle
nationale.
Mots clés : syphilis; épidémiologie; VIH