Introduction
The annual incidence of acquired syphilis in Denmark dropped to a very
low level in the early 1990s. A similar decline was observed in other
Western countries and was believed to be at least partly due to HIV protection
campaigns resulting in changes in sexual behaviour, with increased condom
use as an important factor [1, 2]. Since the late 1990s, syphilis rates
have gone up in many Western countries. In Denmark this trend has been
apparent only during the past few years.
The purpose of this paper is to highlight the recent rise in syphilis cases
in Denmark.
Methods
In Denmark syphilis is a mandatory notifiable disease with universal
reporting from all clinics and physicians. The case definition is the
Latin term syphilis acquisita recens (recently acquired syphilis),
including primary, secondary, and early latent (duration less than
two years) syphilis (from Official Statement of the Danish Ministry
of the Interior and Health, April 2000). Individual cases are reported
to the Department of Epidemiology at the Statens Serum Institut (SSI).
The notifications contain information on gender, ethnicity, sexual
orientation, mode and place of transmission, HIV status and other demographic
data. The form is anonymised by omitting the first four digits in the
ten digit personal number that every person living in Denmark has assigned
to them. This way, the patient remains anonymous, but the notification
forms can be matched to reveal duplicate notifications. The Syphilis
Laboratory at SSI carries out all syphilis testing in Denmark. The
number of laboratory confirmed cases therefore corresponds to the total
number of positive tests, counting both infectious and late cases.
The laboratory tests are done on specimens labelled with the full ten
digit personal number, excluding the possibility of duplicates. There
is no direct link from the laboratory tests to the notifications received
by the Department of Epidemiology.
The number of notifications for each year is generally lower than that
of the laboratory confirmed cases. Each year the laboratory confirmed
cases and the anonymously notified cases are reported in EPI-NEWS [3].
For this paper, the syphilis situation in Denmark has been assessed using
data from the laboratory confirmed cases and the anonymously notified
cases from 1 January 1994 to 15 September 2004
For statistical analyses Stata version 8 was used. Proportions were compared
with chi square test.
Results
During the years 1994 to 2001, both notified cases and laboratory confirmed
cases were stable at low rates with an average of 50 laboratory confirmed
cases and 15 anonymous notifications filed each year.
In 2002 there was a slight, non-significant rise in the number of both
laboratory notifications and anonymous notifications followed by a sharp
increase in 2003 marking the onset of an outbreak [TABLE1]. From 1994
to 2002 42 % of the laboratory confirmed cases were notified. In 2003
and 3004 85% of the laboratory confirmed cases were notified.

In 2003 the department of epidemiology at SSI received 83 anonymous
notifications, and 88 notifications had been received by 15 September
2004. Extrapolating this number yields an estimate of 124 notifications
for all of 2004.
During the outbreak (2003 and 2004), 78% of the notified cases were
in MSM, whereas only 33% of the cases notified from 1994 to 2002 were
MSM (p< 0.001) [FIGURE]. During the outbreak, 37% of the MSM with
notified cases were known to be HIV positive, while this was the case
for 33% of the MSM notified from 1994 to 2002. This difference was not
significant [TABLE 2].


In 2003 – 2004, 75% of the cases were residents of the greater
Copenhagen area;this proportion was only 58% in the earlier period (p=0.001)
There was no significant difference in the proportion of cases acquired
in Denmark in the two periods. During the outbreak, 70% of the cases
were acquired domestically, compared with 65% of the cases in the earlier
period.
The age distribution of the notified cases did not change significantly
between the two periods [TABLE 3].

Discussion
During the late 1990s, increasing rates of syphilis and other STIs were
reported in many Western countries [1, 4-5]. During this time there
was a rise in gonorrhoea among MSM in Denmark [6], but syphilis notifications
remained at a very low level until 2003.
The background for the rise in STIs is probably complex and can not be
explained by any single factor [7].
In Denmark the annual incidence of notified HIV cases has been remarkably
stable, with a mean of 280 cases reported per year for more than 10 years.
There has, however, been a slight rise in the proportion of notified
HIV cases in MSM, starting in 2003 and continuing in 2004. It is too
early to say if this is the start of a true upward trend or just a fluctuation
on the otherwise stable HIV notification curve.
Doctors from venereal clinics and infectious disease clinics in Denmark
report seeing anal chancres as well as penile and oral chancres, indicating
both unprotected oral and anal sex as transmission routes for syphilis.
In the gay community in Denmark, ‘safe sex’ is primarily
understood as ‘safe from contracting HIV infection’, and
the safe sex advice offered on the internet homepage of STOP AIDS, the
Danish gay mens organisation for HIV information, is: ’always use
condoms for anal sex and don’t get semen in your mouth’ (http://www.stopaids.dk/).
Oral transmission of syphilis is very likely in this setting [8].
Unprotected oral sex poses a comparatively low risk of HIV transmission
[9], and a large number of dual transmission of syphilis and HIV via
unprotected oral sex appears unlikely. More likely, syphilis is transmitted
orally on its own, or anally - alone or together with HIV [8].
It is not known how often co-infection with syphilis and HIV occurs
and how often syphilis is contracted by MSM who are already HIV positive.
Since 1994, about a third of the MSM notified with syphilis are known
to be HIV positive. This proportion has not increased significantly during
the outbreak. The HIV prevalence in the Danish MSM population is assumed
to be around 5% [10].
The large proportion of HIV positive MSM in notified syphilis cases in
Denmark gives rise to the speculation that some of these may belong
to a subgroup of HIV positive gay men who engage in unprotected anal
sex with each other. An indication that this scenario could be part
of the explanation of the rise in syphilis incidence is backed by findings
in California in the United States, where there was no increase in
the number of new HIV infections among MSM at public HIV-testing sites
in San Francisco and Los Angeles during 1999-2002, a period when syphilis
cases among MSM increased substantially in both cities [11].
So far, the outbreak of syphilis in Denmark is almost exclusively in
MSM. In an outbreak in Canada, it was shown that MSM used the internet
and bars or bathhouses to initiate sexual contact, whereas heterosexually
acquired infections were largely in sex workers and their clients [12].
Sex workers in Denmark generally insist on condom use, and as a result,
the prevalence of STIs in this group is low [13].
There is no doubt that there is a strong interrelationship between HIV,
syphilis and other STIs [14]. An important question is whether the current
syphilis outbreak in Denmark is facilitating HIV transmission, or whether
syphilis is contained mostly to MSM who are HIV positive.
In an attempt to answer this question and to provide the National Board
of Health with information to use in future prevention strategies, the
Department of Epidemiology at SSI has engaged in a working group together
with infectious disease specialists, laboratory clinicians and MSM representatives
to plan questionnaire-based investigations. The group is communicating
with their Swedish and Norwegian counterparts to try to develop core
questions that can be a common basis in the Scandinavian questionnaires.
In this way, future comparison of results as well as facilitated co-work
is made possible.
At the department of infectious diseases in Copenhagen University Hospital,
a screening program of all HIV positive persons attending the clinic
was initiated in the spring of 2003. So far the screening has revealed
20 syphilis cases out of 1000 tests [15].
In collaboration with the Copenhagen health authorities and the Copenhagen
sexual health clinic, STOP AIDS has carried out a campaign, ‘Time
for a check-up’, where gay men attending a sauna club during the
summer of 2004 were offered a syphilis test with subsequent follow up
at a sexual health clinic. Four out of the 93 men who took the test were
positive for syphilis (http://www.stopaids.dk/).
Hopefully the planned investigations will yield information that can
contribute to a better basis for prevention strategies.
The findings in this report are subject to the limitations inherent
in the Danish national surveillance system. The proportion of laboratory
confirmed syphilis cases that are notified has risen from 42% before
the outbreak to 85% during the outbreak. Since the reported cases are
not linked to the laboratory confirmed ones, we do not know if for instance
the proportion of notified cases is more complete from the venereal clinics
than from the general practitioners. If this was the case, and the populations
of syphilis cases from the two sites differ in terms of demography, the
results could be skewed.
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