In Denmark, anti-HAV IgM positive hepatitis A virus (HAV) infection is
notifiable by clinicians. HAV is not regarded as endemic in Denmark and
susceptibility in the population is high. The majority of infections are
imported by children of foreign origin returning from visits to friends
and relatives in endemic countries . Subsequent secondary spread in
childcare institutions is a common cause of small outbreaks. Outbreaks
of hepatitis A among men who have sex with men (MSM) have been reported
from several cities in Europe and worldwide. In Copenhagen, outbreaks among
MSM occurred in 1977  and in 1991 ; with 21 and 17 reported cases
of hepatitis A respectively. Studies have shown that hepatitis A is a sexually
transmitted infection (STI) in MSM. The main risk factors identified are
oral-anal sex (rimming) or digital-anal sex [4,5], visiting certain bars
or saunas [6,7,8], having sex with anonymous partners or group sex [4,5].
Social contact of a non-sexual nature and contaminated food  also contribute
From January 2004 an outbreak of hepatitis A affecting predominantly
MSM occurred in Copenhagen . In April, active case finding in collaboration
with laboratories was set up. Awareness of hepatitis A diagnosis and
the need for reporting was raised among clinicians. Apart from ordinary
precautions in a hepatitis A outbreak, such as increased hygiene and
immunoglobulin for close contacts, vaccination was recommended for MSM
not living in monogamous relationships. Further information for MSM was
provided by a national STI campaign carried out by the Danish gay organisation
STOP AIDS and the Danish National Association for Gays and Lesbians.
The outbreak continued, and in August 2004, the Statens Serum Institut
(SSI) and STOP AIDS carried out a case-control study to determine risk
factors for hepatitis A infection in this outbreak in order to inform
targeted preventive measures.
A case was defined as an MSM >17 years, living in Copenhagen, in whom
hepatitis A infection with positive anti-HAV IgM was diagnosed between
1 June and 14 August 2004, and who did not have contact to a hepatitis
A case in his household in the six weeks before onset of illness. Cases
were selected from the notifications received.
Controls, frequency matched to the cases date of onset of illness, were
selected at the annual Copenhagen Gay Pride Festival on 14 August 2004
from MSM resident in Copenhagen. Based on the result of a saliva antibody
test (Methods: see ) only persons susceptible to hepatitis A were
included as controls. Data on exposure was collected for a six week period
before illness onset and for the same period in controls using piloted
self-administered questionnaires. To protect privacy, patients were contacted
by their physician who obtained informed consent before posting a questionnaire
to them. Information collected included: eating in restaurants/cafes/bars,
shellfish consumption, whirlpool use, travel abroad, contact with hepatitis
A cases, number of regular and casual sexual partners, venues for sexual
contact, sexual contacts abroad or arranged via internet, oral-anal and
digital-anal sex practices, history of STIs. Additionally, controls were
asked about their attitude towards vaccination.
Data analysis was performed in STATA 8.0. Matched odds ratios and 95%
confidence intervals were calculated for each exposure factor. Adjusted
odds ratios were calculated using conditional logistic regression analysis.
Exposure factors with P values <0.20 and confounding variables such
as age were included. The final model was build by backward elimination
of variables above the threshold of P= 0.10.
In 2004, 163 cases of hepatitis A in men >17 years were notified to
the Department of Epidemiology, SSI. In the past five years the median
number of annually reported cases of hepatitis A among men of this age
group was 13 (range 7-25). Of the 163 cases, 107 were from Copenhagen,
56 from the rest of Denmark. The incidence rate in Copenhagen was 23
per 100 000 and declined with increasing distance from the capital [FIGURE
The following results are restricted to cases in Copenhagen. Of the 107
patients, 68 (64%) were reported to be MSM and five to be heterosexuals.
For 34 patients, the sexual orientation was not known [FIGURE 2].
Patient ages ranged between 19 and 73 years with a median of 41. Ninety
seven (91%) patients were residents in Denmark. Thirty seven (35%) patients
were admitted to hospital.. Forty nine (46%) cases were reported by general
practitioners and 58 from hospital in- or outpatient departments.
The case-control study conducted among MSM included 18 cases and 64 controls.
Physicians of 36 notified cases were asked to recruit their patients
for the study; 30 patients agreed to participate and 24 of these (80%)
returned questionnaires. Six patients did not fulfil the case definition
(four self-identified as heterosexual, one was infected by a household
contact and one did not live in Denmark during the exposure period).
Saliva samples were taken from 105 MSM visiting the Copenhagen Pride
Festival: 86 (82%) had no detectable antibodies against HAV; 15 (14%)
were IgG positive, two of these were also IgM positive; four samples
were inconclusive. Of the 86 without detectable antibodies, 17 reported
having been vaccinated against hepatitis A, three were not in Copenhagen
during the period required and two refused to participate. Therefore,
64 (61%) of the participants were included as controls.
Case patients and controls were similar with regards to residence within
Copenhagen, but patients were older than controls [TABLE 1].The proportion
of HIV-infected people was higher among patients than controls. Neither
patients nor controls reported a previous syphilis infection.
Matched univariate analysis of exposure factors [TABLE 2] suggests that
HAV infection was not associated with consumption of seafood or eating
outside home. There was no evidence of a cluster of cases linked specific
food outlets or restaurants. Travelling abroad was less frequent for
case patients than controls. Patients had a median of three sexual partners
in the six weeks before illness and controls, a median of two.
Patients were more likely to have had sex with casual partners than controls.
One third of both patients and controls had sex with partners they met
via the internet. HAV infection was associated with sex in gay saunas.
This association was very strong in May and June, when 9 of 10 patients
were exposed (ORMH 129.2, 95% CI 7.6-2197.5), but not in the
later part of the study. No single sauna was implicated. Sex at cruising
grounds and toilets was not associated with infection. Sex at private
homes appeared protective. Participation in group sex was reported by
17% of the patients and 5% of controls. High risk practices such as oral-anal
and digital-anal sex were common among both cases and controls, and were
not associated with increased risk of HAV infection.
After adjusting for confounding, sex with casual partners (adjusted odds
ratio(aOR) 8.7; 95% CI 1.6-48.9) and sex in private homes (aOR 0.1; 95%
CI 0.0-0.5) seem to respectively increase and decrease the risk of infection.
Because of the time dependency, sex in gay saunas did not prevail as
an independent risk factor in the multivariate analysis.
Two thirds of controls disclosed their sexual orientation to their general
practitioner. Of 36 controls, who had had casual sex, 11 had been recommended
hepatitis A vaccination (gay campaigns (5), an STI clinic (4), and general
practitioners (2)). Among controls, 53 (83%) were willing to be vaccinated
against hepatitis A. However, of these, only 14 (26%) were willing to
pay for the vaccination.
The study suggests that sexual activity was the major mode of transmission
in this hepatitis A outbreak among MSM. Sex with casual partners and
sex in gay saunas contributed to the spread of hepatitis A among MSM.
However, as the study period encompassed only part of the outbreak, we
must be cautious about extrapolating results to the whole period of the
outbreak. The study may be further limited by a small sample size. Controls
selected at the festival may not be representative of the total MSM population
in Copenhagen. However, since it is impossible to select controls directly
from the study population, we consider our approach the best possible
way to represent a broad spectrum of MSM. Protecting privacy was considered
to be extremely important in this outbreak investigation, and therefore
access to information on the cases was limited due to the sensitive nature
of the subject.
This was the largest recorded outbreak of hepatitis among MSM in Denmark
and the first one in more than a decade. In Europe, cases of hepatitis
A among MSM are reported with increasing frequency: since 1995 there
have been outbreaks in major European cities on an almost annual basis.
Venues for casual sex, such as gay saunas and darkrooms are frequently
implicated [7,8,11,12]. The increased risk of infection is presumably
related to the possibility of having several partners within a short
period of time. In Copenhagen, gay saunas are popular places for both
Danes and visitors from abroad to have casual sex. There are at least
seven saunas, they operate all year round and the largest sauna typically
attracts approximately 700 to 1000 visitors per week. With increasing
tourist traffic between European cities and increasing susceptibility
to HAV in the population, gay saunas offer a perfect venue for endemic
and epidemic spread of hepatitis A among MSM in Europe. The Copenhagen
outbreak caused hepatitis A in at least 13 Swedish men . Most of
these men were from southern parts of Sweden, which is situated close
to Copenhagen, and in some of them, infection could be directly linked
to sex at gay saunas. The outbreak in Copenhagen is most likely also
responsible for an outbreak among MSM in Norway. There, the same outbreak
virus strain circulated among infected MSM that caused the Copenhagen
and Swedish cases .
Hepatitis A is a relatively mild disease with a low case fatality. No
death was recorded in Copenhagen. However, one third of cases were admitted
to hospital. Costs associated with hospital admission and days off work
could be avoided by vaccination. In HIV-infected individuals, HAV infection
has been associated with prolonged HAV viraemia, which might lead to
longer infectivity and increased risk of spread in this population .
Inactivated HAV vaccine is safe in HIV-infected individuals .
The prevalence of anti-HAV antibodies among MSM tested at the Copenhagen
Pride Festival was 14%. This is low compared with a serological study
in two gay saunas in Copenhagen conducted in 1984, where 36% of sauna
attendees were immune to HAV – a figure three times higher than
in the general Danish population at that time . It is uncertain whether
this reflects an overall decline of hepatitis A infections among MSM
over the last 20 years, because sauna attendees may not be representative
of the population of MSM attending the festival. However, it suggests
that the population of MSM in Copenhagen is susceptible to hepatitis
A infection and therefore need to be alerted of the risks of infection
and how to prevent it.
Based on the results of the investigation we suggest recommending hepatitis
A vaccination to all MSM who are not in a monogamous relationship, especially
if they visit gay saunas or other places with frequent partner change.
Opportunities for vaccination could be visits to general practitioners
(although not all MSM disclose their sexual orientation to their doctor),
sexual health clinics or outreach campaigns at saunas or mobile clinics.
Willingness to be vaccinated was high among MSM, but a considerable number
were reluctant to pay for the vaccination. This attitude may be influenced
by information about the importance of vaccination. As free hepatitis
B vaccination is available for MSM in Copenhagen, exchanging the monovalent
vaccine for the combined hepatitis A and B vaccine would make protection
against hepatitis A available at little extra costs.
We further suggest that adequate hygiene should be ensured in saunas.
An information campaign on risks and prevention of hepatitis A transmission
should be targeted at sauna visitors (both Danish and international guests).
To stop spread of hepatitis A among MSM in Europe, a European consensus
on prevention and control measures may be required.
We thank all physicians for their cooperation in recruiting their patients
for the study and the volunteers who helped with control selection
at the Pride Festival. We thank John V Parry from the Sexually-Transmitted & Bloodborne
Virus Laboratory, Health Protection Agency, London, for analysing the
oral fluid samples and for his valuable support in interpreting the