outbreak of norovirus in västra götaland associated with recreational activities at two lakes...
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ORIGINAL ARTICLE
Outbreak of norovirus in Vastra Gotaland associated with recreationalactivities at two lakes during August 2004
BENN SARTORIUS1,2, YVONNE ANDERSSON2, INGA VELICKO1,2, BIRGITTA DE
JONG2, MARGARETA LOFDAHL2, KJELL-OLOF HEDLUND2, GOREL ALLESTAM2,
CLAES WANGSELL3, OLOF BERGSTEDT3, PETER HORAL4, PETER ULLERYD5 &
ANN SODERSTROM5
From the 1European Programme for Intervention Epidemiology Training (EPIET), 2Swedish Institute for Infectious Disease
Control (SMI), Solna, Sweden, 3Gothenburg’s Water and Sewage Works, City of Gothenburg, Sweden, 4Department of
Clinical Virology, University of Goteborg, Goteborg, Sweden, and 5County Medical Office for Vastra Gotaland
AbstractA large community outbreak of norovirus (NV) gastrointestinal infection occurred in Vastra Gotaland County, Sweden inAugust 2004, following attendance at recreational lakes. A frequency age-matched case control study was undertaken ofpersons who had attended these lakes to identify risk factors. 163 cases and 329 controls were included. Analysis indicatesthat having water in the mouth while swimming (OR�/4.7; 95% CI 1.1�20.2), attendance at the main swimming area atDelsjon Lake (OR�/25.5; 95% CI 2.5�263.8), taking water home from a fresh water spring near Delsjon lake (OR�/17.3;95% CI 2.7�110.7) and swimming less than 20 m from shore (OR�/13.4; 95% CI 2.0�90.2) were significant risk factors.The probable vehicle was local contamination of the lake water (especially at the main swimming area). The source ofcontamination could not be determined
Introduction
Viral pathogens are the most common cause of
gastroenteritis in industrialized countries [1], can
survive for long periods of time in water [3], are
relatively stable in external environments and can
persist in the environment as a source of infection
despite attempts at disinfection [4,5]. NV is very
contagious as 10�100 virions may be enough to
cause disease [6] and 1 droplet of faeces or vomit can
contain millions of virions. The known host range of
NV has also expanded (it has been found in mice,
cows, and pigs) and antibodies to bovine strains have
been found in humans, which may suggest zoonotic
transmission [5]. NVs spread very easily from person
to person (dominant mode of transmission) [7], but
have also been associated with numerous nosocomial
[8], foodborne [9] and waterborne [10,11] out-
breaks. Reported waterborne outbreaks due to
norovirus have also been associated with community
water systems, small water systems as well as
privately owned wells [12�14]. In addition, NV
has been detected in recreational surface water
outbreaks (swimming pools, lakes etc.) [15,16].
Advances in molecular diagnostic techniques have
highlighted the clinical and public health importance
of NVs in all age groups, their ability to cause
infection via a number of transmission routes as
well as their considerable genetic diversity [17].
Recently, methods for virus concentration and NV
detection in water have also been improved [18,19].
On 11 August 2004 a first case of gastrointestinal
illness (vomiting and diarrhoea) was reported to the
Vastra Gotaland County Medical Office, following
bathing at Delsjon Lake, Gothenburg, 2 d earlier. By
25 August approximately 400 individuals had re-
ported gastrointestinal illness after swimming in
lakes in the Gothenburg area. Of those, 250 were
believed to have swum in Delsjon and 50 in Aspen
Lake at which daily attendance is, respectively, 1000
and 200�300 persons. These 2 lakes are approxi-
mately 12 km apart and are not directly linked.
Correspondence: B. Sartorius, Epidemiology, Swedish Institute for Infectious Disease Control, Solna, Sweden. E-mail: [email protected]
Scandinavian Journal of Infectious Diseases, 2007; 39: 323�331
(Received 5 May 2006; accepted 28 September 2006)
ISSN 0036-5548 print/ISSN 1651-1980 online # 2007 Taylor & Francis
DOI: 10.1080/00365540601053006
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Delsjon Lake has 1 main swimming area while
Aspen Lake has 2. An investigation of the outbreak
was undertaken by the Swedish Institute for
Infectious Disease Control (SMI) and the Vastra
Gotaland County Medical Office to identify the
source of this outbreak as well as recreational risk
behaviours at these lakes and to provide recommen-
dations to prevent similar occurrences in subsequent
summers.
Methods
Study design
We conducted a frequency age-matched case control
study to identify possible risk activities as well as the
possible source of infection. A case was defined as a
person who attended Delsjon or Aspen Lake be-
tween 7 and13 August 2004 and developed diar-
rhoea and/or vomiting during 7�16 August 2004.
People who satisfied these criteria were asked to
contact the local County Medical Office. Cases were
detected by active case finding through the local
media (newspapers, radio and TV), voluntarily
contacting of the County Medical Office either via
telephone or the home page (e-mail) as well as
through the Environmental Health Boards of
Gothenburg and Lerum. A control was defined as
a person who attended either Delsjon or Aspen Lake
between 7 and 13 August 2004, but had not fallen ill
with gastrointestinal illness. Controls were found
voluntarily through the local media via a press
release on 18 August 2004 (newspapers, radio and
TV), through the home page (e-mail) of the Vastra
Gotaland County medical office or via a dedicated
phone line where persons could leave their name and
contact details.
The categories for the age matching were as
follows: 0�4, 5�9, 10�19, 20�29, 30�39 and
40�/y. We intended to select 3 controls per case
among the volunteer controls where numbers of
controls in the age category were sufficient. If this
was not the case, then all controls in this age group
were selected.
A questionnaire was designed and sent via e-mail
or posted if e-mail was unavailable. Case question-
naires contained questions relating to symptoms,
onset, duration, hospitalization and if other persons
in their family had similar illness. Cases were also
asked about family members who fell ill with
gastrointestinal symptoms and had attended either
lake in the same period. If they met the inclusion
criteria they were also asked to complete a ques-
tionnaire. Cases and controls were asked about lake
attendance (Delsjon, Aspen or both), frequency and
duration of attendance, location of attendance (main
swimming area or other), swimming and other
recreational activities in and around the water, water
consumption or swallowing while swimming, water
taken up the nose while swimming, availability and
use of toilet and hand washing facilities, food stall or
cafe use and items eaten. Copies of questionnaires
are available upon request.
All analyses were conducted using STATA (Stata
Statistical Software version 7.0). To calculate age
stratified (by 0�9, 10�29 and 30�/y) odds ratio
point estimates and 95% confidence intervals (CI),
we used the epitab functions in STATA. To calculate
frequency age-matched (according to the age groups
defined above for control matching) odds ratios and
95% confidence intervals (CI), we used a univariate
conditional (fixed effect) logistic regression for
matched case-control groups. Exact methods were
not used as no cell contained a count of less than 5.
Percentages of cases exposed as well as population-
attributable fractions were also calculated. A multi-
variate conditional (fixed effect) logistics regression
model for matched case-control groups was then
developed, based on significant results obtained
from the univariate analysis, using stepwise forward
and backward elimination at the 10% (p�/ 0.1) level.
Microbiological analyses
The routine analyses (human samples) for gastro-
intestinal bacterial, viral and parasitic pathogens
were conducted at the Clinical Virology and Clinical
Bacteriology departments at Sahlgrenska University
Hospital in Gothenburg and at the SMI. Stool
samples were obtained from some of the cases and
cultured for bacterial enteropathogens (including
Campylobacter spp., Shigella spp., Salmonella spp.,
Yersinia enterocolitica) as well as tested for viruses
(norovirus, rotavirus, astrovirus and adenovirus) and
parasites (Cryptosporidium spp., Giardia spp. and
Entamoeba spp.). Electron microscopy and PCR
were performed for viral pathogens and microscopy
for parasites. Water samples collected between 10
and 30 August from various points around Delsjon
Lake (in addition to routine samples) were cultured
for indicator organisms and certain enteric patho-
gens. Bacteria were analysed according to the bath-
ing water directive (76/160/EEG) of Gothenburg
Water and Wastewater Works, while analysis for
parasites (Giardia and Cryptosporidium) in monthly
raw water intake samples was performed at SMI.
Testing for parasites was also performed at SMI on
additional samples taken for virological tests. At
Aspen Lake samples were also examined for faecal
streptococci, while at Delsjon Lake samples were
also examined for Campylobacter spp. specifically as
a result of the outbreak.
324 B. Sartorius et al.
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Results
Descriptive epidemiology
Of the 240 persons who indicated that they met the
case definition following the press release, 170
(71%) responded to the sent questionnaire. Seven
cases were excluded, as they did not fit the case
definition, giving a final total of 163 cases. Of the
757 potential controls that responded to the request
to participate in this study, 197 were randomly
selected in age groups 20�29, 30�39 and 40�/y. In
age groups 0�4, 5�9 and 10�19 y, all 132 controls
were included as there were insufficient volunteers in
these age categories to allow 3 controls to be selected
for each case. Nine controls were excluded, as they
had not indicated having attended either lake, giving
a final total of 329 controls.
Controls were generally older than cases, with a
mean age of 26.4 and 18.9 y, respectively (median
age was 30 and 12 y, respectively). Females ac-
counted for 52.9% (n�/ 163) of cases and 57.5%
(n�/ 329) of controls.
The majority of cases experienced stomach pain
(89.1%, 123/138), vomiting (85.8%, 139/162) and
diarrhoea (82.4%, 131/159). Differing denomina-
tors are due to missing answers for a given symptom.
Two cases (16 and 36 y of age) were hospitalized.
Incubation period for cases exposed to either lake
only once (n�/74) was on average 2 d (median of 2)
and ranged between 0 and 7 d. Of 128 cases, 92
(71.9%) reported having family members or friends
with similar symptoms. 176 family/friends cases were
reported in 79 households. 32 of these family/friend
cases reported an onset of illness prior to the
responder. Of the 176 suspected family cases, 136
(77.7%) had apparently also attended 1 of the
2 lakes. The remaining 41 cases were distributed in
24 households. The secondary attack rate in family
members of cases that had not attended either lake
was estimated to be 21.0% (37/176). Four suspected
secondary cases were excluded from this calculation
since their onset of illness was prior to that of the
primary household case.
Distribution of cases by d of reported onset
suggests a point common source outbreak with a
peak of onsets on 11 August 2004 (Figure 1);
however, recruitment of cases and controls was
restricted to a 1-week period (7�13 August 2004).
A peak in attendance at Delsjon Lake was on 9 and
10 August 2004. After the outbreak was recognized,
an advice against swimming was put up at the
swimming areas at these lakes by the Environmental
Protection Board of Gothenburg as well as for
Lerum on 13 August 2004. A press release was
also issued on 16 August 2004 recommending that
people avoid these lakes due to possible gastrointest-
inal illness. Thereafter the number of cases de-
creased rapidly.
Analytical epidemiology
More cases (105/163, 64%) attended Delsjon Lake
than Aspen Lake. Five cases and 7 controls indicated
having attended both lakes. Cases were more likely
than controls to have attended Delsjon Lake on 9
and 10 August (OR�/15.1; 95% CI 1.5�148.9 and
OR�/8.9; 95% CI 1.0�78.5, respectively) when
taking attendance on 7 August 2004 as the reference
date. Cases appeared more likely than controls to
have attended Aspen Lake on 10 August 2004
(OR�/6.0; 95% CI 0.5�76.6).
Risk factor analysis for Delsjon Lake
Age matched analysis. Cases were more likely than
controls to have attended the main swimming area at
Delsjon Lake, have swum 2 or more times per d,
spent on average 60 min or more in the water, played
on the shoreline, jumped off the pier, been involved
in boating/windsurfing type activities, had water in
41 No. of cases Legend:40 1 case39 Delsjön38 Aspen37363534333231302928272625242322212019181716151413121110
987654321
4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22
Warning against bathing put upby the Environmental HealthBoard of Gothenburg as wellas Lerum
Figure 1. Cases (n�/160) who had attended either Delsjon and/or
Aspen Lake, by date of onset of first symptoms during August
2004. Note: persons who swam in both lakes are not shown on
this curve.
Outbreak of norovirus at lakes 325
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the mouth while swimming, taken water up the nose,
taken water home from Delsjon spring, indicated the
presence of toilets as well as use of toilets and having
consumed items from shops/vendors/etc. (Table I).
Cases were less likely than controls to have swum
20 m or more from the shoreline (Table I).
Age stratified analysis. Cases in all age groups were
more likely than controls to have attended the main
swimming area at Delsjon Lake (Table II). Controls
in all age groups were more likely than cases to have
swum 20 m or more from shore. Cases aged 0�9 and
30�/y were more likely than controls to have spent
60 min or more on average in the water and used the
toilet facilities. Cases aged 0�9 y were much more
likely than controls to have had water in their mouth
while swimming. Generally, cases aged 0�9 and
30�/y appeared to be at a higher risk.
Conditional logistic regression
The results of the multivariate conditional logistic
regression suggest that cases having attended Dels-
jon Lake were more likely than controls to: 1) have
had water in the mouth while swimming; 2) have
taken water from Delsjon spring and indicated the
presence of toilets near the swimming area, to have
swum 2 or more times per d; and 3) have spent on
average more than 60 min in the water. (Table III).
Controls were more likely than cases to have swum
20 m or more away from the shoreline.
Risk factor analysis for Aspen Lake
Age matched analysis and multivariate conditional
logistic regression. Cases were also less likely than
controls to have swum 20 m or more from the
shoreline than controls (Table IV). Cases were more
likely than controls to have been playing on the
shoreline and jumping/diving in the water and to
have consumed items from shops/cafes/etc. After
multivariate conditional logistic regression of cases
having attending Aspen Lake, controls were only
more likely than cases to have swum 20 or more
metres away from the shoreline (OR�/0.0; 95% CI
0.0�0.3).
Microbiological findings
Patient samples analysis. In total, 38 patients had
samples taken for culture, microscopy and viral
analyses (PCR EM). 25 of the 38 samples, taken
from suspected cases that had swum in lakes in and
around the Gothenburg area, were positive for NV.
18 stool specimens from patients were tested positive
for NV by PCR. Nine of these persons had swum in
Delsjon and the other 9 in Aspen. PCR of samples
indicated that all but 1 was NV genogroup (GG) I.
Two different variants of NV GG I were found, 1
variant in all those people having swum in Delsjon
Lake and another for Aspen Lake. The 1 sample that
was found to be positive for genogroup II was taken
from a young boy, who was also found to be positive
for Campylobacter.
Water samples analysis. One of the routine water
samples taken from the main swimming area at
Delsjon Lake by the Environmental Health Board
for Gothenburg on 10 August 2004 was positive for
NV. The sequence of this NV differed, however,
from the strain observed in the patient samples. An
increase in the number of E.coli per 100 ml (�/100/
100 ml) in the water at the main swimming area at
Delsjon Lake was observed from samples taken on
12 August 2004. Elevated levels were still observed
on 17 August 2004. Elevated levels were not
observed for other sampling points around the
lake. A sample taken from Aspen Lake on 13 August
2004 found 120 E.coli per 100 ml, also above the
100/100 ml threshold. This indicates fresh contam-
ination of the lake water with faecal matter.
Discussion
Key findings and suspected source
The key findings of the multivariate analysis indi-
cated that having water in the mouth while swim-
ming, having taken water home from the fresh water
spring of Delsjon and indication of the presence of
toilets at Delsjon Lake were positively and signifi-
cantly associated with disease. It is likely that the
indication of the presence of toilets as a risk is
probably a proxy for attendance of the main swim-
ming area at Delsjon Lake, as other areas around the
lake did not have toilet facilities and to reach the
main swimming area at Delsjon Lake one has to pass
the toilet facilities. Increasing distance swum from
shore was found to be significantly protective.
Kaplan has reported 4 criteria that indicate with
high sensitivity and relatively high specificity that a
gastroenteritis outbreak is caused by norovirus [20].
In this outbreak all 4 criteria were met. The probable
vehicle of this point source outbreak was contami-
nated lake water at both lakes, particularly close to
the shore and at the main swimming area in the case
of Delsjon. The exact source of the outbreaks could
not be determined. There were more gastrointestinal
illnesses in Gothenburg due to this outbreak, but we
are not aware of any other outbreaks at the same
time (Ann Soderstrom, County Medical Office for
Vastra Gotaland, personal communication). The hot
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Table I. Case and controls by swimming and other water activities at Delsjon Lake during August 2004.
Risk factor Cases Exp �/ Total % Exp Controls Exp �/ Total % Exp Age-matched OR 95% CI p -valuea PAFb
Attended main swimming area 97 102 95.1 155 232 66.8 7.6 3.0�19.7 B/0.001 85.2%
Water activities
2 or more swims per d 57 74 77.0 137 227 60.4 2.0 1.1�3.9 B/0.001 42.1%
Average length of swim 60 min or more 27 94 28.7 25 234 10.7 2.7 1.4�5.2 0.003 20.2%
Swam 20 m or more from shoreline 38 75 50.7 173 198 87.4 0.2 0.1�0.3 B/0.001 74.4%
Other activities:
Swimming only (reference) * * * * * * Ref * * *Playing in water 33 44 75.0 96 158 60.8 1.5 0.7�3.3 * *Playing on shoreline 50 61 82.0 74 136 54.4 2.7 1.2�6.3 0.019 58.5%
Jumping/diving 53 61 86.9 92 136 67.7 1.7 0.6�4.4 * *Boat/windsurfing/etc. 71 81 87.7 109 169 64.5 2.9 1.3�6.6 0.012 65.2%
Jumped from the pier 55 95 57.9 83 241 34.4 2.2 1.3�3.8 0.004 35.8%
Ingestion of lake water
Water in mouth 77 102 75.5 129 229 56.3 1.8 1.0�3.3 0.049 *‘Kallsup’ [water up nose] 46 101 45.5 38 254 15 4.1 2.2�7.6 B/0.001 36.00%
Drank from Delsjokallan (local spring) 3 101 3 11 239 4.6 0.7 0.2�2.5 * *Took water home from local spring 25 97 25.8 28 239 11.7 2.6 1.4�4.8 0.003 15.90%
Toilets presence and usage
Toilets available 90 97 92.8 116 229 50.7 11.7 5.1�26.7 B/0.001 85.40%
Used toilets 18 101 17.8 19 228 8.3 2.8 1.4�5.8 0.005 10.40%
Soap/hand washing facilities 25 100 25 37 187 19.8 1.3 0.7�2.4 * *
Shops/cafes at Lake
Shops/other available 84 95 88.4 144 186 77.4 1.9 0.9�4.0 * *Consumed items from shops 43 102 42.2 43 179 24 2 1.2�3.5 0.012 24.00%
aStandard normal test for the p -value.bPopulation attributable risk percentage.
Outbrea
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weather at this time, the overcrowding of swimming
areas as well as the presence of sick individuals
increase the risk of such NV outbreaks associated
with recreational water. A similar outbreak involving
30 children occurred in the north of Sweden in the
beginning of August 2004, during a period of hot
weather and overcrowding. These children fell ill
after having bathed in a lake (Yvonne Andersson,
SMI, personal communication). Waterborne viral
outbreaks are also often difficult to recognize. If the
contamination level of NV is low, the number of
cases remains low. A rather extensive outbreak is
usually required for medical personnel and autho-
rities to recognize water as a possible source of
infection [13]. Thus it would appear that outbreaks
due to recreational water use in Sweden may be
more common than previously thought, compared to
Hjertqvist et al.’s [21] findings, although in recent y
there have been an increasing number of reports in
other countries, describing waterborne norovirus
outbreaks through contaminated recreational water
[12,22].
Since this NV outbreak lasted more then 1 week,
it is also highly probable that additional second-
ary infections occurred due to person-to-person
transmission. Direct and indirect person-to-person
transmission is well documented. Indirect person-to-
person transmission is probably aided by a low
infectious dose and the widespread dissemination
and hardiness of norovirus in the environment [10].
The toilets were also observed to be very dirty and it
was also indicated that faeces were observed on and
around certain toilets. At Delsjon there were only 5
available toilets.
Table II. Case and controls by selected exposures at Delsjon Lake during August 2004 stratified by age group (0�9, 10�29 and 30�/ y).
Risk factor n OR 95% CI p -valuea PAFb
Attended main swimming area at Delsjon
0�9 75 NCc 1.08 * * *10�29 93 6.7c 1.41 62.00 0.015 79%
30�/ 166 7.4c 2.13 39.30 0.001 79%
2 or more swims per d
0�9 67 0.8 0.20 3.33 0.723 16%
10�29 82 1.7 0.50 6.04 0.367 26%
30�/ 152 3.5c 1.20 12.64 0.016 59%
Average length of swim 60 min or more
0�9 73 3.5c 1.07 11.90 0.022 30%
10�29 94 1.7 0.54 5.40 0.285 13%
30�/ 161 4.2c 0.89 19.38 0.031 11%
Swam 20 m or more from shoreline
0�9 49 0.2d 0.04 0.64 0.004 59%
10�29 93 0.2d 0.05 0.59 0.002 74%
30�/ 131 0.2d 0.07 0.72 0.004 71%
Water in mouth while swimming
0�9 75 9.6d 1.15 437.47 0.038 87%
10�29 97 2.5 0.06 0.53 0.185 43%
30�/ 159 1.2 0.52 2.71 0.643 7%
‘Kallsup’ [water up nose]
0�9 81 2.5 0.90 7.13 0.056 43%
10�29 101 5.9d 2.02 17.55 B/0.001 43%
30�/ 173 5.4d 1.07 28.30 0.016 11%
Used toilets
0�9 73 6.8c 0.74 320.26 0.084 14%
10�29 93 1.4 0.21 8.03 0.635 3%
30�/ 163 2.9c 0.99 8.26 0.027 16%
Bought items from shops
0�9 70 0.7 0.25 2.08 0.509 14%
10�29 74 4.5c 1.37 15.29 0.006 38%
30�/ 137 2.6c 1.03 6.41 0.025 23%
aStandard normal test for the p value.bPopulation attributable risk percentage.cOR significantly �/1.dOR significantly B/1.
NC: cell containing zero.
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Faecal contamination of recreational water and
unintentional ingestion, leading to outbreaks of
gastroenteritis, occur through different means.
Soiled bodies and faecal accidents from swimmers
can cause contamination of the water [23,24]. Young
children defecating in the water could be a potential
source. Contamination of swimming water with
faecal matter has also been observed during an
outbreak of Cryptosporidium in Sweden [25]. Con-
tamination of lake water with vomit at the main
swimming areas/shoreline could provide another
explanation for the outbreak. People were observed
to be vomiting on the shoreline at Delsjon Lake and
the high concentrations of virus particles in vomit as
well as the low infectious dose needed for NV have
already been discussed. As was mentioned earlier,
2 different variants of NV genogroup I were ob-
served in cases from Delsjon and Aspen. Thus there
appeared to be a geographical link between gen-
ogroup and the lake indicating 2 separate outbreaks
that occurred at the same time. Water sample
analysis at Delsjon Lake indicated an increase in
the number of E. coli at the main swimming area
during the period of the outbreak and this increase
indicates fresh faecal contamination. The 1 water
sample from Delsjon that was found to be positive
for NV also points to contaminated lake water being
the source of this outbreak. However one cannot
exclude the possibility of a false positive. A hetero-
geneous mixture of strains in the water is also
possible and may explain the differing sequence of
the NV obtained in the water sample and those
found in human samples (this was seen in an
outbreak in Sweden where 3 different strains were
observed in the 5 human samples that were taken
(Kjell-Olof Hedlund, SMI, personal communica-
tion).
Fresh and marine waters are also subject to faecal
contamination from point sources (i.e. sewage re-
leases), watersheds (i.e. run-off from agricultural,
forest, and residential areas), and floods. We also
cannot exclude the possibility that faecal contami-
nated (containing NV) surface water may have
entered the lakes either due to a break in a sewage
line or overflow/breakage of a septic tank(s) near to
the lake(s).
The septic tank for the toilet facilities at Delsjon
Lake was only emptied on 13 August. Although no
cracks or leakages were observed, an overly full tank
may have presented a possible risk. It should also be
noted that this was a new toilet system (1st y of use).
The Environmental Health Board for Gothenburg
indicated that there was no direct water linkage
between Delsjon Lake and the spring (approximately
1 km apart), thus unlikely for it to have been
contaminated in this way. A tap to draw water
from the spring was located near the parking area
for persons attending Delsjon Lake. This is also a
very popular spot to obtain water during the hot
summer d. A small community with allotment
gardens also resides near the spring water. It was
indicated by the Environmental Protection Board of
Gothenburg that the water from the spring at
Delsjon has rarely been found to have unusually
high coliform counts and is normally potable. Thus
it appears that some other factor may be confound-
ing this relationship.
Weather conditions (e.g. rain and high tempera-
tures) can also affect water quality, can cause over-
crowding and decreased water quality in pools and
lakes [23,24]. There was, however, no noticeable
increase in rainfall in the Gothenburg area between
the end of July and first week of August [26]. An
increase in the temperature just prior to and during
the initial stages of the outbreak was seen, which
might explain large numbers of people in attendance.
In outbreaks of this nature it is very important to
ensure that good analysis of water and human stool
specimens is performed for virus and parasites to
support epidemiological evidence.
Limitations of the study
Case definition used had high sensitivity but low
specificity, thus false positives may have been in-
cluded in our sample. Since controls were selected on
a voluntary basis we cannot exclude the possibility of
Table III. Cases and matched controls by exposures at Delsjon
Lake during August 2004 using a multivariate conditional logistic
regression model (n�/ 124).
Exposure OR 95% CI p -valuec
Presence of toilets near where
bathing
25.5a 2.5�263.8 0.007
Took water home from Delsjon
spring
17.3a 2.7�110.7 0.003
Water in mouth while
swimming
4.7a 1.1�20.2 0.041
Swam for 60 min or more on
average
4.3 0.8�24.7 0.099
Swam more than once 3.0 0.8�11.6 0.110
Took water up nose 2.3 0.4�14.8 0.388
Bought items from shops/cafes/
kiosks etc.
1.9 0.5�7.1 0.316
Use of these toilets 1.4 0.3�5.6 0.665
Attended main swimming area
at Delsjon Lake
1.2 0.2�8.7 0.838
Female gender 0.6 0.2�1.8 0.313
Jumped from pier 0.5 0.1�2.2 0.379
Swam more than 20 m from
shore
0.1b 0.0�0.6 0.011
aOR significantly �/1.bR significantly B/1.cStandard normal test for the p value.
Outbreak of norovirus at lakes 329
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Table IV. Case and controls by swimming and other water activities at Aspen Lake during August 2004.
Risk factor Cases Exp �/ Total % Exp Controls Exp �/ Total % Exp Age-matched OR 95% CI p -valuea PAFb
Attended main swimming area 49 106 46.2 64 15 81.0 1.6 0.6�4.1 0.341 *
Water activities
2 or more swims per d 22 34 64.7 46 72 63.9 1.1 0.5�2.7 0.801 *Average length of swim 60 min or more 18 43 41.9 23 77 29.9 1.3 0.6�3.1 0.485 *Swam 20 m or more from shoreline 13 37 35.1 52 19 83.9 0.1 0.0�0.3 0.000 75.1
Other activities:
Swimming only (reference) * * * * * * Ref * * *Playing in water 15 17 88.2 31 45 68.9 1.8 0.3�10.1 0.489 *Playing on shoreline 35 37 94.6 44 59 74.6 5.6 1.1�28.3 0.038 78.7
Jumping/diving 21 21 100.0 41 52 78.8 N/Cc N/Cc 0.000 N/Cc
Boat/windsurfing/etc. 39 41 95.1 57 72 79.2 5.1 1.0�26.2 0.052 *Jumped from the pier 20 51 39.2 41 79 51.9 0.5 0.2�1.2 0.116 *
Ingestion of lake water
Water in mouth 41 52 78.9 57 82 69.5 1.4 0.6�3.6 0.476 *‘Kallsup’ [water up nose] 21 51 41.2 29 83 34.9 1.03 0.5�2.3 0.952 *
Toilets presence and usage
Toilets available 40 52 76.9 53 75 70.6 1.4 0.6�3.1 0.464 *Used toilets 11 55 20.0 14 81 17.3 1.2 0.5�2.9 0.685 *Soap/hand washing facilities 22 55 40.0 24 83 28.9 1.6 0.8�3.3 0.211 *
Shops/cafes at Lake
Shops/other available 45 51 88.2 60 80 75.0 2.4 0.9�6.4 0.0870 *Consumed items from shops 27 53 50.9 21 81 25.9 2.9 1.4�6.1 0.0050 33.8
aStandard normal test for the p -value.bPopulation attributable risk percentage.cN/C�/cannot be calculated (cell containing zero).
330
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volunteer bias in our study design, i.e. individuals
who volunteered were behaviourally different from
the general population. The higher median age of
controls, particularly the imbalance in the 40�/-y-old
category, may have introduced bias into our findings,
due to behavioural differences between younger and
older individuals. The recruitment of study subjects
from press releases about people who attended these
lakes on certain dates may have biased people who
were ill and swam to respond as cases, and those who
were not ill and did not swim as potential controls,
i.e. selection bias. This occurs when there are
differences in procedures used to select subjects
and/or from factors that influence study participation
(self-selection), the end result being that the relation
between exposure and disease is different for persons
who participate and persons who should theoretically
be eligible for study [27]. Although some degree of
short-term immunity appears to exist against NV and
may have biased the OR towards the null, long-term
immunity seems not to exist [17]. There was also a
possibility of interviewer bias, as many parents would
have filled out the questionnaire for their young
children.
Acknowledgements
This investigation was funded by the Swedish
Institute for Infectious Disease Control and the
County Medical Office for Vastra Gotaland.
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