Vol. 16 | Weekly issue 14 | 7 April 2011
Europe’s leading journal on infectious disease epidemiology, prevention and control
Change of guard in Eurosurveillance
by K Ekdahl
First detection of Echinococcus multilocularis in Sweden, February to March 2011
by E Osterman Lind, M Juremalm, D Christensson, S Widgren, G Hallgren, EO Ågren, H Uhlhorn,
A Lindberg, M Cedersmyg, H Wahlström
Gonorrhoea treatment failures to cefixime and azithromycin in England, 2010
by CA Ison, J Hussey, KN Sankar, J Evans, S Alexander
Outbreak of rotavirus gastroenteritis in a nursing home, Slovenia, December 2010
by A Trop Skaza, L Beskovnik, T Zohar Cretnik
Surveillance and outbreak reports
Outbreak of Shigella sonnei infections in the Orthodox Jewish community of Antwerp,
Belgium, April to August 2008
by K De Schrijver, S Bertrand, I Gutiérrez Garitano, D Van den Branden, J Van Schaeren
Change of guard in Eurosurveillance
K Ekdahl (email@example.com)1
1. Public Health Capacity and Communication Unit, European Centre for Disease Prevention and Control (ECDC), Stockholm,
Citation style for this article:
Ekdahl K. Change of guard in Eurosurveillance. Euro Surveill. 2011;16(14):pii=19835. Available online: http://www.eurosurveillance.org/ViewArticle.
Article published on 7 April 2011
In March 2007, Eurosurveillance moved to the European
Centre for Disease Prevention and Control (ECDC) from
its two previous hosts, the Institut de Veille Sanitaire
in Paris, France (Eurosurveillance Monthly) and the
Health Protection Agency in London (Eurosurveillance
Weekly) . This marked an important date for the then
young ECDC, as this was the first major European Union
funded public health project moving to the Centre 
and I was proud to become the journal’s Editor-in-chief.
From the start, my aim was to build on the success-
ful work of my predecessors in Paris and London and
to continue to provide and further develop a platform
for the exchange of scientific information for all those
engaged in the surveillance, prevention and control of
communicable diseases . Moreover, I was convinced
that the opportunity to have the editorial team for both
publications physically in the same place for the first
time would open new possibilities such as merging the
two formats into one. It would allow Eurosurveillance to
be strengthened and established as a prime European
source of scientific information in its field, in other
words to become Europe’s journal on infectious dis-
ease surveillance, prevention and control.
In fact, relying on a strong network of dedicated
experts across Europe and a committed team of editors
and with the editorial independence guaranteed by two
consecutive ECDC Directors and the ECDC Management
Board, Eurosurveillance is now firmly established.
In 2009, the journal applied for and was accepted
to receive an impact factor  and during the 2009
influenza A(H1N1) pandemic much attention was paid
worldwide to the timely publication of peer-reviewed
papers in our journal [4,5]. Timeliness has been and
will remain a strength and key distinctive feature of the
journal. The rapid sharing of information has on several
occasions contributed to linking and detecting similar
outbreaks and to controlling them [6-9]. Moreover, a
recent reader survey has demonstrated a high level of
satisfaction and much support for our journal.
After four exciting years as Editor-in-chief of
Eurosurveillance, I take over new responsibilities
at ECDC where I will build up the new Public Health
Capacity and Communication Unit . Therefore I
am now handing over the full leadership of the jour-
nal to Dr Ines Steffens. Ines has since the transfer of
the journal to ECDC in 2007 been Managing Editor of
Eurosurveillance, leading the day-to-day work of the
Editorial Office. In this position she has been instru-
mental in the successful development of the journal,
not least broadening the group of authors and readers
to a truly global one.
Ines has a firm public health and communicable dis-
ease knowledge and passion for quality. Together
with an enthusiastic editorial team, her vision is that
of a strong journal, which provides knowledge and
evidence for decisions that help to prevent and con-
trol infectious diseases thus contributes to the many
efforts in improving health overall. I am therefore con-
vinced that Eurosurveillance will continue to thrive, and
although with a sad eye the heart is light when now
stepping down from the lead of the journal. I will con-
tinue to follow the development of the journal and sup-
port it as Associate Editor in the future.
1. Eurosurveillance editorial team. Eurosurveillance changes
hands! Euro Surveill. 2007;12(9):pii=3146. Available
2. Regulation (EC) No 851/2004 of the European Parliament and
of the Council of 21 April 2004 establishing a European Centre
for disease prevention and control. Official Journal L 142,
30/04/2004 P. 1 - 11. Available from: http://www.ecdc.europa.
3. Steffens I, Ekdahl K. Accepted for the impact factor –
what is the impact of Eurosurveillance?. Euro Surveill.
2009;14(38):pii=19339. Available from: http://www.
4. Bloomberg. Swine flu in Greek students may point to outbreak
in Edinburgh. 28 May 2009. Available from: http://www.
5. The Cybercast News Service (CNSNews.com). Republicans
press Sebelius on slow production of swine flu vaccine. 21 Oct
2009. Available from: www.cnsnews.com/news/article/55901
6. Lewis H, Ethelberg S, Lisby M, Madsen SB, Olsen KE,
Rasmussen P, Kjelsø C, Vestergaard LS, Qureshi K,
Howitz M, Mølbak K. Outbreak of shigellosis in Denmark
associated with imported baby corn, August 2007. Euro
Surveill. 2007;12(35):pii=3257. Available from: http://www.
7. Stafford R, Kirk M, Selvey C, Staines D, Smith H, Towner
C, Salter M. An outbreak of multi-resistant Shigella sonnei
in Australia: possible link to the outbreak of shigellosis in
Denmark associated with imported baby corn from Thailand.
Euro Surveill. 2007;12(37):pii=3266. Available from: http://
8. Løvoll Ø, Vonen L, Vevatne T, Sagvik E, Vainio K, Sandbu
S, Aavitsland P. An outbreak of measles among a travelling
community from England in Norway: a preliminary report. Euro
Surveill. 2007;12(21):pii=3198. Available online from: http://
9. Ripa T, Nilsson P. A variant of Chlamydia trachomatis with
deletion in cryptic plasmid: implications for use of PCR
diagnostic tests. Euro Surveill. 2006;11(45):pii=3076. Available
online from: http://www.eurosurveillance.org/ViewArticle.
10. European Centre for Disease Prevention and Control (ECDC).
ECDC changes organisational structure. Available from:
First detection of Echinococcus multilocularis in Sweden,
February to March 2011
E Osterman Lind1, M Juremalm1, D Christensson1, S Widgren1, G Hallgren1, E O Ågren1, H Uhlhorn1, A Lindberg
(firstname.lastname@example.org)1, M Cedersmyg2, H Wahlström1
1. National Veterinary Institute (SVA), Uppsala, Sweden
2. Swedish Board of Agriculture, Jönköping, Sweden
Citation style for this article:
Osterman Lind E, Juremalm M, Christensson D, Widgren S, Hallgren G, Ågren EO, Uhlhorn H, Lindberg A, Cedersmyg M, Wahlström H. First detection of Echinococcus
multilocularis in Sweden, February to March 2011 . Euro Surveill. 2011;16(14):pii=19836. Available online: http://www.eurosurveillance.org/ViewArticle.
Article published on 7 April 2011
Surveillance for the fox tapeworm, Echinococcus
multilocularis, has been carried out in Sweden since
2000, with about 300 red foxes analysed annually. We
report the first finding of E. multilocularis in Sweden,
in a fox shot in December 2010 in the south-west of the
country. A second infected fox shot in the same loca-
tion was detected in March 2011. This paper describes
the national monitoring programme and the ongoing
work to estimate the prevalence and spread of the
Detection of Echinococcus multilocularis
in red foxes in Sweden
In February 2011, E. multilocularis was detected for
the first time in the south-west of Sweden, in a red
fox (Vulpes vulpes) shot in December 2010. A second
infected fox, shot in the same location, was detected
in March 2011.
E. multilocularis is endemic in large parts of Europe
and has been increasingly reported in animals from
countries near Sweden, such as Latvia, Estonia and
Denmark [1-4]. Although a rare disease in humans,
it is of considerable public health concern due to its
high mortality if untreated as well as high treatment
costs . In Sweden, infection with E. multilocula-
ris in humans and all animal species are notifiable.
Due to detection of the parasite in foxes in Denmark
in 2000, a surveillance programme was initiated in
Sweden in the same year. The surveillance is designed
and implemented by the National Veterinary Institute
and financed by the Board of Agriculture. It makes
use of hunters submitting foxes for examination on a
voluntarily basis, against a small remuneration. From
2000 to 2009, a total of 2,962 red foxes (Vulpes vul-
pes), 68 raccoon dogs (Nyctereutes procyonoides)
and 35 wolves (Canis lupus) were examined for
E. multilocularis: all were negative . Samples from
most foxes (n=2,675) were examined by ELISA for the
presence of the E. multilocularis coproantigen  and
the rest, plus those from which samples were ELISA
positive, were examined using the sedimentation and
counting technique (SCT) (n=726) . The raccoon
dogs and wolves were examined by SCT. Since 2000,
a total of 6,455 hunted foxes have been submitted for
E. multilocularis analysis.
Surveillance in 2010
E. multilocularis. A total of 103 were tested by SCT and
201 by taeniid egg isolation and real-time PCR. One
fox, analysed in February 2011, was found to be posi-
tive – a young female, shot in December 2010 in Västra
Götaland county, in south-west Sweden (Figure). A fae-
cal sample from the fox was examined by egg flota-
tion  followed by detection of egg DNA by real-time
PCR, using an in-house protocol. The result was con-
firmed by conventional PCR  followed by sequenc-
ing. Furthermore, the intestine of the fox was examined
by SCT and the parasites present were identified as
E. multilocularis, both morphologically and by detec-
tion of parasite DNA by real-time PCR and sequencing.
Although no formal counting of all worms was done, it
was estimated that the animal harboured more than
500 tapeworms. Of the remaining 303 foxes found to
be negative, 54 originated from the same county.
304 foxes were examined for
Surveillance in 2011
After the positive finding in February 2011, the sam-
pling of foxes was intensified. In the south-western
part of Sweden, hunters were requested to submit
approximately 10 foxes per municipality in the 93
municipalities in the four counties (Skåne, Blekinge,
Halland and Västra Götaland), and four foxes from
each of the remaining 197 municipalities in other parts
of Sweden. This intensified sampling ceased with the
end of the hunting season (i.e. between 28 February
and 31 March, ending at the earlier date in the south).
By 31 March 2011, a total of 3,189 foxes had been sub-
mitted for screening. This sample size is sufficient to
detect a prevalence of 0.1% on a country basis, with
approximately 95% confidence. The intestines of the
foxes were examined by the segmental sedimentation
and counting technique (SSCT), which is more cost-
effective compared with SCT, but still has a very high
sensitivity . A total of 1,140 foxes had been ana-
lysed for E. multilocularis by 31 March 2011: one addi-
tional fox was found to be positive, an adult female,
shot in early March in the same location and by the
same hunter as the first infected fox (Figure).
In addition to surveillance of foxes, faecal samples
are being collected from 140 hunting dogs in the four
municipalities around the parish where the infected
foxes were shot, and surveillance in rodents will be ini-
tiated once the snow cover has melted.
It is not yet known how and exactly when
E. multilocularis was introduced into Sweden. However,
considering the frequency of dog movements between
Sweden and countries in Europe where the parasite is
present, it is regarded as most probable that it was
introduced by a dog, despite the legal requirement to
deworm dogs before entering the country. Assessments
of the risk of introducing E. multilocularis into Sweden
and the United Kingdom have highlighted dog move-
ment as a risk factor [11,12]. An event that further sup-
ports this hypothesis is the introduction in 2003 of
another dog-borne parasite (non-zoonotic), the French
heartworm (Angiostrongylus vasorum) on the coast of
Västra Götaland county, where E. multilocularis has
now been found . This is similar to the situation in
Denmark, where E. multilocularis was first found in the
area where A. vasorum had been introduced some dec-
ades earlier (unpublished data). This emphasises the
need for efficient methods to prevent introduction of
the parasite to other E. multilocularis-free countries.
After the identification of E. multilocularis in Sweden,
deworming of dogs and cats has been recommended
by the authorities in the four municipalities surround-
ing the location where the positive fox was shot. These
recommendations also apply to dogs and cats entering
and leaving this area. Guidance regarding safety pre-
cautions has been issued to hunters handling foxes,
in line with recommendations given in other countries
where E. multilocularis occurs .
At present, the geographical extent of E. multilocula-
ris infection is not known. However, the fact that there
were two positive foxes in the same location indicates
that this may not be merely a place to which the foxes
had wandered and that it may harbour intermediate
hosts. The ongoing surveillance is expected to provide
more information once up to 3,000 foxes have been
examined by early summer this year, and once the dog
and rodent screenings have been finalised. However,
as the prevalence of E. multilocularis infection may be
very low, extensive sampling may be needed to define
the affected area.
Conditions for the establishment of E. multilocularis in
Sweden are likely to be favourable: the climate is tem-
perate, allowing worm eggs to survive in the environ-
ment for extended periods, and rodents reported to be
intermediate hosts of the parasite – such as the water
vole (Arvicola amphibius (terrestris) and the bank vole
(Myodes glareolus) – are prevalent. Furthermore, in
the northern parts of Sweden, other known intermedi-
ate hosts such as muskrats (Ondatra zibethicus) and
lemmings (Lemmus lemmus) are present. The surveil-
lance of rodents is aimed at clarifying which species
in Sweden are intermediate hosts. Future actions will
depend on the results of the surveillance efforts.
Geographical distribution of all georeferenceda foxes shot
in Sweden and analysed for Echinococcus multilocularis,
1 January–31 March 2011 (n=1,025)
The circle indicates the location where the two E. multilocularis-
positive foxes were shot: one in December 2010 and one in March
2011. The lines indicate the county boundaries.
a Coordinate system RT90.
Number of foxes per 400 km2
1. Romig T, Dinkel A, Mackenstedt U. The present situation
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Pawłowski ZS, editors. WHO/OIE Manual on echinococcosis
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Gonorrhoea treatment failures to cefixime and
azithromycin in England, 2010
C A Ison (email@example.com)1, J Hussey2, K N Sankar3, J Evans4, S Alexander1
1. Sexually Transmitted Bacteria Reference Laboratory, Health Protection Agency, London, United Kingdom
2. Carlton Street Clinic, Blyth, Northumberland, United Kingdom
3. New Croft Centre, Newcastle upon Tyne, United Kingdom
4. Health Protection Agency North East, Newcastle General Hospital, Newcastle upon Tyne, United Kingdom
Citation style for this article:
Ison CA, Hussey J, Sankar KN, Evans J, Alexander S. Gonorrhoea treatment failures to cefixime and azithromycin in England, 2010. Euro Surveill.
2011;16(14):pii=19833. Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19833
Article published on 7 April 2011
Successful treatment of gonorrhoea is the mainstay of
public health control. Cefixime and ceftriaxone, highly
active third generation cephalosporins, are today the
recommended first-line agents in most countries and
azithromycin is a second-line agent. However, there is
increasing evidence of decreasing susceptibility and
emergence of therapeutic failures. In this report two
cases of clinical failure to cefixime are described, one
of which additionally shows failure to azithromycin and
selection of a less susceptible strain during treatment.
Cefixime and ceftriaxone are third generation cepha-
losporins recommended for first-line therapy for
gonorrhoea in the United Kingdom . Cefixime is
administered orally in a single dose and is often used
in preference to ceftriaxone, which is given intramus-
cularly (IM). The relationship between dosage given,
susceptibility results and treatment failure is still
poorly understood but recent reports from Norway 
and Sweden  of treatment failures with cefixime and
ceftriaxone, respectively, are beginning to increase our
understanding. Azithromycin is an alternative treat-
ment, as a 2-gram dose administered orally, but again
the relationship between laboratory findings and treat-
ment failure is unclear. We report here two cases of
treatment failure to cefixime, one of which also dem-
onstrated treatment failure to azithromycin, in North
In October 2010, a 51 year-old English man, presented
at a genitourinary medicine (GUM) clinic in North East
England. Prior to this, he had attended his general
practitioner (GP) with urethral discharge and dysuria
and was treated with amoxicillin and clavulanic acid
(co-amoxiclav) for seven days before the tests results
were available, which is not first-line treatment for
either gonorrhoea or chlamydia, the most common
causes of urethral discharge. Tests taken at the visit to
the GP returned positive for gonorrhoea and negative
for chlamydia and he was referred to the GUM clinic.
At the initial visit (day 1) at the GUM clinic he was symp-
tomatic and reported having had a regular female part-
ner for one year, with whom he last had sex two weeks
before. He reported no other sex partners in the last
year and no history of sex abroad. On examination, he
had a profuse urethral discharge which was diagnosed
as presumptive gonorrhoea on microscopy and treated
immediately with cefixime 400 mg orally. The labora-
tory confirmed the diagnosis by isolation of Neisseria
gonorrhoeae (GC) but reported that the infecting strain
of N. gonorrhoeae showed decreased susceptibility to
cefixime. He was negative for chlamydia, syphilis, and
HIV (Table 1).
On recall (day 5), he was still symptomatic and was
retreated with azithromycin. The patient returned a
further two times, on day 22 and day 30, and remained
culture positive for N. gonorrhoeae on both occasions
(Table 1). He was given a further treatment with azi-
thromycin on day 22 and then on day 40 was treated
with ceftriaxone 250 mg IM following the isolation of
N. gonorrhoeae from urethral sample taken on day 30
(Table 1). His test of cure on day 46 was negative. He
reported he had sex with the same contact seven days
following his first azithromycin treatment (day 12) but
no other sexual contact.
The female sex partner attended another GUM clinic,
tested GC culture negative but was treated preven-
tively as a contact of Case 1 with cefixime 400 mg
and subsequently azithromycin. She attended GUM
Northumberland on day 40 with the index case,
declined testing and was treated with ceftriaxone, 250
mg IM. She declared no sex partners other than Case 1.
In October 2010, a 23 year-old man attended a dif-
ferent GUM clinic in North East England, as a contact
of a chlamydia patient (day 1). He had no symptoms,
reported sex with a man two weeks previously, and
was treated with azithromycin one gram as a single
dose because of his contact with the chlamydia case.
He was tested for gonorrhoea (urethra, throat and
rectum) using culture and for gonorrhoea and chlamy-
dia at the same sites using nucleic acid amplification
(NAAT) (Aptima Combo 2, Gen-Probe), all of which
proved negative. He was also tested for syphilis, HIV,
hepatitis B and C markers and was negative (Table 2).
The patient came back to the clinic with symptoms over
a month later, reporting having had sex with the same
male partner one week prior, with whom he had been
having a sexual relationship for the previous eight
weeks. He reported no other sex partner in the previ-
ous six months. It is, therefore, likely that he acquired
his gonococcal infection from this partner since his ini-
tial visit, as he tested negative for gonorrhoea on day
1, or from another source although he denied any other
partners. A presumptive diagnosis of gonorrhoea was
made at this visit (day 37) by microscopy and he was
treated with cefixime 400 mg and doxycycline 100 mg
twice daily for one week. Gonorrhoea was confirmed
by isolation of N. gonorrhoeae from the urethra and
presence of N. gonorrhoeae specific DNA in the urine.
Susceptibility to cefixime and ceftriaxone was deter-
mined using discs and to penicillin and ciprofloxacin
using Etests (Table 2) but the isolate was not available
for confirmatory testing at the reference laboratory.
Samples taken from the rectum and throat were nega-
tive for N. gonorrhoeae using culture and for N. gonor-
rhoeae and Chlamydia trachomatis using NAATs.
The patient came again to the clinic on day 48 and
reported persistent, intermittent dysuria. He reported
no sexual contact since day 30 but was again presump-
tively diagnosed with gonorrhoea by microscopy and
treated with ceftriaxone 250 mg IM. N. gonorrhoeae
was isolated from the urethra and exhibited decreased
susceptibility to cefixime (MIC 0.25 mg/L). Six days
later (day 54) the test of cure showed the patient was
Clinical and microbiological findings and treatment given for gonorrhoea, Case 1, England, 2010
Case 1 Symptoms Test results Susceptibility resultsTreatment
Gonorrhoea: culture and NAAT
Syphilis serology and HIV - negative
Cefixime 400 mg orally
Recalled for treatment
NoneNA Azithromycin 2 grams orally
Day 22 Urethral discharge
Microscopy intracellular GNDC
Culture and NAAT- positive
Azithromycin 2 grams orally
Returned for review
Day 40 Discharge returnedNoneCeftriaxone 250 mg intramuscularly
Day 46 Returned for test of cure
GNDC: Gram-negative intracellular diplococcic; HIV: human immunodeficiency virus; NA: not available; NAAT: nucleic acid amplification tests.
The male sex partner first came to the GUM clinic men-
tioned above in September 2010 for a check-up, as a
chlamydia contact of a female patient and was given
azithromycin one gram. He considers himself gay but
has some female contacts. No link to this patient was
made until eight weeks later when Case 2 was diag-
nosed with gonorrhoea. When he was recalled, he
refused to provide any additional samples although
accepted treatment with cefixime.
The three gonococcal isolates from Case 1 and one
of the two isolates from Case 2 were available for
extended susceptibility tests using Etests. In addi-
tion to decreased susceptibility to cefixime, all were
sensitive to ceftriaxone and spectinomycin and were
resistant to ciprofloxacin and penicillin (Tables 1 and
2). The isolates from Case 1 showed an increase in the
minimal inhibitory concentration (MIC) to azithromycin
from 0.25 mg/L (day 1 and 22) to 1.0 mg/L (day 30) and
Case 2 showed a MIC of 0.5 mg/L. The three isolates
from Case 1 were indistinguishable by Neisseria gonor-
rhoeae multi-antigen sequence typing (NG-MAST) ,
Clinical and microbiological findings and treatment given for gonorrhoea, Case 2, England 2010
Case 2 SymptomsTest resultsSusceptibility resultsTreatment
Contact of a
Gonorrhoea and chlamydia: NAAT
Syphilis serology and HIV- negative
Hepatitis B and hepatitis C markers-negative
NAAzithromycin 1 gram orally
Urethra –intracellular GNDC
Gonorrhoea and chlamydia-NAAT
Urine- GC positive/CT negative
Cefixime 400 mg orally
Doxycycline 100 mg bd /
Purulent discharge on
Ceftriaxone 250 mg intra-
NA None given
bd: twice daily; CT: Chlamydia trachomatis; GC: Neisseria gonorrhoeae; GNDC: Gram-negative intracellular diplococcic; HIV: human
immunodeficiency virus; NA: not available; NAAT: nucleic acid amplification tests.
a Disc sensitivity testing only available.
belonging to sequence type (ST) 3779 (por, 2147; tbpB,
110) but distinct from the isolate from Case 2 which
belonged to ST 3431 (por, 2078; tbpB 110). All isolates
contained the penA mosaic allele . Susceptibility to
cefixime of both isolates from Case 2 had been deter-
mined using discs at the local laboratory and appeared
initially sensitive and then exhibiting reduced suscep-
tibility. This could indicate acquisition of a different
strain but could also reflect difficulties in testing gono-
coccal susceptibility and remains unresolved as the
initial isolate was unavailable for confirmatory testing
at the reference laboratory. In the absence of treat-
ment failures, the relationship of zone size to clinical
failure is unknown and the second isolate was referred
to Sexually Transmitted Bacteria Reference Laboratory
(STBRL) by request of the clinician suspecting treat-
We report two cases of treatment failures to cefixime
in England, one of which fulfils all the criteria for a
verified failure . The second case has limited infor-
mation on the pre-treatment isolate but otherwise is
consistent with a treatment failure and similar to a
previous report . The MICs to cefixime of 0.19-0.25
mg/L are consistent with the report from Norway 
and with the European Committee on Antimicrobial
Susceptibility Testing (EUCAST)  breakpoints of MIC
0.12 mg/L, although these remain putative until the
relationship with clinical failure is fully clarified. They
are also compatible with Monte Carlo Simulation mode-
ling that suggests peak serum cefixime concentrations
are inadequate for successful eradication of infections
exhibiting MICs of 0.125 mg/L and above at the current
doses used .
Case 1 also demonstrated treatment failure to azithro-
mycin on potentially two occasions following treat-
ment, on days 5 and 22. The patient admitted having
had sex with the same contact between the two treat-
ments and so he could have been re-infected with the
same strain, which subsequently then failed azithro-
mycin treatment again. However, the female contact
was never diagnosed with gonorrhoea. The MIC break-
point that equates with treatment failure for azithromy-
cin is not known and is currently arbitrary, but in this
instance the increase in MIC over time suggests selec-
tion of resistant strain during therapy, as previously
demonstrated in the laboratory .
Dissemination of gonococcal isolates with cefixime
decreased susceptibility in England and Wales has
been largely clonal, belonging to ST 1407 or closely
related STs, all sharing the tbpB 110 allele, as in these
isolates [unpublished data]. Public health control of
gonorrhoea is dependent on successful antimicrobial
therapy and lessons should be learnt from the extraor-
dinary ability of the gonococcus to be resistant and
innovative treatment regimens will need to be used to
prevent gonorrhoea becoming an infection difficult to
treat. A viable organism is essential to detect emerging
resistance as well as for susceptibility testing for indi-
vidual patient management and therefore maintaining
culture will be of paramount importance.
The authors would like to thank the staff of the Newcastle
HPA Laboratory and the Sexually Transmitted Bacteria
Reference Laboratory, HPA, Colindale.
1. British Association for Sexual Health and HIV (BASHH).
National guideline on the diagnosis and treatment of
gonorrhoea in adults 2005. London:BASHH. [Accessed
24 Dec 2010]. Available from: http://www.bashh.org/
2. Unemo M, Golparian D, Syversen G, Vestrheim DF, Moi H.
Two cases of verified clinical failures using internationally
recommended first-line cefixime for gonorrhoea treatment,
Norway, 2010. Euro Surveill. 2010;15(47):pii=19721. Available
3. Unemo M, Golparian D, Hestner A. Ceftriaxone treatment
failure of pharyngeal gonorrhoea verified by international
recommendations, Sweden, July 2010. Euro Surveill.
2011;16(6):pii=19792. Available from: http://www.
4. Martin IM, Ison CA, Aanensen DM, Fenton KA, Spratt
BG. Rapid sequence-based identification of gonococcal
transmission clusters in a large metropolitan area. J Infect Dis.
5. Ochiai S, Ishiko H, Yasuda M, Deguchi T. Rapid detection of
the mosaic structure of the Neisseria gnorrhoeae penA gene,
which is associated with decreased susceptibilities to oral
cephalosporins. J Clin Microbiol. 2008;46(5):1804-10.
6. Tapsall JW, Ndowa F, Lewis DA, Unemo M. Meeting the
public health challenge of multidrug- and extensively drug-
resistant Neisseria gonorrhoeae. Expert Rev Anti Infect Ther.
7. Forsyth S, Rooney G. Cefixime resistant Neisseria gonorrhoeae
in the UK: a time to reflect on practice and recommendations.
Int J STD AIDS. Forthcoming 2011.
8. European Committee on Antimicrobial Susceptibility Testing.
Breakpoint tables for interpretation of MICs and zone
diameters. version 1.3, January 5, 2011. [Acessed 6 April
2011]. Available from: http://www.eucast.org/fileadmin/src/
9. Chisholm SA, Mouton JW, Lewis DA, Nichols T, Ison CA,
Livermore DM. Cephalosporin MIC creep among gonococci:
time for a pharmacodynamic rethink? J Antimicrob Chemother.
10. Chisholm SA, Dave J, Ison CA. High-level azithromycin
resistance occurs in Neisseria gonorrhoeae as a result of
a single point mutation in the 23S rRNA genes. Antimicrob
Agents Chemother. 2010;54(9):3812-6.
Outbreak of rotavirus gastroenteritis in a nursing home,
Slovenia, December 2010
A Trop Skaza (firstname.lastname@example.org)1, L Beskovnik1, T Zohar Cretnik1
1. Institute of Public Health Celje, Celje, Slovenia
Citation style for this article:
Trop Skaza A, Beskovnik L, Zohar Cretnik T. Outbreak of rotavirus gastroenteritis in a nursing home, Slovenia, December 2010. Euro Surveill. 2011;16(14):pii=19837.
Available online: http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19837
Article published on 7 April 2011
A gastroenteritis outbreak affected 45 people (40 resi-
dents and five staff) in a nursing home for the elderly
in the Celje region, north-east Slovenia, between 17
December and 31 December 2010. Rotavirus group A
was laboratory confirmed in the stools of five ill indi-
viduals. The outbreak was identified when the number
of affected persons was high but was successfully
controlled after implementing preventive measures.
On 28 December 2010, the regional epidemiologist
of the Institute of Public Health Celje, North East
Slovenia, was informed that several residents and staff
of a nursing home in the Celje region had symptoms
of acute gastroenteritis. Symptoms had first occurred
in two residents on 17 December. On 26 December, an
88 year-old resident had been hospitalised for dehy-
dration because of diarrhoea and vomiting. By 28
December, 32 people (four staff and 28 residents) were
reporting one or a combination of symptoms including
diarrhoea, vomiting, malaise and in four cases elevated
body temperature. On 28 December, the Department of
Medical Microbiology, Institute of Public Health, Celje
confirmed the presence of rotavirus group A antigens
in the 88 year-old resident’s stool.
Rotavirus infections are well documented in preschool
children and present a problem in developed and devel-
oping countries alike. Worldwide, 870,000 children
under five years old die from rotavirus infections every
year [1,2]. In adults, symptomatic rotavirus infections
are relatively rare, but can cause health problems and
outbreaks in the elderly and in immunocompromised
individuals [3,4]. For children under five, there are two
licensed vaccines against rotavirus infections.
Rotaviruses are RNA viruses from the Reoviridae fam-
ily; they are divided into seven serogroups (A to G) on
the basis of antigen groups. Infections in humans are
caused by serogroups A, B and C, serogroup A being
the most common.
On 28 December, an outbreak investigation was ini-
tiated. The nursing home for the elderly comprised
121 residents aged from 66 to 95 years, 85 females
and 36 males. The residents were cared for by 30 of
a total 62 staff which also included 14 kitchen staff
and 18 support personnel (cleaners, drivers and jani-
tor). Of the residents, 66 were fully mobile, 26 were
wheelchair users and 29 were bed-bound. The rooms
for residents are either equipped with one or two beds
and are located in the basement, on the ground floor,
at the first level, and in two lofts. In addition, there
are four small kitchens on each respective floor, a din-
ing hall and a living room. The nursing home does not
have a separate unit for bed-bound residents. Mobile
residents can go about freely in and around the nurs-
Enterovirus infection was suspected based on the
microbiological confirmation of rotavirus gastroenteri-
tis in the hospitalised resident. Every resident and staff
member (epidemiological link) who presented with at
least one of the following symptoms and signs from 17
December was classified as a probable case: diarrhoea
(>three loose stools/day), vomiting and elevated body
temperature (>37°C). A confirmed case was consid-
ered as a case with clinical symptoms and laboratory
A total of 151 epidemiological questionnaires were
distributed to all residents and nursing staff with
questions on the date of onset of symptoms if any,
gastroenteritis-related health problems and their dura-
tion, treatments, and ingestion of food and beverages
outside the nursing home. The residents were also
asked to identify the room they occupied, and the nurs-
ing staff reported which residents they cared for and
possible onset of symptoms of gastroenteritis in their
family members, if applicable. In parallel, information
on measures to prevent the spread of the disease and
instructions on how and what samples to collect (vomit,
stool) for microbiological analysis were distributed .
We received completed questionnaires for all nursing
staff and all residents by 4 January 2011. Residents
from all building levels of the nursing home felt ill;
no level-based clustering was observed. All the staff
affected had provided nursing care to symptomatic
residents. According to the probable case criteria, the
two residents who became ill on 17 December 2010
(11 days before we were informed of the outbreak)
were identified as the first two cases in the outbreak.
Between 28 and 30 December, 15 residents became ill,
and no further cases were identified after 31 December
(Figure). A total of five of 30 nursing staff (16.7%), and
40 of 121 residents (33%) became ill during the out-
break. The overall attack rate was 30%. Only one resi-
dent was hospitalised. None of the kitchen staff and
support personnel became ill as they were informed
about the outbreak and asked to report if they had any
symptoms. The staff did not report any symptoms of
gastroenteritis in their family members.
Diarrhoea was reported by all 45 affected individuals,
19 experienced vomiting and four had elevated body
temperature. Some patients also reported abdominal
pain (Table). The median age of the affected staff was
35 years (mean: 35 years, age range: 23 to 44 years),
the median age of the affected residents was 78 years
(mean: 82.4 years, age range: 66 to 95 years). The
average duration of symptoms of gastroenteritis was
2.4 days (from one to four days) in staff, and three days
in residents (one to nine days). The outbreak affected
26 women and 19 men. The highest proportion of resi-
dent cases was among fully mobile residents (29 of 40
cases), followed by bed-bound residents (seven of 40
cases) and residents on wheelchairs (four of 40 cases).
One stool sample was collected from the 88 year-old
hospitalised resident on 26 December and was sent
to the Department of Medical Microbiology, Institute
of Public Health Celje. On 28 December, results of
enzyme-linked immunosorbent assay (ELISA) testing
for antigens of adenoviruses, astroviruses and group
A rotaviruses were available. Routine diagnostic pro-
cedures for rotavirus infections usually include spec-
trophotometric enzyme immunoassay (EIA), which is
highly sensitive and detects group A rotaviruses only.
Qualitative EIA was used to confirm antigens of group
A rotaviruses (ProSpectTM Rotavirus Microplate Assay,
OXOID). Up to 28 December, cultures for Salmonella
spp., Shigella spp., Campylobacter spp. Yersinia spp.,
Clostridium difficile toxin A and B, and C. difficile did
not point to infection with these bacteria and were con-
firmed to be negative on 30 December.
On 28 and 29 December, taking in consideration the
result of the hospitalised patient, five additional stool
samples from four symptomatic residents and one staff
member were tested only for the presence of antigens
of astroviruses, adenoviruses and group A rotaviruses.
EIA was used to confirm rotavirus group A antigens in
four samples, including three from the residents and
one from the staff; one sample was negative. All indi-
viduals tested were negative for noroviruses.
On 30 December, following the confirmation of a rota-
virus outbreak, a special sanitary inspection of the
Epidemic curve for cases of rotavirus gastroenteritis in a nursing home for the elderly, Slovenia, December 2010 (n=45)
15 161718 192021 22232425 262728293031 01 02 03040506 07 08091011 1213 14 15
Date of onset
Number of cases
Implementation of control measures
nursing home was performed. Measures to prevent the
spread of viral diarrhoea were put in place; strict hand
hygiene and cleaning with an appropriate disinfectant
for viruses, cleaning and disinfection of equipment,
surfaces and rooms. Regular airing of premises was
recommended. Sanitary inspection of proper disposal
of incontinence pads with excrements from residents
was conducted. As a temporary measure, contacts
between the affected and non-affected residents were
limited; cohort isolation of the affected was not imple-
mented. The affected staff were removed from work for
a period of one to four days until they did not present
any more symptoms [6,7].
We describe an outbreak of rotavirus gastroenteritis in
a nursing home for the elderly. On 17 December, two
residents became ill at the same time; the first resident
was bed-bound and the second was mobile and visit-
ing the first one. The first member of the staff fell ill on
19 December (Figure). The outbreak, affected 40 of 121
residents and five of 30 nursing staff. All five affected
members of the staff had provided nursing care to bed-
bound residents. The most frequent symptoms were
diarrhoea, vomiting and elevated body temperature.
The average duration of illness was different for staff
and residents, 2.4 and three days, respectively. All
affected persons made full recovery; only one resident
Rotavirus gastroenteritis symptoms usually accompany
primary infection in childhood, which is followed by
protection against subsequent symptomatic infection.
For this reason, the ratio of symptomatic to asymp-
tomatic infection decreases with age. In prospective
studies, symptomatic infection rates were highest in
children under two years, and lowest in those of 45
years of age . Rotavirus infection in immunocompro-
mised adults can have a variable course from asympto-
matic to severe and sustained infection . Vaccination
for infants from six to 26 weeks of age, which has
already been included in some national vaccination
programmes, will serve to decrease the burden of rota-
virus infections in the future [8,9]. In Slovenia, rotavi-
rus vaccination for infants is available against payment
Before 2008, rotavirus gastroenteritis outbreaks in
Slovenia were reported mostly in preschool and school
environments . In 2008, however, rotavirus gastro-
enteritis outbreaks in nursing homes for the elderly in
Slovenia were first recorded in addition to norovirus
Our investigation shows another outbreak of rotavirus
gastroenteritis in an elderly nursing home, highlighting
the potential of rotavirus outbreaks in such a setting.
Our results are in agreement with other studies report-
ing that long-term residence in a closed community is a
risk for rotavirus illness . Noteworthy in our inves-
tigation, is that five of 30 younger nursing staff (rang-
ing from 23 to 44 years) were affected. This indicates
that rotavirus infections can occur in all age groups
and affect caretakers of an elderly home, who in turn
can contribute to the spread of the disease. This is not
entirely unexpected as faeces and vomit from infected
individuals can contain more than 1013 infectious infec-
tious particles* per gram and only 10 to 100 of these
are required to transmit infection . Future epidemio-
logical studies are needed to assess the impact of rota-
virus infections in the elderly.
To this effect, outbreaks need to be not only registered,
but also reported as close as possible to onset, so that
microbiological diagnostic and complete monitoring
can be implemented as fast as possible. In the present
outbreak, public health authorities were only notified
once the number of affected persons was high. This
situation is likely to occur frequently because of the
speed at which rotavirus gastroenteritis outbreaks can
spread, so our investigation highlights the importance
of a tight collaboration and dialogue between nursing
home staff and public health authorities. More efforts
need to be focused on increasing vigilance among
caretakers for elderly or vulnerable groups and train-
ing caretakers to communicate outbreaks in a timely
manner. This will prevent delays in putting in place
containment measures and will allow for better care of
vulnerable groups such as the elderly or immunocom-
*Erratum: The number 1013 was corrected on 09 April 2011.
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Wielen M, et al. Multicentre prospective study of the burden
of rotavirus acute gastroenteritis in Europe, 2004-2005: The
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2. Parashar UD, Gibson CJ, Bresse JS, Glass RI. Rotavirus and
severe childhood diarrhea. Emerg Infect Dis. 2006;12(2):304-6.
3. Anderson EJ, Weber SG. Rotavirus infection in adults. Lancet
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4. Kirk MD, Fullerton KE, Hall GV, Gregory J, Stafford R, Veitch
MG, et al. Surveillance for outbreaks of gastroenteritis in
long-term care facilities, Australia, 2002-2008. Clin Infect Dis.
Clinical manifestation in ill individuals, rotavirus
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Number of individualsa
a Each individual could record up to six symptoms listed.
5. Guardado JA, Clara WA, Turcios RM, Fuentes RA, Valencia
D, Sandoval R, et al. Rotavirus in El Salvador: an outbreak,
surveillance and estimates of disease burden, 2000-2002.
Pediatr Infect Dis J. 2004;23(10 Suppl):S156-60.
6. Kroneman A, Vennema H, van Duijnhoven Y, Duizer
E, Koopmans M. High number of norovirus outbreaks
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elsewhere: does this herald a worldwide increase?. Euro
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7. Barker J, Vipond IB, Bloomfield SF. Effects of cleaning and
disinfection in reducing the spread of Norovirus contamination
via environmental surfaces. J Hosp Infect. 2004;58(1):42-9.
8. Kudjawu Y, Lévy-Bruhl D, Pastore Celentano L, O’Flanagan
D, Salmaso S, Lopalco PL, et al. The current status of HPV
and rotavirus vaccines in national immunisation schedules
in the EU – preliminary results of a VENICE survey. Euro
Surveill. 2007;12(17):pii=3181. Available from: http://www.
9. Macartney KK, Porwal M, Dalton D, Cripps T, Maldigri T,
Isaacs D, et al. Decline in rotavirus hospitalisations following
introduction of Australia’s national rotavirus immunisation
programme. J Paediatr Child Health. 2011;47:1440-5.
10. The Slovenian immunoprophylaxis and chemoprophylaxis
programme in 2009. Official Gazette of RS No. 24/09.
11. Institute of Public Health of the Republic of Slovenia.
[Epidemiological surveillance of reported communicable
diseases in Slovenia 2009]: Ljubljana: Ministry of Health
of the Republic of Slovenia and Institute of Public Health
of the Republic of Slovenia; Sep 2010. Slovenian. Available
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of norovirus infection in a nursing home in northern Slovenia,
July 2007. Euro Surveill. 2007;12(41):pii=3286. Available
13. Iijima Y, Iwamoto T, Nukuzuma S, Ohishi H, Hayashi K,
Kobayashi N. An outbreak of rotavirus infection among adults
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Infect Dis. 2006;38(6-7):490-6.
Surveillance and outbreak reports
Outbreak of Shigella sonnei infections in the Orthodox
Jewish community of Antwerp, Belgium, April to
K De Schrijver (Koen.email@example.com)1,2, S Bertrand3,4, I Gutiérrez Garitano5,6, D Van den Branden1,
J Van Schaeren7
1. Department of Infectious Disease Control, Antwerp, Belgium
2. Department of Epidemiology and Social Medicine, University of Antwerp, Belgium
3. National Reference Centre for Salmonella and Shigella, Scientific Institute of Public Health, Brussels, Belgium
4. Operational Direction for Transmissible and Infectious Diseases, Scientific Institute of Public Health, Brussels, Belgium
5. European Programme for Intervention Epidemiology Training (EPIET), European Centre for Disease Prevention and Control,
6. Operational Direction for Surveillance and Public Health, Scientific Institute of Public Health, Brussels, Belgium
7. Laboratory of Microbiology Sint Vincentius, Antwerp, Belgium
Citation style for this article:
De Schrijver K, Bertrand S, Gutiérrez Garitano I, Van den Branden D, Van Schaeren J. Outbreak of Shigella sonnei infections in the Orthodox Jewish
community of Antwerp, Belgium, April to August 2008. Euro Surveill. 2011;16(14):pii=19838. Available online: http://www.eurosurveillance.org/ViewArticle.
Article published on 7 April 2011
In the beginning of April 2008 three cases of Shigella
sonnei infection were identified among the Orthodox
Jewish community of Antwerp, Belgium. We conducted
a descriptive study and a household cohort study to
identify potential risk factors. Stool samples were
cultured and antibiotic susceptibility of the isolates
was determined. Between April and August 2008,
42 cases were registered. All characterised isolates
(n=20) shared an identical pulsed-field gel electro-
phoresis profile and were indistinguishable from one
of the twelve main strains detected in Israel in 2008,
where the index case’s father had stayed before the
outbreak. The secondary attack rate in households
was 8.5% (95% confidence interval (CI): 4.3–12.7).
Multivariate analysis identified the following risk
factors for secondary spread: households with more
than three children (adjusted relative risk (RR): 9.17;
95% CI: 1.21–69.13), children younger than five years
(adjusted RR: 5.45; 95% CI: 2.44–12.62), and children
younger than 12 years assisting in washing younger
siblings (adjusted RR: 5.45; 95% CI: 2.44–12.17).
Rigorous hand washing, use of disposable towels,
information for parents and caregivers, and exclusion
of symptomatic children from day care, preschool and
school for a minimum of 48 hours were implemented.
Infection with Shigella sonnei is a major cause of bac-
terial gastroenteritis and a leading cause of bacillary
dysentery in Belgium [1,2]. Shigellosis is a highly com-
municable disease and requires a low dose for infec-
tion [1,2]. In industrialised countries person-to-person
transmission accounts for most cases of S. sonnei
infections, which occur commonly in children aged
between six months and 10 years [2,3].
Shigellosis has been a statutorily notifiable disease
for clinicians and microbiologists in Belgium since 1971
. Between 2000 and 2009, the number of laboratory
isolates of shigellae registered annually by the Belgian
reference laboratory of salmonellae and shigellae
varied from 316 to 500. S. sonnei has been the pre-
dominant agent causing 65% to 75% of all registered
Shigella infections [4,5].
In the beginning of April 2008, a microbiologist of
one of the town hospitals informed the Department
of Communicable Disease Control of Antwerp that
S. sonnei had been isolated from three children. The
patients belonged to the Orthodox Jewish commu-
nity of the town. The standardised post-notification
interview with their general practitioners and parents
showed that the patients had not been out of the coun-
try in the month before onset of symptoms. The father
of the first case had just returned from a stay in Israel
where he felt sick during three days before his return.
Antwerp has an Orthodox Jewish, highly insular com-
munity of approximately 10,000 persons living in one
quarter of town. The community is characterised by
relative social isolation and frequent international con-
tacts especially with New York, London, and Israel .
Although sporadic cases of shigellosis have been iden-
tified among members of the Orthodox Jewish commu-
nity in Antwerp before, a well documented outbreak in
Belgium has never been described .
The first aim of the study was to describe the extent
of the outbreak and to identify risk factors for second-
ary transmission. In addition, we tried to compare the
strains from identified cases to confirm that they were
genetically indistinguishable and to compare them to
the circulating strains in Israel. Using the information
obtained from these objectives, we wanted to imple-
ment appropriate public health control and preven-
tion measures in order to stop the propagation of the
disease. An outbreak control team was established to
oversee the coordination of this study.
A confirmed case was defined as a person living in the
town of Antwerp, who had a positive stool culture for
S. sonnei in the period between 1 April and 31 August
2008. A probable case was defined as a person who
had diarrhoea (three or more loose stools within 24 h),
fever (≥38°C) and nausea, and who lived in a household
where a confirmed case had been detected. An index
case in a household or school was the first laboratory-
confirmed shigellosis case in each household or school
class. A secondary case was a confirmed or a probable
case occurring within seven days after the detection of
an index case in a household or in a classroom.
Cases of shigellosis were reported by peripheral micro-
biological laboratories and clinicians in accordance
to statutory notification of infectious diseases. Active
case finding among members of affected households
and school classes was performed by the local health
authorities. General practitioners and paediatricians
were asked to report cases to the outbreak control
For each identified case, information on demograph-
ics, and clinical and microbiological characteristics
was collected using a standardised questionnaire. The
questionnaire also collected information on possible
exposures including any recent travel, attending fam-
ily gatherings, contacts with other cases, names of
household contacts, and attendance at schools or day
care centres. It was administered by telephone or by
face-to-face interviews at home. Household contacts
were followed prospectively for clinical symptoms dur-
ing one week after contact with the index case. Social
Service of the Antwerp Jewish community assisted in
contacting people in order to avoid language and cul-
tural barriers. Demographic data collected on house-
hold members were compared to data collected from
the municipal registry office.
Secondary attack rate study
To identify specific risk factors for secondary trans-
mission, a retrospective cohort study was conducted
among the household contacts of the index cases.
A household contact was defined as a person living
in the same house as the household index patient.
A secondary attack rate was calculated by identify-
ing secondary cases in proportion to the number of
household contacts after exclusion of the index case.
Potential risk factors for transmission in the household
were assessed as follows: the number of children in
the household, the age of the children, the presence
of children with nappies, the practice of hand washing
after washing children, the number of toilets, whether
children younger than 12 years (primary school chil-
dren) were assisting their parents in washing siblings
with gastrointestinal symptoms or assisting them at
going to the toilet, whether the index case received
antimicrobial treatment or whether the index case was
admitted to hospital.
Shigella strains isolated from patients in peripheral
clinical laboratories were sent on a voluntary basis
to the National Reference Centre for Salmonella and
Shigella for serotyping by slide agglutination with
commercial antisera (Denka Seiken Co). To evaluate
antimicrobial susceptibility, S. sonnei specimens were
tested by disk diffusion (Kirby-Bauer) following recom-
mendations of the National Committee for Clinical and
Laboratory Standards Institute (CLSI), formerly the
National Committee for Clinical Laboratory Standards
(NCCLS) . Antibiotics tested (BioRad disks) were:
ampicillin, amoxicillin/clavulanic acid, cefotaxime,
chloramphenicol, tetracycline, naladixic acid, cip-
rofloxacin, streptomycin, kanamycin, gentamicin,
sulfonamides, trimethoprim, and trimethoprim/sul-
famethoxazole. Interpretation of inhibition zones was
performed according to the CLSI criteria, and quality
control was performed using the Escherichia coli ATCC
25922 reference strain .
S. sonnei strains were analysed by pulsed-field gel
electrophoresis (PFGE) according to the PulseNet
method and digested with the restriction endonucle-
ase XbaI (New England Biolabs) . Salmonella enterica
serovar Braenderup H9812 was used as size marker.
Fingerprinting II Informatix software (Bionumerics,
BioRad) was used to compare the PFGE profiles.
Salmonella enterica serovar Braenderup H9812 was
used as size marker. FingerprintingII Informatix soft-
ware (Bionumerics, BioRad) was used to compare the
PFGE profiles. In addition, we included as internal ref-
erence five unrelated Shigella strains from national col-
lections that had been isolated from Belgian patients
Onset of illness among Shigella sonnei cases, by week,
Jewish community Antwerp, 17 April–31 August 2008
16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34
Date (week 2008)
Number of cases
in 2008. The PFGE profiles of the outbreak strains in
Antwerp were also compared to patterns, obtained
with the same PulseNet method, of S. sonnei isolated
from different orthodox Jewish community outbreaks in
Israel between 2000 and 2008. The PFGE gel for them
was provided by the Central Laboratories Ministry of
Health of Israel. The bands had been analysed using
the Dice coefficient and the unweighed-pair group
method using average linkage with a tolerance of 1%.
Univariate analysis was performed on data collected
in the retrospective household cohort study and crude
relative risk (RR) along with 95% confidence intervals
(CI) were calculated to determine associations between
potential risk factors and infection. Adjusted RRs were
calculated using a binomial regression model. All sta-
tistical analyses were performed using Stata software
version 11 (StataCorp).
Between 17 April and 31 August 2008, 42 cases of
shigellosis were identified in Antwerp and all of them
belonged to the Orthodox Jewish community, with the
highest number of cases in week 24 (Figure 1). Thirty-
two of them were confirmed cases and 10 were prob-
able cases. Cases occurred in 19 Jewish families and
in four confessional schools. Two additional reported
cases of S. sonnei identified outside the Jewish commu-
nity of Antwerp were excluded from the study because
the disease started during a stay in Egypt. They were
classified as travel-associated cases.
Of the 42 cases, 20 were male and 22 female. The arith-
metic mean of age of cases was 4.4 years with a range
from three months to 61 years. Four patients were
younger than two years, 19 were between two and five
years-old, seven were between six and 10 years-old,
six cases were between 11 and 15 years-old, and six
cases were older than 20. The affected families had an
average of 4.6 children (range: 1–12). All patients had
their residence in an enclosed area in the town centre.
Eighteen cases reported fever ≥38°C and bloody or
mucopurulent diarrhoea and abdominal cramps, and
32 cases were hospitalised. The average duration of ill-
ness was eight days with a range from six to 11 days.
The average stay at the hospital was 3.4 days.
Of the 42 cases, 15 cases met the criteria for a sec-
ondary case. The generation interval was 3.5 days
(range from one to four). Three children developed ill-
ness within two to five days of detection of a case in a
We received antibiotic susceptibility results from 28 of
the 32 confirmed S. sonnei isolates. All of them were
resistant to amoxicillin and trimethoprim-sulfame-
thoxazole, but were susceptible to levofloxacin and
Cluster analysis of PFGE fingerprinting of Shigella sonnei
isolated in Antwerp and Israel in 2008
‘Lane 11, 12 and 13 gel Israel’: S. sonnei from different outbreaks in
Orthodox Jewish communities in Israel in 2008.
‘Patient outbreak Antwerp’: S. sonnei strain from the outbreak in
Antwerp in 2008.
‘Control strains’: unrelated S. sonnei strains from the national
collection of the Belgian national reference laboratory in 2008.
cefotaxim. PFGE was performed on 20 of the 32 iso-
lates and showed that all strains isolated during this
outbreak displayed the same restriction-fragment pat-
terns, confirming the relatedness of these isolates.
The outbreak strain in Antwerp was compared to 12
different outbreak strains detected in Shigella sonnei
shigellosis outbreaks in Orthodox Jewish communities
in Israel between 2000 and 2008. Figure 2 presents
the results of a cluster analysis on the basis of PFGE
fingerprinting of isolates from Antwerp and Israel. The
isolate called ‘Lane 13 gel Israel’, S. sonnei isolated in
2008 in Israel, was indistinguishable from the Belgian
outbreak strain. The isolates shown as ‘Lane 11 and 12
gel Israel’, also isolated in Israel in 2008, had a closely
related profile with the Belgian outbreak strain. Five
unrelated S. sonnei strains originating from national
Belgian collections (‘Control strain Belgium’ from
2008) were used as internal reference.
Secondary attack rate study
For the 29 affected households with confirmed cases,
we identified 175 household contacts, of whom 15
developed shigellosis. A secondary attack rate of
8.5% (95% CI: 4.3–12.7) was calculated. Information
on hand washing, the number of toilets in the home
and the use of disposable towels was only provided
by four of the 25 interviewed households. These ques-
tions were excluded in the analysis. The calculated
crude and adjusted RRs for the other risk factors are
shown in the Table. In the uni- and multivariate analy-
sis, having more than three children in the family, hav-
ing children younger than 12 years who assisted their
parents washing siblings and helping them go to the
toilet, and having children younger than five years,
were significantly associated with a higher risk of
secondary transmission. Having more than three chil-
dren in the household was associated with the highest
risk, with an adjusted RR of 9.17 (95% CI: 1.21–69.13).
Hospitalisation and treatment with antibiotics of the
household index cases were not significantly associ-
ated with a lower risk of secondary infection, with a
respectively adjusted RR of 0.88 (95% CI: 0.61-3.1) and
an adjusted RR of 1.8 (95% CI: 0.80-4.34).
To prevent further spread of the disease, parents of
the affected families were advised of the importance of
hand washing with running water and liquid soap after
using the toilet or washing the children and also on
the importance using disposable towels and cleaning
the toilets with chlorine. The need to decontaminate
toys was highlighted. In June 2008 educational pres-
entations for parents, caregivers and teachers were
organised. Information was also published in the local
media. Physicians were informed via articles in the
local medical infectious disease journal. Schools were
informed on the hygiene of hand washing facilities. We
insisted on excluding symptomatic children for a mini-
mum of 48 hours after clinical recovery from day care
centres, preschool and school attendance .
We identified a cluster of 42 cases of shigellosis in the
Orthodox Jewish community of Antwerp with 32 iso-
lates laboratory-confirmed as S. sonnei with the same
genetic profile. Temporal and spatial clustering in one
area of town affecting one specific community sup-
ported the hypothesis of a single ongoing outbreak,
maintained through person-to-person transmission.
Statutory laboratory-based surveillance of shigellosis
failed to identify concurrent cases outside this com-
munity. Two additional S. sonnei cases notified in the
study period in the province of Antwerp in people who
were not Jewish were most probably not linked to the
outbreak. The disease started during a stay in Egypt
and they were classified as travel-associated cases.
The index case was most probably infected by their
father, who had suffered from gastrointestinal prob-
lems during a stay in Tel-Aviv, Israel until two days
before symptom onset in the index case but did not
seek medical care. No exceptional family gatherings
could be identified except for synagogue attendance.
The father also reported having been in contact with
relatives coming from London.
To investigate a possible link between the outbreak
in Antwerp and an ongoing outbreak in Israel , the
circulating strains in both outbreaks were compared.
Such a link was supported by the microbiological anal-
ysis in which the main strain circulating in Israel at the
time and the outbreak strain in Antwerp were indistin-
guishable. The father of the index case also reported
having been in contact with relatives coming from
Risk factors of illness among household contacts of an index case with shigellosis, Jewish community Antwerp, 17 April–31
August 2008 (n=42)
Univariate analysis Multivariate analysis
>3 children in household
Children with nappies
Children <5 years in household
Children <12 years assisting parents washing siblings
Index case in household hospitalised
Index case in household treated with antibiotics
Crude relative risk 95% confidence interval Adjusted relative risk 95% confidence interval
London. Addiman et al. reported on an outbreak of
shigellosis in London starting a month before the onset
of our outbreak in Antwerp in 2008 . A strain from
the outbreak of London 2008 could not be obtained for
Outbreaks of shigellosis with S. sonnei and recurrent
increases in the number of cases in Orthodox Jewish
populations have already been notified in 2008 and
before in different countries. Calderon-Margalit et al.
showed that between 1998 and 2006, outbreaks of
shigellosis followed a biennial pattern in Israel with
annual rates that ranged from 18 to 353 cases per
100,000 population . Also in 2009 outbreaks of
S. sonnei in Israel were still continuing . Close con-
tacts, day care attendance and having many young chil-
dren in the families were considered risk factors. The
characteristics of the outbreak in Antwerp are compa-
rable with prolonged outbreaks of S. sonnei reported
by Sobel et al. in North America in traditionally observ-
ant Jewish communities between 1994 and 1996  ,
with outbreaks reported by Garret et al. in New York in
2005  and with the outbreak in London in 2008 .
The secondary attack rate of 8.5% found in this study
is comparable to those noticed in other studies [2,15].
In larger studies, secondary attack rate differed
according to age and to the species of bacterium .
Due to the limited number of cases in our study, age-
specific attack rates could not be calculated. Dupont
et al. showed that for one to four year-olds, the sec-
ondary attack rate can reach 40% . The combination
of high communicability due to the low infective dose,
crowding, and frequent contacts are known explana-
tions for the high secondary attack rate for shigellosis
[2,14,15]. In our study we analysed specific risk factors
which might explain the noted secondary attack rate.
Having more than three children in the household and
having children younger than five years of age was sig-
nificantly associated with the occurrence of secondary
cases, which is consistent with data from other authors
. Contrary to what we expected, having children
with nappies in the household was not a significant
independent risk factor in our study. This could be due
to good hygienic habits of the adults when providing
care for their babies. That the index case of the fam-
ily was hospitalised was hypothesised to be a pro-
tective factor, but the adjusted RR was 0.88 (95% CI:
0.61–3.10). The low number of cases and the different
intervals between onset of the disease and moment of
hospitalisation of the cases might have interfered with
the association. Being treated with antibiotics was not
significantly associated with a lower risk of second-
ary transmission either. Different delays in the start
of therapy, the broad spectrum of used antibiotics and
the small number of cases might explain the calculated
RR of 1.8 (95% CI: 0.80–4.34).
However, it was remarkable that children younger than
12 years, helping their parents take care of babies,
was associated with a higher risk of secondary cases
(adjusted RR: 5.45; 95% CI: 2.44–12.17). In families
with a high number of children, older children were
asked to help. There is a risk that these young children
are less sensitive or less knowledgeable than their par-
ents on the risk and the practice of hand hygiene.
Visiting friends and relatives in areas with higher risk
of shigellosis might be the seeding event leading to
shigellosis outbreaks in especially susceptible com-
munities. This is the case for Jewish communities in
Antwerp that are more susceptible due to the high
number of children in the families, the many social
contacts, living in a relatively small community, and
the frequent contact with relatives who live in areas of
higher endemic prevalence of shigellosis, like certain
neighbourhoods in London or Israel [11,12].
The high hospital admission rate in our study (32 of
42 cases) suggests that we have probably detected
only the most severe cases, whereas milder cases
could also have been expected. Presenting bloody or
mucopurulent diarrhoea was noted in 18 of the cases.
This is unusual compared to the expected picture of a
S. sonnei infection which is normally associated with
a milder disease [2,3,5]. We have therefore reason to
consider under-diagnosis and under-reporting in this
outbreak, which is also mentioned in similar outbreaks
of shigellosis elsewhere .
Several limitations of the study especially for the sec-
ondary attack rate study should be noted. Firstly, the
number of cases was limited. This raises concerns
about the interpretation of the calculated relative
risks. Secondly, we assumed that secondary cases
acquired their infection at home. Alternatively they
might have been infected during pre-school and school
attendance or by visiting friends and relatives. Thirdly,
personal questions like ‘did you wash your hands after
toilet use?’ and ‘how many toilets do you use at home’
were often not answered, most probably due to their
sensitive and private nature . It is likely that not all
possible risk factors could be explored in the study of
Early notification of shigellosis enabled prompt reac-
tion, and implementation of the advice most probably
put a stop to further propagation. We presume that
especially the intensive hand washing campaign in
families and schools, the educational presentations
and specific information to physicians contributed to
stopping the outbreak.
PFGE in studies of clusters has been shown to be a
highly effective method of characterising S. sonnei
and an important tool for outbreak investigations .
Provided that the same protocol is used, it allows com-
parison of strains detected in different outbreak. The
genetic relatedness of the strains in this study provides
strong evidence that this cluster was a single outbreak
and associated with recurrent endemic shigellosis in
In conclusion, this is the first well-documented out-
break of S. sonnei in the Orthodox Jewish community
of Antwerp and Belgium for which a direct link to an
ongoing outbreak of endemic shigellosis in Israel could
be identified. The combination of case finding, source
tracing, and comparing different strains with PFGE was
essential for confirming the hypothesis of import of an
outbreak strain from Israel into the local community,
and implementation of hand washing was important to
stop the propagation of the epidemic.
We thank physicians, microbiologists and public health
nurses for their collaboration during the study. We thank
Emmanuel Robesyn for his support during the analysis of
the data, Annick Lenglet for the critical comments, and we
are grateful for the assistance of the Social Service of the
Jewish community of Antwerp for contacting people. We also
thank Lea Valinsky from the Central Laboratories Ministry of
Health, Jerusalem Israel who provided the PFGE pictures of
different outbreak strains detected in Israel.
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