Published Date: 2007-12-21 04:00:25
Subject: PRO/AH/EDR> Salmonellosis, serotype Paratyphi var Java - Europe
Archive Number: 20071221.4100
SALMONELLOSIS, SEROTYPE PARATYPHI VAR JAVA - EUROPE
A ProMED-mail post
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International Society for Infectious Diseases
Date: Thu 20 Dec 2007
Source: Eurosurveillance weekly release [edited]
Multinational _Salmonella_ Paratyphi B var Java outbreak, August - December
Background on _Salmonella_ Paratyphi B, variant Java
_Salmonella_ Paratyphi B and Java are biovars of common serotype 1,4,,
12:b:1,2 which respectively cause human paratyphoid fever and
gastroenteritis (1). The d-tartrate fermenting variant _S. enterica_
subspecies _enterica_ serovar Paratyphi B dT+ (formerly called and referred
to in this report as _S._ Java) is thought to be less virulent to humans
than the non d-tartrate fermenting variant, although cases of invasive
infection have been reported (1,5).
_S._ Java is a complex organism with a range of genetically distinct clonal
lineages. Unlike 'classical' _S._ Paratyphi B, _S._ Java has an animal
reservoir and has caused substantive outbreaks as a result of the
contamination of food products. For example, in France in 2003 when 273
people were infected and one death was reported in an outbreak associated
with contaminated goat's milk cheese (5). More recently, 2 distinct clonal
lines characterized by resistance to antimicrobial drugs have been widely
distributed. One of these was frequently found in poultry production, in
the Netherlands, between 2000 and 2004 (4-7), and caused infections in
humans in several countries in Europe as a result of the importation of
infected poultry from the Netherlands (8). The 2nd clonal line,
characterized by possession of Salmonella Genomic Island 1 (SGI1), has
become widely distributed worldwide. These strains are generally resistant
to ampicillin, chloramphenicol, streptomycin, spectinomycin, sulphonamides
and tetracyclines (3,9,10) and have been associated with aquaria, in
particular tropical fish aquariums (11), although outbreaks in cattle have
also been reported (12).
On 15 Aug 2007, Enter-net, the international surveillance network for the
enteric infections Salmonella and VTEC O157, circulated a PFGE profile of
_S._ Java outbreak strain in response to a cluster of cases first
identified in Sweden on 10 Aug 2007. On 5 Dec 2007, the United Kingdom (UK)
issued another urgent inquiry after an investigation of 20 cases of _S._
Java phage type 3b var 9; the majority of isolates were sensitive to all
antimicrobial drugs at the levels used in the HPA Laboratory of Enteric
The rapid inquiry sent through the network requested member states (MS) to
check the occurrence of cases with a strain matching the PFGE pattern seen
in the UK. As of 18 Dec 2007, the results of this inquiry are the following:
- In Sweden, a total of 172 cases have been identified in a large outbreak
between July and September 2007. The strain identified in 2007 demonstrated
a PFGE pattern identical to the strains isolated from cases in the previous
year (September-October, 2006). This PFGE profile has been designated
SPTJXB.0001 in accordance with the Pulse-Net Europe (13) designations for
PFGE profile types. An epidemiological investigation showed a strong
association with imported baby spinach. Spinach samples were taken by the
Swedish food authorities but Salmonella was not detected in any of the food
samples. In the Swedish outbreak, more than 40 percent of the first 116
cases were hospitalized and no deaths have been reported. As a result of
the Swedish investigation linking the outbreak with imported baby spinach,
an alert was issued within the Rapid Alert System for Food and Feed (RASFF)
on 24 Aug 2007 by the Swedish authorities. 5 additional cases have become
ill in November 2007.
- In Denmark, a total of 15 cases with SPTJXB.0001 were identified between
August and November 2007; the PFGE pattern is pending for another 4 recent
cases. In 2006, 7 cases with SPTJXB.0001 were identified in
September-October. Interviews of a subset of the 2007 cases have so far not
confirmed baby spinach as the vehicle of infection nor led to alternative
- The UK is currently investigating 22 cases identified since 1 Nov 2007
(including 3 cases from Scotland and 2 believed to be from secondary
spread). The PFGE pattern has shown to be indistinguishable from that of
SPTJXB.0001. 12 of the 17 primary cases in England have been interviewed to
date to develop a hypothesis for disease transmission. It is notable that
11 of the 12 cases reported the consumption of salad vegetables purchased
from a number of retailing and catering outlets. No single leaf type has
been clearly identified. The frequencies of consumption of other foods were
all markedly lower, and the investigation has ruled out fruit, fish,
shellfish, dairy products, all meats, contact with animals and travel
abroad. No new cases have been identified in December, but earlier cases
occurring in August, September and October 2007 have been reported yet
their exact numbers have not been established yet.
- In Finland, 1 case has been identified in August 2007. Importantly, this
case became ill after visiting Sweden. The strain isolated had the
SPTJXB.0001 profile. No information is available on the food exposures of
- In Norway, 10 cases with SPTJXB.0001 have been identified in August 2007.
8 of these had also visited Sweden before becoming ill. No information on
the food exposures of the 10 cases is available.
- In the Netherlands, 2 cases with SPTJXB.0001 have been identified in
October 2007. One of them had travel history to Bosnia-Herzegovina.
- In the USA, 1 case with an identical PFGE pattern to SPTJXB.0001 has been
reported in August of 2007. This case will be interviewed to learn of any
travel to Europe.
ECDC risk assessment
In an effort to respond to the ongoing outbreak and the increasing numbers
of cases of acute gastroenteritis infected with _S._ Java strain with
SPTJXB.0001 profile, the ECDC produced a risk assessment for the European
Commission with the following conclusions:
Cases have continued to occur since the summer of 2007 and microbiological
evidence of the SPTJXB.0001 profile points towards a dispersed
multinational outbreak with a continuous and sustained risk to human health
in Europe. Of the more than 300 cases of _S._ Java that have been reported
in 2007, many are likely to be linked to this ongoing outbreak.
Based upon epidemiological evidence from Sweden, imported baby spinach
appears to be the most likely vehicle, yet no microbiological confirmation
of this has been obtained.
As there is a potential to have more cases linked to this outbreak in the
future, efforts to confirm a food source through microbiological
investigations should be encouraged via the collaboration between national
public health and food safety authorities, especially in Sweden, the UK,
Summary and conclusion
In 2007, 354 _S._ Java cases have been reported to ECDC by 11 MS (figure 1,
[for figures, see original URL - Mod.LL]). 228 of these cases (as of 18 Dec
2007) have an indistinguishable PFGE pattern, designated SPTJXB.0001, and
are therefore possibly linked to the multinational outbreak (figure 2).
Unfortunately microbiological investigations have failed to confirm the
incriminated vehicle of the Swedish cases.
Evidence for a possible vehicle in this multi-national outbreak is based on
a case control study conducted in Sweden in response to their late summer
surge in cases. There, the cases were strongly associated with the
consumption of imported baby spinach. The spinach was initially sold as a
separate product, yet later distributed as a part of a mixed salad product
and served raw (whereas normal sized spinach is typically not used in
salads but merely in warm meals that undergo heat treatment). Salmonella,
however, was not detected in baby spinach samples taken by the Swedish food
authorities. A RASFF was issued by the Swedish authorities in August of
2007 and subsequently a substantial decrease in cases was observed in
Sweden. In spite of this transient decrease, cases continue to be reported
yet at a lower frequency.
The UK epidemiologic investigation results are consistent with salad
vegetables being a possible vehicle of infection, yet no single product or
outlet was implicated and cases could not identify which type of leaf
vegetable they had eaten. More information is clearly needed on the results
of random sampling of imported spinach products in order to learn if the
risk continues from spinach or is now in a mixed salad vehicle. An in-depth
traceback analysis and analysis of supply channels is essential and would
greatly enhance the efficiency of any microbiological testing of imported
salads by focussing on the most 'at risk' products. ECDC will further
explore this question.
In addition to further exploring the spinach and mixed salad as the
possible vehicle, enhanced efforts to identify a common source for this
_S._ Java SPTJXB.0001 outbreak are needed. The authors hope to raise
awareness through this article and by sending urgent inquiries and their
updates via ECDC and thus contribute to the increase in frequency of
sampling suspected food sources and collaboration between national public
health and food authorities. This may, in consequence, add to the
likelihood of identifying a common source of the outbreak. A more rapid
response to the investigation into S. Java cases should minimize recall
bias and further improve the likelihood of detecting the organism in
suspected products and thus help to solve such kinds of investigations.
1. Threlfall EJ. Salmonella. In: Topley and Wilson's Microbiology and
Microbial Infections, 10th Edition, part VI. Editors: Borriello SP, Murray
PR, Funke G. London: Hodder Arnold, 2005. pp 1398-434.
2. Ezquerra E, Burnens A, et al. Genotypic typing and phylogenetic analysis
of Salmonella paratyphi B and S. java with IS200. J Gen Microbiol 1993;
3. Threlfall EJ, Levent B, et al. Multidrug-resistant Salmonella Java.
Emerg Infect Dis 2005; 11: 170-1.
4. Dorn C, Schroeter A, et al. Increasing number of Salmonella paratyphi B
isolates from slaughtered poultry sent in to the national Salmonella
reference laboratory. Berl Munch Tierarztl Wochenschr 2001; 114: 179-83.
5. Desenclos JC, Bouvet P, Benz-Lemoine E, et al. Salmonella enterica
serotype paratyphi B in goat milk cheese, France, 1993. BMJ 1995; 311: 91-4.
6. Miko A, Guerra B, et al. Molecular characterization of multiresistant
d-tartrate-positive Salmonella enterica serovar paratyphi B isolates. J
Clin Microbiol 2002; 40: 3184-91.
7. Van Pelt W, van der Zee H, Wannet W, et al. Explosive increase of
Salmonella Java in poultry in the Netherlands: Consequences for public
health. Euro Surveill 2003; 8(2): 31-5.
8. Brown D, Mather H, Browning L, Coia J. Investigation of human infections
with Salmonella enterica serovar Java in Scotland and possible association
with imported poultry. Euro Surveill 2003; 8(2):35-40.
9. Weill FX, Fabre L, et al. Multiple-antibiotic resistance in Salmonella
enterica serotype Paratyphi B isolates collected in France between 2000 and
2003 is due mainly to strains harboring Salmonella genomic islands 1, 1-B,
and 1-C." Antimicrob Agents Chemother 2005; 49: 2793-801.
10. Han KH, Choi SY, et al. Isolation of Salmonella enterica subspecies
enterica serovar Paratyphi B dT+, or Salmonella Java, from Indonesia and
alteration of the d-tartrate fermentation phenotype by disrupting the ORF
STM 3356." J Med Microbiol 2006; 55: 1661-5.
11. Gaulin C, Vincent C, et al. Outbreak of Salmonella paratyphi B linked
to aquariums in the province of Quebec, 2000. Can Commun Dis Rep 2002; 28:
12. Evans SJ, Davies RH, et al. Multiple antimicrobial resistant Salmonella
enterica serovar Paratyphi B variant Java in cattle: a case report. Vet Rec
2005; 156: 343-46.
13. PulseNet Europe. The molecular surveillance network for food-borne
infections in Europe. <http://www.pulsenet-europe.org>.
[Byline: Denny J, Takkinen J, Straetemans M, et al]
[An interesting outbreak of an interesting organism.
As readers will note from past outbreaks of salmonellosis, the specific
_Salmonella_ organism involved is usually referred to as _Salmonella
enterica_ followed by its serotype (or servar) name such as _S. enterica_
serotype Tennessee. Serotype Tennessee was associated with the recent
USA-wide peanut butter-associated outbreak affected more than 600 people.
_Salmonella_ as a genus has 2 species, _enterica_ and _bongori_. _S.
enterica_ is divided into 6 subspecies: _enterica_, _salamae_, _arizonae_,
_diarizonae_, _houtenae_ and _indica_. _S. enterica_ subspecies _enterica_
(or subspecies I) strains are the ones usually isolated from humans or
warm-blooded animals and represent a majority of the salmonellas that are
The designation _Salmonella_ I 1,4,, 12:b:1,2 means:
- the "I" reflects subspecies _enterica_;
- the "1, 4, " are the O (or somatic) antigens associated with the
- the nomenclature after the colon, in this case b:1,2, reflect the
flagellar or H antigens. It is these H antigens that define the serotype
identity within an individual group of salmonellae. - Mod.LL]