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Archive Number 20090626.2328
Published Date 26-JUN-2009
Subject PRO/EDR> Shigellosis, imported sugar peas - Norway, Denmark: (ex Kenya) susp.

SHIGELLOSIS, IMPORTED SUGAR PEAS - NORWAY, DENMARK: (ex KENYA) SUSPECTED
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[1] Norway
[2] Denmark

******
[1] Norway
Date: Thu 18 Jun 2009
Source: Eurosurveillance edition 2009; 14(24) [edited]
<http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19243>


_Shigella sonnei_ infections in Norway associated with sugar peas,  
May-June 2009
----------------------------------------------------------------------
[Authors:  T Heier1, K Nygard1, G Kapperud1, BA Lindstedt1, GS  
Johannessen2, H Blekkan3
1. Nasjonalt Folkehelseinstitutt (Norwegian Institute of Public  
Health), Oslo, Norway
2. Veterinaerinstituttet (National Veterinary Institute), Oslo, Norway
3. Mattilsynet (Norwegian Food Safety Authority), Oslo, Norway]

In Norway, shigellosis is a mandatorily notifiable disease, and all  
isolates are submitted to the NIPH [Norwegian Institute of Public  
Health] for verification and typing. Around 150 cases of shigellosis  
are confirmed per year, the majority caused by _Shigella sonnei_. Only  
around 10 to 20 of the shigellosis cases reported each year are  
acquired in Norway, usually as secondary cases caused by fecal-oral  
transmission in households.

On 27 May 2009, the National Reference Laboratory at the NIPH alerted  
about a suspected outbreak involving 4 cases of _Shigella sonnei_  
infection. The infected persons were living in 2 different counties in  
Norway, and they had no foreign travel history during the week before  
onset of illness. On the same day, a municipal medical doctor reported  
to the NIPH 5 suspected cases of shigellosis in 2 separate households.

Epidemiological investigation
-----------------------------
An outbreak investigation was initiated on 27 May 2009 by interviewing  
the 4 confirmed cases using a trawling questionnaire. On the same day  
the NFSA [Norwegian Food Safety Authority] inspectors visited the 2  
households where suspected cases were reported and found an unopened  
package of sugar peas imported from Kenya in one household, and the  
packing of the same brand of sugar peas in the other. The sugar peas  
were bought in the same shop. Based on this suspicion, it was decided  
to focus the interviews on consumption of fresh vegetables and lettuce.

Microbiological investigation
-----------------------------
All suspected human _Shigella_ isolates received at NIPH are routinely  
verified, speciated, and typed with multilocus variable-number  
tandem-repeat analysis (MLVA) using a protocol developed by BA  
Lindstedt et al (manuscript in preparation). Isolates of _Shigella  
sonnei_ showing a distinct MLVA-profile were defined as the outbreak  
strain. Food samples were analyzed at the National Veterinary  
Institute first by using NMKL no. 174 (_Shigella_ spp. PCR method for  
detection in food), followed by immuno-magnetic separation (IMS) and  
plating on selective agar. Positive PCR results were confirmed by  
using a modified version of an octaplex PCR developed for  
identification of human diarrheagenic _Escherichia coli_ and _Shigella  
spp._ (1). Any isolates obtained from food samples would be MLVA-typed  
at NIPH to compare with the patient isolates.

Results
-------
By 16 Jun 2009, the reference laboratory has registered a total of 20  
cases with the outbreak strain of _Shigella sonnei_, who had not  
traveled abroad prior to illness onset. The cases live in different  
municipalities, but mainly in the central and western parts of Norway.  
The date of onset for the 1st case was 10 May 2009 (Figure [for  
figures, see original URL - Mod.LL]). All cases were adults except for  
one teenager, and 16 of them were women. All 20 cases reported to have  
eaten sugar peas, and there were no other obvious common exposures  
identified. The majority of the patients had bought the sugar peas in  
one of the large supermarket chains and only a few in another chain.  
The NFSA traced the suspected food product and found that all the  
implicated sugar peas were produced in Kenya. One sample from the  
unopened package of sugar peas collected in a patient household was  
positive for _Shigella sonnei_ by both PCR methods, but could not be  
culture-confirmed.

International alerts
--------------------
On 27 May 2009 the NIPH sent an urgent inquiry through the European  
Food and Waterborne Diseases Network at the European Centre for  
Disease Prevention and Control (ECDC) asking whether an increase in  
the number of _Shigella sonnei_ cases had been registered in other  
countries. On the same day, the NFSA sent an information notice  
through the European Rapid Alert System for Food and Feed (RASFF).  
Based on information from the interviews, the main importer  
voluntarily recalled the product on 29 May 2009. Further results from  
tracing of the food product and preliminary results from the  
microbiological investigation led the NFSA to prohibit all sales of  
sugar peas imported from Kenya later the same day.

Discussion
----------
As a response to our urgent inquiry Denmark reported an increase in  
the number of domestic _Shigella sonnei_ infections in April and May  
2009. They initiated an outbreak investigation to find out if the  
Danish cases were related to the outbreak in Norway. The investigation  
in Denmark also pointed at sugar peas as the source of the outbreak,  
and microbiological investigations (including MLVA typing) to compare  
the outbreak strains are ongoing.

The trace-back investigation of the food product appeared to be very  
complicated, and the NFSA is still investigating together with the  
industry. Several wholesalers are supplying sugar peas to Norway, and  
the product comes from several producers in Kenya. The 2 supermarket  
chains usually do not share the distribution system, but on some  
occasions they are supplied by the same whole-saler.

Only one previous outbreak in Norway has been associated with fresh  
vegetables. An increase in the number of domestic cases of _Shigella  
sonnei_ infection was detected in several European countries in 1994,  
including Norway, Sweden, and the United Kingdom (2). In Norway 110  
culture-confirmed cases of infection were recorded at the time. In all  
3 countries epidemiological evidence incriminated imported iceberg  
lettuce of Spanish origin as the vehicle of transmission. The pathogen  
was not isolated from the suspected food product.

References
----------
1. Brandal LT, Lindstedt BA, Aas L, et al: Octaplex PCR and  
fluorescence-based capillary electrophoresis for identification of  
human diarrheagenic _Escherichia coli_ and _Shigella_ spp. J Microbiol  
Methods. 2007; 68(2): 331-41 [abstract available at
<http://www.ncbi.nlm.nih.gov/pubmed/17079041>].
2. Kapperud G, Rorvik LM, Hasseltvedt V, et al: Outbreak of _Shigella  
sonnei_ infection traced to imported iceberg lettuce. J Clin  
Microbiol. 1995; 33(3): 609-14 [available at
<http://jcm.asm.org/cgi/reprint/33/3/609>].

--
Communicated by:
ProMED-mail
<promed@promedmail.org>

[The HealthMap/ProMED-mail interactive map of Norway is available at
<http://healthmap.org/r/00uw>. - Sr.Tech.Ed.MJ]

******
[2] Denmark
Date: Thu 18 Jun 2009
Source: Eurosurveillance edition 2009; 14(24) [edited]
<http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19241>


Imported fresh sugar peas as suspected source of an outbreak of  
_Shigella sonnei_ in Denmark, April - May 2009
----------------------------------------------------------------------
[Authors: L Mueller1, T Jensen2, RF Petersen3, K Molbak1, S Ethelberg1,3
1. Department of Epidemiology, Statens Serum Institut (Danish National  
Institute of Health, SSI), Copenhagen, Denmark
2. Fodevarestyrelsen (Danish Veterinary and Food Administration),  
Copenhagen, Denmark
3. Department of Bacteriology, Mycology and Parasitology, Statens  
Serum Institut (Danish National Institute of Health, SSI), Copenhagen,  
Denmark]

On 27 May 2009 Norway sent an urgent inquiry through the European Food  
and Waterborne Diseases Network at the European Centre for Disease  
Prevention and Control (ECDC) reporting an increase in the number of  
_Shigella sonnei_ cases. By 1 Jun 2009 Norway informed that they  
suspected the source to be sugar peas. As an increase in the number of  
_Shigella sonnei_ cases was also observed in Denmark in April and May  
2009, we initiated an outbreak investigation to find out if the Danish  
cases were related to the Norwegian outbreak.

Methods
-------
All laboratory-confirmed _Shigella sonnei_ cases since 1 Apr 2009  
(Figure 1 [for figures, see original URL - Mod.LL]) were interviewed  
by telephone about date of onset, symptoms, travel history,  
consumption of sugar peas and a small set of other exposure variables.  
Previous data on sugar peas consumption in the background population  
was reviewed. Isolates were subjected to typing by pulsed field gel  
electrophoresis (PFGE) using the enzyme XbaI. Sugar peas sold in 3  
major groups of supermarket chains were traced back.

Results
-------
In all, 17 cases of _Shigella sonnei_ were reported from 1 Apr to 1  
Jun 2009. 6 cases were travel-related and one was linked to another  
known outbreak caused by fresh large shrimps from Bangladesh. Of the  
remaining 10 cases, 8 reported having eaten sugar peas prior to onset  
of symptoms. Of these 8 cases all were female and their median age was  
31 years (range 11-46 years). None had travelled abroad, except for  
short trips to Sweden before getting ill. The dates of onset of  
illness ranged from 7 Apr to 8 May 2009. The 2 additional cases could  
be related to the outbreak as likely secondary cases as they were  
children of one of the cases who had eaten sugar peas. The children  
fell ill 3 weeks after their mother.

A case-control study was not performed; instead, previous food-borne  
outbreak investigations were reviewed. Consumption of sugar peas is  
among the questions included in several of the commonly used trawling  
questionnaires in Denmark. We looked into 3 different rounds of  
trawling questionnaire studies performed among cases of a large  
outbreak of _Salmonella_ Typhimurium U292 (1). They were done in  
April, May, and August 2008. In these studies 3/10, 2/17, and 0/15  
cases reported consumption of sugar peas in a period of 7 days prior  
to illness. This crude comparison indicated to us a significant  
association between _Shigella sonnei_ infections and consumption of  
sugar peas (using the persons interviewed in April and May 2009 as  
community controls, comparing 8/8 exposed cases to 5/27 exposed  
controls, gives a Fisher p-value of less than 0.0001).

Preliminary PFGE typing results of isolates from 5 of the 10 cases  
associated with sugar pea consumption suggest highly similar patterns.  
The PFGE patterns of the isolates from Danish patients resemble those  
obtained from the Norwegian patients but it is still too early to say  
if they are identical. Further typing results (which will include  
multilocus variable-number tandem-repeat analysis - MLVA typing) and  
comparisons between isolates from Denmark and Norway are pending.

The cases were generally able to recall in detail the type of product  
they had consumed and in which shop they had bought it; 6 of the 10  
cases associated with the outbreak reported buying sugar peas in  
supermarkets sharing in part the same distribution systems. Trace-back  
investigation of the sugar peas showed that they had been bought from  
a single wholesaler in the Netherlands and that they were of 3  
different varieties, which can be distinguished by their shapes,  
namely sugar snaps, sugar peas (snow peas), and mange touts. They  
originated predominantly from Kenya (from 4 different farms), but  
other batches sold in the same period came from Ethiopia and from  
Guatemala. The Dutch whole-seller was different from the one that  
supplied sugar peas to Norway. The 2 remaining cases may have bought  
their sugar peas in another group of supermarket chains, which in part  
shares distribution systems with the supermarkets that sold the  
incriminated sugar peas in Norway. Further investigation into the  
origin of the sugar peas sold in this chain during April 2009 is still  
ongoing. There were no remains of the batch of sugar peas under  
suspicion and therefore microbiological analysis was not performed.  
Laboratory results from samples taken from later batches in 2 of the  
supermarket chains did not reveal contamination by either _Shigella_  
spp. or _Escherichia coli_ (as indicator for fecal contamination).

Discussion
----------
The investigation points at sugar peas as the source of this outbreak.  
The Danish and the Norwegian outbreaks do not appear to have been  
caused by the same type of peas, the batch of sugar snaps that was  
likely contaminated in Denmark was different from the one imported  
into Norway and also the Danish outbreak occurred one month earlier  
that the Norwegian outbreak. It is possible, though, that both  
outbreaks may have been a result of the same contamination event in  
Kenya; further investigations may cast light on this.

Outbreaks with a high ratio of females among cases may often point to  
fresh produce as the source. Only one previous outbreak in Denmark has  
been associated with sugar peas, an outbreak of _Shigella flexneri_ in  
2002 in which the epidemiological evidence pointed towards fresh  
imported sugar snaps of African origin (unpublished). Other fresh  
tropical vegetables which were eaten raw, have also caused outbreaks  
of shigellosis in Denmark, most notable were 2 _Shigella sonnei_  
outbreaks in 2007 (2,3) and one in 1998 (4) both caused by baby corn  
imported from Thailand.

This outbreak underlines that some fresh vegetables imported into  
Europe from tropic destinations may pose a food safety hazard. In  
Denmark fresh imported sugar snaps are sold as a ready-to-eat product.  
Consumers should be aware that these types of products may pose a risk  
of microbiological contamination. The sugar snaps will remain crispy  
after being blanched or boiled briefly and it may be advisable for  
consumers to heat-treat fresh vegetables of this type before  
consumption.

References
----------
1. Ethelberg S, Wingstrand A, Jensen T, et al: Large outbreaks of  
_Salmonella_ Typhimurium infection in Denmark in 2008. Euro Surveill.  
2008; 13(44): pii=19023. Available from
<http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=19023>.
2. Lewis HC, Ethelberg S, Olsen KE, et al: Outbreaks of _Shigella  
sonnei_ infections in Denmark and Australia linked to consumption of  
imported raw baby corn. Epidemiol Infect 2009; 137(3): 326-34  
[abstract available at
<http://www.ncbi.nlm.nih.gov/pubmed/19134229>].
3. Lewis HC, Kirk M, Ethelberg S, et al: Outbreaks of shigellosis in  
Denmark and Australia associated with imported baby corn, August 2007  
- final summary. Euro Surveill. 2007; 12(40): pii=3279. Available from
<http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=3279>.
4. Molbak K, Neimann J: Outbreak in Denmark of _Shigella sonnei_  
infection related to uncooked 'baby maize' imported from Thailand.  
Euro Surveill. 1998; 2(33): pii=1171. Available from
<http://www.eurosurveillance.org/ViewArticle.aspx?ArticleId=1171>.

--
Communicated by:
ProMED-mail
<promed@promedmail.org>

[The HealthMap/ProMED-mail map of Denmark is available at
<http://healthmap.org/r/00ux>. - Sr.Tech.Ed.MJ]

[An excellent example of how rapidly an outbreak can be worked up.

The following is abstracted from the US FDA (Food & Drug  
Administration) Center for Food Safety and Applied Nutrition, Bad Bug  
Book (<http://www.foodsafety.gov/~mow/chap19.html>):

"The illness caused by shigellosis accounts for less than 10 percent  
of the reported outbreaks of foodborne illness in this country.  
_Shigella_ rarely occurs in animals; principally it is a disease of  
humans except for other primates such as monkeys and chimpanzees. The  
organism is frequently found in water polluted with human feces. The  
infective dose is as few as 10 cells depending on age and condition of  
host. The _Shigella_ spp. are highly infectious agents that are  
transmitted by the fecal-oral route.

Associated foods include salads (potato, tuna, shrimp, macaroni, and  
chicken), raw vegetables, milk and dairy products, and poultry.  
Contamination of these foods is usually through the fecal-oral route.  
Fecally contaminated water and unsanitary handling by food handlers  
are the most common causes of contamination."

Clearly unlike foodborne infections in humans due to _Salmonella_  
(except for typhoid fever), _E. coli_ O157, and _Campylobacter_,  
shigellosis is associated with food contamination with human, not  
animal feces. - Mod.LL]

[see also:
2008
----
Shigellosis - Sweden: intentional exposure susp. 20080927.3059
2007
----
Shigellosis, baby corn - Denmark, Australia ex Thailand 20071004.3290
Shigellosis, Thai baby corn - Australia (QLD, VIC) 20070913.3035
Shigellosis, Thai baby corn - Denmark 20070904.2913
Shigellosis, Mexican baby carrots - Canada: alert, recall 20070822.2741
2005
----
Shigellosis, unpasteurized milk curds, 2004 - Lithuania (Vilnius)  
20051203.3494
1999
----
Shigellosis - Australia (South Australia) 19990101.0004
Foodborne illness, intentional - Romania  19990610.0993
1998
----
Shigellosis, imported food - Denmark 19980813.1604]
........................................ll/mj/jw
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