Following a sustained increase in the incidence of infections caused by
Salmonella Enteritidis phage types (PT) other than PT4 (S.
Enteritidis non-PT4) in England and Wales since 2000, an outbreak control
team was set up to examine the evidence for the increase, to identify interventions
and to make recommendations .
Based on evidence collected over some time (some of which
can be found here: http://www.hpa.org.uk/infections/topics_az/salmonella/se_update.html),
the team concluded that eggs, imported from Spain and used largely in the
catering industry, were the main cause for the increased numbers of infections.
The following actions were agreed:
- Evidence received by the outbreak control team to be presented
to the European Commission;
- The UK Food Standards Agency to continue formal discussions with
the Spanish food safety authorities about measures to reduce salmonella
contamination in the Spanish egg-laying flock;
- The catering industry and egg importers to be advised of the health
risk associated with Spanish eggs;
- The Health Protection Agency (HPA) to publish the results of microbiological
and epidemiological investigations on its website;
- Continued active surveillance of, and response to, outbreaks of
S. Enteritidis infection in England and Wales to be undertaken.
Communication of risk posed by eggs from Spain
In October 2004, there was a concerted effort by United Kingdom (UK) government
agencies to raise awareness of the salmonella risk from Spanish eggs among
egg importers, caterers and the general public [2,3]. This followed local
initiatives in northwest England, where a particularly high number of outbreaks
of S. Enteritidis PT 14b infection occurred . UK and Spanish
food safety authorities met in October and a meeting with representatives
of the Chinese restaurant industry was held in November 2004. Evidence was
presented to the European Commission Standing Committee on the Food Chain
and Animal Health (SCFCAH) in December 2004 . Representatives from the
UK Health Protection Agency, the UK and Spanish egg industries, and the
UK agriculture ministry met several times after that.
Sourcing of non-UK eggs into the UK
Between July and September 2004, 9415 tonnes of eggs were imported into
the UK, and Spain was the single most common supplier (Figure 1). Between
October and December 2004, 7762 tonnes were sourced from other countries
(an 18% decline), and in the first quarter of 2005, the sourcing of eggs
from outside the UK declined further (6614 tonnes, a 15% decline). During
the same period, imports of eggs from Spain declined by 53% (2847 tonnes
to 1325 tonnes). This decline in Spanish imports continued into the second
quarter of 2005 (1190 tonnes; a 10% decline), although the decline in imports
from other countries was not sustained during this period, with increased
imports from France and the Netherlands.
Figure 1. Sourcing of non-UK eggs in the UK showing the
five most common suppliers. Provisional data for January 2000 to June 2005
by quarter (Source: UK Department for Environment, Food and Rural Affairs)
Low levels of non-phage type 4 Salmonella Enteritidis
in British chicken flocks
Most sampling of chicken flocks in Britain is undertaken for statutory monitoring
or for surveillance so most incidents and isolations reported are not associated
with clinical disease in the flock but with identification of subclinical
carriage of salmonella. In 2004, there were 11 reports of S. Enteritidis
incidents in chickens – 34 fewer than in 2003 . The reported phage
types were PT4 (six incidents), PT6 (two) and one each of PTs 7, 11, and
35. One incident occurred in a broiler flock (PT11), and the rest in layer
flocks. The main phage types in British poultry are PTs 4, 6, and 7, which
is consistent with previous years.
Laboratory reports of human S. Enteritidis infection
Between 1 January and 30 September 2004, 6679 human infections with S. Enteritidis
were reported in England and Wales. In the same period in 2005, 5393 human
infections were confirmed, a 19% decrease in incidence. When cases known
to be associated with foreign travel were excluded (965 and 1038 cases respectively)
the decline was 24%.
Two subtypes of S. Enteritidis, PT14b and PT1 resistant to nalidixic
acid with decreased susceptibility to ciprofloxacin (NxCpL), were commonly
reported as the cause in outbreaks linked to the use of eggs from Spain
. In the first nine months of 2005, the incidence of S. Enteritidis
PT14b declined by 63% compared to the same time period in 2004 (1012 to
372 isolates). When known travel-associated cases were excluded, there was
a 68% decline (Figure 2). The incidence of S. Enteritidis PT 1
NxCpL declined by 30% and 34% (non travel-associated cases, Figure 3) over
the same time period). The slower decline in S. Enteritidis PT1
NxCpL infection is due in part to an outbreak in northeast London in February
2005 with 108 confirmed cases.
Figure 2. Non travel-associated S. Enteritidis
PT 14b human infections confirmed by the LEP from January to June. England
and Wales, 2004 and 2005.
Figure 3. Non travel-associated S. Enteritidis PT 1 NxCpL
human infections confirmed by the LEP from January to June. England &
Wales, 2004 and 2005.
The incidence of two common S. Enteritidis phage types, not associated
with the use of non-UK eggs, has increased in the first nine months of 2005
compared with the same period in 2004. The incidence of S. Enteritidis
PT6 infection has increased by 24% (325 to 402 isolates) while the incidence
of S. Enteritidis PT8 infection has increased by 62% (254 to 412
isolates). When cases associated with foreign travel were excluded the increases
were broadly similar (25%, and 58% for PT6 and PT8 respectively).
General outbreaks of S. Enteritidis infection
Between 1 January and 31 December 2004, the Health Protection Agency Centre
for Infections (CfI) received initial reports of 45 general outbreaks of
S. Enteritidis infection. The most commonly reported subtypes were
PT4 (14), PT14b (14) and PT1 NxCpL (4) and most outbreaks occurred in the
second half of the year. Thirty-four outbreaks were linked to commercial
catering premises, with restaurants most commonly reported (28 outbreaks).
Between 1 January and 30 September 2005, CfI received initial reports on
32 outbreaks. The most commonly reported subtypes were PT4 (12), PT6 (6)
PT25 (3), and PT 21 (3), with a single outbreak each of S. Enteritidis
PT14b and PT1 NxCpL infection reported. Twenty-eight of these outbreaks
were associated with commercial catering premises with 18 reported in restaurants.
Investigations into the outbreaks of S. Enteritidis PT6 infection
in 2005 are reported elsewhere .
Decreased sourcing of eggs from outside the UK since autumn 2004 has been
associated with a substantial decline in the incidence of human S.
Enteritidis infection in England and Wales, especially with certain subtypes.
This suggests that even relatively small reductions in the prevalence of
S. Enteritidis in eggs available directly, or indirectly, to UK
consumers can have a significant effect on human infection. Although the
prevalence of S. Enteritidis in UK eggs is low , no egg can
be guaranteed to be free from salmonella. The current UK Food Standards
Agency (FSA) advice to members of the public preparing food for people who
are particularly vulnerable to salmonella infection (babies and toddlers,
the elderly, pregnant women, and those who are already ill) is to make sure
that eggs are cooked until the egg white and yolk are solid .