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 [1].

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:

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 [4]. 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 [5]. 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 [6]. 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 [5]. 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 [7].

Conclusions
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 [8], 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 [9].