SALAD DAYS – an investigation into the microbiological safety of prepared salads

| February 27, 2009

Salad 1 pic

Food poisoning outbreaks caused by fresh produce have been making food safety headlines on a regular basis in recent years, especially in the USA. A series of large, high profile Salmonella and O157 outbreaks linked to salad vegetables have caused untold damage to the fresh produce industry and have left the sector with a reputation for high risk products. But is that reputation really deserved and what can be done to improve food safety in the salad sector? In the first part of this two-part feature, we look at some of the facts and figures and try to put the issue into perspective.

In September 2006 an outbreak of E. coli O157:H7 infection in the USA affected more than 200 people across 26 states. Nearly a third of those affected developed potentially serious complications, such as haemolytic uraemic syndrome (HUS), and at least one person died. The outbreak was investigated by the Centers for Disease Control and Prevention (CDC) in Atlanta and by several state health authorities and it soon became clear that the source of the outbreak was rather unusual. E. coli O157:H7 is usually associated with beef and other meat products, but case-control studies on this occasion pointed clearly to a single brand of fresh bagged baby spinach. Microbiological tests soon confirmed the investigators suspicions, as the outbreak strain was isolated from unopened bags of the implicated spinach. Consequently, consumers were advised not to eat the fresh spinach and the producer recalled all affected product from the marketplace. Subsequent field investigations by the FDA traced the spinach to growers in the Salinas Valley area of California, where the outbreak strain was isolated from water supplies, cattle manure and wild pig faeces in the area.

In many ways this incident illustrates very clearly why it is that fresh produce, and particularly leafy greens and prepared salads, have acquired such a poor safety reputation recently. The outbreak was widespread, serious – indeed fatal in at least one case – received extensive media coverage and was widely perceived as a ‘new’ threat to public health. Suddenly, consumers were being told that a group of food products previously considered both healthy and low-risk might in fact carry a serious danger. Furthermore, there is no obvious way to control the risk and no definitive ‘critical control point’ that could be used to guarantee safety. Meat products can be thoroughly cooked to remove microbial pathogens, but the only option for consumers with a salad vegetable is washing. Unfortunately, the outbreak investigation showed that washing the contaminated spinach made absolutely no difference to the chances of becoming infected. Not surprisingly, US sales of bagged ready-to-eat salads fell in the aftermath of the outbreak and took time to recover. The incident also caused the Canadian government to place restrictions on the import of fresh spinach from the USA and so affected international trade.

The extent of the problem

The outbreak described above, plus many others in North America, Europe and elsewhere have tarnished the safety image of prepared salads. This has coincided with a dramatic rise in demand for these products in response to healthy eating campaigns. The US annual market for prepared salads was estimated at $1.2 billion in 2005 before the spinach outbreak and a conservative estimate of the UK market came in at £256 million for the same year. Salads are big business, but are they also big contributors to foodborne disease as one might imagine from some of the bad press they have received?

Clearly, some reliable facts and figures are needed before that question can be answered and a recent comprehensive review of prepared salad safety by the UK Health Protection Agency provides an excellent starting point. The authors looked at more than 2000 general outbreaks of foodborne disease that were recorded in England and Wales from 1992 to 2006 and found that only 82 (4%) of them were associated with prepared salads. The commonest pathogen involved was Salmonella (48% of outbreaks), followed by noroviruses (43% confirmed and suspected). They also found that these outbreaks tended to be larger than those caused by other food types. This was especially true of outbreaks associated with lettuce, which also tended to be more prolonged. This latter finding raises some interesting questions, to which we will return. The review also points out that most of the outbreaks linked to salads occurred in the foodservice and catering sectors and were associated with infected food handlers, cross contamination and poor storage. Just two outbreaks were associated with salad sold by retailers.

Figures from the USA are more difficult to come by, given the variation in the recording of food poisoning outbreaks by different states. However, analysis of foodborne disease outbreaks in the USA between 1973 and 2005 conducted by CDC shows that “fresh plant produce” was responsible for only 0.7% of outbreaks in the 1970s, but that this had risen to 6% by the 1990s. While some of this increase can be accounted for by increases in consumption, the CDC figures show that, between 1986 and 1995, the number of foodborne disease outbreaks linked specifically to leafy greens rose by 60%, but consumption rose by only 17%. The trend from 1995 to 2005 was similar, pointing to a growing problem with the safety of vegetables like lettuce and spinach.

So what are we to conclude from all this? Perhaps we should not read too much into the figures that are available, but it does seem that in the UK at least, where the data is most complete, prepared salads in general are not a major contributor to foodborne illness and have a relatively good safety record. When one takes the catering sector out of the equation, the situation looks better still. The picture in North America is less clear and the data is less complete. It is difficult to know whether one is comparing like with like, but there is evidence that some types of fresh produce – notably leafy salad greens – are a growing cause of foodborne disease.

Take the fresh produce sector as a whole and the problem seems insignificant, but the data seems to be indicating that one type of product, fresh leafy green salad vegetables, might be punching well above its weight in terms of its food safety risk.

A global perspective

Despite the relatively good food safety record of the bulk of the fresh produce sector, concern over leafy greens is growing at an international level. For example, a joint WHO FAO expert meeting on microbiological hazards associated with fresh produce in October 2007 concluded that leafy green vegetables should be given the highest priority in terms of fresh produce safety. There were a number of reasons for this, but the assembled experts considered that, “from a global perspective,” this group of foods gave rise to the greatest concern because of their potential to cause large and widespread foodborne disease outbreaks and the potential for post-harvest processing to “amplify” contamination. They went on to recommend that WHO and FAO should concentrate their development of scientific advice on this group of products.

Salad 1 pic2

Why were the experts at that meeting so concerned? One of the keys to understanding this the term “global perspective.” A worrying trend that has emerged in recent years is the growing number of international foodborne disease outbreaks that have been linked to green salad vegetables, especially lettuce. A typical example of this type of outbreak was reported in 2000, when at least 140 people in Denmark, Germany, Iceland, the Netherlands and the UK were infected by Salmonella Typhimurium DT204b. The outbreak was associated with iceberg lettuce, but the supply chain was so complex that the origin of the implicated produce was never confirmed. A similar Salmonella Typhimurium DT104 outbreak occurred in the UK the same year and caused 361 cases of illness. Once again the source of the lettuce could not be identified, although it was known to have been imported.

There have also been international outbreaks of E. coli O157 infection associated with lettuce. For example, in 2007 at least 50 people in Iceland and the Netherlands became ill after consuming shredded, pre-packed lettuce from a Dutch processing plant. Other leafy greens too have been involved in outbreaks, such as the 100 cases of Salmonella Thompson infection in Denmark, Norway and Sweden that was eventually linked to rocket lettuce grown in Italy. Fresh herbs have been implicated – a notable example being fresh pre-packed basil grown in Israel that caused at least 50 cases of Salmonella Senftenberg infection in the UK, Denmark, the Netherlands and the USA. This outbreak was only uncovered because a surveillance exercise in the UK found Salmonella Senftenberg in samples of the basil taken from retail outlets and links were then made with reported cases of illness caused by the same strain. In fact, it is quite probable that, until modern genetic typing techniques began to be used widely, some international outbreaks were never recognised as such, but were treated as smaller local events.

These are just a few of many such international outbreaks recorded over the last 15 years or so and they illustrate the problem clearly. The demands of consumers for fresh salad greens all year round mean that lettuce and other vegetables have to be sourced from many different producer countries, creating highly complex supply chains. Produce is often not labelled with details of its point of origin and there may be numerous re-packing operations involved in the supply chain. Produce from a single grower can end up in several countries and can be supplied to many customers. If a contaminating pathogen enters this system it can be spread over a wide geographical area very quickly and can be very difficult to trace even with high levels of international cooperation. In the absence of a foolproof decontamination method, such contaminated foods are a real danger to public health.

A focus of concern

Leafy green salad vegetables seem to be an important and growing source of pathogenic microorganisms in international trade and this is a genuine concern. While fresh produce in general is a relatively small contributor to foodborne disease outbreaks, even in the USA, the disproportionate and increasing number of incidents related to lettuce and some other leafy greens is a different matter. It is this aspect of the produce sector that really needs attention and in part 2 of this feature we look at some of the reasons why lettuce can become contaminated and how the problem might be tackled on an international basis.


Prepared salads and public health
Little, C.L. & Gillespie, I.A.
Journal of Applied Microbiology, 2008, 105, 1729-43

Spinach-associated Escherichia coli O157:H7 outbreak, Utah and New Mexico, 2006
Grant, J. et al
Emerging Infectious Diseases, 2008, 14(10)

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Category: Features

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