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expert reaction to the ability of Salmonella to grow on bagged salad leaves

Researchers publishing in the journal Applied and Environmental Microbiology have reported that leached juices from leafy vegetables enhance growth and harm of the food poisoning bug Salmonella.


Dr Kimon Andreas Karatzas, Assistant Professor in Food Microbiology at the University of Reading, said:

“The study presented in this paper shows how Salmonella can survive and thrive in fresh produce and more specifically in cut salad. It is an important piece of work which explains why fresh produce is responsible for most foodborne illnesses, while more specifically, cut leafy greens are responsible for approximately a fifth of foodborne illnesses over the last decade. We already knew this and it is expected, as these foods are consumed without any processing apart from washing which cannot remove all microorganisms present.

“The interesting element is that chopped fresh produce provides an environment rich in nutrients which can support pathogens such as Salmonella. On the other hand, consumption of fresh produce is important for health too and consumers need to strike a balance between the two. Consumers seem to be more preoccupied with nutritional facts, but they should not forget that foodborne pathogens can be deadly. Avoiding fresh produce is not a solution, but if possible, it would be preferable to buy uncut fresh produce over chopped, and to always wash it before you eat – even the ones that are already washed. Furthermore, keeping these foods in the refrigerator is important.

“Currently, we need better surveillance and further studies to understand how these pathogens survive in different kinds of fresh produce and find methods to eliminate them. Our group is involved in developing disinfectants that can eliminate more efficiently microorganisms from fresh produce with very encouraging results.”


Dr Jeri Barak, Associate Professor of Plant Pathology at the Food Research Institute, University of Wisconsin-Madison, said:

“The most common salad consumed today is ‘ready to eat’ leafy greens sold in a plastic bag. These types of salad are under modified atmosphere packaging within the plastic bag. The specifics vary from one producer to the next but it’s generally agreed that the salad and accompanying microbes are packed in a limited oxygen environment.

“None of the experiments described in the paper mentions using modified atmosphere packaging or a low-oxygen environment. It’s therefore unlikely that the experiments are reflective of the environment experienced by Salmonella before a consumer opens the bag. Also, once the bag is opened, spoilage organisms grow rapidly and consumption of the salad by humans decreases because of rotting appearance of the leaves and unappetizing smells.

“Another point to note concerns experiments that include ‘salad juice’. It’s well understood that salad juice would be a significant addition of carbon and nitrogen (extra food for Salmonella) to the medium giving Salmonella more growth capacity in the one treatment over the other. To determine the role of salad juice, equivalent concentrations of carbon and nitrogen found in the salad juice should be added to the ‘control medium’ or controlled for any additional growth observed due to the differences in the two media.

“It would be fair to conclude that if Salmonella is present in salads, it might grow to infectious doses. The fact that Salmonella can grow in the juices leaking out of cut salad leaves has been known for at least a decade. In addition, it’s well documented that Salmonella would attach to plants, fruit, leaves and roots (sprouts), and could not be washed off. For an immuno-compromised group, consumption of raw produce may be a risk; however, this is not new. Commonly, this population is warned about consumption of certain foods.

“The rest of us should be reassured that contamination levels of raw produce in the supply chain are low with very few bacteria, and the rates of produce that have been found to be contaminated are between 0-3%.

“But consumers should treat bagged salads as temperature-sensitive food products, like milk and ice cream. Temperature adulteration can increase pathogen numbers, such as Salmonella, leading to a more likely outbreak event. Also, salads should be consumed rather shortly after the plastic bag has been initially opened as the protection is lost with packaging opening.

“Consumers are more likely to contract salmonellosis from the consumption of raw produce than meat-based products. Raw produce is grown outdoors and thus exposed to the environment, soil and water, as well as wild animals that may fly, walk, or slither into or through production fields and could carry human pathogens.

“Raw produce is acknowledged by academia and regulators as the most likely source of salmonellosis. In the US, FSMA authorizes the FDA to regulate on farm production practices. This is an important step forward for food safety as the epidemiological data suggests that the point of contamination events of raw produce in on the farm, pre-harvest.”


Prof. Martin Adams, Emeritus Professor of Food Microbiology at the University of Surrey, said:

“Prepared salads are a ready to eat food. Like all foods that are not cooked before consumption the presence of pathogens such as Salmonella would pose a direct risk to the consumer and there have been a number of outbreaks around the world, including the UK, in which prepared salads have been implicated.

“Prepared salads are generally washed in chlorinated water, a process that reduces levels of bacterial contamination substantially but does not guarantee their complete elimination. It is for this reason that reputable supermarkets and food manufacturers take great pains to assure the quality of their sources of supply and that all reasonable steps are taken to minimise the chances of contamination at source and during production. This study addresses the situation when salmonella is already present in the product and would therefore already be a risk to the health of the consumer.

“Much of the paper doesn’t seem very controversial to me.  The fact that growth and other activities of a bacterium are enhanced by the presence of nutrients from a food, in this case the juice from damaged salad leaves, is not very surprising. Much of the work was conducted at an unspecified room temperature rather than at chill temperatures. What did concern me was the report that the particular strain of salmonella used in the work was able to grow at 4oC – refrigeration temperature. The generally accepted view of a number of national and international bodies is that most salmonellas do not grow below about 7oC and several national food safety agencies specify an absolute minimum growth temperature for salmonella of 5.2oC. I think that this particular aspect of the work will need to be confirmed by others.

“If Salmonella did manage to gain access to a prepared salad then the food would obviously be a risk to the health of consumers but if it were able to grow at chill temperatures then that risk would increase over time.

“It is very important that salad vegetables are washed thoroughly before consumption.  This is good advice that goes back many years. Although prepared bagged salads have already been washed, another washing before use would give an added level of reassurance.”


Dr Nicola Holden from The James Hutton Institute said:

“I have some reservations about the study, because the authors show some new data, indicating that Salmonella enterica can grow at 4 degrees centigrade, which goes against the precedent for the minimum growth temperature for this species, which is 5.2 degrees.

“Also, the fact that the researchers see both an increase in biofilm formation coupled with an increase in motility in the presence of extracts from bagged salad goes against what is in the published literature. These two phenotypes are considered mutually exclusive, since they represent different physiological states of the bacterium.

“One of the biggest issues with the work is temperature – many of the experiments were carried out at room temperature and assessed after 24 hours, which is not necessarily relevant to real world situations for how bagged salad is stored and used.

“While disease outbreaks can occur from eating infected vegetables, fresh fruit and vegetables are a vital component of a healthy diet and the health risks from not eating them are larger than the risk of contamination. People should not stop buying bagged salads, but they should store produce properly at the correct temperature and adhere to the use-by dates. When buying fresh produce, don’t let it heat up, e.g. in the back seat of a car, treat it like you’d treat fresh poultry or beef.”


Julie Ashmore, Fellow and Chartered Scientist at the Institute of Food Science & Technology (IFST), said:

“The study shows that under laboratory conditions Salmonella growth may increase and cells may become more mobile when subjected to supplemented levels of juice from leaves. We should not stop eating bagged salad, they are an important part of consumers 5 A Day.

“The conclusions of the study on growth, motility and biofilms do not provide any new information. This study reinforces the importance of consumers following good handling practices when shopping and at home, but the findings are not alarming and should not change customers purchasing choices.

“To stay safe, customers should purchase bagged salad from reputable sources where the bagged salads are refrigerated.  Consumers should shorten the time bagged salads are out of refrigerated temperatures as much as possible, store bagged salads in the fridge at home and make sure their refrigerators are 4°C or colder.

“Manufacturers of bagged salad and other ready to eat food understand the food safety risks associated with their processes and the importance of providing consumers with safe, healthy food. The existing checks are sufficient to protect public health; manufacturers and industry bodies constantly review new research and technology to improve their practices.”


‘Salad Leaf Juices Enhance Salmonella Growth, Colonization of Fresh Produce, and Virulence’ by Giannis Koukkidis et al. published in Applied and Environmental Microbiology on Friday 18 November. 


Declared interests

Julie Ashmore is Manager of PDC & Logistics Food Safety at Walmart Canada

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