What is Salmonella?
Salmonella is a Gram-negative rod-shaped bacterium belonging to a family called the Enterobacteriaceae, but it is not included in the group of bacteria referred to as coliforms. Salmonella is one of the principal causes of foodborne illness worldwide and is also an important pathogen of livestock, causing infections that can be transmitted from animals to humans (zoonotic infections).
Although a great many different strains of Salmonella have been identified, there are actually only two recognised species. These are S. enterica (which includes 6 subspecies) and S. bongori. The subspecies most important in foodborne disease is S. enterica subspecies enterica. Salmonellae are further divided into serotypes (sometimes referred to as serovars), of which there are more than 2,500. Most belong to the species S. enterica including nearly 1,500 contained in S. enterica subspecies enterica. This group includes many that cause foodborne disease, such as the relatively common S. Enteritidis and S. Typhimurium. Each Salmonella serotype can be further divided by phage typing, a classification based on infection of bacterial cells by specific viruses (bacteriophages). A particular phage type can be denoted using the term PT. For example, Salmonella Enteritidis PT4 is an organism commonly associated with eggs and human illness.
What foods can be contaminated?
Food animals can become infected with Salmonella from feed and from the environment, so that many foods of animal origin, such as meat, poultry, eggs and raw milk can become contaminated. Salmonella may also contaminate fresh produce via contact with infected animals or other environmental sources. The pathogen has been isolated from tomatoes, lettuce and salad greens, peppers, sprouting seeds, fruit juice, cantaloupe melons and nuts.
Many studies to determine Salmonella contamination rates in food commodities have been conducted. For example, in 2005 a Europe-wide study found that about one in five large scale commercial egg producing facilities had hens infected with Salmonella. A UK study reported contamination levels in poultry of 5.7 % in 2001, and a 2003 study of UK produced shell eggs found contamination levels of 0.34 %. In the USA, testing during 2003 found that 3.6 % of raw meat and poultry samples were contaminated with Salmonella.
Cooked ready-to-eat foods can become cross contaminated by transfer of bacteria from raw foods, either by direct contact, or via food preparation surfaces and equipment used for both raw and cooked foods. A wide variety of processed foods have been found to be contaminated with Salmonella, including chocolate, breakfast cereal, flavoured potato crisps and snack products, peanut butter, fermented meats, cheeses, milk powder and ice cream.
How does it affect human health?
Some Salmonella serotypes cause specific and often serious clinical disease in one or a few animal species, such as S. Typhi and S. Paratyphi in humans (causing typhoid fever), S. Dublin in cattle, and S. Choleraesuis in pigs. The more common foodborne form of the illness is caused by non-typhoid salmonellae, which invade the cells lining the small intestine. These organisms cause gastroenteritis lasting between 1 – 7 days, with symptoms that include diarrhoea, abdominal pains, nausea, vomiting, and chills, leading to dehydration and headaches. The infection can take between 6 and 48 (usually 12-36) hours to develop and the infective dose is thought to vary widely. Small numbers (between 10 – 100) of cells can cause illness if ingested by the young or the elderly, or if the food consumed has a high fat content (e.g. chocolate, cheese or peanut butter) because the fat is thought to protect the cells from acid in the stomach. But in general it is thought that high numbers (between 105-106 cells) of salmonellae need to be consumed to cause illness.
Vulnerable individuals, such as the young, the elderly and those who are immunocompromised can sometimes develop more severe symptoms from non-typhoid salmonellae, including septicaemia, or chronic conditions, such as reactive arthritis. The death rate for non-typhoid salmonellosis is less than 1%, although this figure is higher amongst some groups, particularly the elderly.
How common is illness?
The incidence of human salmonellosis in Europe has been declining steadily since 1995. In 2008, just over 131,000 cases were reported in 27 countries, though there is likely to be considerable under-reporting. The decline is thought to be mainly due to the success of measures taken to reduce SalmonellaEnteritidis contamination in hens eggs. Similar trends have been observed in other developed countries, including the USA, where there are around 40,000 confirmed cases (with 400 deaths) of non-typhoidal Salmonella illness reported each year.
Foodborne Salmonella outbreaks are commonly associated with inadequately cooked eggs and poultry, or products containing these ingredients, such as egg mayonnaise. However, many other foods have been linked with outbreaks. These include dairy products (such as milk, cheese and ice cream), fruit juice, tomatoes, melons, lettuce and other salad leaves, sprouted seeds, jalapeño peppers, cereals, potato crisps and snack products, coconut, black pepper, chocolate, almonds, products containing sesame seed paste (tahini), peanut butter, herbal infusions, cooked meats, salami and other fermented meats, bottled water and reconstituted dried infant formula. Outbreaks involving processed foods can be very large. For example, an outbreak of S. Enteritidis associated with ice cream that occurred in the USA in 1994 may have affected as many as 224,000 people.
Where does it come from?
Salmonella has evolved to live in the gastrointestinal tracts of animals and so the primary sources of contamination are animals and their faeces. Many different animals can be infected with Salmonella, often without suffering from any obvious symptoms. Birds, rodents, reptiles, frogs, fish and snails can all carry the bacteria. This can result in contamination of soil and surface waters, leading to infection of food animals and contamination of fruits and vegetables, herbs, spices, seeds, nuts and shellfish. Food animals can also become infected via their feed or from other infected animals.
Although some Salmonella serotypes are species specific, many are able to cross between species and cause disease in man. Poultry and pigs are considered to be especially significant reservoirs of Salmonella but many foods of animal origin, such as raw meats and unpasteurised milk, are also important sources.
Salmonella can be shed in the faeces of infected humans for some time after symptoms have subsided and some individuals become chronic carriers. However, foodborne illness caused by an infected food handler is rare and is typically the result of poor personal hygiene.
How is it affected by environmental factors?
Most Salmonella serotypes can grow over the temperature range 7 – 48 ºC, but growth is slow at temperatures below 10 ºC. Reports suggesting that some serotypes can grow at temperatures as low as 4 ºC are not universally accepted. Nevertheless Salmonella is able to survive for extended periods in chilled and frozen foods.
The majority of Salmonella serotypes are not particularly heat resistant and are usually killed by pasteurisation processes. D-values are typically 1 – 10 mins at 60 ºC and less than 1 min at 70 ºC, with typical z-values of 4 – 5 ºC. However, there are some important exceptions. Some rare serotypes such as S. Senftenberg are much more heat resistant (approximately 10 – 20 times) than others at high water activities, and some foods with high fat content or low water activity reduce the effectiveness of heat treatments that would normally destroy the cells.
A few Salmonella serotypes can grow over a range of pH values from 3.7- 9.5 under otherwise ideal conditions, but the optimum is 6.5 – 7.5. Although Salmonella cannot grow under very acid conditions, the cells are able to survive for some time in acid environments.
Salmonellae are not able to grow in dry environments and require water activity values of at least 0.94 to multiply in foods. The cells will die out at lower water activities values, but inactivation can be extremely slow in some products (measured in years), particularly those with very low moisture and high fat content, such as chocolate. Salmonella may also survive for some time on dry food production surfaces.
All salmonellae can grow with or without oxygen (facultative anaerobes) and in atmospheres containing high levels of carbon dioxide (possibly up to 80 % in some conditions).
Salmonella is not especially resistant to sanitisers used in the food industry, but is able to form protective biofilms if cleaning is inadequate.
How can it be controlled?
A HACCP approach is essential for the effective control of Salmonella in food production and it should start on the farm. Many countries have policies that encourage measures to reduce the levels of Salmonella in egg production units, in poultry houses, during the growing of fresh produce and also during transport of raw commodities. Such measures are especially important for products that will not be cooked prior to consumption. Food manufacturers should take care to source their ingredients from producers implementing effective controls, or purchase pasteurized products (such as milk or egg) to reduce the risk of Salmonella contamination.
For food processors
Salmonella can be effectively controlled by relatively mild heat treatments, but it is essential that adequate measures are in place to avoid cross contamination between raw and cooked foods. HACCP should be used to identify and implement adequate controls for Salmonella (ensuring the organism is absent) in all foods that will be supplied to the consumer as ready-to-eat. General good hygiene procedures and effective temperature controls are also very important.
For retailers and consumers
To ensure that ready-to-eat foods remain free from Salmonella, careful handling and storage of product should be encouraged at the retail stage and in the consumer’s home. Avoidance of cross contamination is particularly important in this respect. Careful labeling for raw products is important too, especially when they appear cooked. Raw chicken entrées have caused illness in the USA because they were not clearly labeled as such. Consumers should also be advised to wash fresh produce, such as bagged lettuce, even when it appears ready prepared.
High risk foods include raw or partly cooked egg products, such as home made mayonnaise and ice cream, undercooked meat, unpasteurised dairy products, unpasteurised fruit juices and raw or lightly cooked seed sprouts.
Are there rules and regulations?
There are codes of practice in many countries around the world for the production of various food commodities that include measures to control Salmonella. It is unacceptable for any ready-to-eat product to contain viable salmonellae, but there are regulations in many countries relating to specific products.
European Union regulations cover Salmonella in a wide range of products, including meat, cheese, butter and cream that have not undergone standard pasteurization processes, milk powder, whey powder, some ice cream and egg products, various shell fish products, ready-to-eat sprouted seeds, ready-to-eat fruit and vegetables, unpasteurised fruit and vegetable juices and infant formula. There are also EU requirements for Salmonella testing of cattle, sheep, goats, horses, poultry and pig carcasses.
US food law requires Salmonella to be absent from ready-to-eat food products that are not intended to be heated before being consumed. There are also specific requirements for the labeling of eggs not treated to inactivate the pathogen and for control of Salmonella in foods prepared for vulnerable populations.