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Salmonella Laurie Curtis - November 2007 What is Salmonella? The Salmonellae are gram negative, non-sporeforming rod-shaped bacteria belonging to the family Enterobacteriaceae. However, Salmonella is not included in the group of organisms referred to as coliforms. Salmonella is one of the principal causes of foodborne gastroenteritis worldwide and is also an important pathogen of livestock. Salmonellosis is a zoonotic infection (can be transmitted to humans from animals). Salmonella nomenclature has been revised over the years and is based on biochemical and serological characteristics. Many microbiologists now use a classification that recognises only two species of Salmonella. These are S. enterica (which includes 6 subspecies) and S. bongori. The subspecies most important in foodborne disease is S. enterica subspecies enterica. The genus Salmonella can be further divided into serotypes, of which there are a great many (>2,500). Most serotypes (sometimes referred to as serovars) belong to the species S. enterica and only 20 belong to S. bongori. Salmonella enterica subspecies enterica contains nearly 1,500 serotypes, including many of the serotypes that are known to cause foodborne disease. Under the currently accepted classification, an example of the correct way to denote a serotype would be Salmonella enterica subspecies enterica serotype Enteritidis, although fortunately convention allows this to be abbreviated to Salmonella Enteritidis (S. Enteritidis). In addition, each Salmonella serotype can be divided further by phage typing. 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. Other common serotypes involved in human illness are S. Typhimurium and S. Virchow. Occurrence in foods Food animals can become infected with Salmonella from feed and from the environment, and many foods of animal origin such as meat, poultry, eggs and raw milk can be contaminated with the pathogen. 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, with the lowest levels of infection being found in Sweden and Luxembourg, and the highest levels in Portugal, Poland and the Czech Republic. 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 US, testing during 2003 found that 3.6% of raw meat and poultry samples were contaminated with Salmonella. Fresh produce may also become contaminated with Salmonella from animals and environmental sources. The pathogen has been isolated from tomatoes, lettuce and salad greens, sprouting seeds, fruit juice, cantaloupe melons and nuts. Cooked ready-to-eat foods can become contaminated as the result of cross contamination from raw foods. Although contamination can occur as the result of direct contact, it can also occur via food preparation surfaces or 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, peanut butter, fermented meats, cheeses, milk powder and ice cream Effects on health Some Salmonella serotypes have a limited host spectrum (i.e. they 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. These are not considered further here. The more usual 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. Susceptible individuals, such as the young, the elderly and those who are immunocompromised can sometimes develop more severe symptoms from non-typhoid salmonellae such as septicaemia, or chronic conditions, such as reactive arthritis. The death rate for infection by non-typhoid salmonellosis is <1 % although this figure is higher amongst some groups, particularly the elderly. The incubation time is between 6 and 48 (usually 12-36) hours. The infective dose is thought to vary widely and can depend on the individual consuming the infected food, the type of food involved and possibly the serotype involved. Small numbers (between 10 - 100) of cells can cause illness if consumed 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 the gastric acids. In general however, it is thought that high numbers (between 105-106 cells) of salmonellae need to be consumed to cause illness. Individuals recovering from salmonellosis can continue to shed Salmonella in their stools for some time. Food handlers reporting Salmonella gastroenteritis should be excluded from work until shedding has stopped. Incidence and outbreaks The incidence of human salmonellosis in Europe has been declining steadily since 1995. In 2005, just over 181,000 cases were reported in 27 countries, but this is likely to represent considerable under-reporting. The decline is thought to be mainly due to the success of measures taken to reduce Salmonella Enteritidis contamination in hen's eggs. Similar trends have been observed in other developed countries, including the USA, where the incidence of salmonellosis fell sharply between 1996 and 2001, but has since remained at approximately 15 cases per 100,000 of the population. Foodborne Salmonella outbreaks are commonly associated with inadequately cooked eggs and poultry, or products containing these ingredients, such as egg mayonnaise. However, many other food types 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, cereals, potato crisps, coconut, black pepper, chocolate, almonds, products containing sesame seed paste (tahini), peanut butter, herbal infusions, cooked meats, fermented meats such as salami, 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. Sources Salmonella can be shed in the faeces of infected humans. Shedding can occur 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 the result of poor personal hygiene. Many Salmonella infections in animals are asymptomatic, and many animals such as birds, rodents, reptiles, frogs, fish and snails can be infected with Salmonella. This can result in contamination of the soil and surface waters, leading to the infection of food animals and contamination of fruits and vegetables, herbs, spices, seeds, nuts and shellfish. In addition food animals can also become infected via their feed or from other infected food animals. Although some Salmonella serotypes are species specific, many are able to cross between species and cause disease in man (zoonoses). Both poultry and pigs are considered to be significant reservoirs of Salmonella but many foods of animal origin, such as raw meats and unpasteurised milk are also important sources of the pathogen. Growth and survival in foods Most Salmonella serotypes can grow over the temperature range 7–48°C, although growth is reduced at temperatures below 10°C. Reports in the literature suggest that some serotypes can grow at temperatures as low as 4°C, but this is not universally accepted. Although most Salmonella serotypes are unable to grow at refrigeration temperatures, the organism is able to survive for extended periods at chill temperatures, particularly under freezing conditions. 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. Other factors such as temperature, the type of acid present and the presence of antimicrobials can affect the minimum pH for growth. Although Salmonella cannot grow under very acid conditions, the organism is able to survive for some time in acid environments. Survival times are dependent on type of acid present and temperature (chilled temperatures favour survival). Salmonellae are able to grow at water activities down to 0.94 (and possibly 0.93), lower values are dependent on serotype, food sources, temperature and pH. Salmonella will die out at water activities below that permitting growth, 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 is relatively resistant to drying and can survive on food production surfaces for some time. Salmonellae are facultative anaerobes (can grow with or without oxygen) and growth is only slightly reduced under nitrogen. The organism is able to grow 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 biofilms that may reduce the efficacy of a sanitizer if cleaning is inadequate. Thermal resistance The majority of Salmonella serotypes are not particularly heat resistant and are usually inactivated by pasteurisation or equivalent heat processes. D-values are typically between 1-10 mins at 60°C and <1 min at 70°C, with typical z-values of 4-5°C. However, there are some important exceptions. Some rare serotypes such as S. Senftenberg are much more heat resistant (approximately 10 - 20 times) than other Salmonella serotypes at high water activities, and some foods such as those with high fat content or with low water activities reduce the effectiveness of heat treatments normally expected to inactivate the organism. Control options A HACCP approach is essential for the effective control of Salmonella in food production. Processing The control of Salmonella in food should start on the farm with the careful production of animal-derived raw materials, such as eggs, poultry, pork and fresh produce. 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 receive a heat treatment prior to consumption. Food manufacturers should carefully source their ingredients and supplies from producers implementing such measures, or purchase pasteurized products (such as milk or egg) to reduce the risk of Salmonella entering their facilities or reaching the consumer. Salmonella can be effectively controlled by relatively mild heat processing (e.g. milk pasteurization), but it is essential that adequate measures are in place to avoid cross contamination between raw and cooked product. 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 (or drink). The HACCP plan should be rigorously reviewed when product is reformulated as such exercises can affect the efficacy of heat treatments, or the use of acid or solute as a control for Salmonella. General good hygiene procedures and effective temperature controls are also very important. Product use 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. In the UK consumers and caterers are encouraged to refrigerate eggs once purchased and to adhere to the 'use by date' stamped on the egg, which should mean it is consumed within 3 weeks of date of laying. Careful labeling and cooking instructions for raw product is very important, especially when it may appear cooked. Raw chicken entrée products have caused illnesses in the US because they were not clearly labeled and appeared ready-to-eat. Consumers should also be advised to wash fresh produce, such as bagged lettuce, even when it appears ready prepared. Consumers should be advised of 'high risk' foods. These include raw or partly cooked egg products, such as homemade mayonnaise and ice cream, undercooked meat and meat products, unpasteurised dairy products, unpasteurised fruit juices and raw or lightly cooked seed sprouts. Legislation There are codes of practice in many countries around the world for the production of various food commodities that include measures to control Salmonella. Although it is unacceptable for any ready-to-eat product to contain viable Salmonellae, there are regulations in many countries enforcing requirements in specified products. European Union regulations have specific requirements pertaining to Salmonella in a wide range of products, including meat and meat products, 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-toeat sprouted seeds, ready-to-eat fruit and vegetables, unpasteurised fruit and vegetable juices and infant formula and dried dietary foods. Sampling plans and absence requirements vary depending on product. There are also EU requirements for Salmonella testing of cattle, sheep, goats, horses, poultry and pig carcasses. US food law also 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. Some countries have specific storage, labeling requirements and heat treatments for foods that are aimed at controlling foodborne salmonellosis. In the US these include mandatory refrigerated storage of eggs (from farm to the consumer) and labeling requirements for the inside of egg boxes advising of safe egg handling practices. In the EU, legislation requires many eggs to be stamped with a distinguishing mark and country of origin to help trace the farm of origin in case of an outbreak.