Salmonella is the second most common diarrheal pathogen in Austria and is mainly transmitted through food. Infection occurs through ingestion of food containing salmonella, primarily eggs and egg products, poultry, meat and dairy products, and ice cream (however, there is hardly any food in which salmonella has not been detected). Illness usually only occurs when relatively large amounts of bacteria (more than 100,000 germs) are ingested. This number of germs, known as the infectious dose, is easily reached if food is not stored properly, since Salmonella can multiply explosively in food at room temperature within a few hours (doubling the number of germs every 20 minutes). However, the infection dose may be significantly lower in infants, the elderly, persons with a compromised immune system or also in connection with fatty foods (e.g. chocolate).
Salmonellosis is a diarrheal disease (including vomiting and abdominal cramps) that is common worldwide and is caused by infection with bacteria of the genus Salmonella(S.). Throughout Europe, the two serovars S. Enteritidis and S. Typhimurium are the main causative agents of foodborne salmonellosis in humans. The pathogens of typhoid and paratyphoid fever(S. Typhi and S. Paratyphi) are to be distinguished from them: These do not occur in Austria, but only in tropical and subtropical countries with low hygiene standards; they cause systemic diseases with intestinal involvement.
The transmission routes of Salmonella are very diverse. Farm animals can become infected via Salmonella-contaminated feed. In chickens, Salmonella colonization often remains hidden because the animals do not become ill from it. Occasionally, entire flocks of laying hens become unrecognized permanent excretors. Transfer of the germs to the still unlaid egg in the hen leads to eggs containing Salmonella. If these are not sufficiently heated before consumption, they can pose a health risk to humans.
Salmonella generally grows in a temperature range of 10 to 47 °C and is not killed by freezing. Heating to above 70 °C for at least 15 seconds is considered to kill germs. However, since this temperature must be reached throughout the food during cooking, a cooking time of ten minutes above 70 °C should be observed.
Salmonella is mainly transmitted by eating raw or insufficiently heated food of animal origin (eggs, poultry meat, meat from other animal species and raw milk). Home-made products containing raw eggs, such as tiramisu, mayonnaise, creams and ice cream, may also be contaminated with Salmonella.
Unheated or insufficiently heated meat (such as poultry meat, kebabs, minced meat, raw sausages) can pose a risk during processing if they come into contact with products that are no longer heated (e.g. potato salad). This transmission to other foodstuffs (cross-contamination) can also occur through insufficiently cleaned utensils, such as cutting boards, knives and towels or failure to wash hands. In addition to kitchen hygiene, great attention must be paid to the continuous refrigeration of raw products during food preparation.
A small proportion of salmonelloses occur through smear infections, an unintentional ingestion of Salmonella through contact with infected humans and animals or with objects contaminated with faeces. Exotic small animals (mainly turtles and iguanas) can also be considered as reservoirs for such smear infections. Thorough cleaning of the hands with soap and warm water is recommended after each animal contact.
Symptoms of the disease may include nausea, diarrhea, fever, vomiting, circulatory problems and abdominal cramps. The symptoms usually last only a few days. The course of the disease is often mild or asymptomatic, depending on the number of germs ingested and the immune status of the affected person. In elderly persons, salmonellosis can quickly lead to a life-threatening condition due to the high fluid loss and the associated circulatory stress.
Patients with gastrointestinal complaints without other risk factors should only be treated with antibiotics in special cases, as this can prolong bacterial excretion and develop resistance to antibiotics. In most cases, a therapy that balances the water and electrolyte balance is sufficient.
Food, especially meat, poultry, eggs or pasta with cream filling, should be well boiled and not kept at room temperature for several hours when cooked. After handling raw poultry meat, thorough hand washing is essential before starting other kitchen tasks. Defrosting water from frozen meat should be emptied into the sink and then rinsed hot. All work surfaces and utensils that have been in contact with raw poultry meat, other raw meat or raw eggs should be cleaned with detergent and hot water. Allow freshly prepared food to cool and then store in the refrigerator unless it is to be eaten immediately.
People with salmonellosis must not handle food professionally during the period of illness.
In 2021, 996 laboratory-confirmed cases of disease were reported to the epidemiological reporting system (EMS) (EMS, as of Jan. 25, 2022), corresponding to an incidence of 11.2 cases per 100,000 population:in. Thus, salmonella again represented - behind Campylobacter - the second most frequently reported cause of bacterial food poisoning in Austria.
From 2002 to 2016, the number of salmonelloses decreased by 83% (2002: 8,405 initial isolates; 2002 Salmonella Central Annual Report). This decrease in human salmonelloses was almost entirely due to a decrease in S. Enteritidis infections(2002: 7,459 isolates; 2016: 671 isolates). The increase in salmonelloses in 2019 compared with 2018 can be attributed to an Austria-wide outbreak caused by S. Enteritidis. The infections occurred mainly in Asian restaurants through the use of eggs containing Salmonella. In 2020 and 2021, due to the SARS-CoV-2 pandemic and associated measures, there was a massive decrease in the number of stool sample submissions and resulting isolation of Salmonella.
The spectrum of the most common Salmonella serovars in human cases of illness has changed slightly in recent years. S. Infantis, which is the most common serovar in broiler chickens, and the monophasic variant of S. Typhimurium (probable reservoir: swine) and S . Coeln are becoming increasingly important, along with S . Enteritidis and S. Typhimurium.
Foodborne disease outbreaks
Nine foodborne illness outbreaks (LMbKA) caused by salmonella were reported in Austria in 2021 (as of March 01, 2022). 61 persons were affected, 20 had to be treated in hospital. There were no fatalities. In each of seven outbreaks, only persons in one household were affected. One outbreak was part of an international outbreak with about 350 cases of illness caused by S. Braenderup. The outbreak was caused by imported Galia melons. In Austria, 11 persons were affected, seven of whom had to be hospitalized.
The monophasic variant of S. Typhimurium caused the largest LMbKA in 2021: 31 persons became ill, 10 of whom had to be hospitalized. In the majority of the affected persons, a link could be established to a restaurant in eastern Styria, where the salmonella strain could be isolated from various dishes offered and from animals of the petting zoo or from their enclosure.
In 2021, more than 5,700 food samples were tested for Salmonella, mainly meat and meat preparations (about 1,300 samples), ready-to-eat foods (about 1,700 samples), ice cream (about 650 samples), fruits and vegetables (about 200 samples), milk and dairy products (about 1,000 samples), fish and fish products (about 70 samples), eggs (about 200 samples), baby food (about 120 samples), bakery products (about 250 samples), and spices (about 100 samples). Salmonella was detected predominantly in meat and meat preparations from poultry (62 Salmonella isolates), including S. Enteritidis 2 times and S. Typhimurium 2 times. S. Infantis was isolated most frequently (50 times), including 18 times from fresh chicken meat.
Because of Salmonella, eight samples were harmful (three game products, three ready-to-eat foods, one each of ice cream and a spice mixture). 27 samples of raw poultry meat or raw poultry meat preparation were judged unfit for human consumption because of Salmonella detections.
In addition to the audit and plan samples, 1,029 carcasses of broiler chickens were tested for Salmonella as part of the process hygiene inspections at slaughterhouses (in-house inspections). Salmonella was detected on 147 carcasses (120 times S. Infantis, 16 times S. Paratyphi B, 10 times S. Kentucky, once Salmonella group C1). S. Coeln was identified on five of 135 turkey carcasses examined.
For humans, animal foods are the most important source of Salmonella infection. In order to determine the importance of different animal populations as reservoirs of Salmonella, uniform EU-wide baseline studies have been carried out in various farm animal species in recent years. These studies proved for Austria that poultry (laying hens, broilers and fattening turkeys) play the most important role for Salmonella illnesses in humans and that all other tested animal species (except reptiles) are only rarely carriers of Salmonella.
Based on these studies, the EU has set maximum levels per year at which flocks of poultry may be contaminated with the serovars S. Enteritidis and S. Typhimurium, including its monophasic variant, which are most important in human medicine: This is 2% for laying hens, 1% for broilers and turkeys, and 1% for parent stock of chickens (in addition to S. Enteritidis and S. Typhimurium, S. Infantis, S. Virchow, and S. Hadar also fall within the target here). In 2021, the specified targets were achieved in all other directions of poultry use in Austria, with the exception of parent stock of chickens (target serovars detected in two flocks).
S. Infantis represents an increasingly frequently detected serovar: since 2016 as the third most important serovar in human diseases, in 2021 as the fourth most important serovar and as the most frequent serovar in poultry meat and broiler flocks. This S. Infantis is mostly a multidrug-resistant variant that shows resistance to the three classes of antibiotics: quinolones, sulfonamides, and tetracyclines.
The Salmonella control program in the EU requires that the most significant Salmonella serovars for humans be controlled in animal populations. Since S. Infantis is not included among the serovars to be controlled in broiler chickens, no financial support is provided for control procedures, such as possible vaccination or culling of flocks, across the EU. Although all flocks are tested for salmonella before slaughter, if serovars other than the target serovars are detected, there are no legal consequences. However, more and more slaughterhouse operators refuse to slaughter Salmonella-positive herds at all. As a result, broiler herds are not slaughtered but culled. This S. Infantis strain has become established in domestic broiler flocks and is very difficult to eliminate from the houses despite thorough cleaning and disinfection measures.
In turkeys, the prevalence of Salmonella spp. has been reduced from over 10% to 3% since the control program began in 2010.
Feedstuffs are subject to a permanent monitoring program in Austria. In the course of official controls, samples are taken both on farms and in warehouses, compound feed plants, and commercial operations. Both finished feed mixtures and individual components are officially examined. In 2021, Salmonella was detected in three of 299 farm animal feed samples tested (1%) (once each for S. Havana, S. Mbandaka, and S. Senftenberg). Protein-rich extraction meals or cakes (by-products from the edible oil processing industry) are considered the most significant source of Salmonella. Through these, Salmonella can be introduced into the feed chain and contaminate the compound feed produced from them. In 2021, 43 pet food and dog chew samples were officially tested. Seven serovars were detected in five of them (12%), two different serovars in each of two samples, and only one serovar in each of the others. Handling pet food, especially chew toys, poses a demonstrable risk to humans. Hands should therefore be washed after feeding and after playing with dogs or cats.
If Salmonella are isolated from human medical or animal test material or from foodstuffs, laboratories in Austria are obliged to send these isolates to the National Reference Center for Salmonella (NRZ S) in accordance with the Epidemic Act, the Poultry Hygiene Ordinance and the Food Safety and Consumer Protection Act. There, typing of the isolates is performed to elucidate possible links between the occurrence of the pathogens along the food chain.
In 2021, 1,048 initial human isolates were typed at the National Reference Center for Salmonella. The discrepancy in the number of reported cases to first isolates is due in part to the reference center's practice of counting multiple infections separately (e.g., detection of S. Enteritidis and S. Typhimurium in one submission are counted as two events/first isolates). In addition, isolates from persons infected with Salmonella but not ill, as well as from persons who did not become infected with Salmonella via food but, for example, through contact with reptiles, are also recorded.
The pathogen is usually detected by culturing from stool (feces), possibly also from blood or pus. Examination of blood for specific antibodies is not conclusive.
The National Reference Center for Salmonella at the AGES in Graz performs serotyping according to the White-Kauffmann-Le Minor scheme for all human and non-human salmonellae detected in Austria. In addition, the most important serotypes for human medicine, S. Enteritidis and S. Typhimurium, are further differentiated using MLVA (Multi Locus Variable Number Tandem Repeats Analysis). For isolates suspected of being part of a (food-borne) outbreak, typing by means of sequencing (NGS, next generation sequencing) is performed.
Salmonella can occur in a wide variety of foods, especially animal foods. The assessment of the detection of Salmonella in food depends on the type of food (ready-to-eat; raw; not ready-to-eat) and partly on the serovar detected.
Detection of Salmonella in ready-to-eat food will inevitably lead to a complaint as being harmful to health. Salmonella must not be detectable in minced meat, raw meat preparations (seasoned meat), meat products intended for consumption in the raw state and some other foodstuffs listed in the food safety criteria of Regulation (EC) 2073/2005, otherwise this will lead to a complaint as unsuitable for consumption.
In raw poultry meat, the detection of S. Enteritidis or S. Typhimurium leads to a rejection as unfit for human consumption. In the case of detection of other serovars, no objection will be raised if an appropriate hygiene instruction (COOL - CLEAN WORK - HEAT THROUGH) is present on the packaging.
Salmonella infections can be detected in almost all animal species. Reptiles are particularly affected by latent infections with a broad spectrum of serovars. Salmonellosis in cattle: S. Dublin is adapted to cattle, but other serovars can also cause general infections with severe clinical pictures. Calves from the 2nd week of life are most susceptible. The predominant symptoms are diarrhoea, disturbances of the general condition or pneumonia, which become milder with increasing age. In cows, however, severe diseases with diarrhoea, milk loss and abortions may occur. Salmonellosis in pigs: Adapted species are S. Choleraesuis and S. Typhisuis. Non-adapted serovars cause disease much less frequently, especially with diarrhea. Affected are weanling pigs and young pigs up to 60 kg, the infection usually progresses as a febrile general disease with pulmonary symptoms, more rarely with diarrhoea. Abortions are possible in sows. Salmonellosis in sheep: S. Abortusovis is strictly adapted to sheep and is one of the most important abortive pathogens. Oral or mating infection is followed by a general septicaemic infection. Typical symptom is lambing in the 4th or 5th month of gestation, besides puerperal complications and general diseases of all ages. Non-adapted serovars cause latent infections and diarrhea as well as abortions in sheep. Salmonelloses in horses: S. abortusequi is the adapted type; after oral infection or infection via the mating act, a general infection develops that can lead to foaling in the 4th month of gestation. Life-weak foals are also possible. Mares develop resilient immunity after abortion. Unadapted serovars can lead to asymptomatic disease with shedding of pathogen or mild to severe disease up to septicemia. Salmonellosis in dogs and cats: These species have a higher resistance to Salmonella, there are no adapted serovars. Most often latent infections are observed, under the influence of favoring factors, diarrhea, vomiting and fever may also develop. Salmonellosis in chickens: S. Gallinarum is adapted to chickens, but can also occur in turkeys and some other bird species. Mammals are not susceptible. This serovar occurs in 2 biovars: Biovar Pullorum is responsible for white chick dysentery or pullorum disease and causes acute septicemic infections in chicks up to 3 to 6 weeks of age. Biovar gallinarum is the causative agent of so-called chicken typhus, which occurs primarily in older chickens. Infections with non-adapted types usually do not cause disease in the chicken, but latent infections. However, these are an important source of foodborne infections and therefore receive considerable attention. The most important serovar in this context in Austria is S. Enteritidis, followed by S. Typhimurium. Salmonellosis in waterfowl: has received increased attention as a potential source of infection for humans long before chickens, therefore special rules for the consumption of duck eggs have been in place for a long time. Living in standing water, these animals have increased infection pressure. Diseases with diarrhoea and septicaemia occur mainly in young animals (keel disease: back swimming of diseased animals).
Salmonella in dust: Protein-containing straight feedstuffs such as soybean, rapeseed or sunflower extraction meal are considered a significant source of contamination for compound feed and compound feed operations. In this context, Salmonella is present in feeds in uneven distribution and often in very low concentrations. These factors make sampling and analytical detection of positive batches difficult.
However, even if feedstuffs contain very few Salmonella, optimal multiplication conditions, for example in the poultry intestine, can infect the entire livestock within a few days without clinical symptoms appearing in the animals. The infection of a flock is then only manifested by positive boot swab samples.
For routine controls in a compound feed mill, dust samples from the process environment are particularly suitable in addition to the regular incoming inspection of feed materials. Due to their large surface area, dust particles are an ideal medium for pathogens, thus even low levels of Salmonella contamination can be found. Dust, which is drawn along the entire production chain of a feed, is thus a very sensitive matrix for the detection of Salmonella and reflects, as it were, the hygiene status of a compound feed plant.
Decontamination with organic acids: Salmonella in feed can cause enormous economic damage in the affected compound feed plants and farms, and affected feed is therefore not marketable. As a matter of principle, the greatest possible hygiene must be ensured in all work steps at the compound feed plant and, accordingly, the avoidance of contamination or recontamination with Salmonella after thermal treatment of the feed.
Decontamination of Salmonella in feed is permitted by feed law. There are few options available to a compound feed manufacturer for decontamination. With appropriate effort, hygienization of the feed can be achieved primarily by thermal processes. If heat treatment is not possible or not desirable (e.g. in the case of laying meal), the feed can be treated with organic acids.
Hygienization of feed containing Salmonella by means of organic acids is only recommended for the treatment of single feeds due to the high acid additions required. Decontamination of compound feeds is not recommended due to the high acid additions required, for example because of resulting feed refusal or interactions with other feed components.
Recommendations for the control of salmonella in feed production
Dr. Christian Kornschober
- +43 50 555-61201
Mag. Dr. Claudia Schlagenhaufen
- +43 50 555 61310
Last updated: 18.01.2023