Salmonella

Salmonella is the second most common food-borne pathogen causing diarrhoea in Austria. Infection occurs through ingestion of salmonella with food, especially poultry, eggs and egg products, meat and meat products, dairy products and ice cream (however, there is hardly any food in which salmonella has not been detected). Symptoms usually occurs only if relatively large quantities of bacteria (more than 100,000) are ingested. This "starting number" is easily reached if food is stored improperly, as salmonella can multiply exponentially at ambient temperature within a few hours.

Occurrence

Salmonellosis is a common diarrheal disease (including vomiting and abdominal cramps) and is caused by infection with bacteria of the genus Salmonella (S.). Across Europe, the two serovars S. Enteritidis and S. Typhimurium are the main causes of food-borne salmonellosis in humans. The pathogens of typhoid fever and paratyphoid fever (S. Typhi and S. Paratyphi) do not occur in Austria. These serovars can be found in tropical and subtropical countries with low hygiene standards and cause systemic infections with intestinal involvement.

Salmonellosis is spread worldwide and the transmission pathways of Salmonella are very diverse. Livestock can be infected via contaminated feed. In chickens, colonisation with salmonella is often hidden because the animals do not show symptoms. Entire flocks of laying hens can be infected and shed bacteria. Transmission of salmonella to the unlaid egg results in eggs carrying bacteria. If these eggs are not boiled sufficiently before consumption, they can pose a health risk to humans.

Salmonella grow in a temperature range of 10 to 47°C and are not killed by freezing. Heating to over 70°C for at least 15 seconds is considered to kill the bacteria.

Reservoir

Pets and livestock (especially poultry), wild animals (birds) and exotic reptiles

Mode of transmission

Salmonella are transmitted mainly by consumption of 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, can also be contaminated with salmonella.

During food prearation, unheated or insufficiently heated meat (e.g. poultry meat, kebabs, minced meat, raw sausages) may be a risk if they come into contact with products that are not heated (e.g. potato salad). This transfer of bacteria to other food (cross-contamination) can also occur through not sufficiently cleaned utensils such as chopping boards, knives and towels or unwashed hands. In addition to kitchen hygiene, raw products need to be continuously cooled to prevent bacterial growth.

A small proportion of salmonellosis is caused by smear infections: 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 pathogen reservoirs and a risk for smear infections. It is recommended to clean the hands thoroughly with soap and warm water after each animal contact.

Incubation period

6-72 hours, usually 12-36 hours

Symptoms

Symptoms may include nausea, diarrhoea, fever, vomiting, circulatory problems and abdominal cramps. The symptoms usually last only a few days. Often a mild or asymptomatic course of the disease occurs, which depends, among other things, on the amount of bacteria ingested and the immune status of the person affected. In older people, salmonellosis can quickly lead to a life-threatening condition due to the high fluid loss and the associated circulatory stress.

Treatment

Patients with gastro-intestinal complaints without other risk factors should only be treated with antibiotics in special cases, as this can prolong shedding of bacteria and bacteria may develop resistance to antibiotics. In most cases, balancing the water and electrolyte levels is sufficient.

Preventive measures

Food, especially meat, poultry, eggs or cream-filled pasta, should be stored at cold temperatures and thoroughly cooked before consumtion. After handling raw poultry meat, it is essential to wash your hands thoroughly before starting any other kitchen work. The defrost water of frozen meat should be drained into the sink and the sink should be rinsed with hot water. All work surfaces and equipment that have been in contact with raw poultry meat, other raw meat or raw eggs should be cleaned with detergent and hot water. Freshly prepared food, if not consumed immediately, should be cooled and stored in the refrigerator.

Persons suffering from salmonella must not handle food on a professional basis during the period of illness.

In 2019, 1,865 laboratory-confirmed cases of the disease were registered in the epidemiological notification system (EMS), which corresponds to an incidence of 21 cases per 100,000 inhabitants. Again, salmonella were the second most frequent cause of bacterial food poisoning in Austria - after Campylobacter.

From 2002 to 2016 the cases of salmonellosis decreased by 83% (2002: 8,405 first isolates; annual report of the National Reference Center for Salmonella 2002). This decrease was almost exclusively due to the decrease in S. Enteritidis infections (2002: 7,459 isolates; 2016: 671 isolates). The increase in salmonellosis in 2019 compared to 2018 can explained by an Austria-wide outbreak of S. Enteritidis. The infections occurred mainly in Asian restaurants through eggs containing salmonella.

The spectrum of the most common salmonella serovars in human cases has changed slightly in recent years. S. Infantis, which is the most common serovar in broilers, and the monophasic variant of S. Typhimurium (probable reservoir: pig) and S. Coeln are becoming increasingly important alongside S. Enteritidis and S. Typhimurium.

In 2019, 5,712 samples were tested for salmonella within the framework of the revision and sampling plan and in focus actions. Salmonella was found in 69 samples, with S. Infantis being identified most frequently (52 times). Salmonella were detected in 62 of 443 poultry meat samples examined. Poultry meat samples accounted for 7.8% of the total sample material tested for salmonella, but 89.9% of all positive samples belong to this food category.

28% (36 out of 131) of the raw chicken meat samples tested contained salmonella (34 times S. Infantis, and twice S. Enteritidis).
21 out of 150 samples (14%) of fresh poultry meat were tested positive for salmonella, 15 times S. Infantis was found in these samples.
2 out of 20 of samples of chicken meat preparations (both S. Infantis), one out of 65 fresh turkey meat samples (2%), one of four turkey meat preparations and one of three tested fresh geese contained salmonella.
No salmonella were isolated from samples of chicken meat products (n=11), ready-to-eat poultry meat (n=48), ready-to-eat turkey meat and six samples of duck meat.

Salmonella were detected in three out of 1,465 samples of meat and meat products (excluding poultry), in one of 61 tested egg products, in one of 781 samples of fruit, vegetables, and salads, and in two out of 106 examined samples of eggs.

No salmonella were found in any other food samples: 265 samples of cheese (189 of which were made from raw milk), 871 samples of (raw) milk and dairy products, 304 samples of bakery products, 199 samples of fish, fish products and seafood, 79 samples of cereals, 72 samples of food for special dietary purposes, 57 samples of fruit juice, 50 samples of baby food, 26 samples of sweets, one water sample and 915 samples of other foods.

In addition to the revision and planned samples, 5,633 carcasses of pigs, 870 samples of broiler chickens and 130 samples of turkeys were tested within the framework of hygiene controls at slaughterhouses (self monitoring). Salmonella (S. Typhimurium, monophasic variant) were found on five pig carcasses (all sampled at one slaughterhouse on one day). Salmonella were also detected on 217 chicken samples (176 times S. Infantis) and five turkey samples.

For humans, food of animal origin is the most important source of infection with salmonella. To determine the importance of the salmonella reservoir, EU-wide standardised basic research studies have been carried out in various animal populations in recent years. These studies showed that poultry (eggs and poultry meat) plays the most important role in human salmonellosis in Austria. All other tested animal species (except reptiles) are rarely carriers of salmonella.

Based on these studies, the EU has set yearly maximum levels for an exposure of flocks of poultry with S. Enteritidis and S. Typhimurium, including the monophasic variant. These maximum levels are as follows: 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 are also included here). In 2019, none of the maximum levels were exceeded for poultry in Austria.

The frequency of detection is increasing for the serovar S. Infantis: since 2016 it has been the third most important serovar in human diseases and the most frequent serovar in poultry meat and in broilers. This serovar is usually a multidrug-resistant variant that is resistant to the antibiotic classes quinolones, sulfonamides and tetracyclines.

The Salmonella control programme in the EU aims to control the most important human salmonella serovars in animal populations. These currently only include the serovars S. Enteritidis and S. Typhimurium (including monophasic variant) in broilers, turkeys for fattening and laying hens and S. infantis, S. Virchow and S. Hadar in parent stock of chickens. As S. infantis in broilers is not included in the serovars to be controlled, no financial support is foreseen throughout the EU for control methods such as possible vaccination or culling of flocks. 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 slaughterhouses refuse to slaughter salmonella-positive flocks at all. As a consequence, broiler flocks are not slaughtered but culled. This S. Infantis strain is established in the broiler flocks and is very difficult to eliminate from the flocks despite thorough cleaning and disinfection measures.

Feed is subject to a permanent monitoring programme in Austria. During the official controls, samples are taken on farms as well as in warehouses, mixed feed plants and commercial enterprises. Feed mixtures and individual components are tested. In 2019, salmonella were detected in one of 335 analysed samples of feed for farm animals (0.3 %), in a sample of oilseed (S. Senftenberg). Protein-rich extractions (by-products from the oil processing industry) are considered the most important source of salmonella. These products can bring in salmonella into the feed chain and contaminate the compound feed produced from them.

In 2019, 74 samples of pet food and dog chew were tested. In 12 samples (16%) 19 serovars of salmonella were detected. In one sample four different serovars were found, in one three serovars and in two samples two different serovars of salmonelle were detected. Handling of pet food, in particular dog chews, poses a verifiable risk to humans. It is therefore recommended to wash hands after feeding and after playing with dogs or cats.

Diagnostics

The pathogen is usually detected by culture from stool (faeces), but also from blood or pus. Testing for specific antibodies from blood is not conclusive.

The National Reference Centre for Salmonella at AGES in Graz does serotyping according to the White-Kauffmann-Le Minor Scheme for all salmonella detected in human and non-human samples in Austria. In addition, the most important serotypes for human infections S. Enteritidis and S. Typhimurium are differentiated by means of MLVA (Multi Locus Variable Number Tandem Repeats Analysis).

Salmonella infections can be detected in almost all animal species. Reptiles are particularly susceptible to latent infections with a broad spectrum of serovars.

Salmonellosis in cattle: S. Dublin is adapted to cattle, but other serovars can also cause infections with severe clinical pictures. Calves from the 2nd week of life are most susceptible. The predominant symptoms are diarrhoea, disorder of the general condition or pneumonia, which become milder with increasing age. However, cows can suffer from serious illness with diarrhoea, loss of milk and abortions.

Salmonellosis in pigs: adapted species are S. choleraesuis and S. typhisuis. Non-adapted serovars cause disease less frequently, especially when it comes to diarrhoea. Weaning pigs and young pigs up to 60 kg are affected, the infection usually progresses as a general disease with fever and lung symptoms, less frequently with diarrhoea. Abortions are possible.

Salmonellosis in sheep: S. Abortusovis is strictly adapted to sheep and is one of the most important abortion pathogens. An oral infection or an infection via the mating act is followed by a general septicaemia. A typical symptom is abortion in the 4th or 5th month of pregnancy, in addition there are puerperal complications and general diseases of all age groups. Non-adapted serovars cause latent infections and diarrhoea as well as abortions in sheep.

Salmonellosis in horses: S. Abortusequi is the adapted type; after oral infection or infection via mating, a general infection develops which can lead to abortion in the 4th month of pregnancy. Weak foals are also possible. Mares develop a resilient immunity after abortion. Not adapted serovars can lead to asymptomatic diseases with excretion of the pathogen or mild to severe diseases up to septicaemia.

Salmonellosis in dogs and cats: These animal species have a higher resistance to salmonella, there are no adapted serovars. Latent infections are usually observed, and if other favourable factors for diarrhoea are present, vomiting and fever can also develop.

Salmonellosis in chicken: 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 the causative agent for pullorum disease and causes acute septicaemia in chicks up to the 3rd to 6th week of life. The biovar S. Gallinarum is the cause of the so-called fowl typhoid fever, which occurs mainly in older chickens. Infections with non-adapted types usually do not cause disease in chickens, but cause latent infections. However, these are an important source of food-borne infections and get a lot of attention. The most important serovar in this context in Austria is S. Enteritidis, followed by S. Typhimurium.

Salmonellosis in water fowl:  Water fowl are monitored as a potential source of infection for humans longer than chickens, therefore special rules for the consumption of duck eggs have long been in place. Living in stagnant water means that these animals have an increased risk of infection. Disease with diarrhoea and septicaemia are mainly found in young animals (keel disease: backstroke swimming of sick animals).

Control programmes for laying hens, chickens for fattening and turkeys for fattening

In 2018, target serovars were detected in 1,2% of breeding hens (one flock each with S. Enteritidis and S. Infantis), 0,8 %of laying hens (17 flocks with S. Enteritidis and 8 flocks with S. Typhimurium), <0.1% of chickens for fattening (one flock of each with S. Enteritidis and S. Typhimurium) and 0.4% of turkeys for fattening (two flocks with S. Enteritidis). Thus, the EU targets were met in laying hens, broilers and turkeys, but not in breeding hens. Salmonella spp. were isolated from three breeding flocks (1.8%), 40 laying hens (1.4%), 240 broilers (4.6%) and 15 turkeys (3.3%). The success of the control programme is impressively demonstrated by the reduction of flocks tested positive for Salmonella spp. from 10.1% in 2013 to between 3.6% and 2.5% in the years 2014 to 2018. All other poultry populations have shown a tendency to deteriorate in recent years, underlining the need to maintain measures such as vaccination programmes and the application of strict farm hygiene controls: the number of Salmonella-positive flocks has not changed compared to 2017 in populations of parent birds (three flocks). For laying hens, the proportion of flocks in which salmonella were detected increased slightly compared to 2017 (1.15% to 1.4%); however, the proportion of laying hen flocks with target serovars has more than doubled since 2014 from 0.35% to 0.8%. In the population of broilers, the percentage of Salmonella and target serovar positive flocks has increased compared to 2017, with n = 240, the highest number of salmonella positive flocks ever recorded. Since 2011 (2.4% positive flocks), the trend is increasing (2018: 4.6%).

Salmonella in dust

Feed materials containing protein, such as soya, rapeseed or sunflower extraction meal, are considered a significant source of contamination for compound feed and compound feed plants. Salmonella is often found in feed in very low concentrations. However, low germ contents make the analytical detection of positive samples difficult.

Project SINS: Overview of the contamination rate in Austrian animal feed companies (single or compound feed)

Decontamination with organic acids

Salmonella in feed can cause enormous economic damage to the compound feed and agricultural businesses and the products are not marketable. The decontamination of salmonella in feed is permitted under feed law.

DEKONTAM study on optimal decontamination processes

National Reference Centre for Salmonella

Beethovenstraße 6
8010 Graz

Dr. Christian Kornschober
Telephone: +43 50 555-61201
christian.kornschober@ages.at