Salmonella spp. are bacteria that cause salmonellosis, a common form of foodborne illness with major impact on human health and huge financial losses in poultry industry. The incidence of notified cases of salmonellosis has declined from a peak of 24 per 100,000 in 2009 to 20.4 reported cases per 100,000 population in 2013, with S. enteritidis and S. typhimurium being the most commonly reported serovar in EU. Salmonella spp. has been detected in a range of foods, and outbreaks have predominantly been associated with animal products such as eggs, poultry and dairy products, but also with plant origin food such as salad dressing, fruit juice and sesame. At the time of slaughter, Salmonella-infected poultry may have high numbers of organisms in their intestines as well as on the outside of the bird and are therefore an important source of contamination. Nowadays, food safety has become an important concern for the European society and governments; therefore, more strict and harmonized regulations are being implemented throughout the poultry production chain with the aim to guarantee and increase the consumer confidence in foodstuffs of animal origin. Furthermore, increasing antimicrobial resistance in non-typhoid Salmonella species has been a serious problem for public health worldwide.
- antibiotic resistance
Salmonella species classification
The bacteria of the genus
A few serotypes are host specific; i.e.
3. Transmission routes, public health and economic cost associated with
The gastrointestinal tracts of humans and animals are the primary sources of
Transovarian (vertical transmission) or trans-shell (horizontal transmission) occurs in poultry. In the first case, a contamination of the vitelline membrane, albumen and possibly the yolk of eggs occurs. Following this route,
Plant origin material can be contaminated through direct deposition of
Person-to-person transmission of
In the latest EFSA’s report, a total of 82,694 confirmed salmonellosis cases were reported by 27 European Union (EU) member states in 2013, resulting in an EU notification rate of 20.4 cases per 100,000 population .
A decrease of 7.9% in the EU notification rate compared with 2012 was shown in the above report, which supports the declining trend of salmonellosis in the EU/European Economic Area (EEA) in the 5-year period of 2009–2013 (Figure 1). However, the above was not statistically significant when analysed by month. Nine out of 14 EU member states reported a total of 59 fatal cases, which gave an EU case-fatality rate of 0.14% among the 40,976 confirmed cases. Some researchers claim that human salmonellosis represents a considerable economic impact and the estimated costing can be as €3 billion/year . As in previous years,
In a recent report published by USDA in 2015 , a comparison of the economic burden showed that
According to Decision No. 2119/98/EC and 2000/96/EC, surveillance of foodborne salmonellosis in humans is mandatory in the EU member states as well as setting up a network for the epidemiological surveillance and control of communicable diseases in the Community [36, 37]. Data on humans, animals and food are compiled and analysed jointly by the European Food Safety Agency (EFSA) and the European Centre for Disease Prevention and Control (ECDC) and presented annually in the EU Summary Report on trends and sources of zoonoses, zoonotic agents and foodborne outbreaks .
Salmonella spp. in poultry and poultry products
In the primary production, there are numerous activities that influence the introduction, growth or elimination of
The Panel on Biological Hazards  recommended that the application of hazard analysis critical control point (HACCP) principles, including good manufacturing practices and general hygiene procedures are recognized as important measures for
Nowadays, the trend seems to be towards production becoming more integrated, and many small farms will be replaced in the future by fewer, bigger farms, which will allow a greater integration and consequently to a better control of
Sewage and farm effluents, which can contaminate pasture, soil and water with
5. Primary and secondary poultry processing and retail
The most important control measure at primary production, apart from those focusing in the elimination of
To reduce carcass contamination, decontamination measures can be applied. Many countries after the adoption of the ‘Code of hygienic practice recommended for poultry processing’ by the Codex Alimentarius in 1994, adopted their own code of practices for poultry processing. The requirements for cleaning of de-feathering equipment and recommended list of used disinfectants and practices of physical separation of de-feathering from later primary processing steps, requirements for processors to define acceptable levels of visible faecal contamination following evisceration and monitoring requirements for faecal contamination and practices of spaying or rinsing/dipping are included in this code. As far as these decontamination measures is concerned, one should take into consideration that, there are some regional differences, since chemical treatment is not accepted in the EU at the moment, but is widely used in other parts of the world, e.g. in the USA and New Zealand.
Poultry secondary processing includes portioning and processing of carcasses or portions into value-added products. During secondary processing,
In a New Zealand consumer survey, the times and temperatures of purchased poultry products during transportation by consumers were examined . It showed that thawing poultry at room temperature for up to 12 hours was a common practice and that any
The detection of
Furthermore, interventions at the processing stages are assessed using growth models. These take into consideration several factors such as the levels of contamination when carcasses leave the processing plant, storage time in retail stores, transport time, storage times in homes and the temperatures carcasses were exposed to during each of these periods. It should be mentioned that the presence and level of
6. Food of animal and plant origin as a source of
Salmonella serovars for humans
Both plant and animal product-based animal feed ingredients may be contaminated with
In the European Union (EU), contaminated foodstuffs serving as a source of
A long list of foods that have been contaminated by
In foods from vegetable origin, detection of
In 2002, tomatoes, grown and packed in Virginia state (USA), contaminated with
Unpasteurized orange juice was responsible for foodborne salmonellosis in 152 people in six states in the USA between May and July 2005 . From 1995 to 2005, some researchers reviewed fruit juice-associated outbreaks of illness reported to Centres for Disease Control and Prevention (CDC), in Atlanta, USA . Twenty-one juice-associated outbreaks were reported to CDC; 10 implicated apple juice or cider, eight were linked to orange juice and three implicated other types of fruit juice. These outbreaks caused 1366 illnesses, with an average of 21 cases per outbreak (range, 2–398 cases). Five out of 13 outbreaks of known aetiology, were caused by
Human salmonellosis due to
7. Antibiotic resistance in
Salmonella serovars: a serious problem in public health
Since 2003, according to the U.S. Food and Drug Administration, antimicrobial resistance in
Individual organisms may transfer mutations that render antibiotics ineffective, passing on a survival advantage to the mutated strain, resulting in a normal genetic variation in bacterial populations. Advantageous mutations can also be conveyed via plasmid exchange within the bacterial colony, in the presence of antibiotics, resulting in proliferation of the resistance trait in the bacterial populations. Natural selection leads to an inherent consequence of exposure to antibiotic compounds and then antibiotic resistance arises.
On the other hand, the spread of particularly resistant clones and the occurrence of resistance genes within these clones can be exacerbated by the use of antimicrobials in human and animal populations and its selective pressure . Many factors may also influence the spread of resistant clones, such as foreign travel by humans, international food trade, animal movements, farming systems, animal husbandry and the pyramidal structure of some types of animal primary production. During the late 1990s and early 2000s, several clones of multi-drug-resistant (MDR)
2013/652/EU Commission Decision sets an enhanced monitoring of antibiotic resistance (AMR) in bacteria from food and food-producing animals, which has been successfully implemented in all reporting and non-reporting member states. In accordance with the above legislation, the AMR monitoring started in 2014 and collected data referred on food and food-producing animals specifically targeted in different poultry populations and meat derived thereof. Two agents are responsible in performing the analyses of the data: EFSA and ECDC. The results are published in the first EU Summary Report on AMR  derived from 28 member states which reported data on AMR in zoonotic bacteria to the EFSA and 21 member states which submitted data to the ECDC. In the above report, the results showed that high proportions of human
In another study , it was reported that over 80% of strains from both human and animal sources that were tested for their antimicrobial resistance, showed that resistance patterns were similar among strains from humans and animals: the commonest phenotype comprised resistance to ampicillin, sulphonamides, streptomycin, chloramphenicol, and tetracycline and was found in 76% of human and 73% of animal strains. Between 1972 and 1974, almost 50,000
Overall, antimicrobial resistance varies among different serotypes of non-typhoidal
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