Food-Borne Diseases (FDB) include a large number of diseases resulting from the ingestion of food contaminated with microorganism’s toxins or other chemicals. One of the most common FBD is Salmonellosis, a zoonosis caused by Salmonella, considered as one of the four leading causes of zoonotic diseases in the world. The present review aims to collect and update information about Salmonella and its prevalence in food products worldwide based on published research studying this pathogenic organism in addition to a general view of regulations implemented by the World Health Organizations and recommendations guidelines adapted by food industries. After describing Salmonella and its different bacterial, biochemical and environmental characteristics, several research have been analyzed to determine prevalence of Salmonella in different countries to determine the most important sources of contamination of food products. The first source of contamination found is poultry products and raw egg products due to ease of their contamination by Salmonella, while contamination of other food products was variable. Severe effects of Salmonella prove the importance of having regulations to limit the negative consequences of the emergence of Salmonella.
Keywords: Salmonella, Human Salmonellosis, Prevalence, food product
Food-borne diseases (FBD) include a large number of diseases resulting from the ingestion of contaminated food by microorganisms toxins or other chemicals. Moreover, food contamination can occur at any stage, such as production, transportation and at the consumer level.
FBD are a worldwide growing public health problem and according to the WHO’s first global estimates, every year nearly 600 million people, or almost 1 in 10 people worldwide, become ill after consuming contaminated food. Thus, diseases resulting from this consumption are considered one of the top 10 causes of death in the world with more than 422,000 deaths per year, of which 125,000 (30%) are children under 5 years who are more exposed to these types of diseases (WHO, 2015).
One of the most common FBD is Salmonellosis, a zoonosis caused by Salmonella enterobacterium considered as one of the four leading causes of zoonotic enteric diseases in the world with over 57,000 deaths and 153 million cases of gastroenteritis per year (CDC, 2020).
Salmonellosis poses a public health problem in all the regions of the world, in either high- or low-income countries. In France the National Reference Center for Escherichia coli, Shigella and Salmonella (NRC), estimates about 307 cases of salmonellosis per 100,000 inhabitants per year. In Canada, from 2009 to 2013, 6,500 cases of salmonellosis on average were reported (PHAC, 2016), in the countries of the European Union 91,857 cases were reported each year (AFSA, 2019) and 1,35 million infections were reported in the United States (CDC, 2020). However, the risk of these infections in low- and middle-income countries remains more severe, where it is associated with poor hygiene, food preparation and conservation conditions, and a lack of food safety legislation and its enforcement. In Africa, 80.3 million cases of salmonellosis are detected each year (Shannon et al., 2010).
In Morocco, collective food toxi-infections (TIAC) constitute a public health emergency because of the virulence and pathogenicity of the bacteria involved and their morbidity potential if the source of infection is not identified or controlled. The increase in TIACs in recent years is largely due to the emergence of certain bacteria, in particular Salmonella. In 2006, 1664 TIAC cases were recorded, and only 121 were confirmed in laboratories, of which 50.4% (61 cases) were Salmonellosis.
Salmonella belongs to the proteobacteria genus, which contains many pathogenic bacteria. The genus Salmonella is divided into two species: enterica and bongori.
The enterica species are divided into 6 subspecies:
S. enterica I or subspecies enterica.
S. enterica II or subspecies salamae.
S. enterica IIIa or subspecies arizonae.
S. enterica IIIb or subspecies diarizonae.
S. enterica IV or subspecies houtenae.
S. enterica VI or subspecies indica.
In these 2 species, more than 2,500 different serovars have been identified so far.
Salmonella are straight, non-spore-forming, non-capsulated sticks measuring approximately 0.7-1.5 µm in diameter for 2 to 5 µm in length (Percival and Williams, 2014).
They are usually flagellated in a periodical and mobile way, although non-mobile mutants of natural origin are sometimes encountered; S. pullorum and S. gallinarum are typically non-mobile (Gast and Porter, 2019).
Biochemical and cultural characteristics
The main biochemical characteristics of Salmonella are:
• Oxidase negative,
• Catalase positive,
• Urease negative,
• Lack of indole production,
• Glucose fermentation with gas production,
• No production of hydrogen sulfide,
• Nitrate reductase positive,
• Lactose negative,
• Lysine decarboxylase positive,
• Tryptophan deaminase (TDA) negative.
Salmonella multiply between 7°C and 45°C with an optimum at 35°C / 37°C and at pH of 4.1 to 9.0 with an optimum of 7 to 7.5 (ANSES, 2011).
Salmonella are an optional aerobic bacteria, they grow on an ordinary medium and a selective medium.
The diameter of Salmonella’s typical colonies on agar medium are about 2-4 mm, round with smooth edges, slightly raised and shiny.
The separation of Salmonella into serotypes can be based on the structure of their surface:
• The O antigen is the outermost portion of the bacteria’s surface covering, which has a lipopolysaccharide nature and causes the synthesis of agglutinating antibodies.
• The H antigen is a slender threadlike structure that is part of the flagella, with a protein nature, thermolabiles, and produce agglutinating antibodies.
• The Vi antigen, only exists in three serovars: S. Typhi, S. Para C, S. Dublin. Its presence can mask the antigen O, making the strain “O inagglutinable”. This inhibition can be lifted by the 100°C strain warming, with Vi antigen being thermolabile.
The main reservoir of Salmonella spp. consists of the gastrointestinal tract of mammals (pigs, cattle) and birds (domestic poultry) (ANSES, 2011).
The enterica subspecies is suitable for warm-blooded animals (rodents, poultry) and water.
Other subspecies are associated with cold-blooded animals (reptiles, turtles and batrachians).
Salmonella in animal fecal matter can contaminate pastures, soils and water. It can last for weeks in water and months or years in the earth (Gast and Porter, 2019).
Salmonellosis is mainly occurred by the direct ingestion of food from contaminated animals consumed raw or undercooked (meat, eggs, raw egg products). Other foods, such as green vegetables contaminated with manure, which have been involved in the transmission, or indirectly through the ingestion of a safe food contaminated with other food or water. The part of transmission by contaminated food ingestion is estimated at 95% for non-typhoid Salmonella (WHO, 2018).
Contamination also comes from pets, cats, dogs, birds and reptiles, such as turtles.
Human-to-human transmission via fecal-oral transmission is also possible.
Survival outside host
The Serotype Choleraesuis can survive in wet swine feces and in dry swine feces for at least 3 and 13 months respectively (Gray and Fedorka-Cray, 2001).
Serotype Dublin have the ability to survive in feces spread on concrete, rubber and polyester for 6 years (Block, 2001).
Certain serotypes are capable of surviving on fingertips for 80 minutes, depending on the inoculum size (Pether and Gilbert, 1971), which explain the facility of their transfer to food by handling.
Salmonellosis is usually characterized by sudden onset of fever, abdominal pain, diarrhea, nausea and sometimes vomiting (Table 1).
The incubation period is generally from 6 to 48 hours after consumption of the contaminated food, and the disease lasts from 2 to 7 days (WHO, 2018).
Generally, symptoms of salmonellosis are mild and in most cases the recovery doesn’t require any special treatment. Yet, in some cases, such as young children and the elderly, the dehydration associated to the disease can become severe and lead to a life-threatening prognosis.
Once the symptoms are gone, the bacteria can still be present in the feces and the contaminated person can still contagious for several weeks. About 1 percent of infected adults and 5 percent of children younger than five shed Salmonella in their stool for up to one year (Redbook, 2018).
Stool test is the most effective method in cases of gastroenteritis. In newborns, young children, the elderly and immunocompromised, minor Salmonella (non-typhic) are likely to cross the intestinal barrier and cause typhoid septicemic syndrome with positive blood culture.
Salmonella's resistance to antimicrobials and disinfectants has increased considerably over the years, due to their inappropriate usage
Antimicrobial sensitivity: Salmonella are susceptible to chloramphenicol, ciprofloxacin, amoxicillin, co-trimoxazole, trimethoprim-sulfamide, cephalosporins and norfloxacin.
Physical inactivation: Salmonella are sensitive to heat. Cooking for 5 to 6 minutes at 65°C is sufficient to reduce the risk of salmonellosis. The cold blocks the development of Salmonella but does not eliminate them. Salmonella spp. can also be disinfected with ozone (Block , 2001).
Disinfectant sensitivity: The most commonly used disinfectants contain aldehydes as active substance, or a combination of aldehydes and quaternary ammonium compounds.
Chlorine and peroxides are very good disinfectants but they are entirely inactivated by the slightest presence of organic matter and can’t be used for soil or material disinfection due to the corrosive effect (Pierré, 2013).
SALMONELLA IN FOOD
The involved foods are mainly eggs and egg products made from raw or poorly heat treated eggs, dairy products (raw or low heat milk) and meat (cattle, pigs and poultry). However, the cases described in the literature refer to many other foods (plants, shellfish, etc.) (ANSES, 2011) (Table 2).
Poultry represents the first reservoir of Salmonella (Gupta et al., 1999), so multiple studies have analyzed the prevalence of Salmonella in poultry products mainly for the chicken industry; the results have shown different rates of contamination.
For chicken carcasses, contamination rates were 57% in Portugal, 22% in the United Kingdom, 45.9% in Vietnam, 13% in South Africa, 27% in Columbia and 42% in China.
The contamination rates for chicken meat were 16% in Ecuador, 33% in Wales, 31% in Russia and 36% in Spain were registered.
A study in Morocco has shown a large rate of contamination by Salmonella in broiler chicken in Meknes region, Salmonella was isolated from 24% of the farms examined.
Studies on the prevalence of Salmonella in red meat are fewer, yet researches have shown remarkable contamination rates; 21% in the United Kingdom and 24% in Malaysia.
Relative to pork meat, the National Salmonella Reference Center of Pasteur Institute and the The French Agency for Food, Environmental and Occupational Health & Safety (ANSES) are warning about the increase in the contamination in pork meat by Salmonella, and studies confirm the increase in contamination rates in the main pork meat producing countries.
The egg white is a complex biological fluid that plays a major role in the protection of eggs against microorganisms. Its natural components such as ovotransferrin and lysosyme protect against a large panel of bacteria due to their antibacterial effect.
Those proteins could act in synergy with other components of the egg white such as the natural alkaline pH, and the ambient temperature (GUYOT et al., 2013). However, the contamination of the internal contents of chicken eggs may be due to bird ovary infection (Barnhart et al.,1991), whereas shell contamination may be due to excrement, food, insects or material handling, transport or storage.
Raw milk is not frequently contaminated with Salmonella and this contamination is most often due to external factors, the cleanliness of the animal, in particular the udders, the surrounding environment, the milkman, the milk harvesting equipment, and finally the storage and transport equipment.
However, pasteurized milk is usually free of Salmonella because it is removed during pasteurization (Brisabois et al., 1997).
Salmonella may be present in agricultural and domestic waste water, fresh water, including water intended for human consumption and groundwater, and in seawater (ISO 19250:2010).
In the European Union, Regulation (EC) No 2073/2005 on microbiological criteria for foodstuffs, defined in its first chapter Salmonella as a criterion for the safety of foodstuffs which present a non conformity for products placed on the market during their shelf life (Absence in 25 g) on a sampling plan equal to 5.
In 2011, Regulation (EC) No 1086/2011 and amended Regulation (EC) No 2073/2005 consider Salmonella typhimurium and Salmonella enteritidis as other safety criteria for fresh poultry meat in order to reduce the prevalence of these two Salmonella serotypes in broilers in the Union, therefore systematic serotyping of colonies should be carried out when the presence of Salmonella spp. is detected.
In 2020, Salmonella is defined as a safety criterion for a new matrix. The European Commission regulated reptile meat, even though these types of meat are not widely consumed in the Union except for the parts that are edible such as the tail of the crocodile used for its high protein content and low fatty acid.
In the second chapter of the regulation, Salmonella is considered to be a process hygiene criterion for the different types of carcasses. Moreover, in 2011 the level of tolerance of the presence of Salmonella on poultry carcases on a sampling plan of 50 decreased from 7 to 5 samples.
Also, in Morocco, according to the latest decision of the Minister of Agriculture, Maritime Fisheries, Rural Development and Waters and Forestry and the Minister of Health n°293-19, Salmonella is considered as an indicator of the safety of certain food products and as an indicator of hygiene for poultry slaughter processes (Official Bulletin n°6796 of 18/07/2019, page 1686).
FOOD SAFETY GUIDELINES
In raw eggs products
Since eggs can harbour Salmonella on the surface, and the raw eggs products are generally consumed without any further cooking, it is necessary that they are prepared and handled correctly and safely.
According to guidelines, the handling of eggs and raw eggs products can be done by two different methods: acidification or pasteurization.
The acidification of raw eggs products should be at a pH less than 4.2 through the addition of acidic ingredients such as lemon or vinegar, in order to inhibit the growth of pathogenic bacteria, including Salmonella (NSW Food Authority, 2016). The pH must be checked by pH paper or pH meter to make sure it has reached the 4.2 pH limit, then the product must be refrigerated at or below 5°C.
Eggs can be pasteurized in shell using vacuum method, by putting eggs in a water bath at temperature of 57°C for at least 75 minutes (Baldwin, 2010), at this point the pasteurized eggs must be used immediately or cooled in a 50:50 ice-water bath and refrigerated at or below 5°C for 10 days.
The fermentation of milk products like yogurt can lead to acidification. The fermented product presents naturally a low pH that inhibits the proliferation of Salmonella.
For cheese, the development of Salmonella during processing, refining and acidification is simulated according to the physico-chemical parameters of the product (temperature, pH, water activity (aw) and concentration of lactic acid in its non-dissociated form).
During salting, the growth of Salmonella is inhibited using salt content above 3-4%. However, few cheeses achieve such high salt levels.
During acidification, Salmonella appears to be relatively inhibited by lactic flora, when the lactic acid achieve concentrations above 1%. Lactic acid in its non-dissociated form acts as a bacteriostatic antibiotic especially on pathogenic bacteria such as Salmonella. Moreover, it is considered to be a more effective decontamination agent than acetic acid (Deumier, 2004).
Aquatic by products
The aquatic animal’s by-products should be reduced to fragments in order to apply a thermal treatment, and decrease their pH using formic acid and maintain the pH at or below 4.0.
The mixture must be stay for at least 24 hours before starting the next treatment phase.
The disinfection of water is carried out by using disinfectants such as chlorine, chlorine dioxin or ozone and also by ultra-violet treatment or by physical processes such as membrane filtration.
Compared to chlorine, ozone provides good disinfection, without the risk of chlorinated by-products or taste defects (Anand et al., 2014).
Meat by-products, canned food or cured meats, are generally kept cooked. Two types of treatments are carried out for this type of products. Pasteurization carried out at temperature below 100°C, which allows the destruction of vegetative forms of bacteria such as Salmonella, and appertization, heat treatment carried out at a temperature above 100°C, necessary for the destruction of sporulating bacteria such as Clostridium botulinum.
Salmonellosis is one of the major food born diseases in the world, it constitute a public health emergency since the virulence and pathogenicity related, especially in the lower middle-income countries such as Morocco.
Poultry represents the first reservoir of Salmonella, from there, the study of the prevalence of Salmonella spp. at the level of broiler farming and at the other links (transport, slaughter, re-cleaning, cutting, staging) is necessary in order to know the levels of contamination that would be expected at carcass, cut, or finally on a ready dish to consume.
Additionally, hot countries have to carry out more studies in order to better understand the behavior and strategies to control of Salmonella.
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