Abstract
Ingestion of food is the major way for human beings to obtain nutrient substances for basic living, and therefore, the quality and safety of food is a major concern. Foodborne illness includes any illness resulting from the consumption of contaminated food that contains pathogenic bacteria, viruses, or chemical or natural toxins. Consequently, food safety is considered to be a globally expanding issue and thus a leading topic in public health, no longer limited to foodborne illnesses but extended to nearly every safety issue regarding “farm to table” food approaches. Bacterial foodborne infections occur by ingestion of food contaminated with growth of pathogenic bacteria, toxin production, and continuous bacterial growth in intestines. In the past decade, a large number of cases or reports have been available on food containing unhealthy, harmful, or toxic substances (other than food poisoning outbreaks) worldwide. Foodborne microorganisms, primarily associated with pathogenic bacteria and toxic substances produced in food, have presented major challenges for food safety. As a global foodborne pathogen, Staphylococcus aureus is typically capable of causing a large number of infections, including food poisoning. Thus, this chapter aims to review several factors contributing to the rise of staphylococci as a growing concern for the food safety industry, including the growth of S. aureus, production and regulation of staphylococcal enterotoxins, the viable putative but nonculturable (VPNC) state, and antimicrobial resistance of Staphylococcus caused by the indiscriminate use of antibiotics in both clinical and veterinary settings.
Keywords
- Staphylococcus aureus
- Enterotoxins
- Food poisoning
- Biofilm
1. Introduction
Foodborne illness, also known as foodborne infection, foodborne diseases, or food poisoning, is defined as any illness resulting from the consumption of contaminated food that contains pathogenic bacteria, viruses, or chemical or natural toxins (such as poisonous mushrooms) [1, 2]. Remaining as the leading concern in public health and food safety globally, the annual occurrence of foodborne illness has been reported to be 47.8 million foodborne cases (with 128,000 hospitalizations and 3,000 deaths) in the United States, 750,000 cases (with 113,000 hospitalizations and 460 deaths) in France, and 5.4 million cases (with 18,000 hospitalizations and 120 deaths) in Australia [3–5]. Foodborne infections and diseases are caused by a large variety of pathogens that contaminate food and related products, accounting for the major source of all foodborne illnesses, with an estimate of 14 million illnesses, 60,000 hospitalizations, and 1,800 deaths per year [2]. Therefore, bacterial foodborne infections occur when ingested food is contaminated with pathogenic bacteria, toxins produced (even if the growth of host bacteria is terminated), and continuous bacterial growth in intestines (for setting up an infection that causes illness).
1.1. Staphylococci
As a group of Gram-positive, facultative aerobic, frequently unencapsulated, osmotolerant microorganisms, staphylococci are carried, mostly transiently, by approximately 50% of healthy adults on the skin and anterior nares and widespread in untreated water, raw milk, and sewage. Staphylococci are responsible for various tissue infections and a multitude of diseases [6–9]. Up to date, more than 30 distinct types of staphylococci strains have been verified to be infectious for humans, and the associated illnesses and diseases range from mild to severe, from no treatment required to even potentially fatal [6, 7, 10]. Most of these infections are caused by
1.2. Staphylococcal Food Poisoning (SFP)
Staphylococcal food poisoning (SFP) is a noncontagious gastrointestinal illness caused by the ingestion of food contaminated with preformed staphylococcal enterotoxins (SEs), with low fatality and symptoms commonly including nausea, retching, vomiting, stomach cramps, exhaustion, and diarrhea [1, 15]. The onset of SFP symptoms commonly occurs between 0.5 and 6 h, and the illness typically lasts for 1 day (up to 3 days), with rapid recovery [1]. Serving as one of the most economically important foodborne diseases, SFP is currently a major issue for global public health programs worldwide [16, 17]. In the United States,
Food commonly involved in staphylococcal intoxication include protein food (even salty) such as ham, raw or processed meat, puddings, pastries tuna, chicken, sandwich fillings, cream fillings, potato and meat salads, custards, raw bilk milk, milk products (especially unpasteurized milk), cheese products, and creamed potatoes [22, 23]. In China, raw meat, milk and dairy products, frozen products, and cooked food have been found as major food types contaminated by
2. Staphylococcal Enterotoxins (SEs)
Some
As classified according to the distinct immunological entities, until recently, a total of 25 types of SEs (A–V and X, with 3 subtypes for C) have been identified. The finding of SEs has been in accordance with the development of identification methodologies. In early studies, animal testing experiments had been commonly used for the observation of SE activity, requiring monkey, feline, or cavy models [47–49]. After feeding with contaminated food, animals exhibited abnormal behavior or gross morphology changes, and the SEs contained in food were determined by the number of vomiting events, the time until the first vomiting event, and behavioral changes [47]. These types of animal feeding experiments had been commonly used for the characterization of emetic activities of SEs, thus determining the roles for emetic activities of SEs during SFP. However, such methodologies were also significantly limited by low sensitivity and specificity, poor reproducibility, high expense and laboratory operation, diversity in animals, and incapability of quantification and accurate identification [47]. Therefore, the identification of individual single type of SEs was reported by the availability of serological assays. Based on the specific reaction between antigen and antibody, identification of SEs via specific antibody [50] was first reported in the 1930s. Ouchterlony double immunodiffusion, also known as agar gel immunodiffusion, had become applicable in 1948 [51], and the first serological study on distinct SEs was conducted in 1958 [52]. From 1960s to 1970s, a number of SEs with emetic activities were identified and reported by the employment of serological methodologies including Ouchterlony double immunodiffusion, radial immunodiffusion, and enzyme-linked immunosorbent assays (ELISA). With the development of molecular biotechnology such as PCR and even genome sequencing in the 1990s and 2000s, a large number of newly identified SEs (G–V and X) as well as variants (for instance, 17 distinct variants of
2.1. Classical SEs
Although investigation on the observation and detection of SEs from animal feeding experiments could be dated back from 1930s, the immunological characteristics were not clarified until a number of serological studies had been conducted in the 1950s and 1960s. These studies revealed 6 types (A, B, C1, C2, D, and E) of SEs that were characterized and further referred to as classic SEs (including C3 reported in 1984). Antigenicity of SEs was validated when the antisera prepared from rabbits infected with SEs was demonstrated to protect cats [52], and later from a further serological study, the origins of two heat-resistant types of SEs had been verified [52, 53]. These extracellular immunologically distinct SEs responsible for the clinical manifestation of SFP were first referred to as type F (food poisoning) and type E (mostly produced by strains of “enteritis” origin) and later designated as A and B for a better sequential numbering system, with only type A commonly associated with food poisoning (A-1963). Sharing a similar basic three-dimensional structure, the 5 serological groups of SEs (A–E) exhibit nucleotide sequence identity of 50% to 85%, with types A, D, and E categorized into one group (52–83% amino acid identity) and types B and Cs falling into a separate, more closely related group (62–64% amino acid identity) [53, 54]. As origins and sources, types B and C are important causes of nonmenstrual-associated TSS, and types A and D are common causes of SFP with types B and C to a lesser extent [49].
2.1.1. Staphylococcal Enterotoxin A (sea or SEA)
SEA was first identified in 1959 from
2.1.2. Staphylococcal Enterotoxin B (seb and SEB)
Being the first identified (from
2.1.3. Staphylococcal Enterotoxin C (sec and SEC)
According to the new numbering system agreed on the American Society for Microbiology (ASM) meeting in 1962, the first verification of SEC was then reported in 1965, with its toxicity and specificity also confirmed [96]. In this study, the enterotoxins from
2.1.4. Staphylococcal Enterotoxin D (sed and SED)
In 1967, SED was first reported from
2.1.5. Staphylococcal Enterotoxin E (see and SEE)
In 1971, SEE was reported from a food poisoning
2.2. Staphylococcal enterotoxin-like toxins
Before the 1990s, a total of 7 types of classic SEs (
2.2.1. Staphylococcal Enterotoxin-Like Toxin Type F (sel-f and SEl-F)
In 1981, Bergdoll et al. had noticed an enterotoxin-like protein recovered from 93.8% [61/65]
2.2.2. Staphylococcal Enterotoxin-Like Toxin Type G (sel-g and SEl-G)
In 1998, SEl-G and SEl-I (from
2.2.3. Staphylococcal Enterotoxin-Like Toxin Type H (sel-h and SEl-H)
In 1994, the first discovery of
2.2.4. Staphylococcal Enterotoxin-Like Toxin Type I (sel-i and SEl-I)
As aforementioned, SEl-I were identified together with SEl-G in 1998 [126]. Unlike SEl-G, SEl-I was more similar to SEA, SED, and SEE (26–28% amino acid identity).
2.2.5. Staphylococcal Enterotoxin-Like Toxin Type J (sel-j and SEl-J)
In 1998,
2.2.6. Staphylococcal Enterotoxin-Like Toxin Type K (sel-k and SEl-K)
Despite observation of the
2.2.7. Staphylococcal Enterotoxin-Like Toxin Type L (sel-l and SEl-L)
First noticed on
2.2.8. Staphylococcal Enterotoxin-Like Toxin Type M (sel-m and SEl-M)
In 2001,
2.2.9. Staphylococcal Enterotoxin-Like Toxin Type N (sel-n and SEl-N)
From the
2.2.10. Staphylococcal Enterotoxin-Like Toxin Type O (sel-o and SEl-O)
In 2001,
2.2.11. Staphylococcal Enterotoxin-Like Toxin Type P (sel-p and SEl-P)
In 2001,
2.2.12. Staphylococcal Enterotoxin-Like Toxin Type Q (sel-q and SEl-Q)
In 2002, a member of the new subfamily (group V),
2.2.13. Staphylococcal Enterotoxin-Like Toxin Type R (sel-r and SEl-R)
In 2003,
2.2.14. Staphylococcal Enterotoxin-Like Toxin Type S (sel-s and SEl-S)
Two novel SE-like genes,
2.2.15. Staphylococcal Enterotoxin-Like Toxin Type T (sel-t and SEl-T)
As aforementioned, a first identification of
2.2.16. Staphylococcal Enterotoxin-Like Toxin Type U (sel-u and SEl-U)
From sequencing of 24
2.2.17. Staphylococcal Enterotoxin-Like Toxin Type V (sel-v and SEl-V)
In a broad surveillance on
2.2.18. Staphylococcal Enterotoxin-Like Toxin Type X (sel-x and SEl-X)
In 2011,
2.3. Pathogenicity Islands (PAIs) and S. aureus PIs (SaPIs)
2.3.1. PAIs
In 1986, before the first report of PAIs by Hacker et al. in Werner Goebel’s group of Germany in 1994, two large segments had been found to be capable of deletion and thus enable the host bacterial to produce hemolysin and loss of P. fimbriae [139, 153, 154]. Considered to be foreign DNA segments integrated into the bacterial genome, such segments existed within pathogenic isolates (cause of virulence) but not on highly genetically similar nonpathogenic strains [153]. As a subclass of genomic islands, PAIs are defined as a group of gene clusters encoding bacterial virulence on a large DNA segment (ranging from 20 to l00 kb) located on the bacterial chromosome [139, 154–156]. PAIs are acquired by microorganisms via horizontal gene transfer via transduction, conjugation, and transformation. Acquisition of PAIs may rapidly and radically alter the genome of a bacterium, consequently strengthening or reducing its fitness within the host [154, 157]. Pathogens are capable of harboring one or more PAIs associated with one or more virulence genes. PAIs are capable of encoding genetic products, including secretory proteins (such as type III secretion system), cell surface proteins (such as erythrocytolysin, fimbriae, and heme binding factors), signal transduction systems, and regulation systems [139, 155–157].
As distinct DNA regions are present in the genome of pathogenic bacteria and absent in nonpathogenic strains (despite same or close species), typical PAIs are composed of mobility genes (such as integrases) commonly located at the beginning of the island and close to the tRNA locus or the respective attachment site. A number of virulence genes (V1–V4) are frequently interspersed with other mobility elements including insertion sequence (IS) elements (Isc, complete insertion element) or remnants of IS elements (ISd, defective insertion element) [153, 155, 156]. Commonly flanked by direct repeats (DR) and IS elements, PAIs are often genetically unstable and comprise some potential mobile components, such as IS elements, integrase, transposase, and plasmid replication initiation sites. As DNA sequences ranging from 16 to 20 bp (with maximum of 130 bp) with sequence repetition, DR plays a critical role in insertion and deletion (as recognition sites), such as integration of bacteriophages. Although combination of IS elements may be capable of mediating transfer of large DNA fragments, insertion mediated by IS also leads to inactivation of genes as well [153, 154, 156]. Consequently, PAIs are capable of deletion with distinct frequencies and loss of virulence traits encoded by PAIs are reported to occur at higher frequency than that encoded by mutation. PAIs are commonly inserted in the backbone genome of the host strain, typically located to specific sites such as tRNA loci or adjacent to tRNA genes, or sites associated with plasmid and phage integration, due to highly conserved genes encoding tRNAs among various bacterial species [153, 154].
PAIs differ from host chromosomes in GC content and codon usage, which may account for the discovery of novel PAIs and maintenance of the divergent nucleotide composition from the horizontally acquired DNA. Based on significant differences with respect to bacterial virulence, GC content, and codon usage, a hypothesis was proposed that such characteristics may be bestowed from DNA segments on the plasmid and phage; thus, acquisition of PAIs and the emergence of new pathogenic organisms can be correlated [153, 156].
2.3.2. SaPIs
As mobile pathogenicity islands with length ranging from 14 to 17 kb and carriage of genes for superantigen toxins and other virulence factors, SaPIs have been responsible for the TSS and other superantigen-related diseases, especially SE-like toxins. Located in specific loci of the chromosome and induced by bacteriophages, SaPIs are capable of incorporating small infective phage-like particles via a program of excision-replication-packaging. Containing most of the staphylococcal toxins and virulence factors, SaPIs facilitate the horizontal acquisition of MGEs and, thus, play an important role in the evolution of
2.3.2.1. SaPI families
Aside from SCC
2.3.2.2. νSa families
Up to date, 7 conservative PAI types had been discovered in
2.3.2.3. Development and evolution of pathogenicity
The mechanisms of horizontal gene transfer in prokaryotic cells include transduction, conjugation, and transformation, among which phage transduction has been the primary transmission drivers of genes among different species and thus plays an important role in the formation of PAI [159]. The formation of PAIs may include 5 stages [160] as follows: (i) acquisition of virulence gene via horizontal gene transfer regulated by an operon and derived from “gene pool” of varied environment; (ii) integration of foreign genes (commonly derived from various complex genes of different donors) into the bacterial chromosome or plasmid via site-specific recombination or other mechanisms, following similar rules to complete integration and shaping obvious structure of genetic island; (iii) evolvement of MGEs into PAI via restructure, gene elimination, and acquisition of other genetic materials, during which the gene components associated with mobility may be inactivation or lost, such as origin of plasmid replication, self-transmissible plasmid tra and phage int; (iv) induced expression of foreign genes under temperate environment; and (v) acquisition or elimination of genetic information constantly via a serious of recombination, insertion or elimination, by which PAI may retrieve MGE and obtain the ability of excision and transfer the whole PAI from chromosome to another recipient bacterium.
Evolution of the bacterial genome may significantly influence its pathogenicity, mainly including point mutations, recombination, and horizontal gene transfer. Despite slow evolution due to relatively low frequency of point mutation, the horizontal gene transfer of large genetic segments (such as PAIs and SaPIs) undoubtedly speeds up the exchange of bacterial genes (as “quantum leap” in short time), leading to the consequent appearance and spread of various novel mutations or variants [161, 162].
3. Novel perspectives of Staphylococcus associated with food safety
3.1. Antimicrobial resistance mediated by MGEs
Antibiotics, as compounds or substances that kill or inhibit the growth of microorganisms, have been regarded as one of the greatest contributions to medicine and humanity and used to treat a wide range of infectious diseases caused by bacteria for both animals and human beings [5, 165]. Abuse of existing antibiotics contributes to the spread of antibiotic resistance and poses a predicament for the treatment of several bacterial infections, including therapy for individuals with food poisoning. In China, as one of the currently worst areas for antibiotics abuse, the annual prescription of antibiotics, including both clinical and veterinary treatment, is approaching 140 grams per person and has been roughly estimated to be 10 times higher per capita than that in United Kingdom [6, 7, 163, 164]. From a retrospective study conducted on 1,739
3.1.1. SCCmec
As one of the major foodborne infectious pathogens,
MRSA was found shortly after the common use of methicillin, which was first licensed to treat penicillin-resistant
3.1.1.1. Structure and types
As a major member of the SCC family and a carrier for gene exchange in staphylococci strains, SCC
Up to date, SCC
A thorough understanding of the molecular epidemiology and evolution of MRSA may aid in the further identification, control, prevention, and therapy of
3.1.1.2. Prevalence and occurrence
As different types and subtypes of SCC
3.1.2. Other resistance determinants in Staphylococcus
Aside from SCC
3.1.3. Mobility and evolution of MGEs in staphylococci
As a commonly found MGE with an antibiotic resistance gene (
As a genomic island (G island) and MGE demarcated by a pair of DRs and inverted repeats, SCC
Up to date, the most known functional genes carried by MGES are found to encode resistance to the oldest groups of antibiotics (such as tetracycline, streptomycin, and spectinomycin) that have been discontinued in clinical settings for decades but still available in veterinary practice. Although the indiscriminate use of these older antibiotics is no longer occurring in the clinical setting, their use in veterinary medicine may contribute to a novel and significant concern in food safety. Abuse of antibiotics leads to the emergence of antibiotic resistance and poses a predicament for the future treatment of bacterial infection, with MGEs undoubtedly facilitating the rapid spread and dissemination of a vast number of resistance genes among microorganisms.
3.1.4. Livestock-Associated MRSA (LA-MRSA)
As a common pathogen for both clinical medicine and food safety, MRSA was first reported as hospital associated before the 1990s and thus designated as HA-MRSA. Since the 1990s, CA-MRSA strains have increasingly been reported among groups of patients with no apparent connection to hospitals. It is noteworthy that a large number of such CA-MRSA-infected patients or carriers were pediatric associated. Aside from HA-MRSA and CA-MRSA, LA-MRSA has been recently documented and is known to be more persistent in food products from swine and cattle [258], which is also responsible for pneumonia, endocarditis, and necrotizing fasciitis by LA-MRSA carriers [259]. Nowadays, LA-MRSA acts as an increasing risk for public health and a challenge to livestock farming and related food products. LA-MRSA was mostly found among animals (particularly pigs) and humans with frequent contact to livestock farming or livestock food products [260–262]. After the first isolation of MRSA from livestock (cows with mastitis) [263], a extremely limited number of reports were focused on LA-MRSA. However, after an initial LA-MRSA case occurred in humans, described in 2005 [262], LA-MRSA have been the focus of numerous recent studies. In 2007, a transmission of MRSA (ST1, spa-type t127) between cows and humans was reported, verifying the transmission between animals and humans [264]. Afterwards, different types of LA-MRSA have been continuously discovered globally, and the prevalence and occurrence of LA-MRSA vary significantly in different areas. In Europe and America, the majority of LA-MRSA strains belong to sequence type (ST) 398, whereas ST9 is frequently discovered in Asia [265–268]. Both livestock and humans are potential carriers of LA-MRSA, and individuals working in animal clinics and livestock production environments with direct contact or exposed to MRSA-positive animals or ingestion of the MRSA-positive livestock food products have an increased risk of becoming MRSA carriers [269, 270]. A high risk of animal to human transmission of ST398 was found to result from direct association between animal and/or human MRSA carriages in the farm setting [261, 269, 271–273] despite much lower occurrence of transmission between humans by LA-MRSA and that of HA-MRSA [274–276].
As a clone of typical LA-MRSA, ST398-LA-MRSA has been responsible for serious infections and outbreaks worldwide [277, 278]. Containing various spa-types, ST398-LA-MRSA strains are mostly found to carry type IV or V SCC
Emergence, spread, and dissemination of ST398-LA-MRSA from animals, as well as its transmission between humans and animals, strongly suggest that the antimicrobial resistance caused by veterinary antibiotic abuse poses a hazard to both humans and animals regarding food safety challenges associated with animal origins.
3.2. Viable Putative but Nonculturable (VPNC)
In nature, bacteria exist in various states such as normal growth state, dead state, dormant state, and VPNC state, which was first reported in 1986 [287]. Differing significantly from the “starvation survival” state, VPNC state [previously known as viable but nonculturable (VBNC)] is a specific state under which bacteria remain alive but fail to form a colony on routine bacteriological media that normally support their growth. Consequently, routine bacteriological detection methodology fails to detect the VPNC bacteria. However, given the right conditions, bacteria in the VPNC state remain active and can “resuscitate” to the normal state. Hence, the VPNC food spoilage or pathogenic bacteria are considered to be a stealth source of contamination, posing a significant concern for traditional surveillance and control methodologies of foodborne pathogens.
3.2.1. Induction and resuscitation
Entering into the VPNC state is considered to be a survival mechanism for nonsporulation bacteria under a number of harsh environmental conditions, which is described in detail as follows: [1] Nutrient starvation [288]. Without essential nutrients, bacterial growth and metabolism may be terminated and thus enter the death-like status. Nutrient starvation, such as the absence of carbon source or nitrogen source, which is an extreme condition for the growth of bacteria, can induce the VPNC state. [2] Extreme temperature [289]. The appropriate temperature for typical bacterial growth ranges from 20°C to 37°C, and termination of growth usually occurs under extremely high or low temperature. The temperature of 4°C or -20°C, at which bacteria stop growth and metabolism, is frequently used for induction of VPNC state. The combination of nutrient starvation and low temperature has also been widely applied as an induction condition. [3] pH value [290]. Most microorganisms grow in neutral and slightly acidic or alkaline pH conditions. Strong acidity or alkalinity may lead to bacterial death-like states, which has been occasionally used to induce the VPNC state. [4] Salinity [291]. As an extreme condition for bacterial growth, high salinity has been found to enable the entering of VPNC state. [5] Osmotic stress [291]. Extremely high osmotic stress was reported to be applied for VPNC state induction. [6] Oxygen availability [292, 293]. In an aerobic environment, anaerobic bacteria would enter into the VPNC state and the absence of oxygen would induce the VPNC state of aerobic bacteria and vice versa. [7] Existence of heavy metals [294, 295]. [8] Common food preservatives (cryopreservation, vacuum preservation, etc.). Currently, numerous bacteria are reported to have the ability to enter into VPNC state, such as
Currently, only 2 species of
3.2.2. Characteristics and mechanisms
Remaining metabolically or physiologically active, bacteria in VPNC state maintain cell integrity but exhibit dwarfing, which contribute to protect against a wide variety of stressors. The maintenance of metabolic activity and continuous gene expression under VPNC state [327, 328] indicates that potentially ingested bacteria may still be capable of causing foodborne illnesses. Such microorganisms also possess the capacity to regain culturability
As for the pathogenicity of
3.2.3. Detection and identification
VPNC pathogenic bacteria are considered to be a threat to public health and food safety due to incapability of detection by the “gold standard” methodology for identification of food-associated microorganisms. Hence, the development, evaluation, validation, and further application of rapid and accurate detection methodology for VPNC bacteria are considered to be the leading concerns for the surveillance of bacterial cells in VPNC state as well as further understanding of the mechanisms on their survival and persistence in the extreme environment. The conventional detection method for VPNC bacteria was the combination of acridine orange direct count (AODC) (for total bacterial cell number counting), bright-field microscopy with nalidixic acid (for metabolically active cell number counting), and plate counting (for determination of culturability). The occurrence of entry of bacterial cells into VPNC state was validated and confirmed when colony counts were totally depleted on culture plates (with no observed colonies), which was designated as nonculturable, whereas the total bacterial and metabolically active cells still remained countable. Despite the limited application of nalidixic acid on Gram-negative microorganisms, the novel LIVE/DEAD Bacterial Viability Kit with requirement on differential fluorescence was employed for the detection of both Gram-positive and Gram-negative bacteria [331]. In consideration of the carcinogenesis and expense of fluorescence substances, the development of molecular assays, such as random amplified polymorphism DNA and RT-PCR [328], was recently applied to identify bacterial cells in the VPNC state. As
In conclusion, foodborne pathogens, especially
4. Concluding remarks
Ingestion of food is the major (although, not only) way for human beings to obtain nutrient substances for basic living; therefore, the quality and safety of food have recently become a major concern. Considered to be an expanding global problem and leading topic in public health, food safety is no longer limited to foodborne illnesses but has been extended to all safety issues associated with “farm to table” food approaches. In the past decade, a large number of worldwide cases or reports have been available regarding food containing unhealthy, harmful, or toxic substances (other than food poisoning outbreaks). Foodborne microorganisms, previously limited to pathogenic bacteria and toxic substances produced in food, have played a critical role in food safety. However, now due to diversity in the genus and species of microbes, variety of mechanisms on the regulation of growth and survival, and complexity of ecosystem involving polymicrobial interaction and environmental factors, a number of novel microbial issues associated with food safety have been recently acknowledged. Microorganisms may very well be capable of surviving the journey from farm to table via various evasion mechanisms at various food processing stages, including source (antimicrobial resistance caused by the use of drugs in veterinary medicine or livestock feed), processing (formation of biofilm and further survival of bacterial elimination), storage (formation of VPNC state and “false-negative” detection), and even after cooking (production of heat-stable toxins that remain active despite elimination of host bacteria). The contributions of aforementioned and novel evasion mechanisms with respect to food safety undoubtedly require further investigation in vitro and in vivo for improved diagnostic and decontamination procedures.
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