Resistance phenotype and resistance genes of the strain.
Abstract
Foodborne pathogens of Enterobacteriaceae including Escherichia coli, Salmonella, Shigella, Yersinia, etc., causes a great number of diseases and has a significant impact on human health. Here, we reviewed the prevalence, virulence, and antimicrobial susceptibility of Enterobacteriaceae belonging to 4 genera: E. coli, Salmonella, Shigella, and Yersinia. The routes of the pathogens’ transmission in the food chain; the antimicrobial resistance, genetic diversity, and molecular epidemiology of the Enterobacteriaceae strains; novel technologies for detection of the bacterial communities (such as the molecular marker-based methods, Immunoaffinity based detection, etc.); and the controlling of the foodborne pathogens using chemical/natural compounds or physical methods (such as UV-C and pulsed-light treatment, etc.), is also summarized.
Keywords
- foodborne pathogens
- Escherichia coli
- Salmonella
- Shigella
- Yersinia
- detection and control
1. Introduction
Foodborne illness is the biggest health problem in the world. Due to unsanitary food processing methods, this situation is very serious in developing countries. Approximately 70% of diarrhea cases in developing countries are related to the consumption of contaminated food. An estimated 3.5 billion people have been infected, with 450 million people affected, most of them children [1]. There are many causes of foodborne illness, among which the most important are foodborne pathogens, including
In recent years, the detection of foodborne pathogens has developed rapidly. Many techniques such as PCR, nanotechnology, nucleic acid hybridization are widely used [5]. There are also many control methods for foodborne pathogens. In the present paper, we summarized the transmission, antimicrobial resistance, genetic diversity, and molecular epidemiology of the
2. Transmission of pathogens in the food chain
Foodborne pathogens are transmitted through the food chain in many ways, such as insect transmission, fecal-oral transmission, food and water transmission, animals transmission, and so on. Some pathogens, such as
Insects are considered to be carriers of foodborne pathogens. Their association with degradable substances and their endogenous and coexistence (with humans) are behavioral patterns that are particularly important for the ability of flies, cockroaches, and ants to transmit foodborne diseases. A study conducted in an ant colony in a Brazilian hospital found that several bacteria, including
Water is well-known for its importance in the production, processing, and preparation of food. It is also a medium for the transmission of pathogens during food manufacturing [11]. The quantity of contamination in irrigation water determines pathogen survival, and the higher the degree of contamination, the better. They may survive outside of their human hosts for months to years before being transmitted to humans through water [12].
Many microorganisms that cause foodborne diseases can be transferred directly from animals to people. Mammals such as pigs and cattle are thought to host many foodborne pathogens, which are transmitted to humans either through direct contact with humans or by being processed into food for human consumption.
There are many key points where pathogens can infiltrate and jeopardize human food safety, such as the food itself, the surfaces of food preparation tools or food processors [16]. At each food processing or preparation facility location, a variety of factors may impact contamination and transmission. For example, microbial pathogens can be brought into the kitchen environment through commercial foods, cross-contamination of foods via kitchen equipment, or be reused due to inadequate cooking or storage [17, 18].
3. Antimicrobial resistance, genetic diversity and molecular epidemiology of the Enterobacteriaceae foodborne pathogens
3.1 E. coli
The original
Strain | Resistant phenotype | Resistance genes |
---|---|---|
Streptomycin/spectinomycin resistance Polymyxins resistance Fluorinated and nonfluorinated phenicols resistance β-lactams resistance | ||
Beta-lactam resistance Macrolide resistance Aminoglycoside resistance Amidoalcohol (chloramphenicol) resistance Amido alcohol (chloramphenicol) resistance Other | ||
Cephalosporins and Fluoroquinolones resistance | ||
Tetracycline and minocycline resistance Ticarcillin and amoxicilin resistance Trimethoprim resistance Sulfonamide resistance Chloramphenicol resistance |
The genetic diversity of
The genetic diversity of
3.2 Salmonella
Molecular epidemiology has been used to document vector to human transmission and to investigate outbreaks of
3.3 Shigella
3.4 Yersinia
The genetic diversity of
4. Novel technologies for detecting the pathogens
In recent years, the rapid detection of foodborne pathogens has developed rapidly. Molecular biology, nucleic acid hybridization, and other technologies have been highly valued and widely used in laboratory or factory production.
4.1 Nanoparticles in pathogen detection
Substances are manipulated at atomic, molecular, and supramolecular scales through nanotechnology (“nanotech”). Advances in manipulating these nanomaterials allow specific or non-specific binding of different biomolecules. The large specific surface area allows more biomolecules to be immobilized, thereby increasing the number of reaction sites that can be used to interact with the target species, which is one of the main advantages of biosensing using nanomaterials. In addition, nanomaterials have been widely used in ‘label-free ‘detection due to their excellent electronic and optical properties, and biosensors with enhanced sensitivity and improved response time have been developed [34].
Metal nanoparticles, especially gold and silver (5–110 nm in size) exhibit excellent properties, such as signal amplification, have potential application in various areas such as variable optical and electrical determinations. Gold nanoparticles (AuNPs) change the color aggregation from blue to red with the ability to scatter light, showing excellent chemical stability and electrical conductivity. AuNPs were used to detect Salmonella and
4.2 Polymerase chain reaction (PCR)
Polymerase chain reaction (PCR) plays an important role in molecular methods in detecting foodborne pathogens. As early as 30 years ago, PCR, which was invented for the detection of single bacterial pathogens present in food by identifying specific target DNA sequences [37]. PCR works by amplifying specific target DNA sequences in a three-step cycle [38]. Firstly, single-stranded DNA was obtained from target double-stranded DNA by high-temperature denaturation. Then, deoxyribonucleic acid was lead on the backbone of DNA by adding specific primers and heat-resistant DNA polymerase in the polymerization process of DNA, so a new double-stranded DNA was synthesized. The amplified products of PCR were stained by ethidium bromide on electrophoretic gels [39]. PCR such as loop-mediated isothermal amplification (LAMP), multiplex PCR (mPCR) and RT-PCR, etc. is used to detect foodborne pathogens, including
4.2.1 Loop-mediated isothermal amplification (LAMP)
Now, molecular diagnostic technologies based on nucleic acid amplification have been applied extensively in the detection regions, such as Loop-mediated isothermal amplification (LAMP) developed by Notomi [41, 42, 43, 44, 45]. Various confirmatory studies have been used to evaluate the feasibility of LAMP technology for microbial identification and diagnosis [42]. LAMP kits for detecting
The loop-mediated isothermal amplification method offers several advantages: high sensitivity (2–5 orders of magnitude higher than conventional PCR methods); short reaction time (30–60 min can complete the reaction); no special instrumentation is required for clinical use; the operation is simple (whether DNA or RNA, the detection step is to mix the reaction liquid, enzyme, and template in a reaction tube, place in a water bath pot or incubator at 63°C for about 30 to 60 minutes, observe the results by the naked eye) [42, 43, 44]. There are also some disadvantages of the loop-mediated isothermal amplification method: high sensitivity, easy to form aerosol pollution once the lid is opened, combined with the current majority of domestic laboratories can not strictly partition, false-positive problems are relatively severe, so we strongly recommend using real-time turbidimeter during the development of the kit, do not open the reaction tube after the reaction. Primer design is more demanding, and some disease genes may not be amenable to the use of loop-mediated isothermal amplification methods [41, 42, 43].
4.2.2 Multiplex PCR (mPCR)
mPCR technology is more new-fashioned, which can simultaneously detect more pathogens than before, up to four or more pathogens [45, 46, 47]. Chen et al. simultaneously detected
The characteristics of multiplex PCR are high efficiency, systematic and economic simplicity. High efficiency: a variety of pathogenic microorganisms in the same PCR reaction tube can be detected simultaneously, or multiple pathogens can be detected with multiple types of genes of interest. Systematic: mPCR is suitable for the detection of grouped pathogens. Economic simplicity: this will greatly economical of time, reagent and cost, and provide more accurate diagnostic information for clinical practice, because multiple pathogens are detected synchronously.
4.3 Nucleic acid hybridization technologies in pathogen detection
A general method of fluorescence in situ hybridization (FISH) using oligonucleotide probes of rRNA for nonmolecular technology. Probe lengths of 15 to 25 nucleotides labeled at the 5′ end were used for FISH. The specifically labeled cells were detected by an apparent fluorescence microscope. Rapid culture and independent detection of
Line probe analysis (LIPA) is composed of oligonucleotide probes with specific oligonucleotides and nitrocellulose bands, which are connected by parallel lines along with the bands and discrete lines. The color change of hybridization results can be detected by vision. Innogenetics has produced several line probes for bacterial detection, such as
Nielson et al. found a DNA analog called peptide nucleic acid (PNA) for detecting foodborne pathogens. This probe is more stable because PNA is not charged. In addition, PNA has a greater advantage in that it is relatively hydrophobic and easier to enter nonbacterial cells. PNA has higher specificity than DNA oligomer because the TM of the PNA probe is higher than that of its DNA probe. Theoretically, in addition to PNA and FISH, PNA can also replace DNA oligonucleotides to improve analytical performance [53, 54].
5. Controlling of the Enterobacteriaceae foodborne pathogens
At present, food pollution and poisoning caused by foodborne pathogens have attracted extensive attention. In the food industry, technologies such as irradiation, pulsed light treatment, microwave sterilization, slightly acid electrolytic water and fumaric acid treatment, algae extract treatment,
5.1 Irradiation
In more and more countries, ionizing radiation processing is the most common method of food purification, and in the short run, a growing number of radiation-purified foods are presumed to be approved for production. It is a secure, smart, environmentally clean, and energy-efficient process, and it is especially valuable as a purification process for the final product. Due to the availability of irradiation in handling packaged foods, irradiation is regarded by most food safety officers and scientists as an effective critical control point in the processing of meat and poultry hazard analysis and critical control point (HACCP) system.
The high-energy photons or free radicals generated by ionizing radiation can break the DNA chain and generate reactive oxygen free radicals, and can also cause protein denaturation and cell membrane damage. Hesham reported that an irradiation dose of 4 kGy can effectively control the bacterial pathogens in meat by destroying
5.2 Pulsed-light treatment
Nucleic acids are easily destroyed by pulsed light (PL). Pyrimidine bases form dimers the DNA of bacteria, viruses, and other pathogens through photochemical intervention and block DNA replication, and if there is not enough repair mechanism, it will ultimately lead to the death of microorganisms [56]. Xu et al. [57] investigated the inactivation effect of PL on
However, in the sterilization process of fruits and vegetables, if the PL intensity is too high, due to the effect of PL on protein structure, it will improve the activity of polyphenol oxidase (PPO) to a certain extent and cause browning [61]. In the process of meat sterilization, PL has a poor sterilization effect on uneven surfaces [62], and the sterilization only stays on the surface.
5.3 Microwave sterilization
Microwave sterilization is that microwave constantly changes the direction of electromagnetic field, changes the ion and electron density around microbial cell membrane, destroy the permeability of cell membrane, lead to protein degeneration in cells, destroy cell metabolism, and microbial death [63].
De La Vega-Miranda observed that under 950 W water-assisted microwave treatment,
5.4 Slightly acidic electrolyzed water and fumaric acid
Slightly acidic electrolyzed water (SAcEW) is a type of EW and promising sanitizer for food products. Effects of SAcEW combination with other chemical disinfectants on the ideal bactericidal efficacy of foods. Organic acids can inactivate foodborne pathogens, and show stronger bactericidal effects in organic acids used in meat antibacterial agents.
Ahmad found that a single treatment and combined treatment of fresh meat with micro-electrolyzed water or fumaric acid can reduce
5.5 Other technologies for controlling the Enterobacteriaceae foodborne pathogens
Recent studies have shown that some biological macromolecules can also be used to control foodborne pathogens of
Algae is a multifaceted natural substrate that contains a wide range of bioactive compounds. Antibacterial, analgesic, and antioxidant properties of phytosterols isolated from different algae have been demonstrated. Brown algae fucoidans and green algea ulvans both have antibacterial capacities. The most potent chemicals against
Foodborne pathogens | Treatments | Results/Activity | Reference |
---|---|---|---|
4 kGy dose of radiation | Reduce >5 log units | [66] | |
Slightly acidic electrolyzed water and fumaric acid | Reduce 2.34 log CFU/g | [65] | |
Brown Algae Methanol Extract | Sensitive | [67] | |
Phage cocktail | Spraying the phage mixture resulted in a 4.5 log CFU reduction after 2 h | [72] | |
Phage DT1 and DT6 | 100% reduction in CFU/ml within an hour | [73] | |
Anti-adhesive/ Antibiofilm | [74] | ||
Anti-quorum sensing | [75] | ||
Carvacrol, thymol, trans-cinnamaldehyde | Antibiofilm Reduced expression of virulence genes | [76] | |
Surface-layer protein extract | Anti-adhesive | [77] | |
Resveratrol | Antibiofilm | [78] | |
Microwave radiation | Elimination of the superficial | [79] | |
4 kGy dose of radiation | Not detected | [55] | |
Water-assisted microwave heating | 5.12 log reduction | [64] | |
slightly acidic electrolyzed water and fumaric acid | Reduce 2.88 log CFU/g | [65] | |
Brown Algae Methanol Extract | Sensitive | [67] | |
Phage cocktail | Using MOI 5 leads to about 4.4 log reductions | [60] | |
Phage F01-E2 | The CFU of turkey cooked meat and chocolate milk was reduced by 5 log, and the CFU of hot dog was reduced by 3 log | [80] | |
Phage cocktail PC1 | More than 99% reduction in CFU at MOI 10 or above | [81] | |
Anti-adhesive | [82] | ||
Anti-invasive | [83] | ||
T315 compound | Antibiofilm | [84] | |
Methylthioadenosine | Reduced motility Anti-invasive | [85] | |
Microwave radiation | Theoretical complete inactivation | [86] | |
Phage cocktail | About 4 log reduction | [87] | |
Containing six novel | About 99% decrease | [88] | |
Decreasing by 1–3 logs on food samples | [89] | ||
Bacteriophage specific to serotype O1 | Polysaccharide Depolymerase activity capable of degrading | [90] |
6. Conclusion
A plenty number of studies have been confirmed that foodborne pathogens of
Acknowledgments
This project was funded by the Natural Science Foundation of Zhejiang Province (LR22C200005), the Key Research and Development Program of Zhejiang Province (2020C04002) and the Science and Technology Project of Zhejiang Province (LGN22C200013).
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