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Advanced Research in Foodborne Microorganisms: Detection, Control, Risk Assessment and Prevention Volume II

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A special issue of Foods (ISSN 2304-8158). This special issue belongs to the section "Food Microbiology".

Deadline for manuscript submissions: closed (10 March 2023) | Viewed by 39556

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Prof. Dr. Michel Federighi

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1. EnvA, 7 Avenue du Général de Gaulle, F-94700 Maisons-Alfort, France
2. INRAe, UMR1014 SECALIM, F-44307 Nantes, France
Interests: risk analysis; food safety; biostatistics; veterinary public health
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Special Issue Information

Dear Colleagues,

Volume I of this Special Issue was an incredible success, with the participation of numerous high-profile scientists, all of whom I would like to thank for their support. The topic of foodborne microorganisms continues to play a pivotal role today, and it is for this reason I believe that it is now time now for Volume II to be launched, which can be just as big a success and contribute just as significantly to the field as the first volume did.

Microorganisms and food have been linked since humans first started to examine the role and aspects of human nutrition. Depending on their nature, microorganisms may constitute:

A threat to the health of consumers;
A cause of food spoilage and food waste;
A necessary and indispensable element in the production of food.

Regardless of their nature, though, their relationships with the food that carries them are studied in terms of microbial ecology in order to better understand them. Their identity is increasingly well established and their function, as well as their ability to withstand the conditions of food production and even to communicate with each other, increasingly deciphered. This better knowledge of their properties must continue and be used to, where appropriate, prevent their transfer to food, detect and control them, but also assess them in terms of public health risks.

Prof. Dr. Michel Federighi
Guest Editor

Manuscript Submission Information

Manuscripts should be submitted online at www.mdpi.com by registering and logging in to this website. Once you are registered, click here to go to the submission form. Manuscripts can be submitted until the deadline. All submissions that pass pre-check are peer-reviewed. Accepted papers will be published continuously in the journal (as soon as accepted) and will be listed together on the special issue website. Research articles, review articles as well as short communications are invited. For planned papers, a title and short abstract (about 100 words) can be sent to the Editorial Office for announcement on this website.

Submitted manuscripts should not have been published previously, nor be under consideration for publication elsewhere (except conference proceedings papers). All manuscripts are thoroughly refereed through a single-blind peer-review process. A guide for authors and other relevant information for submission of manuscripts is available on the Instructions for Authors page. Foods is an international peer-reviewed open access semimonthly journal published by MDPI.

Please visit the Instructions for Authors page before submitting a manuscript. The Article Processing Charge (APC) for publication in this open access journal is 2900 CHF (Swiss Francs). Submitted papers should be well formatted and use good English. Authors may use MDPI's English editing service prior to publication or during author revisions.

Keywords

foods
microorganisms
preservation
risk
methods
contamination
microbial ecology
hazard analysis
spoilage

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Published Papers (10 papers)

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Research

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14 pages, 1166 KiB

Open AccessArticle

Staphylococcus aureus in the Processing Environment of Cured Meat Products

by David Pérez-Boto, Matilde D’Arrigo, Ana García-Lafuente, Daniel Bravo, Aida Pérez-Baltar, Pilar Gaya, Margarita Medina and Juan L. Arqués

Foods 2023, 12(11), 2161; https://doi.org/10.3390/foods12112161 - 26 May 2023

Cited by 12 | Viewed by 4355

Abstract

The presence of Staphylococcus aureus in six dry-cured meat-processing facilities was investigated. S. aureus was detected in 3.8% of surfaces from five facilities. The occurrence was clearly higher during processing (4.8%) than after cleaning and disinfection (1.4%). Thirty-eight isolates were typified by PFGE and MLST. Eleven sequence types (STs) were defined by MLST. ST30 (32%) and ST12 (24%) were the most abundant. Enterotoxin genes were detected in 53% of isolates. The enterotoxin A gene (sea) was present in all ST30 isolates, seb in one ST1 isolate, and sec in two ST45 isolates. Sixteen isolates harbored the enterotoxin gene cluster (egc) with four variations in the sequence. The toxic shock syndrome toxin gene (tst) was detected in 82% of isolates. Regarding antimicrobial resistance, twelve strains were susceptible to all the antibiotics tested (31.6%). However, 15.8% were resistant to three or more antimicrobials and, therefore, multidrug-resistant. Our results showed that in general, efficient cleaning and disinfection procedures were applied. Nonetheless, the presence of S. aureus with virulence determinants and resistance to antimicrobials, particularly multidrug-resistant MRSA ST398 strains, might represent a potential health hazard for consumers. Full article

(This article belongs to the Special Issue Advanced Research in Foodborne Microorganisms: Detection, Control, Risk Assessment and Prevention Volume II)

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16 pages, 1492 KiB

Open AccessArticle

Identification, Typing and Drug Resistance of Cronobacter spp. in Powdered Infant Formula and Processing Environment

by Hongxuan Li, Shiqian Fu, Danliangmin Song, Xue Qin, Wei Zhang, Chaoxin Man, Xinyan Yang and Yujun Jiang

Foods 2023, 12(5), 1084; https://doi.org/10.3390/foods12051084 - 3 Mar 2023

Cited by 12 | Viewed by 2595

Abstract

Cronobacter spp. is a food-borne pathogenic microorganism that can cause serious diseases such as meningitis, sepsis, and necrotizing colitis in infants and young children. Powdered infant formula (PIF) is one of the main contamination routes, in which the processing environment is an important source of pollution. In this investigation, 35 Cronobacter strains isolated from PIF and its processing environment were identified and typed by 16S rRNA sequencing and multilocus sequence typing (MLST) technology. A total of 35 sequence types were obtained, and three new sequence types were isolated for the first time. The antibiotic resistance was analyzed, showing that all isolates were resistant to erythromycin but sensitive to ciprofloxacin. Multi-drug resistant strains accounted for 68.57% of the total, among which Cronobacter strains with the strongest drug resistance reached 13 multiple drug resistance. Combined with transcriptomics, 77 differentially expressed genes related to drug resistance were identified. The metabolic pathways were deeply excavated, and under the stimulation of antibiotic conditions, Cronobacter strains can activate the multidrug efflux system by regulating the expression of chemotaxis-related genes, thus, secreting more drug efflux proteins to enhance drug resistance. The study of drug resistance of Cronobacter and its mechanism has important public health significance for the rational selection of existing antibacterial drugs, the development of new antibacterial drugs to reduce the occurrence of bacterial resistance, and the control and treatment of infections caused by Cronobacter. Full article

(This article belongs to the Special Issue Advanced Research in Foodborne Microorganisms: Detection, Control, Risk Assessment and Prevention Volume II)

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19 pages, 3077 KiB

Open AccessEditor’s ChoiceArticle

Salmonella Risk Assessment in Poultry Meat from Farm to Consumer in Korea

by Hyemin Oh, Yohan Yoon, Jang-Won Yoon, Se-Wook Oh, Soomin Lee and Heeyoung Lee

Foods 2023, 12(3), 649; https://doi.org/10.3390/foods12030649 - 2 Feb 2023

Cited by 7 | Viewed by 6077

Abstract

This study predicted Salmonella outbreak risk from eating cooked poultry in various methods. The incidence of Salmonella in poultry meat and the environment from farm to home for consumption was investigated. To develop the predictive models, Salmonella growth data were collected at 4–25 °C during storage and fitted with the Baranyi model. The effects of cooking on cell counts in poultry meat were investigated. Temperature, duration, and consumption patterns were all searched. A simulation in @Risk was run using these data to estimate the probability of foodborne Salmonella disease. In farm, Salmonella was detected from only fecal samples (8.5%; 56/660). In slaughterhouses, Salmonella was detected from feces 16.0% (38/237) for chicken and 19.5% (82/420) for duck) and from carcasses of each step (scalding, defeathering, and chilling) by cross contamination. In chicken (n = 270) and duck (n = 205), Salmonella was detected in 5 chicken (1.9%) and 16 duck meat samples (7.8%). Salmonella contamination levels were initially estimated to be −3.1 Log CFU/g and −2.5 Log CFU/g, respectively. With R² values between 0.862 and 0.924, the predictive models were suitable for describing the fate of Salmonella in poultry meat with of 0.862 and 0.924. The Salmonella was not detected when poultry meat cooks completely. However, if poultry meat contaminated with Salmonella were cooked incompletely, Salmonella remained on the food surface. The risk of foodborne Salmonella disease from poultry consumption after cooking was 3.0 × 10⁻¹⁰/person/day and 8.8 × 10⁻¹¹/person/day in South Korea, indicating a low risk. Full article

(This article belongs to the Special Issue Advanced Research in Foodborne Microorganisms: Detection, Control, Risk Assessment and Prevention Volume II)

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16 pages, 912 KiB

Open AccessEditor’s ChoiceArticle

Quality of Tenebrio molitor Powders: Effects of Four Processes on Microbiological Quality and Physicochemical Factors

by Xin Yan, Sophie Laurent, Isabelle Hue, Sylvie Cabon, Joelle Grua-Priol, Vanessa Jury, Michel Federighi and Geraldine Boué

Foods 2023, 12(3), 572; https://doi.org/10.3390/foods12030572 - 28 Jan 2023

Cited by 8 | Viewed by 3563

Abstract

Tenebrio molitor, the first edible insect approved as a novel food in the EU, is a promising candidate for alternative protein sources, implementing circular and sustainable production systems. This study aims to determine the microbiological quality and physicochemical properties of mealworm powders obtained by four different processing pathways. Contents of dry matter, protein, fat, ash, water activity (aw) and a range of microbial counts were measured and analyzed by one-way ANOVA with Tukey’s test. Results showed small differences in the proximate composition of the powder samples (protein 55.62–57.90% and fat 23.63–28.21% of dry matter, DM), except for the one that underwent a defatting step (protein 70.04% and fat 16.84%), p < 0.05. A level of water activity of less than 0.2 was reached for all pathways. Fresh mealworm samples had high total aerobic counts (8.4 log CFU/g) but were free of foodborne pathogens. Heat treatments applied during transformation were sufficient to kill vegetative cells (reduction of 2.8–5.1 log CFU/g) rather than bacterial endospores (reduction of 0.3–1.8 log CFU/g). Results were confirmed by predictive microbiology. This study validated the efficacy of a boiling step as critical control points (CCPs) of insect powder processing, providing primary data for the implementation of HACCP plans. Full article

(This article belongs to the Special Issue Advanced Research in Foodborne Microorganisms: Detection, Control, Risk Assessment and Prevention Volume II)

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15 pages, 1913 KiB

Open AccessArticle

Identification of Genetic Markers for the Detection of Bacillus thuringiensis Strains of Interest for Food Safety

by Arnaud Fichant, Arnaud Felten, Armel Gallet, Olivier Firmesse and Mathilde Bonis

Foods 2022, 11(23), 3924; https://doi.org/10.3390/foods11233924 - 5 Dec 2022

Cited by 2 | Viewed by 2500

Abstract

Bacillus thuringiensis (Bt), belonging to the Bacillus cereus (Bc) group, is commonly used as a biopesticide worldwide due to its ability to produce insecticidal crystals during sporulation. The use of Bt, especially subspecies aizawai and kurstaki, to control pests such as Lepidoptera, generally involves spraying mixtures containing spores and crystals on crops intended for human consumption. Recent studies have suggested that the consumption of commercial Bt strains may be responsible for foodborne outbreaks (FBOs). However, its genetic proximity to Bc strains has hindered the development of routine tests to discriminate Bt from other Bc, especially Bacillus cereus sensu stricto (Bc ss), well known for its involvement in FBOs. Here, to develop tools for the detection and the discrimination of Bt in food, we carried out a genome-wide association study (GWAS) on 286 complete genomes of Bc group strains to identify and validate in silico new molecular markers specific to different Bt subtypes. The analyses led to the determination and the in silico validation of 128 molecular markers specific to Bt, its subspecies aizawai, kurstaki and four previously described proximity clusters associated with these subspecies. We developed a command line tool based on a 14-marker workflow, to carry out a computational search for Bt-related markers from a putative Bc genome, thereby facilitating the detection of Bt of interest for food safety, especially in the context of FBOs. Full article

(This article belongs to the Special Issue Advanced Research in Foodborne Microorganisms: Detection, Control, Risk Assessment and Prevention Volume II)

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13 pages, 3320 KiB

Open AccessArticle

Studies on Simultaneous Enrichment and Detection of Escherichia coli O157:H7 during Sample Shipment

by Chuyan Chen, Claudia P. Coronel-Aguilera, Bruce M. Applegate, Andrew G. Gehring, Arun K. Bhunia and George C. Paoli

Foods 2022, 11(22), 3653; https://doi.org/10.3390/foods11223653 - 15 Nov 2022

Cited by 3 | Viewed by 3529

Abstract

The USDA-FSIS has zero tolerance for E. coli O157:H7 in raw ground beef. Currently, FSIS collects samples from beef processing facilities and ships them overnight to regional testing laboratories. Pathogen detection requires robust methods that employ an initial 15–24 h culture enrichment. This study assessed the potential of using the ΦV10nluc phage-based luminescence detection assay during enrichment while the sample is in transit. Parameters including phage concentrations, temperature, and media-to-sample ratios were evaluated. Results in liquid media showed that 1.73× 10³ pfu/mL of ΦV10nluc was able to detect 2 CFU in 10 h. The detection of E. coli O157:H7 was further evaluated in kinetic studies using ratios of 1:3, 1:2, and 1:1 ground beef sample to enrichment media, yielding positive results for as little as 2–3 CFU in 325 g ground beef in about 15 h at 37 °C. These results suggest that this approach is feasible, allowing the detection of a presumptive positive upon arrival of the sample to the testing lab. As the current cargo hold controlled temperature is required to be 15–25 °C, the need for elevated temperature should be easily addressed. If successful, this approach could be expanded to other pathogens and foods. Full article

(This article belongs to the Special Issue Advanced Research in Foodborne Microorganisms: Detection, Control, Risk Assessment and Prevention Volume II)

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12 pages, 1646 KiB

Open AccessArticle

Palmatine Inhibits the Pathogenicity of Aeromonas hydrophila by Reducing Aerolysin Expression

by Jing Dong, Tianhui Yan, Qiuhong Yang, Yi Song, Bo Cheng, Shun Zhou, Yongtao Liu and Xiaohui Ai

Foods 2022, 11(20), 3250; https://doi.org/10.3390/foods11203250 - 18 Oct 2022

Cited by 4 | Viewed by 2046

Abstract

Aeromonas hydrophila, an opportunistic aquatic pathogen widely spread in aquatic environments, is responsible for a number of infectious diseases in freshwater aquaculture. In addition, A. hydrophila can transmit from diseased fish to humans and results in health problems. The occurrence of antibiotic-resistant bacterial strains restricts the application of antibiotics and is responsible for failure of the treatment. Moreover, residues of antibiotics in aquatic products often threaten the quality and safety. Therefore, alternative strategies are called to deal with infections caused by antibiotic-resistant bacteria. Aerolysin, one of the most important virulence factors of A. hydrophila, is adopted as a unique anti-virulence target on the basis of the anti-virulence strategy to battling infections caused by A. hydrophila. Palmatine, an isoquinoline alkaloid from a variety of herbal medicines that showed no anti-A. hydrophila activity, could reduce hemolysis of the bacterium by decreasing aerolysin production. The results of the qPCR assay demonstrated that the transcription of the aerA gene was suppressed. Moreover, cell viability and in vivo study showed that palmatine treatment could decrease the pathogenicity of A. hydrophila both in vitro and in vivo. In summary, palmatine is a leading compound against A. hydrophila-associated infection in aquaculture by inhibiting the expression of aerolysin. Full article

(This article belongs to the Special Issue Advanced Research in Foodborne Microorganisms: Detection, Control, Risk Assessment and Prevention Volume II)

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16 pages, 1756 KiB

Open AccessArticle

Biofilm Formation of Listeria monocytogenes and Pseudomonas aeruginosa in a Simulated Chicken Processing Environment

by Qingli Dong, Linjun Sun, Taisong Fang, Yuan Wang, Zhuosi Li, Xiang Wang, Mengjie Wu and Hongzhi Zhang

Foods 2022, 11(13), 1917; https://doi.org/10.3390/foods11131917 - 28 Jun 2022

Cited by 11 | Viewed by 3103

Abstract

This study aims to investigate the mono- and dual-species biofilm formation of Listeria monocytogenes and Pseudomonas aeruginosa incubated in different culture mediums, inoculum ratios, and incubation time. The planktonic cell population and motility were examined to understand the correlation with biofilm formation. The results showed that chicken juice significantly inhibited the biofilm formation of L. monocytogenes (p < 0.05). Pseudomonas aeruginosa was the dominant bacteria in the dual-species biofilm formation in the trypticase soy broth medium. The dynamic changes in biofilm formation were not consistent with the different culture conditions. The growth of planktonic L. monocytogenes and P. aeruginosa in the suspension was inconsistent with their growth in the biofilms. There was no significant correlation between motility and biofilm formation of L. monocytogenes and P. aeruginosa. Moreover, scanning electron microscopy (SEM) results revealed that the biofilm structure of L. monocytogenes was loose. At the same time, P. aeruginosa formed a relatively dense network in mono-species biofilms in an initial adhesion stage (24 h). SEM results also showed that P. aeruginosa was dominant in the dual-species biofilms. Overall, these results could provide a theoretical reference for preventing and controlling the biofilm formation of L. monocytogenes and P. aeruginosa in the food processing environment in the future. Full article

(This article belongs to the Special Issue Advanced Research in Foodborne Microorganisms: Detection, Control, Risk Assessment and Prevention Volume II)

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13 pages, 2182 KiB

Open AccessArticle

A Bayesian Approach to Describe and Simulate the pH Evolution of Fresh Meat Products Depending on the Preservation Conditions

by Ngoc-Du Martin Luong, Louis Coroller, Monique Zagorec, Nicolas Moriceau, Valérie Anthoine, Sandrine Guillou and Jeanne-Marie Membré

Foods 2022, 11(8), 1114; https://doi.org/10.3390/foods11081114 - 13 Apr 2022

Cited by 7 | Viewed by 3091

Abstract

Measuring the pH of meat products during storage represents an efficient way to monitor microbial spoilage, since pH is often linked to the growth of several spoilage-associated microorganisms under different conditions. The present work aimed to develop a modelling approach to describe and simulate the pH evolution of fresh meat products, depending on the preservation conditions. The measurement of pH on fresh poultry sausages, made with several lactate formulations and packed under three modified atmospheres (MAP), from several industrial production batches, was used as case-study. A hierarchical Bayesian approach was developed to better adjust kinetic models while handling a low number of measurement points. The pH changes were described as a two-phase evolution, with a first decreasing phase followed by a stabilisation phase. This stabilisation likely took place around the 13th day of storage, under all the considered lactate and MAP conditions. The effects of lactate and MAP on pH previously observed were confirmed herein: (i) lactate addition notably slowed down acidification, regardless of the packaging, whereas (ii) the 50%CO₂-50%N₂ MAP accelerated the acidification phase. The Bayesian modelling workflow—and the script—could be used for further model adaptation for the pH of other food products and/or other preservation strategies. Full article

(This article belongs to the Special Issue Advanced Research in Foodborne Microorganisms: Detection, Control, Risk Assessment and Prevention Volume II)

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Review

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25 pages, 844 KiB

Open AccessReview

Physical Treatments to Control Clostridium botulinum Hazards in Food

by Muhammad Tanveer Munir, Narjes Mtimet, Laurent Guillier, François Meurens, Phillipe Fravalo, Michel Federighi and Pauline Kooh

Foods 2023, 12(8), 1580; https://doi.org/10.3390/foods12081580 - 7 Apr 2023

Cited by 10 | Viewed by 7555

Abstract

Clostridium botulinum produces Botulinum neurotoxins (BoNTs), causing a rare but potentially deadly type of food poisoning called foodborne botulism. This review aims to provide information on the bacterium, spores, toxins, and botulisms, and describe the use of physical treatments (e.g., heating, pressure, irradiation, and other emerging technologies) to control this biological hazard in food. As the spores of this bacterium can resist various harsh environmental conditions, such as high temperatures, the thermal inactivation of 12-log of C. botulinum type A spores remains the standard for the commercial sterilization of food products. However, recent advancements in non-thermal physical treatments present an alternative to thermal sterilization with some limitations. Low- (<2 kGy) and medium (3–5 kGy)-dose ionizing irradiations are effective for a log reduction of vegetative cells and spores, respectively; however, very high doses (>10 kGy) are required to inactivate BoNTs. High-pressure processing (HPP), even at 1.5 GPa, does not inactivate the spores and requires heat combination to achieve its goal. Other emerging technologies have also shown some promise against vegetative cells and spores; however, their application to C. botulinum is very limited. Various factors related to bacteria (e.g., vegetative stage, growth conditions, injury status, type of bacteria, etc.) food matrix (e.g., compositions, state, pH, temperature, aw, etc.), and the method (e.g., power, energy, frequency, distance from the source to target, etc.) influence the efficacy of these treatments against C. botulinum. Moreover, the mode of action of different physical technologies is different, which provides an opportunity to combine different physical treatment methods in order to achieve additive and/or synergistic effects. This review is intended to guide the decision-makers, researchers, and educators in using physical treatments to control C. botulinum hazards. Full article

(This article belongs to the Special Issue Advanced Research in Foodborne Microorganisms: Detection, Control, Risk Assessment and Prevention Volume II)

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