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Foodborne Pathogens: Detection Methods, Food Safety, and Public Health

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A special issue of Microorganisms (ISSN 2076-2607). This special issue belongs to the section "Food Microbiology".

Deadline for manuscript submissions: closed (30 November 2022) | Viewed by 23637

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Prof. Dr. Abiodun Adewale Adesiyun

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Guest Editor

Department of Production Animal Studies, University of Pretoria, Private Bag X 04, Onderstepoort, Pretoria 0110, South Africa
Interests: veterinary public health; food safety; veterinary microbiology; zoonoses; epidemiology; research
Special Issues, Collections and Topics in MDPI journals

Special Issue Information

Dear Colleagues,

For decades, foodborne pathogens have been responsible for cases or outbreaks of disease in humans, some with high morbidities or case fatality rates. These pathogens include viruses, bacteria, and parasites. The spectrum of pathogens, the frequency of occurrence, and the severity of illnesses they cause vary by food types, eating habits, sanitary practices at retail outlets and public eating outlets, and home kitchens.

In this Special Issue, we plan to highlight the involvements of pathogens such as non-typhoidal Salmonella, Clostridium perfringens, Staphylococcus aureus, Campylobacter spp., Shiga-toxin producing Escherichia coli (STEC) and other E. coli, Listeria monocytogenes, Norovirus, Hepatitis A, Toxoplasma gondii, Cyclospora cayetanensis, among others. An objective of this Special Issue is to present articles that relate the occurrence of these pathogens in foods (raw, minimally processed, ultra-processed, and ready-to-eat) in developing and developed economies to practices that contribute to their survival, multiplication, and entry into the human food chain.

The detection of pathogens in foods is vital in determining and assessing the risk they pose to consumers. This Special Issue is interested in receiving articles on detection methods (conventional/traditional and molecular) of these foodborne pathogens with an emphasis on the comparative sensitivity, specificity, accuracy, and application of these methods. In addition, it is important to know the attributes (toxin, virulence genes, etc.) of these organisms that contribute to their pathogenicity and virulence.

Finally, the Special Issue will entertain studies that provide a link between food safety (preparation, handling, and storage of foods to prevent human exposure to illness) and public health through the farm-to-fork approach.

Prof. Dr. Abiodun Adewale Adesiyun
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. Microorganisms is an international peer-reviewed open access monthly 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 2700 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

foodborne pathogens
bacteria
viruses
parasites
detection methods
virulence
pathogenicity
food safety
public health

Published Papers (10 papers)

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Research

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10 pages, 2063 KiB

Open AccessCommunication

Study on the Effect of Relaying on Norovirus Reduction from Crassostrea gigas Oysters

by Roberta Battistini, Chiara Masotti, Cristiana Maurella, Erica Costa, Mino Orlandi, Mirvana Feletti, Carlo Ercolini and Laura Serracca

Microorganisms 2022, 10(12), 2389; https://doi.org/10.3390/microorganisms10122389 - 1 Dec 2022

Cited by 1 | Viewed by 1745

Abstract

Norovirus (NoV) is the most important cause of seafood-borne gastroenteritis worldwide, mainly associated with the consumption of raw oysters. NoV is often present in oysters that comply with existing control standards for shellfish. Therefore, the improvement of post-harvest treatments and practices can represent one of the main strategies to reduce the incidence of viral diseases related to shellfish. This study aimed to investigate long-term relays for the reduction of NoV levels in live oysters, during the high-risk cold months, by transferring the oysters from a more contaminated site to two sites with lower NoV levels. The efficacy of relaying was evaluated by analyzing oyster samples collected at days 0 (T0) and 30 (T30) for NoV levels using a real-time quantitative PCR (RT-qPCR). The NoV level at the relay sites was consistently lower than at the harvest site. The relay process for 30 days in seawater with a lower NoV level resulted in a decrease in the NoV load compared to day 0 with significant reductions depending on the site and genogroup of NoV considered. These results suggest that long-term relaying of oysters to reduce NoV levels is promising and could help growers to improve oyster safety; however, further investigations are needed. Full article

(This article belongs to the Special Issue Foodborne Pathogens: Detection Methods, Food Safety, and Public Health)

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15 pages, 1964 KiB

Open AccessArticle

Evaluation of Various Lactic Acid Bacteria and Generic E. coli as Potential Nonpathogenic Surrogates for In-Plant Validation of Biltong Dried Beef Processing

by Caitlin E. Karolenko, Jade Wilkinson and Peter M. Muriana

Microorganisms 2022, 10(8), 1648; https://doi.org/10.3390/microorganisms10081648 - 15 Aug 2022

Cited by 2 | Viewed by 1936

Abstract

Validation studies conducted within a food processing facility using surrogate organisms could better represent the manufacturing process than controlled laboratory studies with pathogenic bacteria on precision equipment in a BSL-2 lab. The objectives of this project were to examine potential surrogate bacteria during biltong processing, conduct biltong surrogate validation lethality studies, and measure critical factors and intrinsic parameters during processing. Beef pieces (1.9 cm × 5.1 cm × 7.6 cm) were inoculated with four-strain mixtures of Carnobacterium divergens/C. gallinarum, Pediococcus acidilactici/P. pentosaceous, and Biotype 1 E. coli ATCC BAA (-1427, -1428, -1429, and -1430), as well as a two-strain mixture of Latilactobacillus sakei and other commercially available individual bacterial cultures (P. acidilactici Saga200/Kerry Foods; Enterococcus faecium 201224-016/Vivolac Cultures). Inoculated beef was vacuum-tumbled in marinade and dried in a humidity-controlled oven for 8–10 days (24.9 °C; 55% relative humidity). Microbial enumeration of surviving surrogate bacteria and evaluation of intrinsic factors (water activity, pH, and salt concentration) were performed post inoculation, post marination, and after 2, 4, 6, 8, and 10 days of drying. Trials were performed in duplicate replication with triplicate samples per sampling time and analyzed by one-way RM-ANOVA. Trials conducted with E. faecium, Pediococcus spp., and L. sakei never demonstrated more than 2 log reduction during the biltong process. However, Carnobacterium achieved a >5 log (5.85 log) reduction over a drying period of 8 days and aligned with the reductions observed in previous trials with pathogenic bacteria (Salmonella, E. coli O157:H7, L. monocytogenes, and S. aureus) in biltong validation studies. Studies comparing resuspended freeze-dried or frozen cells vs. freshly grown cells for beef inoculation showed no significant differences during biltong processing. Carnobacterium spp. would be an effective nonpathogenic in-plant surrogate to monitor microbial safety that mimics the response of pathogenic bacteria to validate biltong processing within a manufacturer’s own facility. Full article

(This article belongs to the Special Issue Foodborne Pathogens: Detection Methods, Food Safety, and Public Health)

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11 pages, 503 KiB

Open AccessArticle

Detection of Foodborne Pathogens in Acute Gastroenteritis Patient’s Stool Samples Using the BioFire^® FilmArray^® Gastrointestinal PCR Panel in the Republic of Trinidad and Tobago, West Indies

by Carelene Lakhan, Neela Badrie, Adash Ramsubhag and Lisa Indar

Microorganisms 2022, 10(8), 1601; https://doi.org/10.3390/microorganisms10081601 - 9 Aug 2022

Cited by 4 | Viewed by 2208

Abstract

In 2009, the burden of illness study for acute gastroenteritis in Trinidad and Tobago highlighted that ~10% of stool samples tested were positive for a foodborne pathogen. The study also noted that limited laboratory screening for pathogens contributed to a lack of etiology as public health hospitals only routinely tested for Salmonella and Shigella, and sometimes for Escherichia coli and Campylobacter. To better understand the foodborne pathogens responsible for acute gastroenteritis, enhanced testing using the BioFire^® FilmArray^® Gastrointestinal PCR panel was used to screen diarrheal stool samples for 22 pathogens from patients in 2018. The five general public health hospitals (San Fernando, Mt. Hope, Port of Spain, Sangre Grande, and Tobago) were notified of research activities and diarrheal stool samples were collected from all acute gastroenteritis patients. A total of 66 stools were screened and ~30% of samples tested positive for a foodborne pathogen. The current study showed that a much wider range of enteric pathogens were associated with acute gastroenteritis in Trinidad and Tobago than previously reported in 2009. These findings can be used by health officials to guide appropriate interventions, as well as to provide evidence for adoption of the PCR panel detection method at public health hospitals to benefit patient care. Full article

(This article belongs to the Special Issue Foodborne Pathogens: Detection Methods, Food Safety, and Public Health)

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16 pages, 6875 KiB

Open AccessArticle

Effect of Biltong Dried Beef Processing on the Reduction of Listeria monocytogenes, E. coli O157:H7, and Staphylococcus aureus, and the Contribution of the Major Marinade Components

by Kavya Gavai, Caitlin Karolenko and Peter M. Muriana

Microorganisms 2022, 10(7), 1308; https://doi.org/10.3390/microorganisms10071308 - 28 Jun 2022

Cited by 5 | Viewed by 2479

Abstract

Biltong is a dry beef product that is manufactured without a heat lethality step, raising concerns of whether effective microbial pathogen reduction can occur during biltong processing. Raw beef inoculated with 4-strain cocktails of either E. coli O157:H7, Listeria monocytogenes, or Staphylococcus aureus, and processed with a standard biltong process, were shown to incur a >5-log reduction in 6–8 days after marination by vacuum-tumbling for 30 min in vinegar, salt, spices (coriander, pepper) when dried at 23.9 °C (75 °F) at 55% relative humidity (RH). Pathogenic challenge strains were acid-adapted in media containing 1% glucose to ensure that the process was sufficiently robust to inhibit acid tolerant strains. Internal water activity (A_w) reached < 0.85 at 5-log reduction levels, ensuring that conditions were lower than that which would support bacterial growth, or toxin production by S. aureus should it be internalized during vacuum tumbling. This was further confirmed by ELISA testing for staphylococcal enterotoxins A and B (SEA, SEB) after marination and again after 10 days of drying whereby levels were lower than initial post-marination levels. Comparison of log reduction curves obtained for E. coli O157:H7, L. monocytogenes, S. aureus, and Salmonella (prior study) showed that microbial reduction was not significantly different (p < 0.05) demonstrating that even without a heat lethality step, the biltong process we examined produces a safe beef product according to USDA-FSIS guidelines. Full article

(This article belongs to the Special Issue Foodborne Pathogens: Detection Methods, Food Safety, and Public Health)

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8 pages, 1495 KiB

Open AccessArticle

Genomic Characterization of Escherichia coli O8 Strains Producing Shiga Toxin 2l Subtype

by Xi Yang, Qian Liu, Hui Sun, Yanwen Xiong, Andreas Matussek and Xiangning Bai

Microorganisms 2022, 10(6), 1245; https://doi.org/10.3390/microorganisms10061245 - 17 Jun 2022

Cited by 5 | Viewed by 1843

Abstract

Shiga toxin-producing Escherichia coli (STEC) can cause diseases ranging from mild diarrhea to fatal extra-intestinal hemolytic uremic syndrome (HUS). Shiga toxin (Stx) is the key virulence factor in STEC, two Stx types (Stx1 and Stx2) and several subtypes varying in sequences, toxicity, and host specificity have been identified. Stx2l is a newly-designated subtype related to human disease but lacks thorough characterization. Here, we identified Stx2l from five STEC strains (Stx2l-STECs) recovered from raw mutton and beef in China. Whole-genome sequencing (WGS) was used to characterize the Stx2l-STECs in this study together with Stx2l-STECs retrieved from public databases. Our study revealed that all the analyzed Stx2l-STEC strains belonged to the same serogroup O8. Multilocus sequencing typing (MLST) showed two sequence types (ST88 and ST23) among these strains. Stx2l-converting prophages from different sources shared a highly similar structure and sequence. Single-nucleotide polymorphism (SNP)-based analysis revealed genetic relatedness between the human-derived and food-derived strains belonging to ST23. To conclude, our study supported the designation of Stx2l and demonstrated diverse host range and geographical distribution of Stx2l-STECs.Stx2l-STEC strains from different sources showed a high genetic similarity with an identical O8 serogroup. Further studies are needed to investigate the epidemiological trait and pathogenic potential of Stx2l-STEC strains. Full article

(This article belongs to the Special Issue Foodborne Pathogens: Detection Methods, Food Safety, and Public Health)

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13 pages, 1368 KiB

Open AccessArticle

Antimicrobial Resistance, Enterotoxin and mec Gene Profiles of Staphylococcus aureus Associated with Beef-Based Protein Sources from KwaZulu-Natal Province, South Africa

by Thembeka Thwala, Evelyn Madoroba, Tsolanku S. Maliehe, Kudakwashe Magwedere, Albert K. Basson and Patrick Butaye

Microorganisms 2022, 10(6), 1211; https://doi.org/10.3390/microorganisms10061211 - 14 Jun 2022

Cited by 5 | Viewed by 1826

Abstract

Annually, approximately 23,000 cases of food poisoning by Staphylococcus aureus enterotoxins are reported worldwide. The aim of this study was to determine the occurrence and characterize S. aureus on beef and beef products in South Africa. Organ meats (n = 169), raw processed meat (n = 110), raw intact (n = 53), and ready-to-eat meats (n = 68) were obtained from 25 retail outlets. S. aureus was isolated and enumerated according to the ISO 6888-1 method. Identification of the strains was performed by MALDI-TOF MS. The antimicrobial resistance was determined using the disc diffusion test. The presence of methicillin-resistance genes and the staphylococcal enterotoxin genes was determined by PCR. Prevalence was low (13/400; CI 1.7–5) and all but one positive sample were from organ meats. Eight isolates were resistant to at least one antibiotic. Two isolates carried the mecC gene. All the isolates tested positive for seg, seh, sei, and sep, whilst 53.8% were positive for sea. None of the isolates was positive for ser, sej, seb, sec, or sed. The prevalence of S. aureus was low, with organ meats being the most contaminated. The presence of mecC-positive MRSA and of enterotoxins warrants further investigation and risk assessment. Full article

(This article belongs to the Special Issue Foodborne Pathogens: Detection Methods, Food Safety, and Public Health)

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8 pages, 784 KiB

Open AccessCommunication

Food Is Reservoir of MDR Salmonella: Prevalence of ESBLs Profiles and Resistance Genes in Strains Isolated from Food

by Delia Gambino, Valeria Gargano, Gaspare Butera, Sonia Sciortino, Mariangela Pizzo, Giuseppa Oliveri, Cinzia Cardamone, Chiara Piraino, Giovanni Cassata, Domenico Vicari and Antonella Costa

Microorganisms 2022, 10(4), 780; https://doi.org/10.3390/microorganisms10040780 - 6 Apr 2022

Cited by 10 | Viewed by 1776

Abstract

Salmonella spp. are among the most frequent causes of foodborne diseases, and the increasing occurrence of MDR strains is an additional cause for concern. In the three-year period 2019–2021, we collected Salmonella spp. strains isolated from different food categories analysed in the context of Regulation (EC) No 2073/2005 in order to assess their antibiotic susceptibility profiles and ESBL production. To determine the susceptibility profiles and identify MDR strains, we used the Kirby–Bauer method to test 17 antibiotics. Double-disc and PCR testing then allowed us to assess the production of ESBLs and the presence of beta-lactamase resistance genes. Phenotypic tests showed that 36 out of 67 strains were MDR and 52.7% of these were ESBL producers. Finally, molecular investigations conducted on ESBL-producing strains revealed the presence of bla_SHV, bla_CTX-M and bla_TEM genes. Our results confirmed the prevalence of S. Infantis, an MDR strain and ESBL producer, in chicken meat. This suggests that further research on the prevalence of antibiotic resistance genes (ARGs) in foodborne strains is needed, especially from a One Health perspective. Full article

(This article belongs to the Special Issue Foodborne Pathogens: Detection Methods, Food Safety, and Public Health)

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9 pages, 263 KiB

Open AccessCommunication

Identification and Subtyping of Salmonella Isolates Using Matrix-Assisted Laser Desorption–Ionization Time-of-Flight Mass Spectrometry (MALDI-TOF)

by Anil K. Persad, Hanan A. Fahmy, Nicholas Anderson, Jing Cui, Zeynal Topalcengiz, Saharuetai Jeamsripong, Patrick M. Spanninger, Robert L. Buchanan, Kalmia E. Kniel, Michele T. Jay-Russell, Michelle D. Danyluk, Gireesh Rajashekara and Jeffrey T. LeJeune

Microorganisms 2022, 10(4), 688; https://doi.org/10.3390/microorganisms10040688 - 23 Mar 2022

Cited by 4 | Viewed by 2567

Abstract

Subtyping of bacterial isolates of the same genus and species is an important tool in epidemiological investigations. A number of phenotypic and genotypic subtyping methods are available; however, most of these methods are labor-intensive and time-consuming and require considerable operator skill and a wealth of reagents. Matrix-Assisted Laser Desorption–Ionization Time-of-Flight Mass Spectrometry (MALDI-TOF), an alternative to conventional subtyping methods, offers a rapid, reproducible method for bacterial identification with a high sensitivity and specificity and at minimal cost. The purpose of this study was to determine the feasibility of using MALDI-TOF to differentiate between six Salmonella serovars recovered from experimental microcosms inoculated with known strains of Salmonella. Following the establishment of a MALDI-TOF reference library for this project, the identity of 843 Salmonella isolates recovered from these microcosms was assessed using both MALDI-TOF and conventional methods (serotyping/PCR). All 843 isolates were identified as being Salmonella species. Overall, 803/843 (95%) of these isolates were identified similarly using the two different methods. Positive percent agreement at the serovar level ranged from 79 to 100%, and negative percent agreement for all serovars was greater than 98%. Cohen’s kappa ranged from 0.85 to 0.98 for the different serovars. This study demonstrates that MALDI-TOF is a viable alternative for the rapid identification and differentiation of Salmonella serovars. Full article

(This article belongs to the Special Issue Foodborne Pathogens: Detection Methods, Food Safety, and Public Health)

18 pages, 698 KiB

Open AccessArticle

Molecular Characterization of Salmonella Detected along the Broiler Production Chain in Trinidad and Tobago

by Anisa Sarah Khan, Rian Ewald Pierneef, Narjol Gonzalez-Escalona, Meghan Maguire, Cong Li, Gregory H. Tyson, Sherry Ayers, Karla Georges, Woubit Abebe and Abiodun Adewale Adesiyun

Microorganisms 2022, 10(3), 570; https://doi.org/10.3390/microorganisms10030570 - 6 Mar 2022

Cited by 9 | Viewed by 2259

Abstract

This cross-sectional study determined the serovars, antimicrobial resistance genes, and virulence factors of Salmonella isolated from hatcheries, broiler farms, processing plants, and retail outlets in Trinidad and Tobago. Salmonella in silico serotyping detected 23 different serovars where Kentucky 20.5% (30/146), Javiana 19.2% (28/146), Infantis 13.7% (20/146), and Albany 8.9% (13/146) were the predominant serovars. There was a 76.0% (111/146) agreement between serotyping results using traditional conventional methods and whole-genome sequencing (WGS) in in silico analysis. In silico identification of antimicrobial resistance genes conferring resistance to aminoglycosides, cephalosporins, peptides, sulfonamides, and antiseptics were detected. Multidrug resistance (MDR) was detected in 6.8% (10/146) of the isolates of which 100% originated from broiler farms. Overall, virulence factors associated with secretion systems and fimbrial adherence determinants accounted for 69.3% (3091/4463), and 29.2% (1302/4463) counts, respectively. Ten of 20 isolates of serovar Infantis (50.0%) showed MDR and contained the bla_CTX-M-65 gene. This is the first molecular characterization of Salmonella isolates detected along the entire broiler production continuum in the Caribbean region using WGS. The availability of these genomes will help future source tracking during epidemiological investigations associated with Salmonella foodborne outbreaks in the region and worldwide. Full article

(This article belongs to the Special Issue Foodborne Pathogens: Detection Methods, Food Safety, and Public Health)

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Review

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16 pages, 374 KiB

Open AccessReview

Salmonella enterica Outbreaks Linked to the Consumption of Tahini and Tahini-Based Products

by Geneviève Coulombe and Sandeep Tamber

Microorganisms 2022, 10(11), 2299; https://doi.org/10.3390/microorganisms10112299 - 19 Nov 2022

Cited by 2 | Viewed by 3560

Abstract

Salmonella is a leading cause of bacterial foodborne illness in the world. Although typically associated with foods of animal origin, low-moisture foods, such as tahini, are quickly gaining recognition as an important vehicle of Salmonella exposure. This review offers the Canadian perspective on the issue of Salmonella in tahini and tahini-based products. A summary of several recent food product recalls and foodborne outbreaks related to the presence of Salmonella in tahini and tahini-based products such as halva are presented. The properties of the food vehicles, their production practices, and potential routes of contamination are discussed. Particular focus is placed on the ecology of Salmonella in the tahini production continuum, including its survival characteristics and response to intervention technologies. Full article

(This article belongs to the Special Issue Foodborne Pathogens: Detection Methods, Food Safety, and Public Health)

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