Foodborne Intoxications and Toxicoinfections—Major Pathogens and Challenges

A special issue of Toxins (ISSN 2072-6651). This special issue belongs to the section "Bacterial Toxins".

Deadline for manuscript submissions: closed (1 May 2022) | Viewed by 18514

Special Issue Editors


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Guest Editor
Institute for Food Safety and Hygiene, Vetsuisse Faculty, University of Zurich, Zurich, Switzerland
Interests: Food safety and hygiene; foodborne pathogens; microbial toxins; microbiology; microbial source tracking; novel diagnostic platforms

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Guest Editor
German Federal Institute for Risk Assessment (BfR), Department of Biological Safety Berlin, Berlin, Germany
Interests: Food Microbiology and Safety

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Guest Editor
Institute for Food, Nutrition and Health, Department of Health Sciences and Technology, ETH Zurich, Zurich, Switzerland
Interests: food microbiology; microbial toxins; gene regulation

Special Issue Information

Dear Colleagues,

Microbial organisms producing toxins encountered in food are a major threat to human health and lead to substantial economic losses. While toxins produced by organisms such as Staphylococcus, Bacillus and Clostridium have been the focus of scientific research for decades, major questions remain unanswered. For instance, the regulation of staphylococcal enterotoxins and the role of newly described staphylococcal enterotoxins is still poorly understood. In addition, major advances in whole genome sequencing have led to paradigm shifts and have amongst others initiated a collapse of traditional taxonomy-driven risk assessment in the Bacillus cereus group. Long-standing perceptions of the risk related to certain species have been questioned. While e.g. Bacillus thuringiensis and Clostridium difficile have been discussed as potential causative organisms in outbreaks, species traditionally exclusively associated with high toxicity such as Bacillus cytotoxicus have been shown to exhibit strong strain-specific variation in toxin production. Also, the food matrix itself has a strong impact on the formation and stability of toxins. The lack of accurate and robust high-throughput detection and characterization methods as well as the broad variety of food matrices has limited the data available to date – a situation that is further exacerbated by wide-spread underreporting.

The purpose of this Special Issue is to publish both original research and review articles allowing for an overview of the state of the art in this field.

Dr. Sophia Johler
Dr. Alexandra Fetsch
Dr. Danai Etter
Guest Editors

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Keywords

  • Staphylococcus
  • Bacillus
  • Clostridium
  • regulation of toxin formation
  • outbreak investigation
  • detection
  • risk assessment
  • food matrix
  • detection methods
  • toxicity

Published Papers (5 papers)

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Research

16 pages, 600 KiB  
Article
Detection of Enterotoxigenic Psychrotrophic Presumptive Bacillus cereus and Cereulide Producers in Food Products and Ingredients
by Jelena Jovanovic, Svitlana Tretiak, Katrien Begyn and Andreja Rajkovic
Toxins 2022, 14(4), 289; https://doi.org/10.3390/toxins14040289 - 16 Apr 2022
Cited by 4 | Viewed by 2930
Abstract
In the last decade, foodborne outbreaks and individual cases caused by bacterial toxins showed an increasing trend. The major contributors are enterotoxins and cereulide produced by Bacillus cereus, which can cause a diarrheal and emetic form of the disease, respectively. These diseases [...] Read more.
In the last decade, foodborne outbreaks and individual cases caused by bacterial toxins showed an increasing trend. The major contributors are enterotoxins and cereulide produced by Bacillus cereus, which can cause a diarrheal and emetic form of the disease, respectively. These diseases usually induce relatively mild symptoms; however, fatal cases have been reported. With the aim to detected potential toxin producers that are able to grow at refrigerator temperatures and subsequently produce cereulide, we screened the prevalence of enterotoxin and cereulide toxin gene carriers and the psychrotrophic capacity of presumptive B. cereus obtained from 250 food products (cereal products, including rice and seeds/pulses, dairy-based products, dried vegetables, mixed food, herbs, and spices). Of tested food products, 226/250 (90.4%) contained presumptive B. cereus, which communities were further tested for the presence of nheA, hblA, cytK-1, and ces genes. Food products were mainly contaminated with the nheA B. cereus carriers (77.9%), followed by hblA (64.8%), ces (23.2%), and cytK-1 (4.4%). Toxigenic B. cereus communities were further subjected to refrigerated (4 and 7 °C) and mild abuse temperatures (10 °C). Overall, 77% (94/121), 86% (104/121), and 100% (121/121) were able to grow at 4, 7, and 10 °C, respectively. Enterotoxin and cereulide potential producers were detected in 81% of psychrotrophic presumptive B. cereus. Toxin encoding genes nheA, hblA, and ces gene were found in 77.2, 55, and 11.7% of tested samples, respectively. None of the psychrotrophic presumptive B. cereus were carriers of the cytotoxin K-1 encoding gene (cytK-1). Nearly half of emetic psychrotrophic B. cereus were able to produce cereulide in optimal conditions. At 4 °C none of the examined psychrotrophs produced cereulide. The results of this research highlight the high prevalence of B. cereus and the omnipresence of toxin gene harboring presumptive B. cereus that can grow at refrigerator temperatures, with a focus on cereulide producers. Full article
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18 pages, 1084 KiB  
Article
Multiplex Detection of 24 Staphylococcal Enterotoxins in Culture Supernatant Using Liquid Chromatography Coupled to High-Resolution Mass Spectrometry
by Donatien Lefebvre, Kevin Blanco-Valle, Jacques-Antoine Hennekinne, Stéphanie Simon, François Fenaille, François Becher and Yacine Nia
Toxins 2022, 14(4), 249; https://doi.org/10.3390/toxins14040249 - 31 Mar 2022
Cited by 11 | Viewed by 5017
Abstract
Staphylococcal food poisoning outbreaks are caused by the ingestion of food contaminated with staphylococcal enterotoxins (SEs). Among the 27 SEs described in the literature to date, only a few can be detected using immuno-enzymatic-based methods that are strongly dependent on the availability of [...] Read more.
Staphylococcal food poisoning outbreaks are caused by the ingestion of food contaminated with staphylococcal enterotoxins (SEs). Among the 27 SEs described in the literature to date, only a few can be detected using immuno-enzymatic-based methods that are strongly dependent on the availability of antibodies. Liquid chromatography, coupled to high-resolution mass spectrometry (LC-HRMS), has, therefore, been put forward as a relevant complementary method, but only for the detection of a limited number of enterotoxins. In this work, LC-HRMS was developed for the detection and quantification of 24 SEs. A database of 93 specific signature peptides and LC-HRMS parameters was optimized using sequences from 24 SEs, including their 162 variants. A label-free quantification protocol was established to overcome the absence of calibration standards. The LC-HRMS method showed high performance in terms of specificity, sensitivity, and accuracy when applied to 49 enterotoxin-producing strains. SE concentrations measured depended on both SE type and the coagulase-positive staphylococci (CPS) strain. This study indicates that LC-MS is a relevant alternative and complementary tool to ELISA methods. The advantages of LC-MS clearly lie in both the multiplex analysis of a large number of SEs, and the automated analysis of a high number of samples. Full article
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13 pages, 1302 KiB  
Article
Impact of Phytochemicals on Viability and Cereulide Toxin Synthesis in Bacillus cereus Revealed by a Novel High-Throughput Method, Coupling an AlamarBlue-Based Assay with UPLC-MS/MS
by Markus Kranzler, Elrike Frenzel, Veronika Walser, Thomas F. Hofmann, Timo D. Stark and Monika Ehling-Schulz
Toxins 2021, 13(9), 672; https://doi.org/10.3390/toxins13090672 - 21 Sep 2021
Cited by 2 | Viewed by 3181
Abstract
Due to its food-poisoning potential, Bacillus cereus has attracted the attention of the food industry. The cereulide-toxin-producing subgroup is of particular concern, as cereulide toxin is implicated in broadscale food-borne outbreaks and occasionally causes fatalities. The health risks associated with long-term cereulide exposure [...] Read more.
Due to its food-poisoning potential, Bacillus cereus has attracted the attention of the food industry. The cereulide-toxin-producing subgroup is of particular concern, as cereulide toxin is implicated in broadscale food-borne outbreaks and occasionally causes fatalities. The health risks associated with long-term cereulide exposure at low doses remain largely unexplored. Natural substances, such as plant-based secondary metabolites, are widely known for their effective antibacterial potential, which makes them promising as ingredients in food and also as a surrogate for antibiotics. In this work, we tested a range of structurally related phytochemicals, including benzene derivatives, monoterpenes, hydroxycinnamic acid derivatives and vitamins, for their inhibitory effects on the growth of B. cereus and the production of cereulide toxin. For this purpose, we developed a high-throughput, small-scale method which allowed us to analyze B. cereus survival and cereulide production simultaneously in one workflow by coupling an AlamarBlue-based viability assay with ultraperformance liquid chromatography–mass spectrometry (UPLC-MS/MS). This combinatory method allowed us to identify not only phytochemicals with high antibacterial potential, but also ones specifically eradicating cereulide biosynthesis already at very low concentrations, such as gingerol and curcumin. Full article
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7 pages, 552 KiB  
Communication
Distribution of the Emetic Toxin Cereulide in Cow Milk
by Veronika Walser, Markus Kranzler, Corinna Dawid, Monika Ehling-Schulz, Timo D. Stark and Thomas F. Hofmann
Toxins 2021, 13(8), 528; https://doi.org/10.3390/toxins13080528 - 28 Jul 2021
Cited by 5 | Viewed by 2601
Abstract
Bacillus cereus is frequently associated with food-borne intoxications, and its emetic toxin cereulide causes emesis and nausea after consumption of contaminated foods. The major source for contamination is found within contaminated raw materials containing the highly chemically resistant cereulide, independent of vegetative bacteria [...] Read more.
Bacillus cereus is frequently associated with food-borne intoxications, and its emetic toxin cereulide causes emesis and nausea after consumption of contaminated foods. The major source for contamination is found within contaminated raw materials containing the highly chemically resistant cereulide, independent of vegetative bacteria cells. Up to date, non-existing removal strategies for cereulide evoke the question of how the toxin is distributed within a food sample, especially cow milk. Milk samples with different milk fat contents were incubated with purified cereulide, separated by centrifugation into a lipid and an aqueous phase, and cereulide was quantified in both fractions by SIDA-LC-MS/MS. By artificially increasing the milk fat content from 0.5% to 50%, the amount of cereulide recovered in the lipid phase and could be augmented from 13.3 to 78.6%. Further, the ratio of cereulide increased in the lipid phase of milk with additional plant-based lipid (sunflower oil) to 47.8%. This demonstrated a clear affinity of cereulide towards the hydrophobic, lipid phase, aligning with cereulide’s naturally strong hydrophobic properties. Therefore, an intensified cereulide analysis of lipid enriched dairy products to prevent severe cereulide intoxications or cross-contamination in processed foods is suggested. Full article
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7 pages, 276 KiB  
Communication
Further Insights into the Toxicity of Bacillus cytotoxicus Based on Toxin Gene Profiling and Vero Cell Cytotoxicity Assays
by Johanna Burtscher, Danai Etter, Michael Biggel, Janine Schlaepfer and Sophia Johler
Toxins 2021, 13(4), 234; https://doi.org/10.3390/toxins13040234 - 24 Mar 2021
Cited by 8 | Viewed by 2889
Abstract
Bacillus cytotoxicus belongs to the Bacillus cereus group that also comprises the foodborne pathogen Bacillus cereus sensu stricto, Bacillus anthracis causing anthrax, as well as the biopesticide Bacillus thuringiensis. The first B. cytotoxicus was isolated in the context of a severe food [...] Read more.
Bacillus cytotoxicus belongs to the Bacillus cereus group that also comprises the foodborne pathogen Bacillus cereus sensu stricto, Bacillus anthracis causing anthrax, as well as the biopesticide Bacillus thuringiensis. The first B. cytotoxicus was isolated in the context of a severe food poisoning outbreak leading to fatal cases of diarrheal disease. Subsequent characterization of the outbreak strain led to the conclusion that this Bacillus strain was highly cytotoxic and eventually resulted in the description of a novel species, whose name reflects the observed toxicity: B. cytotoxicus. However, only a few isolates of this species have been characterized with regard to their cytotoxic potential and the role of B. cytotoxicus as a causative agent of food poisoning remains largely unclear. Hence, the aim of this study was to gain further insights into the toxicity of B. cytotoxicus. To this end, 19 isolates were obtained from mashed potato powders and characterized by toxin gene profiling and Vero cell cytotoxicity assays. All isolates harbored the cytK1 (cytotoxin K1) gene and species-specific variants of the nhe (non-hemolytic enterotoxin) gene. The isolates exhibited low or no toxicity towards Vero cells. Thus, this study indicates that the cytotoxic potential of B. cytotoxicus may be potentially lower than initially assumed. Full article
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