Foodborne Pathogens Management: From Farm and Pond to Fork

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

Deadline for manuscript submissions: closed (15 November 2022) | Viewed by 75911

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Institute of Food Safety, Food Technology and Veterinary Public Health, Unit of Food Hygiene and Technology, University of Veterinary Medicine, Vienna, Veterinärplatz 1, A-1210 Wien, Austria
Interests: meat; risk analytical aspects of food hygiene

Special Issue Information

Dear Colleagues,

In the 1930s, the US food microbiologist Samuel Cate Prescott (1872–1962), his Swiss colleague Karl Friedrich Meyer (1884–1974), and the UK microbiologist Sir Graham Selby Wilson (1895–1987) first suggested to follow a more active intervention strategy against food-transmitted diseases of microbial aetiology. In the early 1960s, the US National Aeronautics and Space Administration (NASA) introduced the basics of a novel food safety assurance system (Ross-Nazal, 2007), which evolved, in the 1970s, into the Hazard Analysis Critical Control Point (HACCP) concept (Lachance, 1997; Weinroth et al., 2018).

Thus, the fundaments of the Longitudinally Integrated Safety Assurance (LISA) approach were created (Mossel, 1989). Over the past few decades, the latter concept has inspired many (veterinary) food microbiologists to stress the longitudinal character of this approach by suggesting more ‘jazzy’ terms such as: ‘From Conception to Consumption’, ‘From Production to Consumption’, ‘From Stable to Table’ and ‘From Farm to Fork’ (or variants such as ‘From Pond to Fork’ or ‘From Forest to Fork’ when one wants the reader to concentrate on particular foods such as fish or game). In essence, the researchers took the same path as epidemiologists would have taken when investigating outbreaks of foodborne disease, the only difference being that epidemiologists would follow the ‘top-down’ route, and scientists working to reveal a functioning LISA principle would take a ‘bottom-up’ direction in order to prevent conditions that would render food unsafe for consumption.

‘From Farm to Fork’ was recently chosen by European authorities as the title of a document released in May 2020. This document describes the declared EU policies aiming at reducing the environmental/climate impact of primary production, while at the same time ensuring fair economic returns for farmers and striving to meet the ‘Green Deal’ objectives—that is, achieving Sustainable Development Goals (SDGs) such as improving food security by reducing food loss and waste without impairing food safety. The big question is whether or not the resource footprints of future food production in terms of land, water, energy and resources will be within our common planetary boundaries (Steffen et al., 2015). This means that resolving conflicting goals will become a key challenge. A ‘Farm-to-Fork’ framework might be indispensable for meeting our future challenges in terms of food safety, security and sustainability (Hanning et al., 2012).

Obviously, this interpretation of ‘Farm to Fork’ goes far beyond its original purpose of stressing the longitudinal approach to safety assurance rather than the traditional end-product-oriented control of foods of animal origin.

This realisation might complicate the definition of the scope of this Special Issue. The reader should be aware that the Issue’s authors have been selected based on their familiarity with (the history of) food microbiology and longitudinal safety assurance, and that they represent the ‘thick of the action’ when food safety assurance decisions need to be made, albeit in a complex context. Consequently, this Special Issue’s Guest-Editor encourages contributions on the state of the art in longitudinal food safety assurance, with the ambition to contribute to the evidence-based trade-offs that our future food safety, security and sustainability necessitate.

References

Hanning, I.B., O’Bryan, C.A., Crandall, P.G., Ricke, S.C. (2012). Food Safety and Food Security. Nature Education Knowledge 3(10):9

Lachance, P.A. (1977). How HACCP started. Food Technol., 51:3

Mossel, D.A.A. (1989). Adequate protection of the public against food-transmitted diseases of microbial aetiology. Achievements and challenges half a century after the introduction of the Prescott-Meyer-Wilson strategy of active intervention. Int. J. Food Microbiol., 1989, Dec. 19 (4) 271-94 doi: 10.1016/0168-1605(89)90097-4.

Ross-Nazal, J. (2007). “From Farm to Fork”: how space food standards interpreted the food industry and changed food safety standards. Chapter 12, p 219-236. In:  Steven J. Dick, Roger D. Launius (Eds.): Societal impact of Space Flight, NASA History Division, Office of External Relations, SP-2007-4801.

Steffen, W.K., Richardson, K., Rockström, S.E., Cornell, S.E., Fetzer, I., Bennett, E.M., Biggs, R, Carpenter, S.R., de Vries, W., de Wit, C.A., Folke, C., Gerten, D., Heinke, J., Mace, G.M., Persson, L.M. Ramanathan, V., Reyers, B., Sörlin, S. (2015). Planetary boundaries: Guiding human development on a changing planet. Science 347: 736, 1259855, DOI: 10.1126/science 125985.

Weinroth, M.D. Belk, A.D., Belk, K.E. (2018). History, development and current status of food safety systems worldwide. Anim. Front. 2018 Aug 30;8(4):9-15. doi: 10.1093/af/vfy016. eCollection 2018 Oct.

Emer. Prof. Dr. Dr. h.c. Frans J.M. Smulders, DVM, PhD, Hon.Memb./Dipl. ECVPH
Guest Editor

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Keywords

  • food safety
  • food microbiology
  • risk management
  • Longitudinally Integrated Safety Assurance (LISA)
  • farm-to-fork
  • pond-to-fork
  • sustainable development goals

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Published Papers (19 papers)

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Research

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16 pages, 3188 KiB  
Article
Bacterial Skin Microbiota of Seabass from Aegean Fish Farms and Antibiotic Susceptibility of Psychrotrophic Pseudomonas
by Ali Aydin, Mert Sudagidan, Zhanylbubu Mamatova, Mediha Nur Zafer Yurt, Veli Cengiz Ozalp, Jacob Zornu, Saraya Tavornpanich and Edgar Brun
Foods 2023, 12(10), 1956; https://doi.org/10.3390/foods12101956 - 11 May 2023
Cited by 6 | Viewed by 2130
Abstract
Farming seabass (Dicentrarchus labrax) is an essential activity in the Mediterranean basin including the Aegean Sea. The main seabass producer is Turkey accounting for 155,151 tons of production in 2021. In this study, skin swabs of seabass farmed in the Aegean [...] Read more.
Farming seabass (Dicentrarchus labrax) is an essential activity in the Mediterranean basin including the Aegean Sea. The main seabass producer is Turkey accounting for 155,151 tons of production in 2021. In this study, skin swabs of seabass farmed in the Aegean Sea were analysed with regard to the isolation and identification of Pseudomonas. Bacterial microbiota of skin samples (n = 96) from 12 fish farms were investigated using next-generation sequencing (NGS) and metabarcoding analysis. The results demonstrated that Proteobacteria was the dominant bacterial phylum in all samples. At the species level, Pseudomonas lundensis was identified in all samples. Pseudomonas, Shewanella, and Flavobacterium were identified using conventional methods and a total of 46 viable (48% of all NGS+) Pseudomonas were isolated in seabass swab samples. Additionally, antibiotic susceptibility was determined according to standards of the European Committee on Antimicrobial Susceptibility Testing (EUCAST) and Clinical and Laboratory Standards Institute (CLSI) in psychrotrophic Pseudomonas. Pseudomonas strains were tested for susceptibility to 11 antibiotics (piperacillin-tazobactam, gentamicin, tobramycin, amikacin, doripenem, meropenem, imipenem, levofloxacin, ciprofloxacin, norfloxacin, and tetracycline) from five different groups of antibiotics (penicillins, aminoglycosides, carbapenems, fluoroquinolones, and tetracyclines). The antibiotics chosen were not specifically linked to usage by the aquaculture industry. According to the EUCAST and CLSI, three and two Pseudomonas strains were found to be resistant to doripenem and imipenem (E-test), respectively. All strains were susceptible to piperacillin-tazobactam, amikacin, levofloxacin, and tetracycline. Our data provide insight into different bacteria that are prevalent in the skin microbiota of seabass sampled from the Aegean Sea in Turkey, and into the antibiotic resistance of psychrotrophic Pseudomonas spp. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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13 pages, 864 KiB  
Article
Treatment of Ready-To-Eat Cooked Meat Products with Cold Atmospheric Plasma to Inactivate Listeria and Escherichia coli
by Isabella Csadek, Ute Vankat, Julia Schrei, Michelle Graf, Susanne Bauer, Brigitte Pilz, Karin Schwaiger, Frans J. M. Smulders and Peter Paulsen
Foods 2023, 12(4), 685; https://doi.org/10.3390/foods12040685 - 4 Feb 2023
Cited by 6 | Viewed by 2580
Abstract
Ready-to-eat meat products have been identified as a potential vehicle for Listeria monocytogenes. Postprocessing contamination (i.e., handling during portioning and packaging) can occur, and subsequent cold storage together with a demand for products with long shelf life can create a hazardous scenario. [...] Read more.
Ready-to-eat meat products have been identified as a potential vehicle for Listeria monocytogenes. Postprocessing contamination (i.e., handling during portioning and packaging) can occur, and subsequent cold storage together with a demand for products with long shelf life can create a hazardous scenario. Good hygienic practice is augmented by intervention measures in controlling post-processing contamination. Among these interventions, the application of ‘cold atmospheric plasma’ (CAP) has gained interest. The reactive plasma species exert some antibacterial effect, but can also alter the food matrix. We studied the effect of CAP generated from air in a surface barrier discharge system (power densities 0.48 and 0.67 W/cm2) with an electrode-sample distance of 15 mm on sliced, cured, cooked ham and sausage (two brands each), veal pie, and calf liver pâté. Colour of samples was tested immediately before and after CAP exposure. CAP exposure for 5 min effectuated only minor colour changes (ΔE max. 2.7), due to a decrease in redness (a*), and in some cases, an increase in b*. A second set of samples was contaminated with Listeria (L.) monocytogenes, L. innocua and E. coli and then exposed to CAP for 5 min. In cooked cured meats, CAP was more effective in inactivating E. coli (1 to 3 log cycles) than Listeria (from 0.2 to max. 1.5 log cycles). In (non-cured) veal pie and calf liver pâté that had been stored 24 h after CAP exposure, numbers of E. coli were not significantly reduced. Levels of Listeria were significantly reduced in veal pie that had been stored for 24 h (at a level of ca. 0.5 log cycles), but not in calf liver pâté. Antibacterial activity differed between but also within sample types, which requires further studies. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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13 pages, 265 KiB  
Article
The Value of Current Ante Mortem Meat Inspection and Food Chain Information of Dairy Cows in Relation to Post Mortem Findings and the Protection of Public Health: A Case for a More Risk-Based Meat Inspection
by Pieter Jacobs, Boyd Berends and Len Lipman
Foods 2023, 12(3), 616; https://doi.org/10.3390/foods12030616 - 1 Feb 2023
Cited by 7 | Viewed by 2638
Abstract
In this study, the contribution of the ante mortem (AM) inspection and the food chain information (FCI) to ensuring meat safety and public health was investigated, by evaluating the slaughterhouse findings of 223,600 slaughtered dairy cows in the Netherlands. The outcome of this [...] Read more.
In this study, the contribution of the ante mortem (AM) inspection and the food chain information (FCI) to ensuring meat safety and public health was investigated, by evaluating the slaughterhouse findings of 223,600 slaughtered dairy cows in the Netherlands. The outcome of this study was that the ante mortem (AM) and post mortem (PM) inspections have a substantial overlap, and that with regard to food safety and public health in over 99% of cases the PM could even be omitted on the basis of the AM. In this study, the data provided by the dairy farmers on the current FCI forms contributed little to nothing with regard to the outcomes of AM and PM inspection. It is concluded that current meat inspection procedures need an update and a more risk-based approach needs to be adopted. Regarding this, the AM inspection of dairy cattle should remain, because it plays an important role in ensuring food safety (e.g., by preventing contamination of the slaughter line by excessively dirty animals, or animals with abscesses), monitoring animal welfare and in detecting some important notifiable diseases. The PM inspection, however, could in many cases be omitted, provided there is a strict AM inspection complemented by a vastly improved (automated) way of obtaining reliable FCI. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
13 pages, 1083 KiB  
Article
Small Contaminations on Broiler Carcasses Are More a Quality Matter than a Food Safety Issue
by Kacper Libera, Len Lipman and Boyd R. Berends
Foods 2023, 12(3), 522; https://doi.org/10.3390/foods12030522 - 24 Jan 2023
Cited by 2 | Viewed by 2362
Abstract
Depending on the interpretation of the European Union (EU) regulations, even marginally visibly contaminated poultry carcasses could be rejected for human consumption due to food safety concerns. However, it is not clear if small contaminations actually increase the already present bacterial load of [...] Read more.
Depending on the interpretation of the European Union (EU) regulations, even marginally visibly contaminated poultry carcasses could be rejected for human consumption due to food safety concerns. However, it is not clear if small contaminations actually increase the already present bacterial load of carcasses to such an extent that the risk for the consumers is seriously elevated. Therefore, the additional contribution to the total microbial load on carcasses by a small but still visible contamination with feces, grains from the crop, and drops of bile and grease from the slaughter line was determined using a Monte Carlo simulation. The bacterial counts (total aerobic plate count, Enterobacteriaceae, Escherichia coli, and Campylobacter spp.) were obtained from the literature and used as input for the Monte Carlo model with 50,000 iterations for each simulation. The Monte Carlo simulation revealed that the presence of minute spots of feces, bile, crop content, and slaughter line grease do not lead to a substantial increase of the already existing biological hazards present on the carcasses and should thus be considered a matter of quality rather than food safety. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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12 pages, 951 KiB  
Article
The Heat Is On: Modeling the Persistence of ESBL-Producing E. coli in Blue Mussels under Meal Preparation
by Kyrre Kausrud, Taran Skjerdal, Gro S. Johannessen, Hanna K. Ilag and Madelaine Norström
Foods 2023, 12(1), 14; https://doi.org/10.3390/foods12010014 - 20 Dec 2022
Viewed by 1581
Abstract
Pathways for exposure and dissemination of antimicrobial-resistant (AMR) bacteria are major public health issues. Filter-feeding shellfish concentrate bacteria from the environment and thus can also harbor extended-spectrum β-lactamase—producing Escherichia coli (ESBL E. coli) as an example of a resistant pathogen of concern. [...] Read more.
Pathways for exposure and dissemination of antimicrobial-resistant (AMR) bacteria are major public health issues. Filter-feeding shellfish concentrate bacteria from the environment and thus can also harbor extended-spectrum β-lactamase—producing Escherichia coli (ESBL E. coli) as an example of a resistant pathogen of concern. Is the short steaming procedure that blue mussels (Mytilus edulis) undergo before consumption enough for food safety in regard to such resistant pathogens? In this study, we performed experiments to assess the survival of ESBL E. coli in blue mussel. Consequently, a predictive model for the dose of ESBL E. coli that consumers would be exposed to, after preparing blue mussels or similar through the common practice of brief steaming until opening of the shells, was performed. The output of the model is the expected number of colony forming units per gram (cfu/g) of ESBL E. coli in a meal as a function of the duration and the temperature of steaming and the initial contamination. In these experiments, the heat tolerance of the ESBL-producing E. coli strain was indistinguishable from that of non-ESBL E. coli, and the heat treatments often practiced are likely to be insufficient to avoid exposure to viable ESBL E. coli. Steaming time (>3.5–4.0 min) is a better indicator than shell openness to avoid exposure to these ESBL or indicator E. coli strains. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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11 pages, 857 KiB  
Article
Characterisation of Listeria monocytogenes Isolates from Hunted Game and Game Meat from Finland
by Maria Fredriksson-Ahomaa, Mikaela Sauvala, Paula Kurittu, Viivi Heljanko, Annamari Heikinheimo and Peter Paulsen
Foods 2022, 11(22), 3679; https://doi.org/10.3390/foods11223679 - 17 Nov 2022
Cited by 6 | Viewed by 1872
Abstract
Listeria monocytogenes is an important foodborne zoonotic bacterium. It is a heterogeneous species that can be classified into lineages, serogroups, clonal complexes, and sequence types. Only scarce information exists on the properties of L. monocytogenes from game and game meat. We characterised 75 [...] Read more.
Listeria monocytogenes is an important foodborne zoonotic bacterium. It is a heterogeneous species that can be classified into lineages, serogroups, clonal complexes, and sequence types. Only scarce information exists on the properties of L. monocytogenes from game and game meat. We characterised 75 L. monocytogenes isolates from various game sources found in Finland between 2012 and 2020. The genetic diversity, presence of virulence and antimicrobial genes were studied with whole genome sequencing. Most (89%) of the isolates belonged to phylogenetic lineage (Lin) II and serogroup (SG) IIa. SGs IVb (8%) and IIb (3%) of Lin I were sporadically identified. In total, 18 clonal complexes and 21 sequence types (STs) were obtained. The most frequent STs were ST451 (21%), ST585 (12%) and ST37 (11%) found in different sample types between 2012 and 2020. We observed 10 clusters, formed by closely related isolates with 0–10 allelic differences. Most (79%) of the virulence genes were found in all of the L. monocytogenes isolates. Only fosX and lin were found out of 46 antimicrobial resistance genes. Our results demonstrate that potentially virulent and antimicrobial-sensitive L. monocytogenes isolates associated with human listeriosis are commonly found in hunted game and game meat in Finland. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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17 pages, 2146 KiB  
Article
Symbiotic Husbandry of Chickens and Pigs Does Not Increase Pathogen Transmission Risk
by Emma Kaeder, Samart Dorn-In, Manfred Gareis and Karin Schwaiger
Foods 2022, 11(19), 3126; https://doi.org/10.3390/foods11193126 - 8 Oct 2022
Cited by 1 | Viewed by 2136
Abstract
A symbiotic or mixed animal husbandry (e.g., pigs and chickens) is considered to have a positive effect for animal welfare and sustainable agriculture. On the other hand, a risk of infection and transmission of microorganisms, especially of zoonotic pathogens, between animal species may [...] Read more.
A symbiotic or mixed animal husbandry (e.g., pigs and chickens) is considered to have a positive effect for animal welfare and sustainable agriculture. On the other hand, a risk of infection and transmission of microorganisms, especially of zoonotic pathogens, between animal species may potentially occur and thus might increase the risk of foodborne illnesses for consumers. To prove these assumptions, two groups of animals and their environmental (soil) samples were investigated in this study. Animals were kept in a free-range system. In the first group, pigs and chickens were reared together (pasture 1), while the other group contained only pigs (pasture 2). During a one-year study, fecal swab samples of 240 pigs and 120 chickens, as well as 120 ground samples, were investigated for the presence of Campylobacter spp., Salmonella spp. and E. coli. Altogether, 438 E. coli and 201 Campylobacter spp. strains were isolated and identified by MALDI-TOF MS. Salmonella spp. was not isolated from any of the sample types. The prevalences of Campylobacter coli and C. jejuni in pigs were 26.7% and 3.3% in pasture 1 and 30.0% and 6.7% in pasture 2, while the prevalences of C. coli and C. jejuni in chickens from pasture 1 were 9.2% and 78.3%, respectively. No correlation between the rearing type (mixed vs. pigs alone) and the prevalence of Campylobacter spp. was observed. All swab samples were positive for E. coli, while the average prevalences in soil samples were 78.3% and 51.7% in pasture 1 and 2, respectively. Results of similarity analysis of the MALDI-TOF MS spectra (for C. coli, C. jejuni and E. coli) and FT-IR spectra (for E. coli) of the same bacterial species showed no recognizable correlations, no matter if strains were isolated from chickens, pig or soil samples or isolated at different sampling periods. The results of the study indicate that the symbiotic husbandry of pigs and chickens neither results in an increased risk of a transmission of Campylobacter spp. or E. coli, nor in a risk of bacterial alteration, as shown by MALDI-TOF MS and FT-IR spectra. In conclusion, the benefits of keeping pigs and chickens together are not diminished by the possible transmission of pathogens. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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18 pages, 3130 KiB  
Article
Systematic Review and Meta-Analysis of the Efficacy of Interventions Applied during Primary Processing to Reduce Microbial Contamination on Pig Carcasses
by Nevijo Zdolec, Aurelia Kotsiri, Kurt Houf, Avelino Alvarez-Ordóñez, Bojan Blagojevic, Nedjeljko Karabasil, Morgane Salines and Dragan Antic
Foods 2022, 11(14), 2110; https://doi.org/10.3390/foods11142110 - 15 Jul 2022
Cited by 12 | Viewed by 2852
Abstract
Interventions from lairage to the chilling stage of the pig slaughter process are important to reduce microbial contamination of carcasses. The aim of this systematic review and meta-analysis was to assess the effectiveness of abattoir interventions in reducing aerobic colony count (ACC), Enterobacteriaceae [...] Read more.
Interventions from lairage to the chilling stage of the pig slaughter process are important to reduce microbial contamination of carcasses. The aim of this systematic review and meta-analysis was to assess the effectiveness of abattoir interventions in reducing aerobic colony count (ACC), Enterobacteriaceae, generic Escherichia coli, and Yersinia spp. on pig carcasses. The database searches spanned a 30 year period from 1990 to 2021. Following a structured, predefined protocol, 22 articles, which were judged as having a low risk of bias, were used for detailed data extraction and meta-analysis. The meta-analysis included data on lairage interventions for live pigs, standard processing procedures for pig carcasses, prechilling interventions, multiple carcass interventions, and carcass chilling. Risk ratios (RRs) for prevalence studies and mean log differences (MDs) for concentration outcomes were calculated using random effects models. The meta-analysis found that scalding under commercial abattoir conditions effectively reduced the prevalence of Enterobacteriaceae (RR: 0.05, 95% CI: 0.02 to 0.12, I2 = 87%) and ACC (MD: −2.84, 95% CI: −3.50 to −2.18, I2 = 99%) on pig carcasses. Similarly, significant reductions of these two groups of bacteria on carcasses were also found after singeing (RR: 0.25, 95% CI: 0.14 to 0.44, I2 = 90% and MD: −1.95, 95% CI: −2.40 to −1.50, I2 = 96%, respectively). Rectum sealing effectively reduces the prevalence of Y. enterocolitica on pig carcasses (RR: 0.60, 95% CI: 0.41 to 0.89, I2 = 0%). Under commercial abattoir conditions, hot water washing significantly reduced ACC (MD: −1.32, 95% CI: −1.93 to −0.71, I2 = 93%) and generic E. coli counts (MD: −1.23, 95% CI: −1.89 to −0.57, I2 = 61%) on pig carcasses. Conventional dry chilling reduced Enterobacteriaceae prevalence on pig carcasses (RR: 0.32, 95% CI: 0.21 to 0.48, I2 = 81%). Multiple carcass interventions significantly reduced Enterobacteriaceae prevalence (RR: 0.11, 95% CI: 0.05 to 0.23, I2 = 94%) and ACC on carcasses (MD: −2.85, 95% CI: −3.33 to −2.37, I2 = 97%). The results clearly show that standard processing procedures of scalding and singeing and the hazard-based intervention of hot water washing are effective in reducing indicator bacteria on pig carcasses. The prevalence of Y. enterocolitica on pig carcasses was effectively reduced by the standard procedure of rectum sealing; nevertheless, this was the only intervention for Yersinia investigated under commercial conditions. High heterogeneity among studies and trials investigating interventions and overall lack of large, controlled trials conducted under commercial conditions suggest that more in-depth research is needed. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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17 pages, 2031 KiB  
Article
Prevalence and Persistence of Multidrug-Resistant Yersinia enterocolitica 4/O:3 in Tonsils of Slaughter Pigs from Different Housing Systems in Croatia
by Nevijo Zdolec, Marta Kiš, Dean Jankuloski, Katerina Blagoevska, Snježana Kazazić, Marina Pavlak, Bojan Blagojević, Dragan Antić, Maria Fredriksson-Ahomaa and Valerij Pažin
Foods 2022, 11(10), 1459; https://doi.org/10.3390/foods11101459 - 18 May 2022
Cited by 6 | Viewed by 2883
Abstract
Yersinia enterocolitica is one of the priority biological hazards in pork inspection. Persistence of the pathogen, including strains resistant to antimicrobials, should be evaluated in pigs from different housing systems for risk ranking of farms. In this 2019 study, tonsils were collected from [...] Read more.
Yersinia enterocolitica is one of the priority biological hazards in pork inspection. Persistence of the pathogen, including strains resistant to antimicrobials, should be evaluated in pigs from different housing systems for risk ranking of farms. In this 2019 study, tonsils were collected from 234 pigs, of which 69 (29.5%) were fattened on 3 big integrated farms, 130 (55.5%) on 10 medium-sized farms, and 35 (15%) on 13 small family farms. In addition, 92 pork cuts and minced meat samples from the same farms were tested for the presence of Y. enterocolitica using the culture method. Phenotypic and genetic characteristics of the isolates were compared with previously collected isolates from 2014. The overall prevalence of Y. enterocolitica in pig tonsils was 43% [95% CI 36.7–49.7]. In pigs from big integrated, medium-sized, and small family farms, the prevalence was 29%, 52%, and 40%, respectively. All retail samples of portioned and minced pork tested negative for pathogenic Y. enterocolitica, likely due to high hygienic standards in slaughterhouses/cutting meat or low sensitivity of culture methods in these matrices. The highest recovery rate of the pathogen from tonsils was found when alkali-treated PSB and CIN agar were combined. The biosecurity category of integrated and medium farms did not affect the differences in prevalence of Y. enterocolitica (p > 0.05), in contrast to family farms. Pathogenic ail-positive Y. enterocolitica biotype 4 serotype O:3 persisted in the tonsils of pigs regardless of the type of farm, slaughterhouse, and year of isolation 2014 and 2019. PFGE typing revealed the high genetic concordance (80.6 to 100%) of all the Y. enterocolitica 4/O:3 isolates. A statistically significant higher prevalence of multidrug-resistant Y. enterocolitica 4/O:3 isolates was detected in the tonsils of pigs from big integrated farms compared to the other farm types (p < 0.05), with predominant and increasing resistance to nalidixic acid, chloramphenicol, and streptomycin. This study demonstrated multidrug resistance of the pathogen in pigs likely due to more antimicrobial pressure on big farms, with intriguing resistance to some clinically relevant antimicrobials used in the treatment of yersiniosis in humans. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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Review

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35 pages, 531 KiB  
Review
Presence of Foodborne Bacteria in Wild Boar and Wild Boar Meat—A Literature Survey for the Period 2012–2022
by Caterina Altissimi, Clara Noé-Nordberg, David Ranucci and Peter Paulsen
Foods 2023, 12(8), 1689; https://doi.org/10.3390/foods12081689 - 18 Apr 2023
Cited by 8 | Viewed by 2555
Abstract
The wild boar is an abundant game species with high reproduction rates. The management of the wild boar population by hunting contributes to the meat supply and can help to avoid a spillover of transmissible animal diseases to domestic pigs, thus compromising food [...] Read more.
The wild boar is an abundant game species with high reproduction rates. The management of the wild boar population by hunting contributes to the meat supply and can help to avoid a spillover of transmissible animal diseases to domestic pigs, thus compromising food security. By the same token, wild boar can carry foodborne zoonotic pathogens, impacting food safety. We reviewed literature from 2012–2022 on biological hazards, which are considered in European Union legislation and in international standards on animal health. We identified 15 viral, 10 bacterial, and 5 parasitic agents and selected those nine bacteria that are zoonotic and can be transmitted to humans via food. The prevalence of Campylobacter, Listeria monocytogenes, Salmonella, Shiga toxin-producing E. coli, and Yersinia enterocolitica on muscle surfaces or in muscle tissues of wild boar varied from 0 to ca. 70%. One experimental study reported the transmission and survival of Mycobacterium on wild boar meat. Brucella, Coxiella burnetii, Listeria monocytogenes, and Mycobacteria have been isolated from the liver and spleen. For Brucella, studies stressed the occupational exposure risk, but no indication of meat-borne transmission was evident. Furthermore, the transmission of C. burnetii is most likely via vectors (i.e., ticks). In the absence of more detailed data for the European Union, it is advisable to focus on the efficacy of current game meat inspection and food safety management systems. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
17 pages, 2344 KiB  
Review
Disease Occurrence in- and the Transferal of Zoonotic Agents by North American Feedlot Cattle
by Osman Y. Koyun, Igori Balta, Nicolae Corcionivoschi and Todd R. Callaway
Foods 2023, 12(4), 904; https://doi.org/10.3390/foods12040904 - 20 Feb 2023
Cited by 6 | Viewed by 3268
Abstract
North America is a large producer of beef and contains approximately 12% of the world’s cattle inventory. Feedlots are an integral part of modern cattle production in North America, producing a high-quality, wholesome protein food for humans. Cattle, during their final stage, are [...] Read more.
North America is a large producer of beef and contains approximately 12% of the world’s cattle inventory. Feedlots are an integral part of modern cattle production in North America, producing a high-quality, wholesome protein food for humans. Cattle, during their final stage, are fed readily digestible high-energy density rations in feedlots. Cattle in feedlots are susceptible to certain zoonotic diseases that impact cattle health, growth performance, and carcass characteristics, as well as human health. Diseases are often transferred amongst pen-mates, but they can also originate from the environment and be spread by vectors or fomites. Pathogen carriage in the gastrointestinal tract of cattle often leads to direct or indirect contamination of foods and the feedlot environment. This leads to the recirculation of these pathogens that have fecal–oral transmission within a feedlot cattle population for an extended time. Salmonella, Shiga toxin-producing Escherichia coli, and Campylobacter are commonly associated with animal-derived foods and can be transferred to humans through several routes such as contact with infected cattle and the consumption of contaminated meat. Brucellosis, anthrax, and leptospirosis, significant but neglected zoonotic diseases with debilitating impacts on human and animal health, are also discussed. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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20 pages, 334 KiB  
Review
The Zoonotic Potential of Chronic Wasting Disease—A Review
by Michael A. Tranulis and Morten Tryland
Foods 2023, 12(4), 824; https://doi.org/10.3390/foods12040824 - 15 Feb 2023
Cited by 8 | Viewed by 4881
Abstract
Prion diseases are transmissible neurodegenerative disorders that affect humans and ruminant species consumed by humans. Ruminant prion diseases include bovine spongiform encephalopathy (BSE) in cattle, scrapie in sheep and goats and chronic wasting disease (CWD) in cervids. In 1996, prions causing BSE were [...] Read more.
Prion diseases are transmissible neurodegenerative disorders that affect humans and ruminant species consumed by humans. Ruminant prion diseases include bovine spongiform encephalopathy (BSE) in cattle, scrapie in sheep and goats and chronic wasting disease (CWD) in cervids. In 1996, prions causing BSE were identified as the cause of a new prion disease in humans; variant Creutzfeldt-Jakob disease (vCJD). This sparked a food safety crisis and unprecedented protective measures to reduce human exposure to livestock prions. CWD continues to spread in North America, and now affects free-ranging and/or farmed cervids in 30 US states and four Canadian provinces. The recent discovery in Europe of previously unrecognized CWD strains has further heightened concerns about CWD as a food pathogen. The escalating CWD prevalence in enzootic areas and its appearance in a new species (reindeer) and new geographical locations, increase human exposure and the risk of CWD strain adaptation to humans. No cases of human prion disease caused by CWD have been recorded, and most experimental data suggest that the zoonotic risk of CWD is very low. However, the understanding of these diseases is still incomplete (e.g., origin, transmission properties and ecology), suggesting that precautionary measures should be implemented to minimize human exposure. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
20 pages, 404 KiB  
Review
Foodborne Diseases in the Edible Insect Industry in Europe—New Challenges and Old Problems
by Remigiusz Gałęcki, Tadeusz Bakuła and Janusz Gołaszewski
Foods 2023, 12(4), 770; https://doi.org/10.3390/foods12040770 - 10 Feb 2023
Cited by 14 | Viewed by 10515
Abstract
Insects play a key role in European agroecosystems. Insects provide important ecosystem services and make a significant contribution to the food chain, sustainable agriculture, the farm-to-fork (F2F) strategy, and the European Green Deal. Edible insects are regarded as a sustainable alternative to livestock, [...] Read more.
Insects play a key role in European agroecosystems. Insects provide important ecosystem services and make a significant contribution to the food chain, sustainable agriculture, the farm-to-fork (F2F) strategy, and the European Green Deal. Edible insects are regarded as a sustainable alternative to livestock, but their microbiological safety for consumers has not yet been fully clarified. The aim of this article is to describe the role of edible insects in the F2F approach, to discuss the latest veterinary guidelines concerning consumption of insect-based foods, and to analyze the biological, chemical, and physical hazards associated with edible insect farming and processing. Five groups of biological risk factors, ten groups of chemical risk factors, and thirteen groups of physical risks factors have been identified and divided into sub-groups. The presented risk maps can facilitate identification of potential threats, such as foodborne pathogens in various insect species and insect-based foods. Ensuring safety of insect-based foods, including effective control of foodborne diseases, will be a significant milestone on the path to maintaining a sustainable food chain in line with the F2F strategy and EU policies. Edible insects constitute a new category of farmed animals and a novel link in the food chain, but their production poses the same problems and challenges that are encountered in conventional livestock rearing and meat production. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
21 pages, 1792 KiB  
Review
Transmission Scenarios of Listeria monocytogenes on Small Ruminant On-Farm Dairies
by Dagmar Schoder, Alexandra Pelz and Peter Paulsen
Foods 2023, 12(2), 265; https://doi.org/10.3390/foods12020265 - 6 Jan 2023
Cited by 5 | Viewed by 4475
Abstract
Listeria monocytogenes can cause severe foodborne infections in humans and invasive diseases in different animal species, especially in small ruminants. Infection of sheep and goats can occur via contaminated feed or through the teat canal. Both infection pathways result in direct (e.g., raw [...] Read more.
Listeria monocytogenes can cause severe foodborne infections in humans and invasive diseases in different animal species, especially in small ruminants. Infection of sheep and goats can occur via contaminated feed or through the teat canal. Both infection pathways result in direct (e.g., raw milk from an infected udder or fresh cheese produced from such milk) or indirect exposure of consumers. The majority of dairy farmers produces a high-risk product, namely fresh cheese made from raw ewe’s and goat’s milk. This, and the fact that L. monocytogenes has an extraordinary viability, poses a significant challenge to on-farm dairies. Yet, surprisingly, almost no scientific studies have been conducted dealing with the hygiene and food safety aspects of directly marketed dairy products. L. monocytogenes prevalence studies on small ruminant on-farm dairies are especially limited. Therefore, it was our aim to focus on three main transmission scenarios of this important major foodborne pathogen: (i) the impact of caprine and ovine listerial mastitis; (ii) the significance of clinical listeriosis and outbreak scenarios; and (iii) the impact of farm management and feeding practices. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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27 pages, 1829 KiB  
Review
Foodborne Parasites and Their Complex Life Cycles Challenging Food Safety in Different Food Chains
by Sarah Gabriël, Pierre Dorny, Ganna Saelens and Veronique Dermauw
Foods 2023, 12(1), 142; https://doi.org/10.3390/foods12010142 - 27 Dec 2022
Cited by 18 | Viewed by 5290
Abstract
Zoonotic foodborne parasites often represent complex, multi host life cycles with parasite stages in the hosts, but also in the environment. This manuscript aims to provide an overview of important zoonotic foodborne parasites, with a focus on the different food chains in which [...] Read more.
Zoonotic foodborne parasites often represent complex, multi host life cycles with parasite stages in the hosts, but also in the environment. This manuscript aims to provide an overview of important zoonotic foodborne parasites, with a focus on the different food chains in which parasite stages may occur. We have chosen some examples of meat-borne parasites occurring in livestock (Taenia spp., Trichinella spp. and Toxoplasma gondii), as well as Fasciola spp., an example of a zoonotic parasite of livestock, but transmitted to humans via contaminated vegetables or water, covering the ‘farm to fork’ food chain; and meat-borne parasites occurring in wildlife (Trichinella spp., Toxoplasma gondii), covering the ‘forest to fork’ food chain. Moreover, fish-borne parasites (Clonorchis spp., Opisthorchis spp. and Anisakidae) covering the ‘pond/ocean/freshwater to fork’ food chain are reviewed. The increased popularity of consumption of raw and ready-to-eat meat, fish and vegetables may pose a risk for consumers, since most post-harvest processing measures do not always guarantee the complete removal of parasite stages or their effective inactivation. We also highlight the impact of increasing contact between wildlife, livestock and humans on food safety. Risk based approaches, and diagnostics and control/prevention tackled from an integrated, multipathogen and multidisciplinary point of view should be considered as well. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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21 pages, 883 KiB  
Review
Treatment of Fresh Meat, Fish and Products Thereof with Cold Atmospheric Plasma to Inactivate Microbial Pathogens and Extend Shelf Life
by Peter Paulsen, Isabella Csadek, Alexandra Bauer, Kathrine H. Bak, Pia Weidinger, Karin Schwaiger, Norbert Nowotny, James Walsh, Emilio Martines and Frans J. M. Smulders
Foods 2022, 11(23), 3865; https://doi.org/10.3390/foods11233865 - 30 Nov 2022
Cited by 6 | Viewed by 3701
Abstract
Assuring the safety of muscle foods and seafood is based on prerequisites and specific measures targeted against defined hazards. This concept is augmented by ‘interventions’, which are chemical or physical treatments, not genuinely part of the production process, but rather implemented in the [...] Read more.
Assuring the safety of muscle foods and seafood is based on prerequisites and specific measures targeted against defined hazards. This concept is augmented by ‘interventions’, which are chemical or physical treatments, not genuinely part of the production process, but rather implemented in the framework of a safety assurance system. The present paper focuses on ‘Cold Atmospheric pressure Plasma’ (CAP) as an emerging non-thermal intervention for microbial decontamination. Over the past decade, a vast number of studies have explored the antimicrobial potential of different CAP systems against a plethora of different foodborne microorganisms. This contribution aims at providing a comprehensive reference and appraisal of the latest literature in the area, with a specific focus on the use of CAP for the treatment of fresh meat, fish and associated products to inactivate microbial pathogens and extend shelf life. Aspects such as changes to organoleptic and nutritional value alongside other matrix effects are considered, so as to provide the reader with a clear insight into the advantages and disadvantages of CAP-based decontamination strategies. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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17 pages, 698 KiB  
Review
Asymptomatic Carriage of Listeria monocytogenes by Animals and Humans and Its Impact on the Food Chain
by Dagmar Schoder, Claudia Guldimann and Erwin Märtlbauer
Foods 2022, 11(21), 3472; https://doi.org/10.3390/foods11213472 - 1 Nov 2022
Cited by 21 | Viewed by 7409
Abstract
Humans and animals can become asymptomatic carriers of Listeria monocytogenes and introduce the pathogen into their environment with their feces. In turn, this environmental contamination can become the source of food- and feed-borne illnesses in humans and animals, with the food production chain [...] Read more.
Humans and animals can become asymptomatic carriers of Listeria monocytogenes and introduce the pathogen into their environment with their feces. In turn, this environmental contamination can become the source of food- and feed-borne illnesses in humans and animals, with the food production chain representing a continuum between the farm environment and human populations that are susceptible to listeriosis. Here, we update a review from 2012 and summarize the current knowledge on the asymptomatic carrier statuses in humans and animals. The data on fecal shedding by species with an impact on the food chain are summarized, and the ways by which asymptomatic carriers contribute to the risk of listeriosis in humans and animals are reviewed. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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24 pages, 454 KiB  
Review
Microbiological Safety and Shelf-Life of Low-Salt Meat Products—A Review
by Coral Barcenilla, Avelino Álvarez-Ordóñez, Mercedes López, Ole Alvseike and Miguel Prieto
Foods 2022, 11(15), 2331; https://doi.org/10.3390/foods11152331 - 4 Aug 2022
Cited by 30 | Viewed by 6592
Abstract
Salt is widely employed in different foods, especially in meat products, due to its very diverse and extended functionality. However, the high intake of sodium chloride in human diet has been under consideration for the last years, because it is related to serious [...] Read more.
Salt is widely employed in different foods, especially in meat products, due to its very diverse and extended functionality. However, the high intake of sodium chloride in human diet has been under consideration for the last years, because it is related to serious health problems. The meat-processing industry and research institutions are evaluating different strategies to overcome the elevated salt concentrations in products without a quality reduction. Several properties could be directly or indirectly affected by a sodium chloride decrease. Among them, microbial stability could be shifted towards pathogen growth, posing a serious public health threat. Nonetheless, the majority of the literature available focuses attention on the sensorial and technological challenges that salt reduction implies. Thereafter, the need to discuss the consequences for shelf-life and microbial safety should be considered. Hence, this review aims to merge all the available knowledge regarding salt reduction in meat products, providing an assessment on how to obtain low salt products that are sensorily accepted by the consumer, technologically feasible from the perspective of the industry, and, in particular, safe with respect to microbial stability. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)

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Jump to: Research, Review

19 pages, 1267 KiB  
Perspective
The Environment, Farm Animals and Foods as Sources of Clostridioides difficile Infection in Humans
by Declan Bolton and Pilar Marcos
Foods 2023, 12(5), 1094; https://doi.org/10.3390/foods12051094 - 4 Mar 2023
Cited by 16 | Viewed by 4197
Abstract
The recent discovery of the same Clostridioides difficile ribotypes associated with human infection in a broad range of environments, animals and foods, coupled with an ever-increasing rate of community-acquired infections, suggests this pathogen may be foodborne. The objective of this review was to [...] Read more.
The recent discovery of the same Clostridioides difficile ribotypes associated with human infection in a broad range of environments, animals and foods, coupled with an ever-increasing rate of community-acquired infections, suggests this pathogen may be foodborne. The objective of this review was to examine the evidence supporting this hypothesis. A review of the literature found that forty-three different ribotypes, including six hypervirulent strains, have been detected in meat and vegetable food products, all of which carry the genes encoding pathogenesis. Of these, nine ribotypes (002, 003, 012, 014, 027, 029, 070, 078 and 126) have been isolated from patients with confirmed community-associated C. difficile infection (CDI). A meta-analysis of this data suggested there is a higher risk of exposure to all ribotypes when consuming shellfish or pork, with the latter being the main foodborne route for ribotypes 027 and 078, the hypervirulent strains that cause most human illnesses. Managing the risk of foodborne CDI is difficult as there are multiple routes of transmission from the farming and processing environment to humans. Moreover, the endospores are resistant to most physical and chemical treatments. The most effective current strategy is, therefore, to limit the use of broad-spectrum antibiotics while advising potentially vulnerable patients to avoid high-risk foods such as shellfish and pork. Full article
(This article belongs to the Special Issue Foodborne Pathogens Management: From Farm and Pond to Fork)
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