Current Clinical Microbiology Reports https://doi.org/10.1007/s40588-018-0090-1
FOODBORNE PATHOGENS (S JOHLER, SECTION EDITOR)
Listeria monocytogenes in the Food Processing Environment Kieran Jordan 1 & Karen Hunt 1 & Antonio Lourenco 1 & Vincenzo Pennone 1
# Springer International Publishing AG, part of Springer Nature 2018
Abstract Purpose of Review Listeria monocytogenes is a foodborne pathogen that causes listeriosis, a relatively rare but potentially fatal disease with a 19% mortality rate and a 99% hospitalisation rate. It affects mainly elderly and immunocompromised individuals. Ready-to-eat (RTE) foods are particularly dangerous with regard to L. monocytogenes as there is no further anti-microbial step between production and consumption. The purpose of this work is to review the importance of Listeria monocytogenes in the food processing environment. Recent Findings Cross-contamination from the processing environment to the food at production or at retail level is the most common route of RTE food contamination. If present on a food matrix, L. monocytogenes has a remarkable ability to survive and can grow during refrigeration to sufficient numbers to cause disease. Summary While hygiene processes and awareness can help control of L. monocytogenes in food processing environments, new methods such as bacteriophages and bacteriocins are being applied to control it in food, reducing public health issues. Keywords Listeria monocytogenes . Food processing environment . Control
Introduction Listeriosis, caused by Listeria monocytogenes, is a foodborne disease that causes gastrointestinal illness, which is sometimes a self-limiting disease, but can result in more serious illnesses. It has a mortality rate of 19% [1] and among the foodborne diseases has the highest hospitalisation rate of about 99% [2••]. L. monocytogenes has the ability to cross three key barriers—the intestinal barrier, the blood–brain barrier and the fetoplacental barrier, so that it can infect organs such as the brain or uterus, and cause severe life-threatening infections such as meningitis, encephalitis, spontaneous abortion, or miscarriage. Healthy individuals are normally not susceptible to Listeria monocytogenes, but it can have severe implications
This article is part of the Topical Collection on Foodborne Pathogens * Kieran Jordan
[email protected] 1
Teagasc Food Research Centre, Moorepark, Fermoy, Cork, Ireland
for those with compromised immune systems, such as the elderly, new-borns and pregnant women. From 2008 to 2014, the number of recorded cases in Europe has increased significantly [3]. The EU notification rate was 0.44 cases per 100,000 population in 2013 representing an 8.6% increase compared with 2012. L. monocytogenes is ubiquitous in the environment [4]; therefore, contamination of the food processing environment is inevitable unless stringent efforts are in place to prevent such contamination. L. monocytogenes can survive for long periods of time in a seemingly hostile environment such as a food processing facility partially due to its ability to endure various stresses, such as sanitizers, pH and temperature [5, 6], and its ability to form biofilm [7, 8], leading to persistence. If the food processing environment is contaminated, crosscontamination of L. monocytogenes to food is a major possible route of food contamination [9]. As the public health consequences of listeriosis are so serious, occurrence of L. monocytogenes in the food processing environment and the possible cross-contamination to food is a major problem for the food industry. In particular, it is a problem for the ready-to-eat food industry as there is no heat or other antimicrobial step between production and consumption.
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As a foodborne disease, a reduction in the occurrence of listeriosis is possible. Measures can be taken to prevent food processing environment contamination in the first place, to reduce its occurrence in the food processing environment through adequate hygiene measures and to reduce crosscontamination to food. Furthermore, preventing growth of L. monocytogenes at retail and onwards could lead to a 37% reduction in listeriosis [10]. The focus of this review is on the occurrence of L. monocytogenes in the food processing environment that has been reported in the last 3 years, to discuss characterisation of the isolates obtained with a view to understanding such contamination, and exploring options for its reduction.
Current Regulations on Occurrence of L. monocytogenes in Food The current legislation for L. monocytogenes in the EU, Regulation (EC) No 2073/2005 [11], sets the criteria that foods must comply with regarding L. monocytogenes. It requires absence (10 × 25 g samples) for foods intended for infants and special medical purposes and allow presence at different levels depending on the ability of the food to support growth of the bacterium. For ready-to-eat (RTE) foods unable to support the growth of L. monocytogenes, the numbers should be < 100 CFU/g throughout the shelf-life of the product (5 × 25 g samples). For RTE foods able to support growth, L. monocytogenes must be absent in 5 × 25 g samples at the time of leaving the production plant or it may not exceed 100 CFU/g throughout its shelf-life (5 × 25 g samples). If the ability of a food to support growth has not been determined, it is assumed that growth will occur and the criterion of absence is applied. There are similar regulations in Canada [12] and in Australia/New-Zealand [13]. In the USA, a stricter regulation is in place. Absence of L. monocytogenes in 5 × 25 g of food, and in the processing environment, is required at all times [14]. These strict policies pose a serious challenge to small producers and companies in developing counties that are exporting to the USA and are required to meet US regulations. In general for, companies in the export business use the relevant regulation in the country they export to. Further discussion on regulations in different jurisdictions is reviewed in a special issue of Food Control published in 2011 [15].
Methodologies of Sampling for L. monocytogenes As Listeria monocytogenes is ubiquitous in the environment, there is a risk of contamination of food processing environments. Maintaining the processing environment free from
L. monocytogenes is important especially in high-risk areas where there is the risk of cross-contamination to the food. Sampling through appropriate Environmental Monitoring Programmes of the processing environment for presence of L. monocytogenes is necessary in order to control [16••]. The responsibility for such monitoring lies with the food business owner (FBO). Sampling programmes should target areas where contamination would occur, for example, drains, floors, wet areas, hard to clean niches in the equipment, doors, windows and air handling systems. Additionally, samples should not be taken directly after cleaning/disinfection as sampling in this manner would severely decrease the chances of finding L. monocytogenes. In order to obtain the most accurate representation of the contamination present, sampling plans must attempt to obtain as many positive samples as possible so that positive areas can be targeted for more rigorous hygiene measures. The European Union Reference Laboratory on L. monocytogenes has published a guidance document on sampling that can help with controlling L. monocytogenes [17]. A history of testing and sample results should also be established to verify that cleaning methods are sufficient, where positive results should be acted on immediately by cleaning to eradicating contamination, and then confirmed free from Listeria by retesting. End-product testing is a useful part of controlling L. monocytogenes, however, it is not sufficient on its own to control L. monocytogenes as low numbers are difficult to detect in large batches where not all units of the batch will be tested. Process control testing should be undertaken in association with end-product testing. All samples should be taken and tested immediately or stored at 4 °C and then tested with 24 h of collection.
Methodologies for Sample Analysis of L. monocytogenes Conventional and rapid methods are available for the detection and enumeration of L. monocytogenes. The International Standardisation Organisation (ISO) standard method for detection is ISO 11290-1:2017, and for the enumeration is ISO 11290-2:2017. The detection method is a two-step enrichment, using half Fraser broth (containing half the antibiotic concentration) and full Frazer broth (containing the full concentration of antibiotics), taking a total of 4 days to complete. The selective plating medium used for both methods is Agar Listeria according to Ottaviani and Agosti (ALOA) and any other equivalent selective media. The Bacteriological Analytical Manual (BAM) detection method uses a buffered Listeria enrichment broth (BLEB) incubated for 24–48 h enrichment. Alternative methods exist for rapid testing and screening, according to validated methods (ISO 16140-1:2016, ISO
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16140-2:2016), most notability AOAC International and/or Association Française de Normalisation (AFNOR, en: French Standardization Association) validated methods, where the AOAC database alone contains almost 50 products. Alternative methods are based on different technologies, including molecular and immunological techniques. Molecular methods include DNA hybridisation and real time PCR (RT PCR), results in a more rapid detection of L. monocytogenes, although it has the disadvantages of a direct detection limit of about 100 CFU/ml (depending on the test used) and the lack of a bacterial isolate for further characterisation. Using molecular testing in combination with agar plates [18], isolates can be obtained for further characterisation. One advantage of molecular methods is that they provide confirmation of L. monocytogenes as they target virulence genes such as actA or hly. Immunological methods are based on the antibody-antigen reaction, where antibodies specific for L. monocytogenes are used, for example in flow-cytometry assays. Enzyme-linked immunosorbent assay (ELISA)-based assays incorporate fluorescent or colorimetric detection, or a newer method combining immunoassay techniques to realtime immunoquantitative PCR (iqPCR).
Characterisation of L. monocytogenes Isolates Obtained Serotyping/Serogrouping Subspecies differentiation of L. monocytogenes by serotypes has been carried out by an agglutination method developed in 1979 by Seeliger and Hohne [19], based on the reactions of somatic (O) and flagellar (H) antigens. In 2004, a multiplex PCR-based method was developed [20]. This PCR-based assay is a multiplex of five genes: Imo0737, Imo1118, ORF2819, ORF2110 and prs, to differentiate the major serogroups into five phylogenetic groups. Currently, a combination of serotyping and serogrouping is used [21]. In 2013, Vitullo et al. [22] developed a real-time PCR assay to allow serogrouping of L. monocytogenes and differentiate from other Listeria species. It combines the results of two triplex PCRs, targeting ORF2110, ORF2819 and Imo1118, and then targeting Imo0737, plc A and prs.
Other Subtyping Methods Beyond the species level, subtyping of L. monocytogenes strains is useful to track routes of contamination throughout the processing environment, and to give some indication of the source of such contamination. Typeability, discrimination power, reproducibility, speed, cost and lab capacity will be the main factors in deciding the appropriate method to use. Bandbased methods, or DNA fingerprinting, include Pulse Field
Gel Electrophoresis (PFGE), which is the current gold standard method for assessing L. monocytogenes strain interrelatedness [23] for monitoring routes of contamination in food processing environments [24••]. PFGE results in DNA patterns which differ from one strain to the other depending on the number and size of DNA fragments obtained. Pulsotypes, indicating closely related strains, can be identified using bioinformatics software. The PulseNet International network [25] uses standardised PFGE protocols for the study of L. monocytogenes (and other pathogenic bacteria), although this is now moving towards whole genome sequencing (WGS). Other molecular typing methods include multi-locus sequence typing (MLST), multi-locus variable-number tandem repeat analysis (MLVA), Restriction Fragment Length Polymorphism (RFLP), amplified fragment length polymorphism (AFLP) [26] randomly amplified polymorphic (DNA RAPD) [27]. A database for MLST contains the reference allele sequences and sequence types for different organisms and for isolate epidemiological data. Interrogation and analysis software which facilitates a query of the allele sequences and sequence types in the databases are available [28–30].
Whole Genome Sequencing of L. monocytogenes Isolates Whole genome sequencing, which involves getting the entire DNA sequence of the strain, is becoming increasingly popular as an analysis tool for bacterial strains. In recent years, the cost of WGS has decreased dramatically, and as a result, the number of whole genome sequences for strains of L. monocytogenes has increased. In 2013, through the Genome TRAKR Network, the Centre for Disease Control and Prevention in the United States of America (CDC) and the Food and Drug Administration (FDA) commenced a study on the use WGS for tracking L. monocytogenes isolates from food processing environment analysis and during disease outbreaks [31]. Similar studies have been undertaken in other countries leading to the availability of thousands of whole genome sequences of L. monocytogenes strains. Such data has been used, for example, in the Quargel cheese outbreak in Austria in 2009/2010, where WGS facilitated the identification of two distinct 1/2a L. monocytogenes strains (QOC1 and QOC2) which overlapped to form the outbreak [32]. The WGS data can also be used for subtyping [28], outbreak detection [31], persistence [33] and antimicrobial resistance (AMR) predictions [34], etc. Databases on core genome (cg) MLST and whole genome (wg) MLST are available for strain comparisons [35] and analysis of single nucleotide polymorphisms (SNPs) can give information on strain relatedness [36, 37]. Such information will provide a large database of wellcharacterised environmental (food, water, processing facility, clinical, etc.) isolates that will facilitate a better understanding
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of L. monocytogenes and its switch from saprophyte to virulent pathogen. However, WGS will only allow accurate and reliable identification of outbreaks and outbreak sources in conjunction with solid epidemiological data on food consumption. Similar strains can be obtained from apparently unrelated locations [36]. Therefore, epidemiological data collection and analysis are still critical in order to take full advantage of WGS-based subtyping data for foodborne pathogens. In addition, standardisation of DNA extraction, sequencing methodology and analysis, quality control of sequence data, etc. are also required for validation and accreditation of the methods. Finally, it must be remembered that the currently widely used sequencing technologies, for example Ilumina, result in a number of contigs—fragments of the genome DNA, rather than a complete genome sequence as obtained with PacBio sequencing. Therefore, standardisation is more important with Illumina sequencing, rather than the more expensive PacBio sequencing.
Prevalence of L. monocytogenes in the Environment and on Food Food Processing Environment Occurrence There are many surveys published on the prevalence of L. monocytogenes in food processing environments. However, comparison of the survey results from one survey to another is not always possible. The following variables can influence the observed prevalence: 1. Different methodologies for sampling are used, for example the swab size and the area that is swabbed (which can vary from 10 cm2 to 1 m2) [38, 39]. 2. Different methodologies for L. monocytogenes analysis are used, for example the ISO, BAM or alternative methods [40, 41••]. 3. Different frequencies of repeated facility testing, for example Sala et al. [40] surveyed on one occasion, where another facility is surveyed on several occasions [42] and several facilities are surveyed on several occasions [16]. 4. A facility that has been shown to be positive is targeted. 5. Different sample numbers and different sampling locations can influence the results. The source of processing environment contamination may be determined to some extent by PFGE analysis of isolates from different locations. For example, an isolate from raw materials with a similar PFGE profile to a food processing environment isolate indicates that the contamination was from the raw material. Rückerl et al. [43] verified that out of the seven genotypes detected in the food processing environment
(FPE) at the beginning of their survey, four were also isolated from the raw materials. Similarly, identification of a similar PFGE type inside a food processing facility and in the area outside the food processing facility can indicate a potential source of contamination [44]. In both cases, transfer from the environment to the raw material or from the inside to the outside cannot be ruled out.
Persistence of L. monocytogenes in the Processing Environment Persistence of L. monocytogenes in a processing environment is generally defined as repeated isolation of an indistinguishable pulsotype from the same facility for longer than 6 months [44, 45]. This indicates that the strain with that pulsotype can persist in the processing environment, despite the hygiene procedures of the facility. It is possible that repeated occurrence of a strain in a processing environment may result from repeated contamination of the processing facility from an outside source, but even in that situation it is necessary for the strain to survive and persist outside. The basis of such persistence is unknown. A genetic marker for persistence has not been identified. Some candidate genes for a genetic marker include qacH, SSI, biofilm-forming genes. However, persistent strains that do not have these genes have been identified and transient strains that do not persist have been shown to have these genes. An alternative hypothesis is that the harbourage sites and niches where persistent strains survive give them protection from the cleaning procedures (for review, see [46]). Some examples of recent food processing environment surveys, highlighting the differences in methodologies, are given in Table 1.
Occurrence of L. monocytogenes at Retail Level Awareness about the presence of L. monocytogenes at retail level is relevant because it is the last step before the product reaches the consumer. For that reason, it is important to evaluate the prevalence of L. monocytogenes at retail level. Recently conducted risk assessments for L. monocytogenes in deli meats indicated that the majority of listeriosis cases and deaths associated with deli meats are probably due to contamination of products at retail. Endrikat et al. [68] estimated that 83% of human listeriosis cases and deaths attributable to deli meats are due to retail-sliced products, and Pradhan et al. [69] performed a risk assessment using product-specific growth kinetic parameters that indicated that 63 to 84% of human listeriosis deaths linked to deli ham and turkey can be attributed to contamination at retail. Occurrence and cross-contamination at retail level are not as frequent as processing environment studies, but are obviously an important source of listeriosis.
120 (10 industries, 9 retail) 2864 (n.a., industry and retail) 778 (n.a., retail from 12 cities) 301 (n.a., retail) 555 (n.a., traditional markets) 200 (n.a., retail)
457 (n.a., dairy farms from 15 cities) 200 (n.a., retail) 27,389 (n.a., retail) 475 (54 food shops, 24 salad bars, 19 supermarkets) 193 (2 fish markets)
850 (n.a., retail)
Portugal Spain Italy Poland Nigeria China China
China
India Thailand USA Singapore Nigeria
Chile
EN ISO 11290-1:1996, EN ISO 11290-2:1998
EN ISO 11290-1:1996/Amd 1:2004 and EN ISO 11290-2:1998/Amd 1:2004. EN ISO 11290-1:1999 - A1:2005; EN ISO 11290-2:2000/A1:2004 EN ISO 11290-1:2004 Enrichment + PCR
GB 4789.30-2010
GB 4789.30–2010 + MPN
McClain and Lee (1987) MDA-LM; 3M, St. Paul, MN + OCLA plates; FDA-BAM in parallel MPN + API + BAX PCR
One enrichment + RAPIDEC (BioMerieux)
Oxoid Listeria Précis method, Oxoid Biochemical Identification System, Oxoid Listeria Test Kit and MICROBACT Listeria 12 L system VIDAS kit + API
EN ISO 11290-1, EN ISO 11290-2
1036 (134 retail)
648 (16 retail + 4 dairy farms)
862 (n.a., retail and catering)
480 (5R markets) 339 (n.a., retail)
EN ISO 11290-, EN ISO 11290-2
387 (n.a., retail)
N samples (N companies)
EN ISO 11290-1 + API EN ISO 11290-1, EN ISO 11290-2:1996
Country
Czech Republic India Czech Republic UK
Retail EN ISO 11290
Detection method
1- Year study
2011–2015
2010–2013
[64]
[63]
[62]
[61•]
[59] [60]
[58]
2012–2014
2014 - 2015 2013
[57]
[55] [56]
[54]
[53]
[52]
[51]
[50]
[48] [49]
[47]
Reference
2013–2014
2012–2013 n.a.
2014–2016
2011
2006–2012
2011–2013
2013
2013–2014 2014
2007–2016
Survey period
Raw meat and poultry, cheese, cooked 2008–2009 sausage, frozen seafood, smoked fish, fresh and frozen vegetables
Seafood
Ready-to-eat vegetables Chilled and frozen animal derived products Raw milk and milk products, raw meats, cooked meats, quick-frozen food, vegetables and bean products, aquatic products Vegetables, edible mushrooms, raw meat, aquatic products, quick-frozen products Raw milk Seafood and products of animal and vegetal origin, aquatic products Seafood, produce, dairy, meat, eggs and combination foods RTE salad
Smoked fish
Smoked fish
Ready-to-eat meat-based food products Food
Meat pies
Vegetables Vegetables
Cheese
Samples type
Table 1 Some surveys on the occurrence of L. monocytogenes in food at retail level and in food processing environments, conducted between 2015 and 2017. Due to the different methodologies used, comparison of the results for occurrence is not appropriate
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183 raw milk samples, 4430 environmental samples (9) 97 swabs (1)
USA
45—2008/2009 (21), 255—2009/2010 (32), 654—2010/2013 (48)
Italy
Brazil
Taiwan
ISO 18593, confirmation: 16s-MLST, serogroup
U.S. Food and Drug Administration Bacteriological Analytical Manual standards (4 h + 20 h enrichment, Oxford plates). Conf: iap PCR. Serotyping, PFGE
n.a. not available
USA
Enrichment + mini VIDAS
Plant A: 1248 environmental samples and 16 food samples. Plant B: 736 environmental samples and 16 food samples (2)
255 environmental samples NFCS (1) 437 (5 dairy + retail)
20 food and 60 swabs (10)
Ireland
EN ISO 11290-1. Confirmation: PCR. serogroup, serotype, PFGE EN ISO 11290-1. L.spp PCR, virulence genes PCR, serogroup, antibiotic susceptibility, PFGE EN ISO 11290-1:1996/Amd 1: 2004 and EN ISO 11290-2:1998/Amd 1: 2004 Portugal
Japan
226 environmental and raw materials samples (1) 100 retail food samples (55), 87 production swabs and samples (2) 5869 (54)
Romania
Romania
270 environmental samples (21)
N samples (N companies)
Spain
Country
EN ISO 11290-1, EN ISO 11290-2:2004, serotyping, ribotyping, PFGE
Food processing environment 50 ml BPW, 1 ml + 25 ml HF broth. 30 °C 24 h. 100 μl from tubes w/black media in 10 ml FF, 37 °C 24 h. 100 μl on Chromogenic agar. 16 s, PFGE, serogrouping PCR, RAPD-PCR, biofilm (SS), fluorescence microscopy Bacterial Analytical Manual protocol. Conf: sigB AT Sequencing. PFGE EN ISO 11290/2000 A1/2005. Gram staining and catalase, oxidase, and motility tests, VITEK 2, confirmation PCR, antibiotics susceptibility test with VITEK 2. Antimicrobial agents EN ISO 11290-1
Detection method
Table 1 (continued)
Tilapia sashimi. Cotton swabs, 10 × 10 cm
500 ml milk, brine; 500 g cheese; swabs and cotton swabs
RTEMP, no swab description in the methods Sausages, salami and soppresse samplings from the start to the end of production. 197 swabs analysed for Lm presence Cotton swabs + sponge swabs
[66] 12/2013–07/2014 2-year period [67]
[65]
[41]
2008–2013
2012–2013
[51]
[24]
[38]
[42]
[40]
[16]
[39]
Reference
2015?
2013–2015
2013–2015
Pickled vegs, cotton swabs (10 × 10 cm) Food samples, sponge swabs, liquid
2012–2013
2015?
2013–2016
2010–2011
Survey period
Sponge swabs
Cotton swabs. Analysed in groups of five if from the same area
3M sponges
Sponges moistened with LPT neutralising broth. 200 cm2
Samples type
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Curr Clin Micro Rpt Table 2
Reported Listeria monocytogenes outbreaks in the EU (2013–2015) [70] and in the USA (2013–2016) [71]
Year
Food vehicle
Reporting country
Cases
Hospitalised
Deaths
2013
Not available
Austria*
7
7
0
2013
Cheese
Belgium
2
0
0
2013 2013
Pig meat and products thereof Crustaceans, shellfish, molluscs and products thereof
Belgium France
2 3
0 1
0 0
013 2013
Vegetables and juices and other products thereof n.a.
Germany Netherlands
3 2
3 0
1 0
2013
n.a.
Sweden
2
0
0
2013 2013
Meat and meat products n.a.
Sweden UK
34 3
0 3
0 0
2013 2013
Crustaceans, shellfish, molluscs and products thereof Hummus
UK* USA-California
7 28
7 25
2 3
2013
n.a.
USA-Florida
9
9
4
2013 2013
n.a. Cheese-le frere
USA-Massachusetts USA-multistate
2 6
2 6
0 1
2013 2013
Latin style soft cheese Mexican style cheese, pasteurised
USA-multistate USA-multistate
8 9
7 8
1 1
2013
Frozen vegetables
USA-multistate
10
9
3
2013 2013 2014 2014
Hummus n.a. Bovine meat and products thereof Fish and fish products
USA-multistate USA-Rhode Island Belgium Denmark
8 4 2 6
7 2 1 6
1 2 0 0
2014 2014 2014 2014 2014
Other foods Mixed food Unknown Mixed food Unknown
Denmark Denmark Denmark Germany Germany*
41 6 8 2 4
0 0 0 2 1
0 0 0 0 0
2014 2014 2014 2014 2014
Unknown Vegetables and juices and other products thereof Unknown Other or mixed red meat and products thereof Fish and fish products
Malta Spain Spain Sweden Sweden
2 3 2 4 17
1 3 0 0 0
0 0 0 0 0
2014 2014 2014 2014 2014
Unknown Buffet meals Fresh curd cheese n.a. Peaches, unspecified; nectarine
Sweden UK USA-California and Maryland USA-Maine USA-multistate
5 4 8 2 2
1 4
0 0
2 2
0 1
2014 2014 2014 2014 2014 2014 2014 2014 2014 2015 2015 2015 2015
Mung bean sprouts Caramel apple Raw milk Smoked fish n.a. n.a. Sprouts Mexican style cheese, pasteurised Milkshake Unknown Buffet meals Mixed food Unknown
USA-multistate USA-multistate USA-multistate USA-multistate USA-New York USA-New York USA-Virginia USA-Washington USA-Washington Denmark Finland Germany Germany#
5 35 2 4 2 2 2 3 2 2 24 159 6
3 34 2 4 2 2 2 2 2 2 1 2 0
2 7 1 0 2 0 0 1 0 0 0 0 0
Curr Clin Micro Rpt Table 2 (continued) Year
Food vehicle
Reporting country
Cases
2015 2015
Unknown Pig meat and products thereof
Greece Italy
2015
Unknown
Latvia*
4
2
0
2015 2015
Fish and fish products Mixed food
Netherlands Portugal
3 3
0 3
0 0
2015
Vegetables and juices and other products thereof
Spain
3
1
0
2015 2015
Mixed food Unknown
Sweden Sweden
13 2
1 0
0 0
2015 2015
Lettuce, prepackaged American cheese, pasteurised
USA-multistate USA-New York
19 2
19 1
1 1
2015
Sour cream
USA-Oregon
2
0
0
2016 2016
n.a. Frozen foods
USA-multistate USA-multistate
5
5 9
1 3
2016 2016
Salads Artisanal soft cheese, unpasteurized
USA-multistate USA-multistate
19 9
1 2
2 12
10
Hospitalised
Deaths
2 12
2 2
n.a. not available *Two outbreaks #Three outbreaks
Comparing surveys on prevalence of L. monocytogenes at retail level has the same limitations as comparing surveys at processing level, as shown in Table 2.
EFSA Baseline Survey In 2010–2011, a European Union-wide baseline survey on the prevalence of L. monocytogenes at retail level was undertaken [72]. Similar methodologies were used to determine the prevalence of L. monocytogenes in packaged (not frozen) hot or cold smoked or gravad fish, packaged heattreated meat products and soft or semi-soft cheeses in 26 member states and one non-member state. A total of 3053 batches of fish, 3530 batches of deli-meat and 3452 batches of cheese were analysed at the end of their shelflife for detection and enumeration of L. monocytogenes. A prevalence of 10.3% was determined for the fish samples while the prevalence on meat and cheese was 2.07 and 0.47%, respectively. The number of samples with a L. monocytogenes count exceeding the level of 100 CFU/g at the end of shelf-life was 1.7, 0.43 and 0.06% for fish, meat and cheese samples, respectively. Surveys conducted during a long period or on thousands of samples usually result in more valuable data on the prevalence and persistence of L. monocytogenes and can give the FBOs a greater opportunity to improve their hygiene practices, focusing on specific issues, for example staff workflows, sanitising regimes, etc. [24, 38, 42, 65, 73].
Growth of L. monocytogenes on Food If L. monocytogenes is present in the food processing environment, it can cross-contaminate the food being produced and, therefore, the ability of the food to support its growth becomes important. The EU and other jurisdictions have published guidelines for undertaking challenge studies to determine the ability of food to support the growth of L. monocytogenes [12, 13, 74]. In general, determining the ability of foods to support the growth of L. monocytogenes must be done for each food as many RTE foods are traditionally produced in local regions using variable formulations which may have an impact on the growth of L. monocytogenes. Also, any changes in the ingredients or processing method, either due to the desire to extend the shelf-life of a product or to address the consumer’s demand for the reduction of preservatives in their food, may lead to new risks [75] and therefore impact on the ability of L. monocytogenes to grow. Challenge studies must therefore be undertaken with every newly formulated food. In cases where growth potential is demonstrated (≥ 0.5 log increase in numbers from day 0 to day end), the initial numbers and the growth rate determine if the numbers will exceed the limit of 100 CFU/g during shelf-life. The EURL Lm Technical Guidance document [74] includes a section on undertaking challenge studies to determine growth rate. The major differences between the challenge studies to determine growth potential and the challenge studies to determine growth rate are that when testing growth rate, each strain must be tested individually,
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sampling must be undertaken on at least 10 occasions and food storage must be carried out at a uniform temperature. The survival and growth of L. monocytogenes in food depends on factors intrinsic to the food, for example pH and water activity, and extrinsic factors such as relative humidity, storage temperature and packing material. Processing techniques used in food production, temperature flux and the physiological state of cells can cause variations of survival and growth. Previously stressed cells exposed to sublethal conditions can cause L. monocytogenes to be more resistant to additional stressors [76, 77]. Prior to undertaking challenge studies in food, predictive modelling can be used to give an indication of the ability of the food to support growth. Computer programmes such as “Combase” [78, 79], “Food Spoilage and Safety Predictor” [80] and “Pathogen Modelling Programme” [81] can be used to facilitate such estimations. It is important to remember that predictive modelling is only an estimation of the ability of the food to support growth. If growth is predicted, there could be other characteristics of the food that would inhibit growth, such as competing microflora, that are not accounted for in the models. Using Combase, Schvartzman et al. [82] determined that in 40% of cases where growth in cheese was predicted, no growth actually occurred in the cheese. Therefore, while predictive modelling is a good place to start, the results are not definitive.
Food Recalls and Outbreaks Due to L. monocytogenes Listeria monocytogenes is a public health hazard that leads to incidences of listeriosis which has a high mortality rate. For that reason, the occurrence of L. monocytogenes in food is treated as a very serious issue by regulatory authorities. Such occurrence leads to recalls/withdrawals of food and to outbreaks of listeriosis.
Recalls Positive results for L. monocytogenes in food must lead to the protection of public health and the recall/withdrawal of contaminated food from the market. L. monocytogenes contamination of a product can be very low and not evenly distributed on the food, therefore, testing of the food is important. If any contamination is detected either before or after product release, then a product recall/withdrawal, either voluntary or compulsory, may be instigated. Such recall/withdrawal can have major consequences for food businesses, especially where a product from one company is used as an ingredient by other companies. Economic loss, combined with reputational damage can be detrimental for companies. As an example, the “US recalls, Market Withdrawals & Safety Alerts”
website has on file 52 alerts involving L. monocytogenes between January and September 2017 involving a large number of foods and food companies [83]. Where products are used as ingredients by other companies, recalls can be very extensive and can result in hundreds of products being recalled [84–86].
Outbreaks Despite the efforts of the food industry to prevent and control L. monocytogenes both in Europe and USA, currently the incidence is about 0.2–0.5 cases/100,000 population [70, 71]. On Table 2 are presented the most recent outbreaks in the EU (2013–2015) [70] and in the USA (2013–2016) [71]. It is however important to keep in mind that the majority of the L. monocytogenes cases are sporadic and many are not reported [87].
Control of L. monocytogenes in the Food Processing Environment Traditional Methods for Control of L. monocytogenes in the Food Processing Environment Creating and maintaining a completely L. monocytogenes-free processing environment is important in ensuring the production of safe food. The occurrence of L. monocytogenes in the processing facility can result from a number of different sources, for example, contaminated incoming raw materials, staff members acting as L. monocytogenes carriers, insufficient cleaning strategies and sampling programmes in place, the facility design and location. Each of these factors must be c on t rol l ed in or de r t o r ed uc e t h e oc cu rre nc e of L. monocytogenes, to interrupt the route of transfer to the food. Although expensive, subtyping of isolates, using methods such as PFGE, can facilitate the identification of putative routes of contamination and persistence [67]. Awareness of L. monocytogenes (facilitated by detailed documentation) that can be obtained from having an appropriate processing environment sampling plan, sampling appropriate places at the right frequency, is an important step in controlling the organism. There is a need for standardisation of sampling, which should be done with a sponge-type swab, allowing sufficient surface area to be sampled. If occurrence of L. monocytogenes is detected, it can be eliminated through targeted intervention strategies that help to prevent product contamination. Adequate sampling will allow problems of contamination to be pre-empted and addressed in a timely manner [88]. L. monocytogenes can be resistant to sanitisers and detergents and can form biofilm, making it difficult to inactivate [89]. This can be compounded by its survival in niches and harbourage sites that can be difficult to clean. Therefore,
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attention to detail in cleaning and disinfection, hygienic design of equipment and the establishment of critical control areas close to any food contact surface will all contribute to the control of L. monocytogenes. Maintaining good hygiene practices during installation of new equipment or during construction at a processing facility can be challenging [24].
Novel Methods for Control of L. monocytogenes in Food While methodologies for the control of L. monocytogenes in food are necessary, avoiding food contamination by having a L. monocytogenes-free processing environment can reduce the risk of food contamination. New and exciting methodologies include research on the use of lytic bacteriophages and bacteriocins as an alternative, or in addition to, commonly used L. monocytogenes control practices [90, 91]. Commercial bacteriophages products against L. monocytogenes, such as Listex™ P100 and ListShield™, are available for use, primarily in food. Both are approved by the USA FDA as Generally Recognised as Safe (GRAS) antimicrobial agents in food production in the USA [92, 93], while in Europe, Listex™ P100 is currently in the process of approval by the European Food Safety Authority (EFSA) [94]. Studies have highlighted the effectiveness of the bacteriophage treatments at inactivation of L. monocytogenes in various situations [95]. They have also shown that effectiveness is related to various factors, such as the host range of the bacteriophage, the bacteriophage resistance of some strains, the quantity of the L. monocytogenes and phage inoculum and physical factors related to the environment (i.e. temperature) and to the food itself (pH, texture, etc. [96•, 97–101]). As only a limited number of lytic bacteriophage are available, purified bacteriophage-derived lytic enzymes, such as endolysins, which specifically cleave the peptidoglycan wall of the cells are being investigated (for review see references [102, 103••]). To increase their effectiveness, high hydrostatic pressure can be used in combination with endolysins [104]. Alternatively, bacteriocins are antimicrobial compounds produced by bacteria against competitors and their utilisation for control of L. monocytogenes in food production is being investigated [105, 106]. Resistance of some L. monocytogenes to bacteriocins, and subsequent growth of these resistant strains, is a challenge in the use of bacteriocins [107, 108]. The most promising results are by a combination of novel biotechnologies, including a mixture of natural antagonistic bacteria and their bacteriocins, or a combination of antagonistic bacteria, bacteriocins and bacteriophages [106], or the utilisation of bacteriocins and bacteriophages [109].
Conclusions A L. monocytogenes-free food processing environment will facilitate the prevention of cross-contamination of food, thus avoiding recalls and withdrawals, preventing public health issues. Sampling and analysis for L. monocytogenes in the food processing environment helps to create awareness and understating of L. monocytogenes, informing targeted corrective actions. If foods are contaminated with L. monocytogenes, novel methods for control of its growth, such as bacteriophage and bacteriocins, are being investigated. Further research on these is required in order to fully capitalise on their potential.
Compliance with Ethical Standards Conflict of Interest The authors declare that they have no conflict of interest. Human and Animal Rights and Informed Consent This article does not contain any studies with human or animal subjects performed by any of the authors.
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