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Grigore-Gurgu, L.; Bucur, F.I.; Mihalache, O.A.; Nicolau, A.I. Biocontrol of L. monocytogenes in Meat Products. Encyclopedia. Available online: https://encyclopedia.pub/entry/55977 (accessed on 14 April 2024).
Grigore-Gurgu L, Bucur FI, Mihalache OA, Nicolau AI. Biocontrol of L. monocytogenes in Meat Products. Encyclopedia. Available at: https://encyclopedia.pub/entry/55977. Accessed April 14, 2024.
Grigore-Gurgu, Leontina, Florentina Ionela Bucur, Octavian Augustin Mihalache, Anca Ioana Nicolau. "Biocontrol of L. monocytogenes in Meat Products" Encyclopedia, https://encyclopedia.pub/entry/55977 (accessed April 14, 2024).
Grigore-Gurgu, L., Bucur, F.I., Mihalache, O.A., & Nicolau, A.I. (2024, March 07). Biocontrol of L. monocytogenes in Meat Products. In Encyclopedia. https://encyclopedia.pub/entry/55977
Grigore-Gurgu, Leontina, et al. "Biocontrol of L. monocytogenes in Meat Products." Encyclopedia. Web. 07 March, 2024.
Biocontrol of L. monocytogenes in Meat Products
Edit

Listeria monocytogenes is a foodborne pathogen that causes listeriosis, a group of human illnesses that appear more frequently in countries with better-developed food supply systems. Meat and meat products, especially the ready-to-eat (RTE) ones, have been reported as being a major food vehicle for L. monocytogenes transmission to humans. The cause of this phenomenon is mainly attributed to the contamination during processing or post-processing steps, such as slicing and packaging, followed by the growth of the pathogen during storage to numbers that endanger the consumers’ health.  In the attempt to satisfy the consumers’ demand with respect to both healthy and safe foods, studies have focused on biocontrol methods, including bacteriophages, antagonistic microbial interactions, and plant- or microbe-derived substances having antilisterial activity.

bacteriophage lactic acid bacteria bacteriocins endolysins antilisterial listeriosis active packaging

1. Introduction

Listeria monocytogenes is a foodborne pathogen responsible for listeriosis, the fifth most reported zoonosis in humans in the European Union (EU). In 2022, in Europe, 2.738 listeriosis cases were reported, with a notification rate of 0.62/100,000 individuals leading to 1.330 hospitalizations (48.6%) and 286 deaths (10.4%). L. monocytogenes was also responsible for 35 foodborne outbreaks and 296 foodborne illnesses-related to the outbreaks, with 242 hospitalizations (81.8%) and 28 deaths (9.5%) [1]. Listeriosis mainly affects vulnerable consumer groups such as children, pregnant women, the elderly, and individuals with immunocompromised systems. This is also validated by the fact that most of the foodborne illness cases were reported in the age group of over 64 years old [1]. While in healthy individuals listeriosis manifests itself as mild influenza and gastroenteritis, in vulnerable consumers, it results in severe symptoms like septicemia, meningitis, and miscarriage/stillbirth [2]. L. monocytogenes is often associated with pig meat and products thereof, fish and fish products, mixed food, vegetables and juices, and dairy products other than cheese. This is confirmed by the Rapid Alert System for Food and Feed (RASFF), in which 340 alerts were reported in the last three years, mainly with L. monocytogenes in fish, meat, and dairy products [1]. L. monocytogenes is a food safety threat due to its ubiquitous nature and ease of entering the processing environment through raw ingredients. Some strains of L. monocytogenes can survive for many years and serve as a source of ongoing cross-contamination due to their ability to cling to a range of abiotic surfaces [3][4][5]. Out of 37,779 samples tested at the manufacturing stage, 578 (1.53%) were positive for L. monocytogenes. In 2022, the highest notification rate and number of cases of listeriosis were recorded since 2007, indicating the need for ongoing research and mitigation strategies for the reduction in L. monocytogenes [1]. However, L. monocytogenes is known to be a difficult organism to eradicate even when the best safety management plans are implemented [6][7].

2. The Use of Bacteriophages in Meat Products

Nowadays, two phage biocontrol products against L. monocytogenes are commercially available: ListShieldTM (formerly known as LMP-102TM) produced by Intralytix Inc. (Baltimore, MD, USA) and PhageGuard Listex™ (formerly known as ListexTM or P100) produced by Micreos Food Safety (Wageningen, The Netherlands). The LMP-102™ is a mixture of six purified phages with specific activity against the pathogen that could be applied on the surface of the meat products by spraying at a level not exceeding 1 mL per 500 cm2 [8]. Unlike the ListShield phage product, the PhageGuard Listex contains only one phage, P100 [9].
Table 1 summarizes studies regarding the efficacy of commercial antilisterial bacteriophages aimed to control L. monocytogenes in meat and meat products. The degree of L. monocytogenes reduction has been shown to depend on several factors: the ratio between bacteriophages titer and contamination level [10], diversity of pathogenic strains [10], the contact between the phages and the host [11], occurrence of host resistance to phages, products’ chemical composition and characteristics, and storage conditions [10].
Table 1. Studies exploring the application of bacteriophages as biocontrol tools against L. monocytogenes in meat and meat products.
PFU—plaque-forming units; CFU—colony-forming units; and RT—refrigeration temperature.
Regarding the contact between bacteriophages and L. monocytogenes cells contaminating the meat products, one study tested the efficiency of Listeria bacteriophage A511 in a cooked-meat model system under multiple scenarios: both bacteriophage and pathogen in the meat, bacteriophage in the meat and pathogen on its surface, pathogen in the meat and bacteriophage on its surface, and both bacteriophage and pathogen on the meat surface. The research revealed that the phages’ ability to control the growth of L. monocytogenes on the meat product is limited because their direct contact with the targeted bacterial cells is limited [11].

3. Endolysins in Meat Products

There is no sufficient data available in the scientific literature regarding the use of endolysins to control L. monocytogenes in meat and meat products. The inactivation of L. monocytogenes by endolysins in combination with high-pressure processing (HPP) was described by Nassau et al. [18]. Three strains of L. monocytogenes (ATCC 15313, WSLC 11043, WSLC 11048) were co-incubated with different endolysin concentrations, ranging from 0.16 mg/mL to 20 mg/mL for PlyP40 and Ply511, respectively, and 100 mg/mL for PlyP825. The enzyme activity was assessed at 90 and 180 min before HPP treatments. The HPP parameter level of 200 MPa maintained for 2 min is usually too low to kill the pathogenic cells when this type of treatment is applied without any other cell sensibilization. Interestingly, the results obtained highlighted a good reduction in Listeria spp. cells (up to 5 log CFU/mL), when a synergic effect between endolysins and the HPP treatment (200 MPa/2 min/30 °C) was obtained. The use of endolysins not only significantly enhanced the bactericidal impact of HPP but also facilitated the deactivation of bacterial cells at considerably lower pressure thresholds [18]. A similar strategy by combining endolysin PlyP825 and HHP processing was applied to inactivate L. monocytogenes artificially inoculated in smoked salmon, in a concentration of 107 CFU/g. The results showed a reduction of only 1.6 log cycles even when a higher level of endolysin (34 µg/mL) and HPP treatment (500 MPa/10 min/25 °C) were used [19].

4. Lactic Acid Bacteria (LAB) in Meat Products

Another biocontrol method used to prevent the proliferation of L. monocytogenes in meat products is fermentation either occurring naturally, as a result of indigenous LAB presence, or stimulated by adding starter cultures. Fermentation results in a pH decrease through the formation of lactic acid. Following fermentation, meat products need to be subjected to a drying step, so that the final water activity drops below the limit that allows L. monocytogenes to grow. On the other hand, the inhibitory effect of LAB against the pathogen during fermentation may be caused by the production of antimicrobial peptides called bacteriocins.
Several studies evaluated the behavior of L. monocytogenes in fermented meat products in terms of interaction between the pathogen and LAB. Huang et al. [15] showed that LAB addition at a concentration of ~7 log CFU/g to meat sausages subjected to simultaneous fermentation and drying (incubation at 30 °C and relative humidity RH of 76% for 5 days) caused the inhibition of the L. monocytogenes population (initially inoculated at ~5 log CFU/g) growth. Moreover, the number of pathogenic cells indicated a slow decrease during the process, by ~0.5 log CFU/g. A similar experiment was reported by Giello and colleagues [20] who co-cultured L. monocytogenes OH and Scott A (104 CFU/g) and Lactobacillus curvatus 54M16 (107 CFU/g), a strain-producing bacteriocin, in sausages ripened for three days at 20 °C (RH: 75–85%) followed by other 25 days at 15 °C (RH: 65–70%). Their results showed that the number of L. monocytogenes decreased under the detection limit within the 5 days of co-incubation at 15 °C. Moreover, after 48 h at 15 °C, the only surviving strain was the OH strain, as this was demonstrated by the RAPD-PCR profile [20].
The effect of the product’s changing pH on L. monocytogenes capacity to multiply during fermentation was also assessed. Kamiloğlu and co-workers [21] concluded that the reduction in L. monocytogenes population (2.74 log CFU/g) during the ripening of suçuk (Turkish sausages), for 11 days, was especially due to the fast acidification (pH below 5) caused by the autochthonous L. plantarum S50, added as starter culture. The authors did not exclude the antagonistic activity of LAB against the pathogen as a supplementary inhibitory factor, as the strain was confirmed to produce bacteriocins by in vitro tests [21].
An innovative approach to benefit from LAB biopreservation potential is to incorporate postbiotics, namely, the substances released during their growth, such as bacteriocins, organic acids, carbon dioxide, and di-acetylene, into polymeric films, which are then used as active packaging materials. In this regard, Beristain-Bauza and co-workers [22] supplemented whey protein films with L. sakei cell-free supernatant and used them to wrap beef cubes artificially contaminated with L. monocytogenes (~3 log CFU/g). The antimicrobial film reduced L. monocytogenes population by 1.4 log CFU/g during refrigerated storage (4 °C) for 120 h [22]. More recently, Shafipour et al. [23] obtained an antimicrobial meat wrapping paper based on bacterial nanocellulose that contained postbiotics produced by L. plantarum. The nanopaper proved to have a strong antilisterial activity, as it was shown to reduce L. monocytogenes counts in ground meat by ~5 log CFU/g after storage at 4 °C for 9 days [23].

5. Bacteriocins in Meat Products

Nisin’s efficacy in reducing Listeria spp. cells in meat and meat products has been demonstrated in various studies [24][25][26]. However, the occurrence of nisin resistance in L. monocytogenes cells after exposure to this peptide is not an uncommon phenotype [27], and this fact led to the necessity of combining it with other hurdles, represented by either antimicrobial substances or physical treatments. Wongchai et al. showed that nisin (62.5 µg/mL) combined with salts of organic acids could overcome this problem, as the synergism with citric acid (1000 µg/mL) prevented the growth of L. monocytogenes on pork ham during storage at 4 °C for 4 days [28]. Hammou et al. also noticed that nisin (200 µg/g) combined with NaCl (salt; 12%) can significantly inhibit the growth of the pathogen on natural sheep casing during 90 days of storage at 6 °C [29].
Other researchers focused on the synergism between nisin and EOs as a preventive strategy regarding L. monocytogenes proliferation in meat and meat products. Raeisi and colleague [30] investigated the fate of L. monocytogenes (at an initial concentration of 3.2 log CFU/g) during storage at 4 °C for 15 days on chicken meat coated with sodium alginate that contained either nisin (N) alone or in combination with Cinnamomum zeylanicum EO (CEO + N) and rosemary EO (REO + N). The results of the study indicated a better efficiency in controlling L. monocytogenes growth of the coatings supplemented with CEO + N (final concentration of 6.4 log CFU/g) and REO + N (final concentration of 6.6 log CFU/g) than that containing only N (final concentration of 7.5 log CFU/g) [30]. Carvacrol, the main constituent of thyme or oregano EOs, was shown to affect L. monocytogenes cells by inducing irreversible damage to their cell wall and cellular membranes [31]. Therefore, it is considered a good candidate in combating the occurrence of L. monocytogenes resistance against nisin. Indeed, the pathogen’s growth on sliced bologna sausage was significantly decreased in samples treated with nisin (25 µg/mL) together with carvacrol (62.5 µg/mL) compared to those treated with these antimicrobial substances separately. Moreover, due to the synergism between the two additives and, as such, the side effects concerning the sensorial properties, consumers’ acceptance of meat products treated with EOs can be increased [31].
Nisin was shown to increase the L. monocytogenes inactivation rate in meat products by high-pressure processing (HPP) [32][33]. Teixeira et al. [34] obtained a reduction in L. monocytogenes counts on ham by more than 5 log CFU/g when the meat product was subjected to a combined treatment consisting of HPP (500 MPa, 5 °C, 3 min) and nisin (~2 µg/cm2). Moreover, after 4 weeks of refrigerated storage of ham, L. monocytogenes cells remained undetectable [34]. By achieving microbial safety, synergism with nisin may also contribute to the reduction in the HPP expenses at a level comparable to that of the traditional methods of meat product processing, such as heat treatments [32]. This bacteriocin was also successful in the enhancement of gamma radiation treatments against L. monocytogenes [35][36][37]. The study conducted by Mohamed and co-workers combined gamma radiation with nisin and showed an antimicrobial additive effect against L. monocytogenes, during the first 24 h after treatment, and a synergistic one, during the next 48 h of storage at 4 °C. The authors suggested as a potential strategy for L. monocytogenes elimination the combined treatment consisting of nisin (103 IU/g) and gamma radiation applied at 1.5 kGy [38].
The next most studied bacteriocin in L. monocytogenes biocontrol research is pediocin. The pediocin-like peptides belong to class IIa of bacteriocins, being produced by Pediococcus spp. and described as biologically active against Listeria spp. [39][40]. Their effectiveness in the reduction of L. monocytogenes load in meat products by direct addition or produced by LAB strains has been demonstrated by former studies [41][42][43]. More recently, the biocontrol of L. monocytogenes by pediocin was evaluated by its incorporation in active packaging materials. Such materials are intended to inhibit or delay the growth of undesired microorganisms while minimizing preservatives’ addition to food products [44]. The in vivo approach showed encouraging results [45]. For instance, Woraprayote [46] developed an antilisterial polylactic acid/sawdust particle biocomposite film incorporated with pediocin PA-1/AcH. The highest anti-listeria activity was achieved by pediocin adsorption to the coating at 11.63 ± 3.07 μg protein/cm2. The authors indicated that the obtained material’s potential of L. monocytogenes inhibition in contact with the contaminated raw sliced pork could be of 99%, as suggested by a model study [46]. Another study assessed the efficacy of a film based on cellulose-containing 25% or 50% pediocin against Listeria spp. on sliced ham. While the film containing 25% pediocin could not prevent the growth of L. innocua, the one containing 50% pediocin reduced the bacterium by 2 log cycles after 15 days of storage at an abusive temperature (12 ± 1 °C) compared to the control (without bacteriocins) [44]. Pediocin was shown to enhance the inactivation of Listeria in meat products treated with HPP. The HPP (300 MPa, 10 °C, 5 min) in conjunction with the ex or in situ pediocin bacHA-6111-2 production was applied in the study of Castro et al. [47] to inactivate L. innocua inoculated in fermented meat sausages and to evaluate the survival of the bacterium during 60 days of storage at 4 °C. Considering a contamination level more likely to occur during the sausages’ processing (~104 CFU/g), it was shown that both ways of pediocin production resulted in a synergistic effect with HPP, as the counts of Listeria spp. after the combined treatment decreased by >2 log CFU/g. However, the analysis of bacterium behavior during the storage of sausages revealed that in situ bacteriocin production was more efficient regarding the control of its growth [47].

6. Essential Oils in Meat Products

Many studies evaluated EOs’ potential to control L. monocytogenes in meat and meat products. The aromatic oils have been applied either as such [37][48][49][50], encapsulated [51], or incorporated into edible coatings [52] (Table 2). The last two delivery systems were reported to be more acceptable to consumers in terms of meat products’ organoleptic properties after being applied. Besides this, the encapsulation of EOs and their addition to various active packaging materials have been shown to solve the inconveniences regarding EOs’ instability to external factors [53] and poor solubility in foods with low-fat content [54]. Also, due to the need for relatively high amounts of EOs to achieve a satisfactory degree of pathogens’ inactivation, the treated meat products can become inappropriate for consumption as a result of altered sensorial characteristics and possible toxicity [55]. Lower concentrations of EOs can be used if combining them with other natural antimicrobial substances, such as bacteriocins [56] or physical treatments, results in a synergistic effect. Bearing in mind that minced beef supplemented with 0.9% thyme oil was unacceptable in terms of organoleptic properties, to achieve a sufficient inactivation degree of L. monocytogenes, Solomakos et al. instead recommended a combined treatment consisting of 0.6% thyme oil and 1000 IU/g nisin [56]. In the study by Huq et al. [37], it was shown that during storage at 4 °C, the synergism between oregano (250 µg/mL) or cinnamon (250 µg/mL) EOs and nisin (16 µg/mL) determined slower growth rates of L. monocytogenes on cooked ham (0.20 and 0.11 ln CFU/g/day, respectively) compared to EOs alone (0.21 and 0.18 ln CFU/g/day, respectively) [37]. Moreover, the encapsulation of cinnamon EO combined with nisin and the treatment of the RTE ham with the obtained capsule resulted in a much lower growth rate of the bacterium, of 0.05 ln CFU/g/day. The increased efficiency was attributed to better preservation of the antimicrobials’ biological activity when entrapped in the biopolymeric matrix and their better distribution on the meat product’s surface [37][57].
The nanoemulsion of EOs has been shown to generate better results in terms of L. monocytogenes biocontrol in comparison with emulsions. Some of the advantages of using EOs in this form are the improved stability and increased physical resistance of the EOs, and better transferability of the hydrophobic bioactive compounds. Kazemeini [58] compared the antimicrobial activity of an alginate edible coating containing the nanoemulsion of Trachyspermum ammi EO to that of the coating containing the emulsion of the same EO against L. monocytogenes inoculated on turkey fillets. By the end of the contaminated meat product’s storage (4 ± 1 °C for 12 days), the counts of L. monocytogenes were lower in the meat treated with T. ammi EO nanoemulsion (7.12 ± 0.09 log CFU/g) compared to that treated with T. ammi emulsion (5.53 ± 0.13 log CFU/g) [58].
Dini et al. [59] assessed the efficacy of a chitosan film containing 1% nanoemulsion of cumin EO combined with low-dose gamma irradiation (2.5 kGy) against L. monocytogenes on beef loan during refrigerated storage. While the edible film alone did not exert good control on the pathogenic bacterium’s growth, its combination with the physical treatment generated an enhanced antilisterial effect, which might become an effective strategy to ensure the microbiological safety and improved shelf-life of the meat product [59]. Khaleque et al. [50] showed that the reduction in L. monocytogenes population in ground beef treated with 5% clove EO was more accelerated at refrigeration (8 °C) and chill (0 °C) temperatures compared to the storage at freezing temperatures (−18 °C) [50]. Solomakos and colleagues noticed that the antilisterial effect of EOs was also influenced by the storage temperature, and a stronger antimicrobial activity of thyme EO against the pathogen in minced beef was found when stored at 10 °C than at 4 °C [56].
Table 2. Studies exploring the application of essential oils as biocontrol tools against L. monocytogenes in meat and meat products.

Meat or Meat

Products

Application of EOs

Contamination

Procedure

Storage Conditions

and Results

References

Beef meatballs

Addition of O. vulgare,

R. officinalis, and T. vulgaris at concentrations of 0.5%, 1%, or 2% (v/w)

Inoculation with a five-strain cocktail

(L. monocytogenes HSD 2434, HSD3261, HSD 3705, HSD 3948, HSD 4210) at 10, 102, 103, and 104 CFU/g

Concentrations of 2% and 1%

restricted the growth of

L. monocytogenes, regardless of the initial microbial loading, during storage at 4 °C for 14 days, but affected the meatballs' flavor.

The concentration of 0.5% restricted the growth of L. monocytogenes at initial counts of <102, and the taste of

meatballs was acceptable.

[48]

Italian

mortadella

Addition of combined

T. vulgaris and R. officinalis at concentrations of 0.025% and 0.05% during

manufacturing

Contamination of

mortadella slices with a three-strain cocktail

(L. monocytogenes

ATCC 19111,

ATCC 13932,

and ATCC 19117)

at ~2.5 log CFU/g

Compared to the untreated

contaminated mortadella, the addition of combined EOs to the concentrations of 0.025% and 0.05% led to a reduction in L. monocytogenes by 2.29 log CFU/g and 2.79 log CFU/g by the end of storage at 4 °C for 30 days.

[60]

Ground beef

Addition of crude and commercial C. cassia and

S. aromaticum EOs at

concentrations of 5% and

10%, and 2.5% and 5%,

respectively

Inoculation with a five-strain cocktail

(L. monocytogenes

ATCC 43256,

ATCC 49594,

JCM 7676,

JCM 7672, and

JCM 7671)

The ground beef was stored at 8 °C and 0 °C for 7 days and at −18 °C for 60 days.

A 10% concentration of clove EO (both crude and commercial) completely inactivated L. monocytogenes within 3 days of storage, irrespective of temperature.

A 5% concentration of clove EO (both crude and commercial) reduced L. monocytogenes gradually throughout storage, irrespective of temperature, without achieving complete

inactivation.

The 2.5% and 5% concentrations of crude and commercial cinnamon EO did not inactivate L. monocytogenes throughout storage.

Consumers did not find the ground beef treated with 10% clove EO

acceptable, while some of them found the meat treated with 5% clove EO acceptable.

[16][30][50]

Dry-cured

ham-based medium

Addition of C. cassia EO in dry-cured ham-based medium with water activity of 0.93 or 0.95 at a concentration of 10%

Inoculation with a serotype 4 L. monocytogenes strain at ~4 log CFU/mL

During storage at 7 °C for 7 days, 10% cinnamon EO completely inhibited

L. monocytogenes growth irrespective of the ham-based medium’s aw.

[16]

Fresh chicken meat

Corn starch edible coating containing Zataria multiflora EO nanoemulsion alone and fortified with cinnamaldehyde

Contamination of the meat with

L. monocytogenes to a final concentration of ~104 CFU/g followed by its immersion in the corn starch solutions

The coating with fortified nanoemulsion was more effective in controlling L. monocytogenes than that with the nanoemulsion alone during storage at 4 ± 1 °C for 20 days, with a growth difference between the treatments of ~1 log CFU/g.

[52]

Fresh beef

Soy protein edible coatings containing 1%, 2%, or 3% thyme or oregano EOs

Contamination with

L. monocytogenes at

5.59 log CFU/g followed by beef pieces immersion in the coating solutions

At the end of storage (14 days at 4 °C) period, compared to the uncoated beef pieces, coating with 1, 2, and 3% thyme and oregano EOs reduced

L. monocytogenes by

1.02, 1.73, and 1.97 log CFU/g and 0.91, 1.66, and 1.90 log

CFU/g, respectively.

The treatments improved the color of beef, and its organoleptic properties were acceptable.

[61]

Spiced beef

Chitosan films incorporated with apricot (Prunus armeniaca) kernel EO at 0%, 0.125%, 0.25%, 0.5%, and 1% (v/v)

The beef slices were inoculated with

L. monocytogenes to

104 CFU/g and placed in contact with the antimicrobial films

After 15 days of storage at 4 °C, compared to the control samples (film without EO addition), the chitosan films containing 0.5 and 1% apricot kernel EO reduced L. monocytogenes by 3.3 and 4.1 log CFU/g.

After 24 days of storage, the sensorial attributes (taste, color, texture, and overall acceptance) of the spiced beef packed with the chitosan film containing 1% apricot kernel oil were significantly improved compared to those of the unpacked one.

[62]

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