Activity and Safety Evaluation of Natural Preservatives

Food Research International 190 (2024) 114548
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Food Research International

journal homepage: www.elsevier.com/locate/foodres
Review
Activity and safety evaluation of natural preservatives

Huiying Dong a, 1, Yang Xu a, 1, Qingqing Zhang a, Hua Li a, b, *, Lixia Chen a, **
a
Wuya College of Innovation, Key Laboratory of Structure-Based Drug Design & Discovery, Ministry of Education, Shenyang Pharmaceutical University, Shenyang
110016, China
b
Institute of Structural Pharmacology & TCM Chemical Biology, Fujian Key Laboratory of Chinese Materia Medica, College of Pharmacy, Fujian University of Traditional
Chinese Medicine, Fuzhou 350122, China
A R T I C L E I N F O A B S T R A C T
Keywords: Synthetic preservatives are widely used in the food industry to control spoilage and growth of pathogenic mi
Safety evaluation croorganisms, inhibit lipid oxidation processes and extend the shelf life of food. However, synthetic preservatives
Food additives have some side effects that can lead to poisoning, cancer and other degenerative diseases. With the improvement
Essential oils
of living standards, people are developing safer natural preservatives to replace synthetic preservatives,
Tea polyphenols
Nisin
including plant derived preservatives (polyphenols, essential oils, flavonoids), animal derived preservatives
Natamycin (lysozyme, antimicrobial peptide, chitosan) and microorganism derived preservatives (nisin, natamycin,
Phage ε-polylysine, phage). These natural preservatives exert antibacterial effects by disrupting microbial cell wall/
membrane structures, interfering with DNA/RNA replication and transcription, and affecting protein synthesis
and metabolism. This review summarizes the natural bioactive compounds (polyphenols, flavonoids and ter
penoids, etc.) in these preservatives, their antioxidant and antibacterial activities, and safety evaluation in
various products.
1. Introduction essential nutrient (Gutiérrez-del-Río et al., 2018).

Currently, natural preservatives are a research focus and people
Food preservatives are compounds that occur naturally in foods or generally believe that they have beneficial properties and few side ef
are added directly to them. They inhibit the growth of spoilage micro fects (Pateiro et al., 2021). As a substitute for synthetic compounds,
organisms, pathogens, and lipid oxidation, extend the shelf life of food essential oils and other natural substances have been widely used in the
and ensure product safety (Mittal et al., 2023). Various preservatives on meat industry and have been approved by the Food and Drug Admin
the market, including sodium benzoate and sodium propionate, potas istration (FDA) for using in food (Food and Drug Administration, 2023).
sium sorbate, sorbic acid, nitrite, sulfite, nisin, natamycin, potassium However, their natural source does not necessarily mean that they are
lactate, ascorbic acid, citric acid, tartaric acid, etc., have been approved safe to use. It is necessary to evaluate important aspects such as dosage,
by regulatory authorities for use as food preservatives (Kuorwel et al., efficacy, mechanism of action and toxicity. Sometimes it is necessary to
2011). However, the excessive use of some preservatives poses a threat use them in higher concentrations to achieve the same effect as com
to the nutrition or health of consumers. For example, sorbic acid can mercial additives, which can have adverse effects on the product and
combine with sulfhydryl bonds in many microbial cell enzymes, inhibit even toxicity problems. Therefore, it is necessary to consider combina
cell growth and microbial reproduction, slow down the production of tion with other preservatives to achieve synergistic effects allowing
mold and yeast, but also inhibit probiotics, resulting in intestinal flora better activity at lower concentrations. The application of natural pre
disorder, low immunity (Ismail et al., 2020). Excessive intake of nitrite servatives in food has been reported, but the summary of their safety
and nitrate can increase the risk of cardiovascular disease, and sodium evaluation in terms of dosage and toxicity is not comprehensive enough.
nitrite can be carcinogenic when processed at high temperatures. Sulfite This article provides a more comprehensive review of the activity,
can cause the degradation of vitamin B1 (thiamine) in food, which is an application, and safety of natural preservative, the combined use of
* Corresponding author at: Wuya College of Innovation, Key Laboratory of Structure-Based Drug Design & Discovery, Ministry of Education, Shenyang Phar
maceutical University, Shenyang 110016, China.
** Corresponding author.
E-mail addresses: [email protected] (H. Li), [email protected] (L. Chen).
1
These authors have the equal contribution to the article.
https://doi.org/10.1016/j.foodres.2024.114548
Received 8 December 2023; Received in revised form 29 February 2024; Accepted 25 May 2024
Available online 29 May 2024
0963-9969/© 2024 Elsevier Ltd. All rights are reserved, including those for text and data mining, AI training, and similar technologies.
H. Dong et al. Food Research International 190 (2024) 114548
multiple preservatives, and the combined production of preservatives membrane (Rashidaie Abandansarie et al., 2019). Studies have shown
with other substances. The safety assessment of natural preservatives is that beef patties containing copaiba essential oil (CEO) and oregano
shown in Fig. 1. essential oil (OEO) exhibit good antioxidant activity and reduce lipid
oxidation, and their antioxidant effect is stronger than synthetic additive
2. Plant derived preservatives (Leite et al., 2022). The antibacterial effects of CEO and OEO are largely
attributed to their chemical components. As bioactive compounds with
2.1. Essential oils and their anti-corrosion activity antioxidant properties, polyphenols can provide a hydrogen atom to free
radicals and form a stable free radical intermediate, thereby delaying or
Essential oil (EO) is a lipid soluble secondary metabolite extracted inhibiting lipid oxidation. The antibacterial and antioxidant effects
from plants. Many essential oils have a long history of use as natural depend on the number and position of the hydroxyl groups (Martinengo
antimicrobials, health promoters, and food flavorings. EOs are et al., 2021). OEO has the effect of inhibiting Enterococcus faecalis. OEO
composed of hydrocarbons (monoterpenes and sesquiterpenes) and induces an increase in reactive oxygen species levels, resulting in lipid
oxygenated compounds (alcohols, esters, ethers, aldehydes, ketones, peroxidation of the cell membrane, damaging the permeability and
lactones, phenols, and phenol ethers) (Da Silva et al., 2021). The anti integrity of the membrane, thereby changing the shape of the bacteria
bacterial activity of EOs is driven by complex interactions between these and inactivating E. faecalis. OEO can be used as a natural antibacterial
components. EOs that contain certain aldehydes or phenols as their main preservative to control E. faecalis in food production (Zhan et al., 2022).
components have the highest antibacterial activity (Gurtler & Garner, OEO has been shown to cause potassium and phosphate leakage in
2022). Staphylococcus aureus and Pseudomonas aeruginosa, leading to cell death
The antibacterial mechanism of EOs is shown in Fig. 2, essential oils (Lambert et al., 2001). CEO had an obvious oxidative damaging effect on
exert antibacterial effects by acting on the cell membrane of microor Salmonella enteritidis, CEO treatment caused the disruption of the bal
ganisms, disrupting the integrity of the cell membrane. The hydropho ance of the cellular antioxidant enzymes (SOD, CAT, POD) system,
bicity of essential oils allows them to cross the cell cytoplasmic resulting in an increase in the content of malondialdehyde, a membrane
membrane and mitochondria, increasing membrane permeability, lipid metabolite, and increased protein carbonylation, which ultimately
causing leakage of critical components in cells and eventual death of the inhibited the growth of S. enteritidis (Zhang et al., 2022). The inhibitory
bacteria cells (Falleh et al., 2020). Several reports have suggested that effect of cinnamon essential oil on the growth of S. enteritidis cells is also
gram-positive bacteria are more sensitive to antibacterial compounds related to cell membrane damage and the induction of oxidative stress,
compared with gram-negative bacteria. This reason may be due to and its antibacterial activity is related to phenolic substances. The
absence of lipopolysaccharide in cell wall of gram-positive bacteria antioxidant effect of rosemary is also related to the content of phenolic
which prevented the entry of active compounds into the cytoplasmic components (carnitine, rosemary phenol, and rosemary diphenol) as
Fig. 1. The safety evaluation of natural preservatives.
2
Fig. 2. The antibacterial mechanism of essential oils.
hydrogen donors (Kamel et al., 2022). of carvacrol, caryophyllene oxide, and ascaridole, which induce sup
Garlic essential oil also has good antibacterial effects and inhibits the pression of the respiratory function in the mitochondria, or in the
growth of Trametes hirsuta and Laetiporus sulphureus. The most biologi complex I of the mitochondrial electron transport chains, this toxic ef
cally active are organic sulfur compounds and their precursors, such as fect emerging on the kidneys, liver, and intestine (Dagni et al., 2022).
allicin, ajoene, and diallyl disulfide (Gong et al., 2021). Among them, α-Pinene can induce cell death by regulating signaling pathways related
sulfur compounds react with cysteine and inhibit mercaptan enzymes to oxidative stress (Jin et al., 2010). Rosemary essential oils (REOs) rich
(protease and alcohol dehydrogenase) or lipid metabolism. It also in in α-pinene are toxic to HaCaT and this toxicity is strongly related to the
hibits microbial respiration, alters RNA synthesis, and increases the α-pinene content (Huang et al., 2023). During the production process,
permeability of cell membranes, leading to ion leakage and cell death. attention should be paid to the concentration and safety of REO with
Diallyl trisulfide is the most effective component in inhibiting T. hirsuta high α-pinene content in food packaging. There are few experiments
and L. sulphureus, and can be used for preventing food spoilage (Pranoto evaluating the safety of EOs in humans, but some compounds in essen
et al., 2005). Some studies showed that EOs extracted from Rosmarinus tial oils can be toxic and cause side effects. The lack of in vivo/in vitro
officinalis, Thymus capitatus, Origanum majorana, and Salvia officinalis, research on essential oils is one of the limiting factors for their appli
which inhibited the survival, growth, and reproduction of Staphylo cation. Therefore, well-designed studies in animals and humans are
coccus aureus, Escherichia coli, and Candida albicans in fresh fruit juices, demanded to assess efficacy and safety of EOs, and it is recommended to
indicating that these essential oils have antibacterial effects (El-Kased & conduct detailed toxicological assessments for each EOs and intended
El-Kersh, 2022). Rosemary-magnolia composite essential oil was found application Due to the complex mixture of many volatile components in
to have a significant inhibitory effect on Staphylococcus aureus, and its essential oils, it is difficult to standardize the application amount of
antioxidant effect is attributed to the high content of β-pinene (Song essential oil preservatives for optimal in vitro effects in food preserva
et al., 2023). Pectin and gelling biopolymer film rich in natamycin and tion. Essential oils have a certain impact on the texture and sensory
clove essential oil have an antibacterial effect against Staphylococcus properties of food themselves, and when researching or applying them,
aureus and Candida parapsilosis in the packaging corn tortilla (Callejas- it is necessary to comprehensively consider the preservative effect and
Quijada et al., 2023). food quality. In addition, it has been found that essential oils can cause
The antibacterial activity of essential oils such as CEO, OEO, cinna skin irritation and allergies in some cases.
mon essential oil, and rosemary essential oil may be related to the al
dehydes and alcohols in their chemical components. The high antifungal 2.2. Flavonoids and their antimicrobial activity
activity of garlic essential oil is due to the presence of sulfur ethers, of
which diallyl trisulfide (allicin) has the highest content. Essential oils Flavonoids are widely found in natural organic compounds and have
have a good antibacterial effect on Gram-positive bacteria, Staphylo various pharmacological activities, including significant antibacterial
coccus aureus is a common Gram-positive bacterium and also a food effects. Flavonoids belong to the category of polyphenols, and their
borne pathogen, most essential oils have a significant inhibitory effect highly hydroxylated structures give them strong antioxidant properties,
on Staphylococcus aureus, and their antibacterial activity is dose- which can eliminate free radicals and inhibit bacteria. Some studies
dependent. Some essential oils even have better antimicrobial effects have shown that flavonoids with good hydrophilicity have better anti
than some chemical preservatives. However, natural preservatives from bacterial effects than flavonoids with poor hydrophilicity. The position
plants have many negative effects on food and have not yet been widely of free hydroxyl groups in the molecule is also important for activity,
used. There are several main issues that need further research: although and all flavonoid aglycones have better antibacterial and antifungal
the biological characteristics of EOs have been extensively studied, few activity than flavonoid glycosides (Rashed et al., 2014).
studies have examined their toxicity and side effects. Some in vitro and in The flavone extract in licorice can destroy the cell membrane and
vivo experiments have confirmed that EOs can be toxic even at low cause the contents to leak out. After the extract enters the cell, it can
concentrations, which can lead to health problems, such as skin, eye, disrupt the normal metabolism and physiological activities of the cell by
and mucosal irritation, and also cause allergic reactions when taken destroying the structure of macromolecular substances or inhibiting
orally (Lanzerstorfer, 2021). Research has shown that the essential oils protein synthesis, thereby achieving its bacteriostatic effect (Ahn et al.,
in Dysphania can affect mitochondrial function, related to the presence 2014). Naringin is a natural flavonoid extracted from grapes and citrus
3
fruits (Peng et al., 2024), which has an inhibitory effect on Pseudomonas gallate (ECG), and (− )-epigallocatechin gallate (EGCG) (Jia et al.,
spp., inhibiting bacterial biofilm and clearing preformed biofilms. It has 2018). EGCG is the main component of green tea polyphenols, which is
a strong binding affinity for biofilm related proteins, thereby inhibiting widely used as food preservatives.
or reducing bacterial colonization. Bacteria associated with food Tea polyphenol can be used to extend the shelf life of Pacific white
spoilage form biofilms on nonbiological surfaces, and cells with biofilms shrimp. They can inhibit the activity of peroxidase and protein enzyme
exhibited greater resistance to antimicrobial agents. Extracellular by attacking oxygen and free radicals and scavenging free radicals, such
polysaccharides help maintain the structure of biofilms and protect them as α-amylase, pepsin, trypsin, and lipase, and prevent lipid oxidation,
from harmful environmental influences. Alginate is also crucial for the reduce the activity of enzymes in frozen Pacific white shrimp, and delay
biofilm of Pseudomonas spp., as it has a dual effect of protecting cells lipid oxidation (Li et al., 2022). Tea polyphenol also plays an important
from adverse external conditions and promoting bacterial adhesion to role in preserving fish, adding tea polyphenol can prolong the preser
the substrate. Naringin can effectively inhibit the production of extra vation of fish by inhibiting lipid oxidation (Xu et al., 2023). Adding tea
cellular polysaccharides and alginate in Pseudomonas spp. (Husain et al., polyphenol to the polysaccharide composite film can effectively
2021). The study found that luteolin has antibacterial activity against improve the physical properties and antibacterial/antioxidant functions
Escherichia coli and Enterobacter cloacae. Luteolin can destroy the of the composite film. The films of sodium alginate and konjac gluco
integrity of the cell membrane and has a strong inhibitory effect on the mannan mixed by Lycium ruthenicum anthocyanins and tea polyphenol
biofilm formation. The number and degree of cell damage are dose- (TP-LRA-SA-KGM) exhibit a good preservative effect on milk and can
dependent (Qian et al., 2021). effectively inhibit the growth of bacteria in milk. LRA shows a signifi
Prescribed doses of flavonoids, such as those found in our daily diet, cant inhibitory effect on the proliferation of Staphylococcus aureus and
may be safe for human health. Research has shown that dietary intake of Escherichia coli. By adding tea polyphenol, the inhibitory effect on bac
flavonoids is approximately 50–800 mg/day with no associated side terial proliferation is significantly enhanced (Wang et al., 2023). The TP-
effects (Wu et al., 2023). Chrysin is a flavone that can be obtained from SA-KGM films have a good preservative effect on beef and apples by
different natural sources, such as Alpinia oxyphylla, mushrooms (Pleu effectively inhibiting microbial activity and food oxidation, thereby
rotus ostreatus), passionflower, and Indian trumpet flower (Tekeli et al., significantly delaying the process of food spoilage. The TP-SA-KGM films
2023). Acute dosages of 400 mg chrysin do not show any observable can be used as a natural bioactive film to replace plastic films for beef
toxic effects in humans (Naz, 2019). Normal volunteers have received an preservation (Wang et al., 2023).
oral dose of 625 mg/day of chrysin for 28 days without any reported Tea polyphenols can inhibit most microorganisms, with a broad
toxicity. Dihydromyricetin is a natural flavonoid compound extracted antibacterial spectrum, and inhibit most food-borne pathogens (Li et al.,
from the stems and leaves of Ampelopsis grossedentata (Brown et al., 2020), such as Costridium botulinum, Pseudomonas aeruginosa, Escherichia
2001), which was administered to rats at doses of 1.5 g/kg and 0.3 g/kg coli, Salmonella typhimurium, Listeria monocytogenes, Staphylococcus
for 12 weeks without significant toxic effects (Wu et al., 2023). Senna aureus and Candida albicans. Its main inhibitory effect is to destroy the
italica leaves contain various flavonoids such as kaempferol, quercetin cell membrane, increase the permeability of the outer and inner mem
and apigenin, and it had no toxic effects or death in rats administered a branes of Pseudomonas aeruginosa, and destroy the cell membrane by
dose of 5000 mg/kg, indicating that they are non-toxic at the prescribed releasing of small cell molecules (Tang et al., 2022). Due to their anti
dose (Towanou et al., 2023). bacterial properties, tea polyphenols have an inhibitory effect on pu
Some flavonoid compounds exhibit direct antibacterial effects by trescine, cadaverine and histamine. Tea polyphenols retard spoilage
destroying cell membranes, inhibiting nucleic acid synthesis, inhibiting bacteria and inhibit bacterial growth (Xu et al., 2023).
energy metabolism, and inhibiting cell wall and membrane synthesis. More and more studies have shown that excessive consumption of tea
They can destroy a variety of biofilm cells, inhibit the growth of various polyphenols can cause several harmful effects (Molinari et al., 2006.).
bacteria, and play an important role in food preservation. Future High doses of tea polyphenols not only cause cytotoxicity in vitro, but
research should be conducted on a comprehensive assessment of the also lead to hepatotoxicity, nephrotoxicity, and gastrointestinal disor
safety and potential of flavonoids in conjunction with in vitro and in vivo ders (Keller & Wallace, 2021). When tea polyphenols reach high con
toxicity assessments. The food industry should pay attention to the centrations in the blood, they trigger cytotoxicity and oxidative stress. It
dosage of each type of flavonoids to avoid toxic situations. Although has been found that high levels of catechins can increase the carcino
flavonoids have high antimicrobial activity, they have problems such as genic effects caused by carcinogens (Akagawa et al., 2003). Studies have
poor water solubility, poor stability and low bioavailability. In order to shown that EGCG has a protective effect on DNA at low concentrations,
fully exploit the antimicrobial effect of flavonoids, it is worth examining but at higher concentrations, it exacerbates DNA oxidative damage
their compatibility with other components (Han et al., 2022). At present, (Guan et al., 2012). Under the prescribed safe dose of tea polyphenols,
protein–flavonoid complexes are widely used to improve the poor water chronic and subchronic experiments were conducted on dogs for 9
solubility and low bioavailability of flavonoids, and have stronger months and 13 weeks, and no side effects were observed (Kapetanovic
oxidation capacity than flavonoids (Diao et al., 2021). With the in-depth et al., 2010). Taking tea polyphenols at the optimal dosage showed no
study of flavonoid structure and activity as well as their antibacterial side effects on humans (Rashidinejad, 2021). The European Food Safety
mechanisms, this will expand new space for the development of anti Authority believes that intake of 800 mg/day EGCG may lead to an in
bacterial flavonoids. crease in transaminases (Ouyang et al., 2020). Tea polyphenols can play
a preservative role in food, with a positive effect on the body and
2.3. Tea polyphenols and their antimicrobial activity maintaining redox homeostasis in the body. However, exceeding a
certain limit can cause damage to the body. In the food industry, when
Tea polyphenol is the most important component of tea. Due to its using tea polyphenols, the dosage should be strictly controlled, and its
enzyme inhibition as well as antibacterial and antioxidant effects, it is toxicity should be reduced as much as possible while exerting its anti
widely used in various foods such as meat, aquatic products, fruits and microbial effect.
vegetables (Dai et al., 2022). Tea polyphenol has potent antibacterial Many plant extracts, such as cinnamon extract, clove extract, rose
and antioxidant properties, and studies have examined the antioxidant mary extract, and garlic extract, have strong antioxidant and bacteri
activity of black tea. The results show that its antioxidant activity is cidal effects and can be used as natural preservatives. Essential oils are
positively correlated with the content of phenolic hydroxyl groups often used as seasonings and food additives, they are also used in the
(Chen et al., 2023). Tea polyphenol contains potent antibacterial and cosmetic industry. Tea polyphenols also have excellent antimicrobial
antioxidant compounds, particularly catechin compounds, including and preservative effects and are widely used in food and medicine. An
(− )-epicatechin (EC), (− )-epigallocatechin (EGC), (− )-epicatechin overview of natural antimicrobial from plant sources is shown in
4
Table 1 Table 1 (continued )

The antibacterial effect of natural preservatives. Preservatives Microorganism References
Preservatives Microorganism References
Escherichia faecalis, Collins et al.
Essential oil Copaiba essential oil Enterococcus Leite et al. (2022) Staphylococcus (2019)
and oregano essential faecalis, aureus,
oil Staphylococcus Paenibacilluslarvae
aureus, spp.,
Pseudomonas Salmonella
aeruginosa, typhimurium,
Salmonella enteritidis Bacillus subtilis
Protamine Shewanella Li et al. (2016).
Cinnamon essential Salmonella enteritidis Kamel et al. putrefaciens,
oil (2022) Pseudomonas spp.
Garlic essential oil Trametes hirsuta, Gong et al. Bacteriocin Nisin Staphylococcus Wu et al. (2023)
Lactobacillus sulfate (2021) aureus,
Essential oils of Staphylococcus El-Kased and El- Escherichia coli
rosemary, thymus aureus, Kersh (2022) KCA018 bacteriocin Listeria Kim et al. (2022)
gland, oregano and Escherichia coli, monocytogenes
salvia miltiorrhiza Candida albicans Bacteriocin LFX01 Staphylococcus Xin et al. (2023)
Flavonoids Pseudomonas spp. Husain et al. aureus,
(2021) Escherichia coli
Escherichia coli, Qian et al. (2021) Lacticaseibacillus Staphylococcus Wu et al. (2022)
Enterobacteriaceae rhamnosus ZFM216 aureus
cloacae bacteriocin
Tea polyphenol Costridium Tang et al. (2022) Actinomycin Natamycin Candida tropicalis Agustín et al.
botulinum, Aspergillus (2019)
Pseudomonas ochraceopealiformis
aeruginosa, Polylysine Penicillium Bai et al. (2022)
Escherichia coli, expansum, Cai and Kuo
Salmonella Colletotrichum (2022)Zhu et al.
typhimurium, gloeosporioides, (2022)
Listeria Gloeophyllum
monocytogenes, trabeum,
Staphylococcus Rhodonia placenta,
aureus, Trametes versicolor,
Candida albicans Irpex lacteus,
Chitosan Escherichia coli Volmajer Valh Staphylococcus
O157:H7, et al. (2022)Díaz- aureus,
Listeria Cruz et al. (2022) Escherichia coli,
monocytogenes, Listeria
Staphylococcus monocytogenes,
aureus, Pseudomonas
Shewanella lundensis
putrefaciens, Phage Lytic bacteriophage Vibrio You et al. (2021)
Pseudomonas VPT02 parahaemolyticus
fluorescens Polyvalent phage Coagulase-negative Sofy et al. (2020)
Lysozyme Listeria Ajourloo et al. CoNShP-3 staphylococci
monocytogenes, (2021)Xu et al. Staphylococcus
Shewanella (2020) aureus,
putrefaciens, Staphylococcus
Pseudomonas aureus,
fluorescens, Bacillus cereus,
Staphylococcus Bacillus subtilis
aureus, Phage UAE_MI-01 Escherichia coli Sultan-Alolama
Escherichia coli, et al. (2021)
Pseudomonas Bacillus phage Klebsiella Sarjoughian et al.
aeruginosa endolysin pneumoniae, (2020)
Antimicrobial peptide Escherichia coli, Cournoyer et al. Salmonella
Listeria ivanovii, (2022)Abou-Diab typhimurium,
Mucor racemosus, et al. (2022)Shen Proteus,
Penicillium et al. (2022) Escherichia coli
chrysogenum,
Aspergillus versicolor,
Paecilomyces,
Table 1.
Rhodotorula
mucilaginosa,
Saccharomyces 3. Animal derived preservatives
boulardii,
Kluyveromyces
3.1. Chitosan and their antimicrobial activity
marxianus,
Candida
guilliermondii, Chitosan, a natural marine polysaccharide, consists of 1,4-linked
Salmonella glucosamine and N-acetylglucosamine, which is derived through
typhimurium deacetylation of chitin in alkaline medium (Mondéjar-López et al.,
Propolis Aspergillus spp., Vasilaki et al.
2022). Chitosan can be extracted from the cell walls of fungi, the shells
Macrospora spp., (2019)Postali
Listeria et al. (2022) of crustaceans, and the stratum corneum of insects (Yi et al., 2024).
monocytogenes, Chitosan is widely used in biomaterials, healthcare, environmental, and
other industrial fields due to its good biocompatibility, antibacterial
5
activity, and safety (Ruan et al., 2022). the shelf life of fish and meat. The reaction mechanism for the synthesis
Hummus is a food paste commonly consumed in the Middle East. Its of CS-g-CA by EDC/NHS is shown in Fig. 3 (Sun et al., 2022). Chitosan
major ingredients include boiled chickpeas and tahini pulp. Chitosan has and flaxseed gum form flaxseed gum/chitosan/flaxseed gum composite
extensive antimicrobial properties and the addition of chitosan to coating, which has high total antioxidant capacity and DPPH scavenging
hummus can result in a significant reduction in the number of Escher capacity. They have good antibacterial properties against Shewanella
ichia coli O157:H7 and Listeria monocytogenes (Osaili et al., 2022). Chi putrefaciens and Pseudomonas fluorescens. The composite coating slows
tosan coating can be used as an antibacterial agent and extend the shelf the reduction of antioxidant enzyme activity and inhibits protein
life of packaged foods. Studies have shown that chitosan-coated pack oxidation in rainbow trout fillets, which can be used for food preser
aging materials can reduce the number of Staphylococcus aureus and vation (Yang et al., 2022).
Escherichia coli, extending the shelf life of food (Volmajer Valh et al., Chitosan is biocompatible and has been approved by the FDA as
2022). The inhibitory effect of chitosan in the corn starch-chitosan generally recognized as safe (Khubiev et al., 2023). A series of toxico
composite film was confirmed on both Listeria monocytogenes and logical tests have been conducted with chitosan, including acute toxicity
Staphylococcus aureus (Díaz-Cruz et al., 2022). Chitosan can be used to (Liang et al., 2011), subacute toxicity (Sonawnae et al., 2012), chronic
preserve fruits during storage, it can inhibit the production of ethylene, toxicity, chromosomal malformation test, embryonic toxicity and tera
delay the aging of fruits, and does not affect the taste or appearance of togenic test (Khan et al., 2023), indicating that chitosan is non-toxic to
food (Liu et al., 2021). Chitosan treatment was found to trigger anti humans. Due to the lower antibacterial activity of chitosan under
oxidant systems, thereby scavenging reactive oxygen species (ROS) and neutral and alkaline conditions compared to acidic environmental
ensuring the integrity of the fruit membrane (Ackah et al., 2022). conditions, as well as its low antioxidant activity and water resistance,
Chitosan shows a stronger inhibitory effect at lower pH and its the application of chitosan in food preservation is limited. Therefore,
inhibitory effect decreases with the increase of pH. To improve anti materials modified with chitosan are widely used, mainly for fruit
bacterial activity, complexes of chitosan and certain materials were preservation. They form a barrier on the fruit surface, limit the spread of
prepared (Jana & Jana, 2019). Chitosan-nano-zinc oxide composite oxygen and extend the shelf life of the fruit. The antibacterial chitosan
films showed a good preservative effect on cherry tomatoes. The coating film has great prospects as a widely used and environmentally friendly
formed a barrier on the fruit surface, which inhibited to a certain extent material. Their unique properties, including biodegradability, biocom
the respiration intensity and growth of surface microorganisms, slowed patibility and antibacterial activity, have been extensively studied for
down the aging process and nutrient consumption, and had a preser food packaging applications to extend shelf life, maintain quality and
vative effect (Li et al., 2021). Chitosan and gelatin form an edible reduce spoilage due to microbial contamination.
nanocomposite film that has antibacterial effects on Escherichia coli and
Staphylococcus aureus. It can be used to protect fruits and slow spoilage
(Fu et al., 2021). Due to the low antioxidant activity and weak water 3.2. Lysozyme and their antimicrobial activity
resistance of chitosan, grafting phenol derivatives onto chitosan mac
romolecules can effectively improve its antioxidant and hydrophobic Lysozyme, also known as 1,4-β-D-N-acetyl cell wall amidase is an
properties. It was also studied that lauryl gallate was grafted onto chi alkaline enzyme that can hydrolyze mucopolysaccharides in bacteria.
tosan, which significantly increased the oxidation resistance, hydro This enzyme is widely present in various tissues of the human body and
phobicity and moisture resistance (Liu et al., 2021). Chitosan combined is the main component of animal products (egg white, egg white lyso
with apple polyphenols coating can effectively inhibit the growth of zyme). Microorganisms also contain this enzyme, with egg white being
microorganisms, delay the biochemical changes of ice stored large yel the most abundant. Lysozymes have good antibacterial activity, espe
low croaker and extend its shelf life (Lan et al., 2022). The antioxidant cially against Gram-positive bacteria (Alhadrami et al., 2022). Gram-
and antibacterial activities of chitosan could be enhanced by grafting positive bacteria have a single lipid membrane surrounded by a thick
caffeic acid onto chitosan, which could inhibit microbial growth, reduce layer of peptidoglycan cell wall. In Gram-negative bacteria, the cell wall
lipid oxidation and protein degradation, and was suitable for extending consists of a thin layer of peptidoglycan between the cytoplasm and the
outer lipid membrane. Lysozymes can hydrolyze peptidoglycans, which
Fig. 3. Reaction mechanism for the synthesis of caffeic acid-g-chitosan by EDC/NHS chemical coupling.
6
are the main components of the cell wall of Gram-positive bacteria. This enhance the antibacterial activity against Shewanella putrefaciens and
hydrolysis destroys the integrity of the cell wall and leads to lysis of the Pseudomonas fluorescens, delay lipid oxidation, and could be used for
bacteria (Primo et al., 2018). The antibacterial effect of lysozyme is preserving fish fillets (Xu et al., 2020). The chitosan-lysozyme coating
mediated by its cell wall amidase activity. It catalyzes the reaction be has a good antibacterial effect against Gram-positive bacteria (Staphy
tween the 1-carbon atom of N-acetylmuramic acid (NAM) and the 4-car lococcus aureus) and Gram-negative bacteria (Escherichia coli and Pseu
bon atom of N-acetylglucosamine (NAG) in the peptidoglycan layer of domonas aeruginosa), which can inhibit the lipid oxidation of
the cell wall of Gram-positive bacteria β-1,4 hydrolysis of glycosidic Pseudomonas aeruginosa, thus extending the shelf life of yellow croaker.
bonds. Lysozyme molecules are spherical structures with hydrophilic (Wu et al., 2018).
groups on the outside and hydrophobic groups on the inside. There is Lysozyme, as a natural antibacterial substance, can target the cell
also a groove structure on the surface that serves as an active site for wall of the cell without affecting other parts of the cell, and can be
binding and cutting bacteria. Polysaccharides consisting of six amino digested and absorbed in the stomach without affecting human health.
sugars are used as binding substrates for active localization through Lysozyme generally does not affect the nutritional components in cold
hydrogen bonding and hydrophobic interaction (Leśnierowski & Yang, and fresh meat and can be used to preserve chilled meat. Lysozyme is
2021). Acid catalyst residues such as glutamic acid (Glu) and general widely used as a safe and effective preservative in dairy products, meat,
alkaline catalyst residues such as aspartic acid (Asp) or cysteine (Cys) aquatic products and other foods. Lysozyme from egg white has been
destroy the carbon–oxygen bonds between the fourth and fifth sugar reported to have insignificant acute, subacute and chronic toxicity in
units, resulting in an increase in their glycosidic bonds. Glutamic acid animals. However, lysozyme has the problems of anaphylaxis and an
acts as a proton donor via free carbon groups on its side chains, while tigenicity in the digestive process. Studies have shown that individuals
aspartic acid as a nucleophilic reagent to form glycosyl enzyme in who are sensitive to eggs have no side effects or immune responses after
termediates that react with water molecules to produce hydrolysis consuming cheese containing lysozyme (Rossi et al., 2012). Egg white
products (Fig. 4) (Nawaz et al., 2022). Lysozyme is a heat-stable enzyme lysozyme has been declared as Generally Recognized As Safe (GRAS) by
and can therefore be used to extend the shelf life and improve the safety the FDA for use in cheese. Due to the allergenic potential of lysozyme,
of various foods. the FDA has concluded that “Egg white lysozyme” labeling is mandatory
Although lysozyme has strong antibacterial activity against Gram- for bulk and packaged foods containing lysozyme(Food and Drug
positive bacteria, this ability is weaker in Gram-negative bacteria due Administration, 2023) . In response to some of the problems that exist
to the presence of an outer membrane to protect the cell wall. This with lysozyme, further research and investigation into the application of
limitation can be eliminated by combining it with other preservatives lysozyme in the food industry is needed. Although the scope of appli
that can increase the antibacterial spectrum (Moshtaghi et al., 2018). cation of lysozyme is still relatively limited, it is expected to be an
The combination of epigallocatechin gallate and lysozyme has a good important functional food additive for the food industry.
inhibitory effect on Pseudomonas spp., can extend the shelf life of large
yellow croakers (Pei et al., 2022). Ziziphora clinopodioides essential oil 3.3. Antimicrobial peptide and their antimicrobial activity
(ZCEO) and lysozyme showed good antibacterial and antioxidant effects
against Listeria monocytogenes and could be used as a preservative in Antimicrobial peptide (AMP) is a low molecular weight polypeptide
fresh sausage (Ajourloo et al., 2021). The combined treatment with or protein synthesized by ribosomes and composed of 10–50 amino acid
lysozyme and cinnamaldehyde can significantly inhibit the growth of residues (León Madrazo et al., 2022). Most AMPs are cationic peptides
microorganisms in refrigerated olive flounder (Paralichthys olivaceus), with cationic and amphiphilic structures. The cationic structure
Fig. 4. Hydrolytic mechanism of action of lysozyme on β-1,4 linkages between NAM and NAG residues of the bacterial cell wall backbone.
7
electrostatically interacts with the negatively charged cell membrane, internal substances and disrupting the normal metabolism of bacteria,
destroying the integrity of the membrane and making it impossible for thereby achieving an antibacterial effect. It can be used as a preservative
bacteria to survive (Zhao et al., 2022). The amphiphilicity of AMP in food processing and aquaculture. Research has shown that propolis
contributes to AMP entering the cell membrane, destroying the lipo extract has a stronger inhibitory effect against mold, particularly
polysaccharide layer of the cell membrane, and leading to the death of Aspergillus spp. and Macrospora spp. (Vasilaki et al., 2019). Red propolis
bacteria (Dong et al., 2022). hydroalcoholic extract can effectively delay the decay and lipid oxida
The small molecule peptide porcine myeloid antimicrobial peptide tion of tilapia salami. It has obvious antibacterial activity against Gram-
37 (PMAP-37) isolated from pig bone marrow has broad-spectrum positive bacteria and strong inhibitory activity against Listeria mono
antibacterial activity. The peptide has been shown to inhibit the activ cytogenes and Escherichia faecalis (Mafra et al., 2022). Studies have
ity of Gram-positive and Gram-negative bacteria. The interaction be shown that propolis can inhibit the growth of Staphylococcus aureus and
tween positively charged PMAP-37 and negatively charged bacterial cell Listeria monocytogenes (Postali et al., 2022). Caffeic acid esters are active
membranes disrupted the integrity of the cell membrane and resulted in ingredients extracted from propolis. The results indicate that caffeic acid
leakage of bacterial contents (Dong et al., 2023). Antimicrobial peptides esters can eliminate bacterial growth through oxidative stress mecha
can be produced from porcine hemoglobin after pepsin hydrolysis. Pork nisms and have inhibitory effects on Paenibacilluslarvae spp. (Collins
hydrolysates have been shown to exhibit antibacterial activity, et al., 2019).
including bacteria (Gram-positive and Gram-negative bacteria), fila The combination of propolis and edible coatings can also be used for
mentous molds and yeasts (Cournoyer et al., 2022). Similar to porcine meat preservation. Carboxymethyl cellulose containing 3 % ethanol
hemoglobin, bovine hemoglobin hydrolysate also has significant anti propolis extract can be coated on chicken breast meat and stored in cold
bacterial activity against many bacterial strains (Gram-positive and storage, which can extend the storage time of chicken breast meat (El
Gram-negative bacteria) and fungal strains (mold and yeast) (Abou-Diab Sheikha et al., 2022). Propolis combined with other preservatives can
et al., 2022). Shen et al. designed and synthesized four antimicrobial improve its antimicrobial effect as a composite material. The composite
peptides that have an inhibitory effect against Salmonella typhimurium, material formed by chitosan nanoparticles, propolis and nano selenium,
preventing the formation of biofilms, interacting with the bacterial cell as a potential antibacterial nano compound, was found to have a strong
membrane and penetrating, resulting in loss of membrane potential, antibacterial effect on Escherichia coli, Staphylococcus aureus and Sal
damage to membrane integrity and bacterial death (Shen et al., 2022). It monella typhimurium (Youssef et al., 2022). Propolis ethanol extract and
can also bind to the DNA of Salmonella typhimurium, causing DNA ag glycerin can significantly inhibit the growth of Listeria monocytogenes
gregation or precipitation. A peptide with a molecular weight of 9.77 when added to milk stored at 4 ◦ C (Michailidis et al., 2021). A sodium
kDa was isolated from the supernatant of Saccharomyces cerevisiae strain alginate bilayer coating incorporated with green propolis extract can
ATCC 36858. It inhibited the growth of Escherichia coli and Staphylo reduce microbial deterioration and extend the shelf life of Colossoma
coccus aureus (Thyab Gddoa Al-sahlany et al., 2020). Chitin has shown macropomum fillet (Cruz et al., 2021).
antibacterial activity against Listeria monocytogenes, Staphylococcus Propolis has an efficient and broad-spectrum bacteriostatic effect.
aureus, Enterococcus faecalis, Escherichia coli, and Salmonella enteritidis, Propolis has significantly greater bacteriostatic ability to Gram-positive
with the best antibacterial effect against Salmonella enteritidis in chilled bacteria than Gram-negative bacteria, and has a good antibacterial ef
pork samples. Toxic effects of this antimicrobial peptide on human fi fect on Salmonella spp., Staphylococcus aureus, Enterococcus spp., Strep
broblasts and red blood cells have not been reported, indicating its tococcus spp., Bacillus subtilis, and almost no bacteriostatic activity to
safety for consumption (León Madrazo & Segura Campos, 2023). The Escherichia coli. As the concentration of propolis alcohol extract in
results of cytotoxicity tests of antimicrobial peptides show that they are creases, the antibacterial effect becomes more apparent. A series of
toxic only at higher concentrations (20–25 µM), while their toxicity is toxicological tests have been conducted on Brazilian red propolis,
very low at lower concentrations (<15 µM) (Arasu & Al-Dhabi, 2023). including cytotoxicity, genetic toxicity and in vivo genotoxicity, indi
Although antimicrobial peptides have good antibacterial potential, their cating that it has no toxicity (Aldana-Mejía et al., 2021). With long-term
toxicity as food preservatives is rarely researched. It is hoped that future oral administration of 1000 mg/kg Brazilian red propolis to males,
research can focus more on the application of antimicrobial peptides in biochemical changes in liver and kidney parameters were detected, but
food and maximize their antimicrobial effects within the allowable no histopathological changes in any tissue or organ (Aldana-Mejía et al.,
range of toxicity. 2023). Clinical and in vivo animal studies have shown that propolis is
Antibacterial peptides are widely distributed in organisms and have safe and non-toxic (Castaldo & Capasso, 2002). However, at higher
broad-spectrum antibacterial properties, green and anti-pollution doses, some side effects and allergies may occur (Choudhary et al.,
properties, and even nutritional and health benefits. As a natural pre 2023). The main sensitizers in propolis are 3-methyl-2-butenyl caffeic
servative, it has achieved good results and is widely used in the field of acid ester, phenylethyl caffeic acid ester, benzyl salicylate ester, benzyl
food preservation. However, due to the disadvantages of low yield, cinnamate ester, and 1,1-dimethylallyl caffeic acid (Burdock, 1998).
complex manufacturing process, high cost, and the fact that antimicro Propolis also has various biological activities and functional health
bial peptides cannot be produced on a large scale, this limits their benefits, such as clearing reactive oxygen species and playing an anti
commercialization process. Therefore, developing the manufacturing oxidant role. Therefore, propolis has broad application prospects in food
process of antimicrobial peptides, increasing production, reducing costs, preservation and preservation. At present, research has shown that
and studying the details of their dynamic mechanism of action can propolis has good effects on the preservation of poultry eggs, aquatic
effectively promote the entry of antimicrobial peptides into the field of products, meat products, dairy products, and fruits.
food preservation and preservation.
3.5. Protamine and their antimicrobial activity
3.4. Propolis and their antimicrobial activity
Protamine is a cationic peptide rich in proline and arginine. It is an
Propolis is a kind of bee product that contains a variety of organic alkaline protein that is tightly bound to DNA in the form of nuclear
compounds and is a resinous material. It consists of tree and plant se protamine. At present, protamine has been extracted from mature testis
cretions, pollen and enzymes collected by bees. The antibacterial tissues of various fish species (such as salmon, red trout, herring, etc.)
properties of propolis are attributed to its flavonoids and phenolic acids and mammals (such as mice, humans, wild boars, etc.). In neutral and
(Sánchez-Martín et al., 2022). alkaline media, protamine has a strong antibacterial ability and thermal
Propolis has an antibacterial effect by increasing the permeability stability, a broad spectrum of antibacterial activity and a strong inhib
between bacterial cell walls and cell membranes, causing the outflow of itory effect on yeasts, molds and Gram-positive bacteria such as bacillus
8
and lactic acid bacteria (Aspedon & Groisman, 1996). Nisin is a bacteriocin produced by lactic acid bacteria. Nisin can kill
Protamine can inhibit the metabolism process dependent on the cell Gram-positive bacteria and bacterial spores, but not Gram-negative
plasma membrane, target the cell plasma membrane by destroying en bacteria, yeasts, molds, and other fungi. Nisin has no toxic effect on
ergy and inhibiting the uptake of nutrients, and inhibit certain compo the human body and is very sensitive to proteolytic enzymes (pancre
nents of the mitochondrial electron transfer system without causing cell atin, salivary enzyme, digestive enzyme, etc.)(Patil & Kunda, 2022).
lysis or changing the permeability of the cell plasma membrane. The After human consumption, it is quickly hydrolyzed into amino acids in
mode of action of protamine is the electrostatic attraction between the digestive tract, and does not change the normal bacterial colony in
positively charged molecules and negatively charged cell envelopes, the intestinal tract (Zimet et al., 2018).
which leads to inhibition or cell death due to the leakage of K+, ATP and The mode of action of nisin on microorganisms is to inhibit cell wall
intracellular enzymes (Truelstrup Hansen et al., 2001). The activity of formation, causing cytoplasmic leakage, which may be related to the
protamine is affected by the size of the electric membrane potential, and ability of nisin to adhere to lipid II. Lipid II is a precursor material used
its antibacterial effect can be reduced by low pH culture or treatment for bacterial wall biosynthesis. Nisin infiltrates into lipid II, hindering
with respiratory toxins that reduce membrane potential. the growth of peptidoglycan network. When the N-terminal part of nisin
Protamine is widely used for fish preservation. Shewanella putrefa is connected with the carbohydrate pyrophosphate part of lipid II, pores
ciens is the main spoilage bacteria of grass carp slices during the whole appear on the cell membrane, thus inhibiting microorganisms (Popa
storage period, which may lead to the spoilage of fish stored in aerobic et al., 2022). The antimicrobial mechanism of nisin is shown in Fig. 5. It
condition under cold storage. Protamine can effectively inhibit the was found that the nanogel containing nisin also has an antibacterial
growth of Shewanella putrefaciens, improve the quality of grass carp fillet effect and can inhibit the growth of Staphylococcus aureus and Escherichia
and extend its shelf life (Li et al., 2016). Protamine also has a strong coli (Wu et al., 2023). Although a single natural preservative can inhibit
inhibitory effect on Pseudomonas spp., but has a weak inhibitory effect microorganisms, its range of action on microorganisms is limited. The
on Psychrobacter, Acinetobacter and Brevibacterium (Duan et al., 2018). composite preservative has a broader antibacterial spectrum, stronger
Some studies have shown that salmon protamine can kill the growing antibacterial activity. Studies have demonstrated that the tender coco
Gram-positive bacteria, and significantly inhibit the growth of Gram- nut water (TCW) quality can be extended up to 10 days after treatment
negative bacteria in Tryptone Soy Broth (Johansen et al., 1995). EDTA with nisin, and the TCW quality can be maintained for up to 15 days
and protamine have a synergistic effect. The combination of protamine after treatment with polylysine. The combination of nisin and polylysine
and EDTA enhances the inhibition of Gram-negative bacteria including showed good antimicrobial performance, which could extend the shelf
Aeromonas hydrophila, Morganella morganii and Yersinia enterocolitica). life of TCW to 20 days (Pandiselvam et al., 2022). Chitosan, tea poly
The most sensitive organisms are Brochothrix thermosphacta and Lacto phenols, and nisin have better antimicrobial effects than single pre
bacillus sakei (Truelstrup Hansen et al., 2001). servatives when used to treat plant-based meat products, demonstrated
Protamine exhibits strong antibacterial activity in neutral and alka that compared with a single preservative, the compound preservatives
line media and has high thermal stability. It has a broad-spectrum were more effective in preventing lipid oxidation in plant-based meat
antimicrobial effect on bacteria, yeasts and molds, especially against products, and its inhibitory effect on microorganisms was also better
Gram-positive bacteria. As a food preservative, protamine has the ad than that of a single preservative (Dai et al., 2022). The combination of
vantages of broad-spectrum antibacterial activity, high safety, good bacteriophages and nisin is more effective than single bacteriophages or
thermal stability, and no smell or taste, making it a promising natural nisin, and the antibacterial activity of nisin increases with the increase of
preservative. Protamine is very effective in extending the shelf life of fish concentration. The results show the potential of combining phages with
cake products and flour and rice foods. Combining fish sperm with other nisin and polylysine for the biocontrol of Salmonella enteritidis, Salmo
natural preservatives can enhance the antibacterial effect and expand nella typhimurium, and Escherichia coli O157:H7 in food industry (Wu
the scope of food preservation applications. Compared to other natural et al., 2023).
preservatives, protamine is relatively expensive and less commonly used Nisin is a natural preservative that is non-toxic, efficient, and has
in meat products. Currently, the main research focuses on the prepara strong bactericidal effects, and has been recognized internationally.
tion of protamine and its preparation into nanocapsules. So far, no toxic Nisin, as a bacteriocin preservative used in food, is widely used in dairy
incidents have occurred to the human body when using protamine. products such as fresh milk, yogurt, milk powder, and cheese, as well as
Studies on the safety of protamine have shown that the protamine LD50 in beverages, meat products, canned foods, and other fields. Nisin does
is above 10 g/kg. According to the toxicity classification of chemical not affect the flavor, texture, and product structure of food. When nisin
substances, protamine can be considered a non-toxic substance (Soko is used to preserve chilled meat, the total number of bacteria in the
lowska et al., 2016). No teratogenic or mutagenic effects on the chro chilled meat significantly decreases. At the same time, the higher the
mosomes of primary spermatocytes in the testis of mice were detected. concentration of nisin the more obvious its preservation effect. The
Through various toxicological experiments, it has been proven that antibacterial effectiveness of nisin in food preservation is compromised
protamine is actually non-toxic, has no chromosomal aberration effect, by the emergence of resistance to nisin in various bacteria. Antibacterial
and has no genetic mutation effect. Therefore, protamine can be agents that work synergistically with nisin were proved to minimize its
considered as a new type of food preservative, which is harmless, highly resistance. The combination of nisin and cinnamaldehyde can not only
safe, and highly nutritious to the human body (Lee et al., 2023). An serve as a promising natural food preservative but also reduce bacterial
overview of natural antimicrobial from animal sources is shown in resistance problems (Shi et al., 2017).
Table 1. The bacteriocin produced by Carnobacterium maltaromatium KCA018
isolated from raw milk has higher antibacterial activity against Gram-
4. Microorganism derived preservatives positive bacteria than against Gram-negative bacteria and can effec
tively inhibit the activity of Listeria monocytogenes (Kim et al., 2022).
4.1. Bacteriocin and their antimicrobial activity Studies have shown that the bacteriocin LFX01, produced by Lactoba
cillus plantarum LF-8 isolated from the intestine of tilapia (Oreochromis
Bacteriocin is a safe and effective antibacterial peptide synthesized mossambicus), has an antibacterial effect against the growth and biofilm
by ribosomes during bacterial metabolism (Jiang et al., 2022). The study formation of Staphylococcus aureus and Escherichia coli. And bacteriocin
found that Lactococcus lactis can inhibit pathogenic and putrefactive LFX01 could reduce the metabolic activity of cells, disrupts the perme
bacteria, including 10 Gram-positive bacteria and 16 Gram-negative ability and integrity of the cell membrane, and lead to the leakage of
bacteria. The hemolytic activity test of bacteriocin showed that it has intracellular material (Xin et al., 2023). The bacteriocin from Lactica
no toxicity to eukaryotic cells (Fotso Techeu et al., 2022). seibacillus rhamnosus ZFM216 has broad-spectrum antibacterial activity
9
Fig. 5. Antimicrobial mechanism of nisin killing bacteria.
and can inhibit Gram-positive bacteria and Gram-negative bacteria. including high separation and purification costs, narrow inhibition
Bacteriocin has an antibacterial effect on Staphylococcus aureus, spectra, susceptibility to enzymatic degradation, and susceptibility to
destroying the membrane and wall of Staphylococcus aureus cells, complex food environments. Different types of bacteriocins may not
resulting in cytoplasm leakage (Wu et al., 2022). A new antibiotic develop cross-resistance against bacteria because they have different
(Plantaricin Bio-LP1) produced by Lactiplantibacillus plantarum NWAFU- structures and targets of action. Numerous studies have shown that the
BIO-BS29. It shows strong inhibitory activity against both Gram-positive combining treatment of bacteriocins and various chemicals has a syn
bacteria and Gram-negative bacteria, and has a broad antibacterial ergistic antibacterial effect on spoilage microorganisms and foodborne
spectrum, with no biological human risk, it can use as a potential bio- pathogens-causing, effectively extending the shelf life of food and
preservative in food and feed (Ismael et al., 2023). Bacteriocin XJS01 ensuring food safety (Yu et al., 2023).
derived from Lactobacillus salivarius can inhibit the growth of foodborne
Staphylococcus aureus, proving the inhibitory effect of XJS01 on the 4.2. Actinomycin
spoilage of raw pork (Ying et al., 2023). Bacillocin 490 is a low molec
ular weight (2 kDa) bacteriocin produced by a thermophilic strain iso 4.2.1. Natamycin and their antimicrobial activity
lated from dairy products. But Bacitracin 490 only has inhibitory effects Natamycin is a natural polyene macrolide antifungal agent fer
on some Gram-positive bacteria (Shleeva et al., 2023). mented by Streptomyces natalensis (Mohamadi et al., 2021). The anti
Bacteriocins have properties that can be used for a wide range of food bacterial mechanism of natamycin is that it can bind with ergosterol on
and medical applications. Therefore, the safety of bacteriocins requires the cell membranes of fungi and yeast, change the permeability of the
high attention. Since 2011, nisin has been widely used as a food pre cell membrane, and is ineffective against bacteria and viruses without
servative (Soltani et al., 2021) and has no chronic, subchronic toxicity, ergosterol in the cell membrane (Chen et al., 2021). The eukaryotic cell
reproductive toxicity, genetic toxicity, carcinogenic and teratogenic ef membrane composed of lipids, phospholipids, proteins, and sterols is
fects (Hagiwara et al., 2010). However, there have been reports of high called ergosterol. Sterols provide selective binding sites for Natamycin.
concentrations of nisin causing some toxicity or side effects (De Almeida Due to its high affinity for ergosterol, Natamycin irreversibly combines
Vaucher et al., 2011). Researches have shown that bacteriocins possess with ergosterol in fungal cell membrane to form a polyene sterol com
low toxicity. The Spizizenii strain Ba49 isolated from Allium cepa showed plex. This complex alters the permeability of the membrane, causing the
low toxicity to 293 mammalian cell lines when administered at con rapid leakage of essential ions and small peptides, thus preventing the
centrations several times higher than the minimum inhibitory concen growth of yeast and fungi, however, natamycin is ineffective against
tration (Taggar et al., 2021). Most bacteriocins are non-toxic to bacteria and viruses without ergosterol in the cell membrane. The
eukaryotic cells, but enterococcal cytolysin has been found to be toxic schematic diagram representing the mode of action of Natamycin on a
(Cox et al., 2005). More comprehensive studies on the safety of bacte fungal cell is illustrated in Fig. 6 (Meena et al., 2021). Natamycin has
riocins are needed, and various measurements are required to evaluate been approved as a food additive in over 40 countries and has been
their cytotoxicity, ability to induce apoptosis, growth inhibition, he considered as a GRAS product by FDA (He et al., 2019).
molytic activity, and acute and subchronic toxicity in eukaryotic cells. Natamycin is commonly used as an additive in the food industry and
Bacteriocins have broad application prospects in food processing, has been registered as a biological fungicide for postharvest use of citrus
preservation, and food safety. With the progress of molecular biotech and other fruits. Citrus sour rot caused by Geotrichum citri-aurantii is one
nology and the maturity of genetic engineering technology, new types of of the most important postharvest diseases in citrus fruit, after using
bacteriocins can be produced through genetic and protein engineering, natamycin, the incidence rate is significantly reduced, indicating that
thereby enhancing the application potential of bacteriocins. Although natamycin can be used to sour rot control (Fernández et al., 2022). The
some bacteriocins such as nisin have been commercially applied in study showed that that natamycin significantly reduced the incidence
specific food systems, there may be limitations to use bacteriocins alone, and lesion size of fruit Botrytis cinerea, and reduced the conidial
10
Fig. 6. Mode of action of Natamycin on a fungal cell. (A) The schematic diagram of fungal cells and location of sterol and membrane channels within cells. (B)
Affinity of Natamycin towards sterol resulting in formation of polyene sterol complex. (C) Leakage of membrane channel with loss of ions and peptides from
fungal cells.
germination and mycelial growth of Botrytis cinerea (Saito et al., 2020). body. When natamycin is directly added to yogurt, it only inhibits the
Natamycin can reduce the decay rate of mulberry fruit. Mulberries with growth of mold and yeast, without affecting the bacteria (bifidobacteria)
increased concentration of natamycin could significantly inhibit the in the yogurt. In addition, it is odorless and colorless, and does not affect
growth of fungal pathogens in mulberry fruit and improve the quality of the taste when consumed. It is now the only internationally recognized
mulberry (Wen et al., 2019). Natamycin is a safe preservative that can antifungal food preservative and is used in the production and storage of
effectively inhibit the growth of mold and yeast in mulberry fruits and baked goods, fruit and vegetable drinks, dairy products and meat
improve their quality throughout the storage period after harvest. products.
Natamycin can also effectively inhibit fungal growth in soft Galotyri
cheese. At high concentrations, natamycin leads to a significant reduc 4.2.2. Polylysine and their antimicrobial activity
tion in the number of Candida tropicalis biofilm cells and damages the Polylysine is formed by the combination of ε-amino and α-carboxyl
biofilm structure. The combination of farnesol and natamycin, effec groups of lysine in alkaline solution through peptide bonds. Polylysine is
tively reduced cell counts and disrupted the structure of C. tropicalis a natural polycationic peptide produced by Streptomyces albicans. When
biofilms. The combination of natamycin and other substances to prepare the degree of polymerization is lower than decapeptide, polylysine will
composite materials also has an antifungal effect (Agustín et al., 2019). lose its antibacterial activity. Polylysine has broad-spectrum antibacte
The gum acacia-gold nanocomposite fabricated with antifungal preser rial activity and strong inhibitory effects on microorganisms such as
vative agent natamycin, has good antifungal activity against the fungus fungi, bacteria, and yeast (Wang et al., 2021). The antibacterial activity
strain Aspergillus ochraceopealiformis (Karthick Raja Namasivayam et al., of ε-polylysine is due to its positive charge can be adsorbed on the
2022). Natamycin blocks the growth of fungi through specific combi surface of microorganisms with negative charge, and its combination
nation with ergosterol, without membrane permeability. Natamycin can can change the permeability of bacterial cell membrane (Wang et al.,
also timely inhibit the lateral transport of amino acids and glucose to the 2023). The cytoplasm entered through membrane pores by polylysine
plasma membrane, leading to complete damage to fungal hyphae. and two parallel reactions occurred afterward, that is, an increase in
Natamycin has a wide range of applications, with a small dosage, reactive oxygen species (ROS) levels and the DNA genome interactions,
significant effect, and long antibacterial time. Natamycin can exert resulting in cell death (Zarrintaj et al., 2022). In 2013, polylysine was
antibacterial activity at lower concentrations, and its antibacterial ac approved by the FDA as a safe food preservative, and in 2014, it was
tivity is almost unaffected by pH. When natamycin acts together with approved by China for use in food preservation.
nisin, its antibacterial spectrum is complementary. Several studies Polylysine can be used for storage and preserve of fruits after harvest,
conducted toxicity tests with natamycin and found that it had no sub it was demonstrated that ε-polylysine has a strong inhibitory effect on
chronic toxicity, chronic toxicity (Levinskas, 1966), cytotoxicity, or the fruit pathogenic bacteria Penicillium expansum and Colletotrichum
genetic toxicity (Rasgele & Kaymak, 2013). However, long-term gloeosporioides and to delay the decline in fruit quality during storage of
administration of high doses may result in some side effects such as juniper apples and guava fruits, inducing resistance to fruit diseases and
nausea, vomiting and diarrhea (Meena et al., 2021). Natamycin is being used as a preservative for post-harvest storage (Bai et al., 2022).
difficult to be digested and absorbed in the human body and consuming ε-Polysine treatment can significantly inhibit the black spot rot of apple,
natamycin at the prescribed dose has no toxic side effects on the human jujube, and tomato, and has antifungal activity against Alternaria rot. By
11
interfering with the integrity of pathogen membrane and inducing the infect or colonize eukaryotic cells, nor do they have harmful effects on
formation of endogenous reactive oxygen species in pathogens, it can human health. A bacteriophage extracted from sewage, and adding DNA
inhibit the growth of colonies and spore germination and induce the extracted from Shiga toxin-producing Escherichia coli (STEC) to these
ultrastructural changes of pathogens. ε-Polysine not only shows anti bacteriophages can effectively combat STEC (El-Sayed et al., 2022).
bacterial activity, but also enhances the expression of genes involved in VPT02, a new cleaving bacteriophage isolated from oysters, was
the pathogenesis resistance pathway in the host (Shu et al., 2021). When confirmed to kill the seafood pathogen Vibrio parahaemolyticus and
malt agar was used as a substrate, it was found that Epsilon poly-L-lysine enhance the survival rate of brine shrimp infected with
can inhibit the growth of Gloeophyllum trabeum, Rhodonia placenta, V. parahaemolyticus. The VPT02 genome does not contain toxin and
Trametes versicolor and Irpex lacteus and other fungi (Cai & Kuo, 2022). antibiotic resistance genes that can be used as food preservatives (You
Compared to using each natural preservative alone, mixed natural pre et al., 2021). Phages have lytic activity against pathogenic bacteria, not
servatives have better antibacterial effects. ε-Polylysine, 70 % ethanol altering the quality of food. It was demonstrated that DNA extracted
extract of chestnut and hydrothermal extract of cinnamon showed sig from enteropathogenic Escherichia coli in beef lung was added to bac
nificant synergistic antibacterial effect on the growth of Staphylococcus teriophages, which could achieve antibacterial effects on lettuce and
aureus (Lee et al., 2022). Polylysine and chitosan both have antibacterial milk (Waturangi et al., 2021). Bacteriophage VVP001 can inhibit the
activity themselves, but ε-polylysine combined with chitosan-based growth of Vibrio vulnificus and protect the host from the invasion of
coatings has better antibacterial and antioxidant activity, and can V. vulnificus, and can be used as a seafood preservative (Kim et al.,
effectively inhibit the growth of spoilage microorganisms (Zhang et al., 2021). Studies show that bacteriophage P100 can inhibit the growth of
2022). Cobalt-chromium-molybdenum and ε-polylysine composite Listeria monocytogenes in ready-to-eat sliced pork ham and fresh cheeses
coatings have antibacterial and antibiofilm effects, and has obvious (Figueiredo & Almeida, 2017). The bacteriophage Spp001 reduces the
inhibitory effects on Staphylococcus aureus and Escherichia coli, leading to level of Streptococcus putrescens in marine fish Paralichthys olivaceus
the reduction of a bacterial cell aggregation and activity (Guo et al., under cold storage to prevent spoilage and achieve antiseptic effect. It
2021). Poly (L-diaminopropionic acid) and poly (ε-L-lysine) showed was demonstrated that the multivalent bacteriophage CoNShP-3 can not
strong antibacterial activity in fresh grape juice and has great potential only lyse Coagulase-negative staphylococci (CoNS), but also lyse other
as a biological preservative(Wang & Rong, 2022). ε-Polylysine hydrox genera including Staphylococcus aureus, methicillin-resistant Staphylo
ide (ε-PLH) is a homopolymer of ε-polylysine and also has antibacterial coccus aureus (MRSA), vancomycin-resistant Staphylococcus aureus
activity. Research shows that ε-PLH can inhibit the formation of Listeria (VRSA), Bacillus cereus and B. subtilis. Moreover, the CoNShP-3 phage
monocytogenes biofilms, significantly enhances the inhibition of biofilms also exhibited anti biofilm effects on Staphylococcus epidermidis CFS79
when combined with cinnamon essential oil, and shows a synergistic and Staphylococcus hemolyticus CFS43, respectively, while the biofilm of
anti-biofilm effect on Listeria monocytogenes and Pseudomonas lundensis, Staphylococcus saprophyticus CFS28 was completely removed (Sofy et al.,
which can be used in food preservatives (Zhu et al., 2022). 2020).
Polylysine is a broad-spectrum antibacterial, it can be decomposed Enteropathic Escherichia coli (EPEC) is a leading cause of foodborne
into L-lysine in the human body and completely digested and absorbed illness and poses a threat to human health. Phages have the potential to
by the human body. Moreover, polylysine has good thermal stability and be used as a natural food preservative that can be used to combat
does not decompose at high temperatures (120 ◦ C, 120 min). It can be foodborne pathogens in food preservatives. Phage UAE_MI-01 is a
sterilized together with the raw materials, so it has broad application bacteriophage of Escherichia coli O157: H7, which is isolated from the
prospects in meat products. Although polylysine has a slightly bitter feces of wild pigeons (Columba livia home) and inhibits the growth of
taste, an addition of micrograms can achieve ideal antimicrobial effects. Escherichia coli by destroying the host cell membrane (Sultan-Alolama
Therefore, the addition of trace amounts of polylysine has no effect on et al., 2021). The Bacillus phage endolysin has antibacterial activity
the taste of foods. Two-week oral administration of polylysine to rats against Klebsiella pneumoniae, Salmonella typhimurium, Proteus, and
showed no signs of toxicity and no changes in the organs, suggesting that Escherichia coli (Sarjoughian et al., 2020). Phage can also be used with
polylysine is not toxic when administered orally (Titlow et al., 2013). other preservatives to exert synergistic antibacterial effects. Phage-
Subchronic oral toxicity experiments also showed it is no toxicity (Hiraki antibiotic synergism can inhibit food borne disease bacteria (Salmo
et al., 2003). In the chronic feeding study in rats, oral administration of nella, Staphylococcus aureus and Escherichia coli). Bacteriophages and
high doses of polylysine had no significant toxicological effects on the chemical disinfection have a synergistic effect on the opportunistic
health of the experimental animals. The oral dose of polylysine in the fed pathogen Pseudomonas aeruginosa. Research has shown that the combi
mice corresponds to 100 times the maximum allowable content of nation of bacteriophage and chemical disinfectant can improve the
polylysine in human food (Song et al., 2017). Therefore, at the allowable removal of surface wet biofilm and bacteria and prevent the regenera
level of polylysine in the human body, polylysine is safe, and oral tion of dry biofilm (Stachler et al., 2021).
administration of polylysine does not cause systemic organ or systemic Phages have excellent food preservation properties and are crucial
toxicity. Polylysine has excellent biological activity and high safety. In for preclinical safety and toxicity testing of mammalian cells and tissues.
addition to being approved as a food preservative by countries such as The FDA has approved the use of phages as food preservatives to combat
the United States, Japan, and South Korea, China has also added poly foodborne bacteria and treat bacterial infections (Jault et al., 2019).
lysine to the list of approved food preservatives (Yang et al., 2023). Phage preparations against Listeria monocytogenes (Listshield TM), Sal
monella enterica (SalmFresh TM), and Escherichia coli (Ecoshield TM)
4.3. Phage and their antimicrobial activity have received Generally Recognized As Safe (GRAS) designation from
the FDA for direct use on food (Nazir et al., 2023). Studies have evalu
Phage is a virus that specifically infects bacteria and can be used as a ated the safety of the pneumococcal endolysins Cpl-1 and Pal, including
natural food preservative. The antibacterial mechanism is due to the an in vivo safety assessment of mouse models and gene expression
high specificity, self-replication, and rapid killing characteristics of profiling, all of which confirmed no adverse effects in mice (Harhala
phages on host cells. Phages attach specifically to their host bacterial et al., 2018). Phages with high specificity and a narrow lysis spectrum,
strains, inject DNA or RNA genome, and replicate and express their can specifically cleave harmful microorganisms and have no infective
genes through the mechanism of hijacking host cells. Then the new virus ability against humans, animals and plants outside the host range (Gyles,
particles are assembled in the host cell, the cell is split, and the virus of 2018). Phages have rapid self-reproduction and short screening cycles
offspring is released (Ibarra-Sánchez et al., 2018). and are widespread in nature. In recent years, phages have been
Lytic phages are viruses that cause specific bacterial hosts to lyse, not increasingly recognized for their efficient, rapid and safe properties. In
disrupting the normal microbial community of humans. They will not addition, while phages kill bacteria, they have no harmful effects on
12
food sensory organs (Khan et al., 2023). Although safety research results Research Center for Molecular Biotechnology of Fujian & Taiwan TCM,
so far support the claim that phages are a potentially safe antibacterial Fujian Key Laboratory of Chinese Materia Medica at Fujian University of
agent. Further research is needed to confirm that different types of Traditional Chinese Medicine.
bacteriophages do not have significant effects on humans. Phages have
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Activity and Safety Evaluation of Natural Preservatives

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Food Research International 190 (2024) 114548

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Food Research International

Activity and safety evaluation of natural preservatives

1. Introduction essential nutrient (Gutiérrez-del-Río et al., 2018).

Fig. 1. The safety evaluation of natural preservatives.

Fig. 2. The antibacterial mechanism of essential oils.

Table 1 Table 1 (continued )

Fig. 5. Antimicrobial mechanism of nisin killing bacteria.

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