Antibiotics: nisin and natamycin are examples of antibiotics used to preserve a variety of food items
[16].
-
Presently, the United States Food and Drug Administration (US FDA) has approved over 3000 food additives. A comprehensive and authoritative list of all the diverse food additives utilized in the United States can be accessed at EAFUS (everything added to food in the United States)
[17]. Food additives that possess antimicrobial properties, effectively safeguarding foods against the growth of microorganisms such as fungi and bacteria, are crucial in extending the shelf life of various food items. One of the oldest and most widely used preservatives is sodium chloride, commonly known as salt. Additionally, organic acids, including benzoic acid (E210), acetic acid (E260), sorbic acid (E200), propanoic acid (E280), and many more, are extensively utilized (
Figure 1)
[16].
Figure 1.
Example of some artificial antimicrobial food preservatives used in the food industry.
3. Side Effects of Artificial Food Preservatives
Artificial food preservatives refer to chemical substances that are added to food products in order to limit bacterial growth and chemical alterations. The use of artificial food preservatives is intended to prolong the longevity of food items by impeding the proliferation of microorganisms, encompassing bacteria, yeast, and molds, which can cause spoilage and foodborne illnesses
[18], in addition to inhibiting food oxidation reactions, especially by scavenging free radicals that may lead to food rancidity
[19]. Hence, artificial food preservatives can help maintain the freshness, flavor, and overall quality of food products
[16].
The era of agri-food industries is known for the introduction of various artificial food preservatives, including benzoates in acidic foods and beverages, sulfites to prevent browning and discoloration in fruits and vegetables, nitrites and nitrates to prevent the growth of harmful bacteria in meat products, propionates, which are used in the preparation of bread and other baked products, antioxidants to prevent the oxidation of fats and oils, etc. In fact, although there are beneficial effects from using artificial preservatives to extend the shelf life and maintain food quality, their widespread use has been accompanied by harmful side effects on human health
[16].
In this regard, recent studies have targeted concerns about the side effects of artificial food preservatives, including allergic reactions, carcinogenic concerns, hyperactivity in children, gastrointestinal distress, asthma and respiratory issues, disruption of the gut microbiota, hypersensitivity, and sensitization
[20][21] (
Figure 2). Regulatory agencies such as the FDA (Food and Drug Administration) in the United States set limits on the use of these preservatives in foods to ensure they are safe for consumption. In addition, it was recommended that a safe daily intake should not exceed 5 milligrams per kilogram of body weight for sodium benzoate, which is widely used due to its antibacterial and anti-fungal properties
[22]. However, recent research suggests that the combination of sodium benzoate and artificial colors in food can lead to hyperactivity
[23]. This neurodevelopmental disorder affects millions of people, causing difficulties regarding time management and task completion. While there is no specific treatment for this disorder, affected individuals may benefit from medication and behavioral therapy. Additionally, it has been shown that artificial food preservatives may induce serious allergic reactions
[24] and asthma
[25], which could be considered triggers or aggravating factors in sensitive individuals. For example, sulfites can cause allergic reactions and asthma in some people, leading to symptoms such as hives, itching, difficulty breathing, and even anaphylaxis in severe cases
[26]. Furthermore, some studies and animal trials have raised concerns about the potential carcinogenicity of certain artificial preservatives. For instance, there has been some debate over the safety of nitrites and nitrates in processed meats, as these compounds can form nitrosamines, which are potentially carcinogenic
[27]. Moreover, artificial food preservatives may induce digestive discomfort, including symptoms such as bloating, gas, and diarrhea. A study has reported the correlation between carrageenan exposure and the manifestation of colonic ulcerations and gastrointestinal neoplasms in animal models
[28]. Some studies have also suggested that certain artificial preservatives may have an impact on the composition of the gut microbiota, potentially affecting gut health. Based on in vitro studies, animal models, and human clinical trials, Cao et al.
[29] reported that food additives could modify the gut microbiota and human health status. However, prolonged or high-level exposure to certain artificial food preservatives may lead to hypersensitivity or sensitization, whereby individuals become more reactive to the preservative over time
[30].
Figure 2.
Possible side effects of artificial food preservatives.
4. Food Spoilage Microorganisms
In fact, food spoilage is a complex process biotic factors, such as microorganisms and enzymes, interact with abiotic factors such as temperature, humidity, light, and oxygen levels to influence food deterioration and spoilage. Maintaining optimal storage conditions and minimizing microbial contamination are crucial for preserving food quality and safety
[31][32].
Spoilage, which is defined as “an organoleptic change in food”, can happen at any point in the food chain
[33]. Insects, physical damage, native enzyme activity, and microbes can all contribute to the deterioration of foods. Indeed, food spoilage microorganisms are defined as various types of bacteria, yeasts, molds, and other microorganisms that can grow on or within food, leading to changes in its quality, flavor, texture, and appearance
[3]. These microorganisms thrive in different conditions and can cause the spoilage of various types of foods. Psychrotrophic bacteria can grow at low temperatures and are responsible for spoilage in refrigerated foods such as dairy products and meats
[34]. Thermophilic bacteria thrive at high temperatures and can cause spoilage in processed foods, canned products, and sauces
[35]. Lactic acid bacteria contribute to the fermentation of foods but can also cause spoilage if they proliferate excessively, especially with some strains that possess proteolytic activity when in meat products
[36]. Additionally, yeasts and molds are often responsible for spoilage in sweet products, including bread, fruits, vegetables, syrups, and dairy products
[37][38].
The biochemical activity of microbial chemical processes has led to this complicated ecological phenomenon, which will ultimately be dominated by pre-existing ecological variables. When microbes multiply in food, they secrete enzymes that induce off-putting byproducts
[39]. Metabolic processes in microbial food degradation yield substrates such as organic acids, esters, carbonyls, diamines, alcohols, sulfur compounds, hydrocarbons, and fluorescent pigments. The detection of microbial toxins or spores causing food contamination is difficult, as they often remain latent until a foodborne illness outbreak transpires, despite our reliance on chemical and physical attributes for microorganism spoilage detection. Hence, the intricate mechanisms and interplays driving food deterioration largely persist as subjects of significant obscurity
[33]. This is despite the fact that food spoilage has substantial health and economic implications.
5. Natural Antimicrobial Agents
In the realm of contemporary medicine, the vast array of compounds found in nature serves as a rich source, with the potential to combat pathogens. This assumes paramount importance, particularly in the face of the growing crisis of antimicrobial resistance. Prominent origins of natural compounds endowed with valuable antimicrobial properties encompass fungi, bacteria, medicinal plants, marine organisms, and terrestrial organisms (
Figure 3). Nevertheless, a substantial diversity of flora and fauna remains largely untapped, holding great potential for yielding further antimicrobial candidates and pharmaceutical agents when subjected to systematic exploration
[40].
Figure 3.
Diverse sources of antimicrobial agents from nature, involving either phytochemicals, peptides, or other molecules.
The increasing demand for chemical-free food and the limited efficacy of traditional food preservation methods in inhibiting foodborne pathogens have driven the adoption of antimicrobials by the food industry
[41]. This emerging technology aims to prolong the shelf life of food products and address issues related to food quality and safety. Antimicrobials can be either natural or synthetic, with a growing emphasis on the importance of natural antimicrobials over their synthetic counterparts. Despite the approval of synthetic preservatives for human consumption given by government organizations, concerns persist regarding their potential adverse effects on health
[42].
Various sources provide natural antimicrobials that are employed to safeguard food against spoilage and pathogenic microorganisms. Plants, including herbs, spices, fruits, vegetables, seeds, and leaves, constitute the primary reservoir of antimicrobial compounds, many of which contain essential oils with potent antimicrobial properties
[43]. Notably, herbs and spices such as rosemary, sage, basil, oregano, thyme, cardamom, and clove are abundant in essential oils. These oils play a crucial role in enhancing food quality and extending shelf life by efficiently combating a wide range of pathogenic and spoilage microorganisms, including
Salmonella spp.,
Escherichia coli,
Listeria monocytogenes,
Campylobacter spp., and
Staphylococcus aureus [44][45]. Furthermore, these antimicrobial substances find applications as edible food coatings, which effectively prevent the proliferation of bacteria on food and the surfaces of food-related products.
Antimicrobial activity is of paramount importance in modern medicine, referring to the ability of a substance to eliminate or impede the growth of microorganisms such as bacteria, viruses, fungi, and protozoa. These antimicrobial substances find widespread applications in areas such as food preservation, medicine, and personal hygiene. The advent of antimicrobial drugs has heralded groundbreaking advancements in the treatment of infectious diseases, leading to the preservation of numerous lives
[46].
Antimicrobial compounds can be synthesized in laboratories or may be found naturally in microorganisms, animals, and plants. Throughout history, the natural antibacterial chemicals present in various herbs and spices have been utilized to preserve food freshness and prevent spoilage. Furthermore, certain invertebrates and mammals produce antimicrobial peptides, which serve as defense mechanisms against diseases.
6. Spices as a Source of Natural Antimicrobial Agents
Spices refer to the aromatic components derived from various plant parts such as seeds, fruits, roots, barks, or other plant substances, and are primarily employed for enhancing the flavor or adding color to food. These substances are distinct from herbs, which comprise the leaves, flowers, or stems of plants and serve different culinary purposes
[47]. The Food and Drug Administration (FDA) defines spices as “whole, broken, dried, or ground vegetable substances used for flavoring and seasoning food”
[48].
Throughout ancient and medieval culinary history, spices have played a pivotal role, with their utilization influenced not only by taste preferences but also by prevailing medical theories concerning diet and health. Spices have a rich history of traditional medicinal use for treating a wide range of ailments. In recent decades, numerous preclinical and clinical studies have provided compelling evidence supporting the beneficial effects of spices and their active components in preventing and managing various diseases, such as diabetes, arthritis, cancer, asthma, cardiovascular diseases, and neurodegenerative diseases
[49]. Spices emanate from desiccated botanical components such as flower buds and blooms (e.g., cloves and saffron), subterranean rhizomes (ginger and turmeric), inner bark (cinnamon), reproductive structures such as fruits and berries (e.g., cloves, chili, and black pepper), or embryonic propagules (e.g., cumin)
[50]. They may also include various herbs such as marjoram, parsley, mint, rosemary, oregano, and thyme
[51]. The spice trade has evolved into a significant economic activity due to its favorable characteristics and diverse applications. In 2020, spice exports were valued at USD 3.61 billion, experiencing a 23.2% increase from 2019. In terms of global trade, spices account for 0.022%
[52]. Spice sales are increasing annually worldwide and modern food production and trade globalization have made spices readily available year-round in developed nations
[53]. Spices have demonstrated significant antimicrobial properties, which make them valuable in countering microbial infections. Their active constituents often exhibit natural antimicrobial properties that help to inhibit the growth and proliferation of various pathogenic microorganisms, such as bacteria, fungi, and even some viruses. Moreover, due to their inherent ability to inhibit the growth of spoilage-causing microorganisms, spices have been utilized as natural food preservatives since ancient times
[54].
3.6. Suggested Antimicrobial Spices for Food Preservation
7. Suggested Antimicrobial Spices for Food Preservation
Quantifying the precise number of spices in the world proves challenging, due to the influence of multi-cultural and culinary practices. Based on the existing literature, an exact count of the spices that are currently employed remains elusive. Nonetheless, it is estimated that there are roughly 112 types of spices in use worldwide today
[55]. The present re
vise
warch has identified a restricted selection of 25 spice types that exhibit significant antimicrobial properties (
Table 1). Given the diverse array of chemical compound groups present in herbs and spices, it is probable that their antimicrobial activity does not hinge on a singular mechanism. Instead, multiple mechanisms likely come into play, each targeting various aspects of microbial cells. Nevertheless, these various mechanisms can generally be categorized into two overarching objectives: impeding the proliferation of spoilage microorganisms to facilitate food preservation, and restraining or modulating the growth of pathogenic microorganisms
[11][56].
Table 1. Prominent spices exhibiting remarkable antimicrobial activities, proposed as natural preservatives for the food industry.
No.
|
Spice
|
Scientific Name
|
Botanical Family
|
Major Bioactive Compound
|
Chemical Structure
|
Antimicrobial Activity
|
Ref.
|
1
|
Allspice
|
Pimenta dioica (L.) Merr.
|
Myrtaceae
|
Eugenol
|
|
Listeria monocytogenes CECT 933, Vibrio vulnificus CECT 529, Salmonella enterica CECT 443, Shigella flexeneri CECT 4804, Escherichia coli ATCC 35218, Staphylococcus aureus ATCC 6538, and Aspergillus flavus.
|
[57][58]
|
2
|
Anise
|
Pimpinella anisum L.
|
Apiaceae
|
Anethole
|
|
Escherichia coli ATCC 25922, Staphylococcus aureus ATCC 25923, Pseudomonas aeruginosa ATCC 27853, Streptococcus pyogenes ATCC 19615, and Candida albicans ATCC 10231.
|
[59][60]
|
3
|
Basil
|
Ocimum basilicum L.
|
Lamiaceae
|
Methyl cinnamate
|
|
Staphylococcus epidermidis MTCC 435, Streptococcus mutans MTCC 890, Escherichia coli MTCC 723, Candida kefyr ATCC 204093, and Candida albicans ATCC 14053.
|
[61][62]
|
4
|
Bell pepper
|
Capsicum annuum L.
|
Solanaceae
|
Capsaicinoids
|
|
Listeria monocytogenes, Salmonella typhimurium, Staphylococcus aureus, Escherichia coli, Bacillus subtilis, Proteus mirabilis, Lactobacillus plantarum, Lactobacillus acidophilus, and Cochliobolus spp.
|
[63][64]
|
5
|
Black Pepper
|
Piper nigrum L.
|
Piperaceae
|
Piperine
|
|
Klebsiella pneumonia ATCC 27853, Escherichia coli ATCC 25922, Salmonella enterica ATCC 43972, Staphylococcus aureus ATCC 25923, Enterococcus faecalis ATCC 29122, Staphylococcus epidermidis ATCC 14990, Bacillus subtilis ATCC 6633, and Aspergillus flavus CGMCC 3.06434.
|
[65][66]
|
6
|
Black seeds
|
Nigella sativa L.
|
Ranunculaceae
|
Thymoquinone
|
|
Escherichia coli, Klebsiella pneumoniae, Staphylococcus aurous, Enterobacter aerogenes, Fusarium Solani, Candida albicans AUMC 1299, Aspergillus flavus AUMC 1276, Fusarium oxysporum AUMC 215, Scopulariopsis brevicaulis AUMC 1653, Geotrichum candidum AUMC 226, and Trichophyton rubrum AUMC 1804.
|
[67][68]
|
7
|
Caraway
|
Carum carvi L.
|
Apiaceae
|
Carvone
|
|
Escherichia coli, Pseudomonas aeruginosa, Staphylococcus aureus, Bacillus cereus, and Aspergillus flavus.
|
[69][70][71]
|
8
|
Cardamom
|
Elettaria cardamomum (L.) Maton
|
Zingiberaceae
|
Cardamonin
|
|
Bacillus subtilis, Staphylococcus aureus, Pseudomonas aeruginosa and methicillin-resistant Staphylococcus aureus (ATCC 43300), Salmonella typhimurium (ATCC 14023), and Escherichia coli (ATCC 25922).
|
[72][73][74]
|
9
|
Cinnamon
|
Cinnamomum verum J.Presl
|
Lauraceae
|
Cinnamaldehyde
|
|
Micrococcus luteus, Bacillus subtilis, Bacillus cereus, Klebsiella aerogenes, Escherichia coli, Salmonella enterica, Penicillium expansum, Candida albicans, and Candida tropicalis.
|
[75][76]
|
10
|
Clove
|
Syzygium aromaticum (L.) Merr. & L.M.Perry
|
Myrtaceae
|
Eugenol
|
|
Staphylococcus aureus, Listeria innocua, Pseudomonas aeruginosa. Serratia marcescens, Bacillus subtilis, Penicillium commune, Penicillium expansum, Penicillium glabrum, and Penicillium chrysogenum
|
[77][78][79]
|
11
|
Coriander
|
Coriandrum sativum L.
|
Apiaceae
|
Linalool
|
|
Bacillus subtilis, Stenotrophomonas Penicillium expansum, Streptococcus pyogenes, Listeria monocytogenes, Enterobacter aerogenes, Salmonella typhimurium, and Shigella dysenteriae.
|
[80][81][82]
|
12
|
Cumin
|
Cuminum cyminum L.
|
Apiaceae
|
Cuminaldehyde
|
|
Staphylococcus aureus, Bacillus cereus, Escherichia coli, Salmonella typhi, Botrytis cinerea, Penicillium expansum, and Aspergillus niger.
|
[83][84][85]
|
13
|
Dill
|
Anethum graveolens L.
|
Apiaceae
|
Carvone
|
|
Escherichia coli, Staphylococcus aureus, Yersinia enterocolitica, Geotrichum candidum, Salmonella typhimurium, Rhodotorula glutinis, Saccharomyces cerevisiae, and Candida albicans.
|
[86][87]
|
14
|
Fennel
|
Foeniculum vulgare Mill.
|
Apiaceae
|
Anethole
|
|
Staphylococcus albus, Bacillus subtilis, Salmonella typhimurium, Shigella dysenteriae, Escherichia coli, Bacillus cereus, Staphylococcus aureus, Candida albicans, and Aspergillus flavus.
|
[88][89][90]
|
15
|
Fenugreek
|
Trigonella foenum-graecum L.
|
Fabaceae
|
Sotolone
|
|
Staphylococcus aureus ATCC 25923, Escherichia coli ATCC 25922, Bacillus subtilis NCTC 8236, Pseudomonas aeruginosa ATCC 27853, Aspergillus niger ATCC 9763, and Candida albicans ATCC 7596.
|
[91][92]
|
16
|
Garlic
|
Allium sativum L.
|
Amaryllidaceae
|
Allicin
|
|
Staphylococcus saprophyticus, Staphylococcus aureus, Staphylococcus epidermidis, Bacillus cereus, Streptococcus pneumoniae, Shigella flexneri, Proteus vulgaris, Klebsiella pneumoniae, Escherichia coli, Aspergillus versicolor, Penicillium expansum, Penicillium citrinum, and Candida albicans.
|
[93][94][95]
|
17
|
Ginger
|
Zingiber officinale Roscoe
|
Zingiberaceae
|
Gingerol
|
|
Staphylococcus epidermidis, Staphylococcus aureus, Enterococcus faecalis, Streptococcus faecalis, Bacillus subtilis, Bacillus megaterium, Bacillus cereus, Escherichia coli, Klebsiella pneumoniae, Salmonella typhimurium, Salmonella typhi, Pseudomonas aeruginosa, Proteus spp., Aspergillus niger, Aspergillus flavus, Penicillium expansum, Alternaria alternata, Fusarium oxysporum, Mucor hemalis, Penicillium notatum, Candida albicans, and Fusarium oxysporum.
|
[96][97][98]
|
18
|
Mastic
|
Pistacia lentiscus L.
|
Anacardiaceae
|
α-pinene
|
|
Escherichia coli, Staphylococcus aureus, Bacillus subtilis, Helicobacter pylori, Streptococcus mutans, Microsporum canis, Trichophyton mentagrophytes, and Trichophyton violaceum.
|
[99][100]
|
19
|
Nutmeg
|
Myristica fragrans Houtt.
|
Myristicaceae
|
myristicin
|
|
Staphylococcus aureus MTCC 737, Bacillus subtilis MTCC 441, Pseudomonas putida MTCC 1072, Pseudomonas aeruginosa MTCC 7903, Listeria monocytogenes, Aspergillus flavus MTCC 277, Aspergillus niger MTCC 282, and Aspergillus fumigatus MTCC 343.
|
[101][102][103]
|
20
|
Parsley
|
Petroselinum crispum (Mill.) Fuss
|
Apiaceae
|
Apigenin
|
|
Salmonella enterica, Staphylococcus aureus, Listeria monocytogenes, Penicillium ochrochloron, and Trichoderma viride
|
[104][105]
|
21
|
Rosemary
|
Rosmarinus officinalis L.
|
Lamiaceae
|
Rosmarinic acid
|
|
Bacillus cereus, Staphylococcus aureus, Salmonella choleraesuis, Clostridium perfringens, Aeromonas hydrophila, Escherichia coli, Listeria monocytogenes, and Brochothrix thermosphacta.
|
[106][107]
|
22
|
Saffron
|
Crocus sativus L.
|
Iridaceae
|
Crocin
|
|
Klebsiella pneumoniae, Pseudomonas aeruginosa, Proteus vulgaris, Staphylococcus aureus, Escherichia coli, Candida albicans, Aspergillus fumigatus, and Aspergillus niger.
|
[108][109]
|
23
|
Thyme
|
Thymus vulgaris L.
|
Lamiaceae
|
Thymol
|
|
Pseudomonas aeruginosa ATCC 27853, Staphylococcus aureus ATCC 25923, Salmonella typhimurium ATCC 14028, Klebsiella pneumoniae ATCC 13882, Enterococcus faecalis ATCC 29212, Escherichia coli ATCC 25922, and Candida albicans ATCC 10231.
|
[110][111]
|
24
|
Turmeric
|
Curcuma longa L.
|
Zingiberaceae
|
Curcumin
|
|
Staphylococcus aureus ATCC 25923, Staphylococcus epidermis ATCC 12228, Escherichia coli ATCC 25922, Klebsiella pneumoniae ATCC 10031, Vibrio harveyi, Vibrio cholerae, Bacillus subtilis, Bacillus cereus, Aeromonas hydrophila, Staphylococcus intermedius, Edwardsiella tarda, Streptococcus agalactiae, Cryptococcus neoformans, Candida albicans, and Fusarium solani.
|
[112][113]
|
25
|
Vanilla
|
Vanilla planifolia Andrews
|
Orchidaceae
|
Vanillin
|
|
Staphylococcus epidermidis, Staphylococcus saprophyticus, Staphylococcus aureus, Streptococcus pyogenes, Enterococcus faecalis, Enterobacter hormaechei, Enterobacter cloacae, Klebsiella pneumoniae, Salmonella typhimurium, Escherichia coli, and Pseudomonas aeruginosa.
|
[114][115]
|