• Open Access
    Review

    Ellagitannins from Eucalyptus camaldulensis and their potential use in the food industry

    Eliseo Sánchez-Loredo 1
    Leonardo Sepúlveda 1
    Jorge E. Wong-Paz 2
    Lissethe Palomo-Ligas 1
    Raúl Rodriguez-Herrera 1
    Cristóbal N. Aguilar 1
    Juan A. Ascacio-Valdés 1*

    Explor Foods Foodomics. 2024;2:83–100 DOI: https://doi.org/10.37349/eff.2024.00027

    Received: September 27, 2023 Accepted: January 04, 2024 Published: February 27, 2024

    Academic Editor: José Pinela, Polytechnic Institute of Bragança, Portugal

    This article belongs to the special issue The food (r)evolution towards food quality/security and human nutrition

    Abstract

    Plants play a key role in the treatment and prevention of diseases since ancient times. Eucalyptus has been traditionally used in the treatment of conditions related to the respiratory system, such as flu, colds, sore throats, bronchitis, as well as neuralgia, and stiffness. Eucalyptus camaldulensis has several phytoconstituents such as ellagitannins endowed with bioactivity, including antioxidant and inhibitory potential on various microorganisms causing foodborne diseases. Tellimagrandin I, pedunculagin, castalagin/vescalagin are among the most representative and have activity against pathogens such as Staphylococcus aureus, Escherichia coli, Listeria monocytogenes, and Bacillus cereus. These antioxidant ellagitannins may have potential application in the food, pharmaceutical, and cosmetic industries. The main industrial uses of E. camaldulensis are related to the production of wood, paper, and charcoal, with its leaves and branches considered by-products from these industrial activities. However, these plant by-products could be used to obtain bioactive compounds for the development of new and improved consumer goods. Therefore, the aim of this work was to review the main ellagitannins of E. camaldulensis and their antioxidant and antibacterial activities in foodborne microorganisms, as well as the relevance that these compounds may have in the food industry and related sectors.

    Keywords

    Antioxidants, ellagitannins, Eucalyptus camaldulensis, foodborne microorganisms, natural ingredients

    Introduction

    In human traditions, herbal medicine has played a role in treating and preventing ailments and diseases, bringing wellness to human beings [1]. One of the most widely used plants in traditional remedies is plants of the Eucalyptus genus. Eucalyptus has traditionally been used as a remedy for conditions related to the respiratory system [2] as Eucalyptus camaldulensis to treat flu, common colds, and nasal infections, through decoctions. Also, Eucalyptus globulus for asthma, cold, cough, as decoction and extracts [3], and in Latin America, has also been used for nasal congestion, throat pain and inflammation, chest pain, airway clearance, removal of phlegm, pharyngitis and as a disinfectant and antiseptic, either as an infusion, ointment, ointment, tea, vaporization, and aromatic water [4]. Eucalyptus essential oils (EOs) are among the first oils marketed in the world besides, they have bioactivity that allows them to be used in traditional remedies for the treatment of gastrointestinal disorders and wound healing, as a herbicide, and against some pests, acaricide, nematicide, its use in perfumery, soap making, in addition as an antiseptic, antioxidant, against some fungi and bacteria that can be pathogenic [5].

    Several species of the Eucalyptus genus have spread in many parts of the world due to its great qualities such as rapid growth rate and high biomass production, the ability to grow in various environments and soils, its short cellulose fiber, and the high quality of the wood, as well as its pulp for the paper industry, the timber industry for the production of plywood and solid wood [6] and production of EO in the cosmetic industry, since the oil of other eucalyptus species has been used in the cosmetic industry, some of the most used species were E. globulus [79] and Eucalyptus citriodora [5, 10]. E. camaldulensis is a plant source very rich in EO with bioactive properties, and phenolic compounds, that could be used in medicine and food preservation. Thus, in the Asian continent, E. camaldulensis is used in traditional medicine to mitigate various symptoms of respiratory diseases, such as cough, sore throat, and sinusitis [3, 11]. The EO of E. camaldulensis has shown a potential to inhibit malatogensis in the skin with mice and decrease intracellular oxygen reactant species, which makes its use as a skin care pharmaceutical product possible [12].

    These EO are usually recovered from various parts of the plant, ranging from wood, leaves, roots, flowers, and fruits [13]. Different class of secondary metabolites can be found, among which terpene compounds stand out, especially monoterpenes, sesquiterpenes, alcohols, ketones, esters, aldehydes, and phenols [5].

    Within the Eucalyptus genus, the most cultivated species in plantations are Eucalyptus grandis, E. globulus, E. camaldulensis, as well as the hybrids made from these species [6]. In addition, E. camaldulensis is a plant rich not only in EOs with bioactive properties, but also in the content of phenolic compounds as flavonoids and ellagitannins that can be used in medicine and food preservation [11]. The use of new sources of antioxidants and antimicrobials is necessary due to the potential use of these compounds and their multiple applications, avoiding the depletion of sources and taking advantage of by-products from agri-food industries. The aim of this work was to make a particular compilation about of the main ellagitannins of E. camaldulensis, and their antioxidant, antibacterial activities in food pathogenic microorganisms and the relevance that these may represent in food trends.

    General information

    E. camaldulensis is a plant native to Australia [11], known in the world as red gum, red gum Murray, red, and river gum [14]. It is employed industrially mainly in the paper industry (70–80%) [7], followed to that carbon (10–15%) and finally only 5% of the tree is used for pool construction; this type of industrial exploitation generates waste as leaves and branches that could whereas be a good potential source of bioactive compounds [11]. The botanic structure E. camaldulensis is composed of a bark that varies from white shades and smooth surface, dull green leaves in adulthood, narrow and pointed, the juvenile leaves are usually more oval. It has a strongly beaked operculum between 0.3–0.7 cm long at maturity and a long operculum of 0.9–1.6 cm long with curvature in some subspecies. In addition, it has a capsule that houses the seeds in its interior [14] (Figure 1). E. camaldulensis trees can generate tall forests and adapt to diverse climatic regions, from areas of high rainfall to semi-arid regions in high and low regions at sea level [6].

    Upper parts from E. camaldulensis. A. Leaves; B. operculum; C. capsule from E. camaldulensis

    Chemical composition

    E. camaldulensis is a plant with a wide variety of chemical constituents among which stand out the terpenoids, alkaloids, flavonoids, tannins, saponins, and glucosides among others such as phenolic acids as seen in Table 1 [15], and the main compounds found is 1,8-cineole mainly in fresh leaves [16].

    Volatile and phenolic profile of E. camaldulensis extracts (expressed as % in the sample) [15, 17]

    ClassCompoundEO (leaves, %)Extract (leaves, %)
    Monocyclic monoterpeneα-Pinene14.68-
    Bicyclic monoterpeneCamphene0.87-
    Monocyclic monoterpeneβ-Pinene6.66-
    Non-cyclic monoterpeneα-Pinene epoxide0.27-
    Monocyclic monoterpeneγ-Terpinene9.42-
    Monocyclic monoterpeneδ-Terpinene1.11-
    Acyclic terpeneIsoamyl isovalerate1.07-
    Monocyclic monoterpeneFenchyl alcohol0.79-
    Monocyclic monoterpeneα-Camphodenic aldehyde0.66-
    Monocyclic monoterpeneTrans-pinocarveol8.36-
    Monocyclic monoterpeneMytenal0.94-
    Monocyclic monoterpeneZ-Carveol1.15-
    Monocyclic monoterpened-Carvone0.51-
    Monocyclic monoterpeneo-Cymen-5-ol0.46-
    Acyclic terpeneBenzyl valerate0.14-
    Bicyclic monoterpeneα-Gurjunene0.26-
    Bicyclic monoterpeneβ-Gurjunene0.22-
    Tricyclic monoterpeneAromadendrene2.63-
    Tricyclic monoterpeneAlloaromadendrene0.89-
    Tricyclic monoterpenePhenethyl isovalerate0.90-
    Monocyclic monoterpeneLedene0.45-
    Monocyclic monoterpeneEpiglobulol1.83-
    Monocyclic monoterpeneLedol7.42-
    Monocyclic monoterpeneViridlorol1.13-
    Monocyclic monoterpeneEremophilene1.13-
    Monocyclic monoterpeneγ-Cadinene0.29-
    SesquiterpenesCamaldulinP-
    SesquiterpenesUrsolic acid lactoneP-
    SesquiterpenesBetulinic acidP-
    SesquiterpenesOleanolic acid and ursolic acidP-
    Cyclic monoterpeneEucalyptol (1–8 cineol)34.42-
    Hydrolyzable tanninHHDP-glucopyranose-8.07
    Hydrolyzable tanninGalloylglucopyranose-4.11
    Hydrolyzable tannin Galloyl quinic acid-3.59
    Hydrolyzable tanninGalloyl shikimic acid-2.44
    Phenolic acidPhloroglucinol derivative-3.41
    Phenolic acidChlorogenic acid-14.20
    Hydrolyzable tanninDigalloylglucopyranose-4.25
    FlavonoidCypellocarpin B-8.08
    Condensed tanninBenzyl-galloylglucose-8.16
    FlavonoidQuercetin glucuronide-5.15
    FlavonoidKaempferol glucuronide-3.36
    Hydrolyzable tanninGalloyl-HHDP-glucopyranose-13.38
    Hydrolyzable tanninVescalagin-

    6.10

    Hydrolyzable tanninGalloyl-HHDP-glucopyranose-15.09
    Hydrolyzable tanninPedunculagin isomer-9.40
    Hydrolyzable tanninCastalagin-1.10
    Hydrolyzable tanninDigalloylglucopyranose-2.28
    Hydrolyzable tanninValoneoyl-HHDP-glucopyranose-1.40
    Hydrolyzable tanninDigalloylglucopyranose-2.28
    Condensed tanninpterocarinin A-0.56
    Hydrolyzable tanninValoneic acid dilactone-1.65
    Hydrolyzable tanninGalloyl cypellocarpin B-2.59
    FlavonoidQuercetin pentoside-2.64
    Hydrolyzable tanninEllagic acid derivative-2.08
    Hydrolyzable tanninPedunculagin isomer-6.18
    Hydrolyzable tanninEllagitannin dimer-6.75
    Hydrolyzable tanninSanguiin H10-like ellagitannin dimer-9.79
    Hydrolyzable tanninTellimagradin I-31.97
    Hydrolyzable tanninGalloyl-bis-HHDP-glucopyranose isomer-1.02
    Hydrolyzable tanninValoneoyl-digalloyl-glucopyranose-1.45
    Hydrolyzable tanninValoneic acid dilactone-2.70
    Hydrolyzable tanninTetragalloylglucopyranose-1.79
    Hydrolyzable tanninSanguiin H10-like ellagitannin dimer-0.47
    Hydrolyzable tanninEllagitannin dimers-18.22
    Hydrolyzable tanninTrigalloyl-HHDP-glucopyranose-2.69
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    P: for only the compounds present without identifying the percentage; HHDP: hexahydroxy diphenic acid; -: not involving

    Moreover, other chemical constituents very important and high value reported for E. camaldulensis are phenolic compounds among which are flavonoids, and ellagitannins in more abundance. The total content of polyphenols in this species was estimated to be about 364.1 mg ± 8.2 mg, data reported in gallic acid equivalents, of which about 80.5 mg ± 0.9 mg appear to be flavonoids determined as quercetin equivalents [17].

    Extraction is the most important step to obtain phenolic compounds from plant sources and this can be carried out by various extractions and solvents [18]. It has been possible to extract compounds from E. camaldulensis with different solvents. The use of different solvents varies in the type of compounds extracted as well as the amount, which makes the difference in obtaining these [17]. For example, flavonoids can be found in ether-soluble fractions of leaf extracts [10]. Whereas among the compounds found in aqueous fractions are flavones, different glycosides, and important phenolic compounds like phenolic acids, ellagitannins and their derivates, gallotannins and phloroglucinol derivatives [17]. It may also present other compounds such as alkaloids, caffeine derivatives, purine derivatives, and some acids [19].

    Also, the extract in acetone was reported as rich in bioactive compounds as the ellagitannins pedunculagin and tellimagrandin I, flavonols, as well as terpenoids. Other fractions with 60% methanol have allowed the separating of ellagitannins, ellagitannins isomer, and ellagitannin dimers mainly among they are pedunculagin isomer and other compounds [17] as can be seen in Table 1.

    Although E. camaldulensis has compounds that could be beneficial, it also has saponins, which could have a negative effect on health. On the other hand, it has also been reported that E. camaldulensis can retain trace elements such as zinc (Zn), copper (Cu), arsenic (As), magnesium (Mg), calcium (Ca), sulfur (S), iron (Fe), aluminum (Al), boron (B) [11, 19]. However, through conventional extractions for traditional treatments it has not been reported that dangerous quantities are extracted [20].

    Ellagitannins in E. camaldulensis

    In E. camaldulensis there are three main classes of bioactive compounds among are ellagitannins, flavonoids, and terpenes [17]. Flavonoids have been reported as one of the main compounds in E. camaldulensis [21], possessing antiviral, antioxidant, antibacterial and anticancer properties, as well as providing flavor to flowers, fruits, and seeds in plants [22]. Also, E. camaldulensis have terpenes and terpenoids [23] commonly present in EOs, which possess antimicrobial, antioxidant, anti-allergic and anticancer activities [24]. Apart from that, ellagitannins have only been found in parts such as leaves [17, 25, 26] in bark and wood [27, 28] as well as in seeds [29] but there have not been many recent reports where ellagitannins are present in E. camaldulensis. EOs have been recovered from bark, buds, flowers, fruits, leaves, husks, or roots, however, the yield of these is low and the use of solvents such as petroleum ether, ether, and hexane among others is necessary [24], unlike oils, ellagitannins can be recovered with ethanol, methanol, and aqueous mixtures. In addition, the bioactivity of ellagitannins has shown great variety due to their structure. Ellagitannins are an important group of phytochemicals, these compounds belong to the hydrolyzable tannins that have a high bioactivity value. Ellagitannins represent the defense in fruits and nuts, and they are phytochemicals with antioxidant powder, anticancer, and anti-atherosclerotic properties. Ellagitannins are hydrolyzable tannins with abased HHDP esterified to a polyol core. They can be found in plants as secondary metabolites, where one of their main roles is defense, and are found in flowers, leaves, stalks, peels, and fruits. They are localized in the cytoplasm and cell vacuoles [30, 31], and among fruits that can contain ellagitannins are the berries, contributing to the health of the fruit itself due to the antioxidant properties of these compounds [32].

    The use of different solvents varies in the type of compounds extracted as well as the amount, which makes the difference in obtaining these [33]. Solvents with water allow the extraction of different compounds like ellagitannins [34]. Been reported some ellagitannins in extracts from E. camaldulensis with acetone: water, highlighting HHDP-glucopyranose, as well as galloyl-HHDP-glucopyranose positional isomers, pedunculagin, tellimagrandin I, and ellagitannins dimers. Furthermore, other compounds are found in aqueous fractions such as HHDP-glucopyranose, and galloyl-HHDP-glucopyranose [17].

    Acetone and ethanol have played an important role in the extraction of different compounds from E. camaldulensis that has allowed to recovery of these solvents. Has been reported to extract HHDP, which is an intermediary molecule in obtaining ellagic acid [35]. On the other hand, methanol has presented a role in the recovery of ellagitannins. Methanol allowed the recovery of ellagitannins, mainly pedunculagin isomers, ellagitannin dimer, sanguine H10 like ellagitannin dimer, tellimagrandin I, galloyl-bis-HHDP-glucopyranose isomer, and in fractions with methanol to 100% can be found dimers from ellagitannins in greater quantity as sanguiin H10-like ellagitannin dimer too, in addition to galloyl-HHDP-glucopyranose, vescalagin, galloyl-HHDP-glucopyranose, castalagin, digalloylglucopyranose, valoneoyl-HHDP-glucopyranose, pterocarinin A, valoneic acid dilactone, galloyl cypellocarpin B, quercetin pentoside, and ellagic acid derivative [17].

    These compounds possess antibacterial, antifungal, antidiabetic, and antioxidant activity, antimutagenic, and antiproliferative activities [32]. Among all the compounds of E. camaldulensis leaves, ellagitannins such as telimagrandin I, pedunculagin, vescalagin and castalagin stand out for their structure [17, 27] (see Figure 2). However, there are not many reports mentioning the presence of ellagitannins in the plant.

    Chemical structures of tellimagrandin I, pedunculagin, and vescalagin/castalagin

    Other species of E. globulus have reported the presence of ellagitannins such as pedunculaginm tellimagrandin I and II, hexahydroxydiphenoyl-β-D-glucose, as ellagic acid in leaves [36, 37] and wood [28]. nitens ellagic acid, HHDP-glucose, pedunculagin, tellimagrandin I and II, HHDP-digalloylglucose, casuarinin, casuarictin, Di-HHDP-galloylglucose, HHDP-trigalloylglucose in wood [38] as well as in E. citriodora, pedunculagin, vescalagin/castalagin, acustissimin A, pterocarinin A, tellimagrandin I, and casuarininin have also been found [39], however, there are reports in the literature on other Eucalyptus species.

    E. camaldulensis and foodborne pathogens

    Foodborne pathogens are disease-causing pathogens that come from contaminated food somewhere in the food chain [40]. These microorganisms are the cause of various diseases that not only affect health but also the economy of the people [41]. Foodborne pathogens have caused a cost in the treatment of foodborne illnesses of around $55.5 billion annually in the United States and are dangerous because of the population that is more susceptible to them, such as the elderly, immunocompromised people, infants, and pregnant women [42]. However, even with technology applied to food safety, the foodborne illness still represents a public health problem [43].

    Among the most common microorganisms that cause foodborne illness are: Staphylococcus aureus, Shigella spp., Salmonella spp., Yersinia enterocolitica, Escherichia coli, Listeria monocytogenes, Vibrio spp., Cronobacter sakazakii, Bacillus cereus, Campylobacter jejuni, Clostridium botulinum, Clostridium perfringens, not to mention viruses and parasites such as viruses as hepatitis A and noroviruses as well as the parasites Toxoplasma gondii, Cyclospora cayetanensis, and Trichinella spiralis [41]. Besides, some of these microorganisms cause the deterioration of food in physical appearance, aroma, nutritional value and not only diseases [42].

    Pathogenic microorganisms are a problem of great relevance and seriousness for health today, due to the resistance that these microorganisms have developed [44]. These microorganisms contaminate numerous food products, such as fruits, vegetables, water, seafood, cereals, and meat, dairy products, and during food processing the equipment and the human operator can be used to process food [42].

    The use of antimicrobial agents prevents the proliferation of microorganisms that cause food spoilage [11]. Some of secondary metabolites produced by various natural sources such as plants have antimicrobial potential against pathogenic microorganisms and can inhibit virulence factors [1]. These compounds with antibacterial properties have been used in food processing, acting as preservatives and preventing the deterioration of food products both in food pathogenic and non-pathogenic microorganisms [19], and have also been used antioxidant, and antitumor activities [44].

    It has been reported that medicinal plant extracts such as Eucalyptus have shown activity against microorganisms, including B. cereus, Alicyclobacillus acidoterrestris, Enterococcus faecalis, and E. coli, Propionibacterium acnes, S. aureus, and methicillin-resistant S. aureus (MRSA), Trichophyton mentagrophytes [5].

    Crude extracts of E. camaldulensis leaves have been reported to contain phenolic compounds with antimicrobial properties effective against L. monocytogenes, S. aureus, and B. cereus [11]. In addition, minimum inhibitory concentrations (MIC) of ethanol fraction have been reported between 16–64 µg/mL. As well as MIC of 158–316 µg/mL and minimum bactericidal concentrations (MBC) of 316–2,528 µg/mL of aqueous fraction of E. camaldulensis [11]. Also, Eucalyptus EOs have been tested on E. coli and S. aureus. Other reports have shown that EOs of E. camaldulensis have demonstrated inhibition on other microorganisms including S. aureus, E. coli, Salmonella enteritidis, Bacillus subtilis, and Enterococcus faecalis [16] (see Table 2).

    E. camaldulensis inhibition of bacterial growth

    MicroorganismMIC concentrationType of extractPart of the plantReference
    B. cereus16 µg/mLEthanolLeaves[11]
    158 µg/mLAqueousLeaves[11]
    31.36 µg/mLEOLeaves[16]
    L.monocytogenes32–64 µg/mLEthanolLeaves[11]
    316 µg/mLAqueousLeaves[11]
    S. aureus32 µg/mLEthanolLeaves[11]
    158 µg/mLAqueousLeaves[11]
    100 µl/mLEOLeaves[45]
    33.2 µg/mLEOleaves[16]
    E. coli100 µl/mLEOLeaves[45]
    85 µg/mLEOLeaves[16]
    Salmonella enteritis51.36 µg/mLEOLeaves[16]
    Enterococcus faecalis30.0 µg/mLEOLeaves[16]
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    On the other hand, Eucalyptus oil has shown antimicrobial activity, which has been mainly attributed to several compounds, among which terpenes such as 1,8-cineole, α-pinene, β-pinene, and limonene stand out [5]. E. camaldulensis oil has shown bioactivity on gram-positive bacteria that are more sensitive compared to gram-negative bacteria. This activity increased with increasing EO; however, at lower concentrations of 0.5 g/kg no activity was observed, and for gram-positive bacteria (S. aureus and Streptococcus). E. camaldulensis leaf EO showed activity at 1.0 g/kg and 5.0 g/kg, while for gram-negative bacteria such as S. enteritidis, Klebsiella pneumonia, Pseudomonas aeruginosa, and E. coli it was 1 g/kg and 15 g/kg, respectively. In addition, the MBC against S. aureus, Streptococcus aureus, and E. coli was shown to be 5 g/kg, 10 g/kg, and 25 g/kg, respectively [5] as can be seen in Table 2.

    Ellagitannins from E. camaldulensis and their potential in foodstuffs

    Tellimagrandin I

    One of the ellagitannin found in E. camaldulensis is tellimagrandin I that abound mainly in the young leaves in April and these after are replaced for casuarinin in July, that later change to pedunculagin. These compounds are the principal tannins that are found in the leaves from summer to fall [46]. Tellimagrandin is made up of a molecule of HHDP and a D-glucopyranosyl with two galloyl units and this molecule has been widely used against bacterial and viral infections [47].

    Effect of tellimagrandin I on pathogenic bacteria

    Tellimagrandin I has been effective in the inhibition of S. aureus and E. coli [48, 49]. It has been reported that tellimagrandin I isolated from the rose extract was effective in reducing the MIC of oxacillin against methicillin-resistant S. aureus, acting together with tellimagrandin I and oxacillin. Reducing the MIC of oxacillin from 128 µg/mL to 1 µg/mL, when 50 µg/mL of tellimagrandin I was added to the medium [50]. On the other hand, tellimagrandin I also contributed to the reduction of the MIC of tetracycline in the MRSA strains OM481, OM505, OM504, and OM506. In addition, the MIC of other antibiotics such as benzylpenicillin and ampicillin was reduced with the addition of tellimagrandin I to MRSA [50].

    S. aureus is one of the ten main microorganisms causing a food illness produced by bacteria and safety indicators. The foods most susceptible to contamination by S. aureus are all those that have had contact with animal skin, among which dairy meat and sausage products stand out [51, 52].

    Also, the effect of isolated tellimagrandin I monomers was favorable against 32 strains of Helicobacter pylori. However, on E. coli only a MIC greater than 100 µg/mL could be obtained. In addition, the bactericidal effect of tellimagrandin I could be demonstrated according to time and dose against H. pylori in vitro showing that the effect is faster with 50 µg/mL [53]. Several extracts rich in tellimagrandin I extracts, and the pure compound isolated from E. globulus, has to be effective on bacteria such as S. aureus [54]. Its antimicrobial potential has also been proven by Boulekbache-Makhlouf et al. [55], who reported that extracts of E. globulus rich in tellimagrandin I inhibit S. aureus and B. subtilis.

    It has been reported that tellimagrandin I on MRSA acts on penicillin-binding protein 2a (PBP2a) decreasing its production and inactivating it [56]. PBP is a protein enables resistance to β-lactam antibiotic drugs in MRSA, PBP2a is encoded by the mecA gene found in MRSA strains, which gives resistance to beta-lactam antibiotics due to its low affinity for them, and PBP2a provides transpeptidase activity to allow cell wall synthesis at concentrations that inhibit the sensitive PBPs normally produced by S. aureus [57]. Likewise, in E. coli, the characteristics of the free galloyl groups of the ellagitannins increase the hydrophobicity of the structure, promoting their interaction with bacterial lipid membranes [58], through inactivation of essential surface proteins, interaction with membrane lipids and causing membrane phase separation [59].

    Pedunculagin

    Among the important ellagitannins found in leaves of E. camaldulensis is pedunculagin [60]. Pedunculagin is a phenolic compound belonging to group of the ellagitannins which exhibit various antioxidant, anti-inflammatory, antitumor, gastroprotective, and hepaprotective activities [61].

    Effect of pedunculagin on pathogenic bacteria

    In phenolic compounds, antibacterial activity is one of the most sought-after due to its great capacity to inhibit pathogenic bacteria and the bactericidal effect that some of them have [62]. In antibacterial activity, pedunculagin has shown an anti-hemolytic effect on S. aureus [63] as well as in fractions of pedunculagin-rich extracts [64, 65], which is a bacterium commonly found in some foods causing food poisoning, being the main cause of food poisoning worldwide [51]. Anti-hemolytic effect is important due to the hemolysis produced by the alpha toxin of S. aureus. This hemolytic toxin causes the rupture of the red blood cell membrane. The α-hemolysin binds to the cell surface and facilitates the transport of molecules such as potassium ion (K+) and Ca2+ ions, which causes necrotic death of the host cell [66], On the other hand, fractions obtained from Clidemia hirta, rich in pedunculagin have been effective to inhibit E. coli at concentrations greater than 100 μg/mL [64], as well as extracts of Geum rivale L. rich in pedunculagin were able to inhibit E. coli and L. monocytogenes at lower concentrations [65].

    The individual activity of ellagitannins has not been extensively studied, but some of the mechanisms on which they act are the ability to interact with the cell wall and nucleic acids [67], however it has been proven that pedunculagin decreases the ability of S. aureus to cause hemolysis, as well as some phenolic groups cause enzymatic inactivity due to their hydroxyl groups, as well as affect the cell membrane by forming complexes with proteins and polysaccharides [63].

    Effect of vescalagin and castalagin on pathogenic bacteria

    It has been proven that ellagitannins such as vescalagin/castalagin isolate have bactericidal capacity on one of the main food pathogenic bacteria which is S. aureus [44].

    In addition, extracts rich in vescalagin and castalagin have also shown antibacterial activity on several foodborne pathogens [68]. Extracts of Myrciaria cauliflora seeds with high values of vescalagin and castalagin (1,999 mg/100 g ± 24 mg/100 g and 1,872 mg/100 g ± 18 mg/100 g respectively) have shown inhibition against microorganisms such as L. monocytogenes, Salmonella typhimurium, S. Enteritidis, B. cereus, E. coli, S. aureus [69]. Myrciaria dubia extract has also reported activity against S. typhimurium, E. coli, B. cereus, S. aureus, and L. monocytogenes [70].

    Fujita et al. [71] have also reported inhibition of Myrciaria dubia McVaugh rich in vescalagin and castalagin too, possess antibacterial activity on S. aureus at concentrations ranging 0.08–0.63 mg/ml. It has been demonstrated that vescalagin and castalagin have been able to inhibit microorganisms with extracts rich in these ellagitannins, as in the case of Lythrum salicaria L. acting on E. coli, B. cereus, B. subtilis, Staphylococcus epidermidis, S. aureus, S. enteritidis, S. typhimurium [72]. In addition, other microorganisms have been inhibited by vescalagin and castalagin, such as methicillin-resistant S. epidermidis, methicillin-resistant S. aureus, Pseudomonas aeruginosa, breaking and inhibiting the films by modulating the assembly of peptidoglycans on the bacterial surface, breaking the cell wall and bacterial death [44]. The inhibition concentrations of tellimagrandin I, pedunculagin, castalagin and vescalagin on food pathogenic bacteria are shown in Table 3.

    Antibacterial activity of tellimagrandin I, pedunculagin, and vescalagin/castalagin

    MicroorganismEllagitanninsInhibition of microorganisms at MICReference
    E. coliTellimagrandin I50 µg/mL[53]
    500 ppm[54]
    Pedunculagin> 100 μg/mL[64]
    15.6 μg/mL[65]
    Vescalagin/Castalagin9.04 mm ± 0.65 mm[69]
    6.74 mm ± 0.80 mm[70]
    2.5 mg/mL[72]
    S. aureusTellimagrandin I50 µg/mL[50]
    1,000 ppm[54]
    Pedunculagin< 100 ug/mL[64]
    15.6 μg/mL[65]
    Vescalagin/Castalagin9.47 mm ± 1.86 mm[69]
    9.70 mm ± 1.92 mm[70]
    0.08–0.63 mg/mL[71]
    0.625 mg/mL[72]
    H. pyloriTellimagrandin I12.5 µg/mL[54]
    L. monocytogenesPedunculagin62.5 μg/mL[65]
    Vescalagin/Castalagin8.87 mm ± 0.49 mm[69]
    8.58 mm ± 0.82 mm[70]
    B. cereusVescalagin/Castalagin8.07 mm ± 0.96 mm[69]
    9.04 mm ± 1.36 mm[70]
    2.5 mg/mL[72]
    Display full size

    The antibacterial activity of castalagin and vescalagin have also been shown to interact with PBP2a in MRSA, rendering the bacteria susceptible to lysis and its inhibition [46]. In addition, extracts with castalagin act on H. pylori, preventing adhesion to the gastric mucosa, as well as allowing the disintegration of the membrane of salmonella and B. subtilis [73].

    Antioxidant activity

    Antioxidant effect of tellimagrandin I

    Tellimagrandin has been found in different extracts as Cornus mas L. These extracts have had antioxidant activity at 2,2-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid) (ABTS), ferric reducing antioxidant power assay (FRAP), and 2,2-diphenyl-1-picrylhydrazyl (DPPH) with a range of 255.9 mmol/100 g ± 8.48 mmol/100 g, 210.62 mmol/100 g ± 5.45 mmol/100 g, 191.00 mmol/100 g ± 0.04 mmol of Trolox (Tx)/100 g respectively [74]. In an essay on the antioxidant capacity of some ellagitannins performed by Moilanen et al. [75] with tellimagrandin showed radical scavenging antioxidant properties at concentrations of 3 mmol/L and 5 mmol/L, however, at fewer concentrations they exhibited prooxidant activity enhancing the degradation of 2-deoxyribose used in the assay.

    Within the Eucalyptus genus, it has been mentioned that they are high in ellagitannins among they are tellimagrandin I, with high antioxidant potential, as is E. globulus with extracts, where the presence of ellagitannins is higher and gives it activity [76]. Furthermore, in extracts of Plinia cauliflora, showed a DPPH inhibitory concentration (IC50) of 1.45 µg/mL ± 0.02 µg/mL, as well as a peroxidation inhibition greater than 70% [77].

    Antioxidant effect of pedunculagin

    Due to its antioxidant potential, pedunculagin has been one of the ellagitannins of great interest. Extracts from natural sources such as walnuts have been identified with the presence of pedunculagin, obtaining antioxidant potential by inhibiting lipid peroxidation in mice, as well as the ferric reducing antioxidant power [78]. However, the antioxidant capacity of Eucalyptus isolates has also provided antioxidant activity on DPPH and ABTS [79]. Other extracts, including Geum rivale L. extract with the presence of pedunculagin, have shown antioxidant potential with great inhibition against DPPH (about 90%) and ABTS [65].

    Due to the number of compounds found in crude plant extracts or residues, chromatography is usually performed to allow the recovery of fractions with more specific compounds in each one. Oliveira et al. [80] in 3 feijoa fractions with the presence of pedunculagin reported antioxidant potential on ABTS.

    In addition, pedunculagin from Quercus mongolica in vitro has been evaluated for inhibition of inflammatory cytokines [interleukin-6 (IL-6) and IL-8], as well as 5α-reductase inhibitory activity by western blotting, being pedunculagin were able to inhibit nitric oxide production, as well as decrease IL-6 and IL-8, and exhibited potent 5α-reductase type 1 inhibitory activity [81].

    Antioxidant potential of vescalagin/castalagin

    Interestingly, in antioxidant and prooxidant assays, castalagin/vescalagin has exhibited the opposite of antioxidant for 2-deoxyribose used in the assay, obtaining prooxidant results at concentrations from 1–5 mmol/L [75]. Other reports on isolated vescalagin have reported around 5 mg/L for DPPH inhibition, however, from the same extract castalagin contained slightly low values compared to that of castalagin [44]. Fidelis et al. [70] in extracts of Myrciaria dubia have reported DPPH inhibition. Myrciaria dubia, among its main components, is mainly pedunculagin. Also, within the same genus Myrciaria cauliflora containing pedunculagin presented DPPH inhibition at higher values, as well as lipid peroxidation values, as well as lipid peroxidation values slightly greater than 80% inhibition [69]. Other important extracts of Jabuticaba extracts rich in vescalagin and castalagin vescalagin and castalagin showed a DPPH inhibition capacity of about 33.643 mmol ± 3.129 mmol of Tx/100 g fruit [82] (see Table 4).

    Antioxidant activity of tellimagrandin I, pedunculagin, and vescalagin/castalagin

    CompoundABTSFRAPDPPHLipoperoxidationReference
    Tellimagrandin I---51.34% ± 0.72%[76]
    Tellimagrandin I255.9 mmol/100 g ± 8.48 mmol/100 g210.62 mmol/100 g ± 5.45 mmol/100 g191.00 mmol ± 0.04 mmol of Tx/100 g-[74]
    Tellimagradin I--1.45 µg/mL ± 0.02 µg/mL71.47% ± 5.64%[77]
    Tellimagrandin I54.5 μmol/L ± 0.6 μmol/L-73.5 μmol/L ± 2.5 μmol/L-[79]
    Tellimagrandin I73.6 μmol/L ± 3.2 μmol/L-65.8 μmol/L ± 1.2 μmol/L-[79]
    Pedunculagin83.69% ± 4.28% inhibition 0.111 mg/mL-0.139 mg/mL-[83]
    Tellimagrandin I0.03 μmol/L ± 0.02 µmol/L Tx equivalent/µg-94.65% ± 0.29%-[65]
    Pedunculagin10.8 μg/mL ± 0.7 μg/mL---[80]
    Vescalagin--5 mg/mL-[44]
    Castalagin--4 mg/mL-[44]
    Vescalagin/Castalagin--4,455 mg ± 15 mg AAE/100 g86% ± 1%[70]
    Vescalagin/Castalagin--33.643 mmol ± 3.129 mmol of Tx/100 g-[82]
    Pedunculagin--1.55 µmol ± 0.12 µmol of Tx equivalent/µmol-[37]
    Tellimagrandin I--1.33 µmol ± 0.03 µmol of Tx equivalent/µmol-[37]
    Display full size

    AAE: ascorbic acid equivalent; -: not involving

    Future trends

    It is important to take into account that in plants of the Eucalyptus genus the use is oriented towards the use of EOs and compounds of these, but making use of extracts rich in ellagitannins allows them to be applied in various matrices, from supplements to functional foods for preservation or functional foods, in addition to the fact that they have provided coloration. Many of the extracts of phenolic compounds from natural sources have been mostly oriented to the pharmaceutical and cosmetic industry [84, 85]. There are several studies on the use of ellagitannins in the cosmetic industry [86, 87], showing their possible use in the pharmaceutical industry against cell oxidation, as well as in products aimed at cellular rejuvenation. Others have highlighted the potential use of ellagitannins in the pharmaceutical, food, and nutraceutical industries [36, 88] either for its prebiotic potential [89], as is pedunculagin from walnuts [90], and for the treatment of gastric ulcers, wounds, and ulceration [39].

    However, the use of phenolic compounds such as hydrolyzable tannins, especially ellagitannins for the food industry, may be an option to solve problems such as lipid oxidation [91]. Pomegranate extracts with a high presence of ellagitannins have been investigated for the inhibition of lipid oxidation in sausage, where the peroxide value was decreased by the effect of pomegranate extract [92].

    Well as for the conservation against pathogenic microorganisms in food, since several studies have shown the inhibition of microorganisms in food, extracts themselves as Mantzourani et al. [93] with extracts from Vaccinium macrocarpon and Punica granatum L., applied on pork meat to inhibit Enterobacteriaceae, total mesophilic bacteria, yeasts/molds, Staphylococcus spp., Pseudomonas spp. and lactic acid bacteria and EOs for chicken meat preservation [91, 94]. As in the case of pomegranate extract films with the presence of ellagitannins including pedunculagin, for the inhibition of microorganisms such as L. monocytogenes and E. coli [95]. On the other hand, extracts with ellagitannins have been shown to improve the antioxidant and meat quality of broiler meat by supplementing it, which helped to improve the intestinal bacterial population in the chicken [83]. In addition, the use of ellagitannins is possible in the formation of materials with antibacterial potential, such as the case of vescalagin/castalagin that can be loaded into alginate hydrogels to generate antibacterial biomaterials [44]. This is a step in the development of products in the food area that can aid in the inhibition of oxidation, as well as the use of antibacterial agents for the inhibition of food pathogens.

    Conclusions

    E. camaldulensis is a plant commonly used in industries such as wood, paper, and oil production. However, the residues of its leaves and small branches are often left unused, presenting an opportunity for utilization. This review focuses on the potential of E. camaldulensis residues particularly the phenolic compounds they contain, including hydrolyzable tannins such ellagitannins. Ellagitannins are known for their antioxidant and antimicrobial proprieties, making them valuable for various applications, specifically in the food industry for inhibiting lipid oxidation in oils and meat products. It is worth noting that there is a limited number of studies that specifically isolate ellagitannins, with most research focusing on their presence in extracts. This lack of isolated compound studies makes it challenging to gather comprehensive information about ellagitannins. Therefore, this review aims to contribute essential knowledge about these compounds and their potential uses.

    Abbreviations

    ABTS:

    2,2-azino-bis (3-ethylbenzothiazoline-6-sulfonic acid)

    DPPH:

    2,2-diphenyl-1-picrylhydrazyl

    EOs:

    essential oils

    HHDP:

    hexahydroxy diphenic acid

    IL-6:

    interleukin-6

    MIC:

    minimum inhibitory concentrations

    MRSA:

    methicillin-resistant Staphylococcus aureus

    PBP2a:

    penicillin-binding protein 2a

    Tx:

    Trolox

    Declarations

    Author contributions

    ESL: Conceptualization, Visualization, Investigation, Writing—review & editing. LS: Validation, Resources, Writing—review & editing. JEWP: Validation, Supervision, Writing—review & editing. LPL: Validation, Writing—review & editing. RRH and CNA: Validation, Supervision, Writing—review & editing. JAAV: Conceptualization, Resources, Validation, Visualization, Writing—review & editing.

    Conflicts of interest

    The authors declare that they have no conflicts of interest.

    Ethical approval

    Not applicable.

    Consent to participate

    Not applicable.

    Consent to publication

    Not applicable.

    Availability of data and materials

    Not applicable.

    Funding

    Not applicable.

    Copyright

    © The Author(s) 2024.

    References

    Mickymaray S. Efficacy and mechanism of traditional medicinal plants and bioactive compounds against clinically important pathogens. Antibiotics. 2019;8:257. [DOI] [PubMed] [PMC]
    Knezevic P, Aleksic V, Simin N, Svircev E, Petrovic A, Mimica-Dukic N. Antimicrobial activity of Eucalyptus camaldulensis essential oils and their interactions with conventional antimicrobial agents against multi-drug resistant Acinetobacter baumannii. J Ethnopharmacol. 2016;178:12536. [DOI] [PubMed]
    Kayani S, Ahmad M, Zafar M, Sultana S, Khan MPZ, Ashraf MA, et al. Ethnobotanical uses of medicinal plants for respiratory disorders among the inhabitants of Gallies-Abbottabad, Northern Pakistan. J Ethnopharmacol. 2014;156:4760. [DOI] [PubMed]
    Zurita M, Posligua A, Mora M, Carranza L, Bacusoy M. Plantas medicinales, su uso en afecciones respiratorias en comunidades rurales, provincia Los Ríos-Ecuador. J Sci Res. 2021;6:5772. Spanish.
    Dhakad AK, Pandey VV, Beg S, Rawat JM, Singh A. Biological, medicinal and toxicological significance of Eucalyptus leaf essential oil: a review. J Sci Food Agri. 2018;98:83348. [DOI] [PubMed]
    Labate CA, de Assis TF, Oda S, de Mello EJ, Mori ES, de Moraes MLT, et al. Eucalyptus. In: Kole K, Hall TC, editors. Compendium of transgenic crop plants. Blackwell Publishing Ltd; 2008. pp. 35–108
    Lee MH. Chemical profile, antimicrobial and anti-oxidative activity of commercial eucalyptus and lavender essential oils and their applicability in cosmetics. Indian J Sci Technol. 2016;9:100181106. [DOI]
    Sharmeen JB, Mahomoodally FM, Zengin G, Maggi F. Essential oils as natural sources of fragrance compounds for cosmetics and cosmeceuticals. Molecules. 2021;26:666. [DOI] [PubMed] [PMC]
    Becker LC, Akinsulie A, Bergfeld WF, Belsito DV, Hill RA, Klaassen CD, et al. Safety assessment of Eucalyptus globulus (Eucalyptus)-derived ingredients as used in cosmetics. Int J Toxicol. 2023;42:57S92S. [DOI]
    Tolba H, Moghrani H, Benelmouffok A, Kellou D, Maachi R. Essential oil of Algerian Eucalyptus citriodora: chemical composition, antifungal activity. J Mycol Med. 2015;25:e12833. [DOI] [PubMed]
    Nwabor OF, Singh S, Syukri DM, Voravuthikunchai SP. Bioactive fractions of Eucalyptus camaldulensis inhibit important foodborne pathogens, reduce listeriolysin O-induced haemolysis, and ameliorate hydrogen peroxide-induced oxidative stress on human embryonic colon cells. Food Chem. 2021;344:128571. [DOI] [PubMed]
    Huang Q, Liu X, Zhao G, Hu T, Wang Y. Potential and challenges of tannins as an alternative to in-feed antibiotics for farm animal production. Anim Nutr. 2018;4:13750. [DOI] [PubMed] [PMC]
    Panamito MF, Bec N, Valdivieso V, Salinas M, Calva J, Ramírez J, et al. Chemical composition and anticholinesterase activity of the essential oil of leaves and flowers from the ecuadorian plant Lepechinia paniculata (Kunth) epling. Molecules. 2021;26:3198. [DOI] [PubMed] [PMC]
    Aleksic Sabo V, Knezevic P. Antimicrobial activity of Eucalyptus camaldulensis Dehn. plant extracts and essential oils: a review. Ind Crops Prod. 2019;132:41329. [DOI] [PubMed] [PMC]
    Al-Snafi PDAE. The pharmacological and therapeutic importance of Eucalyptus species grown in Iraq. IOSR J Pharm. 2017;7:7291. [DOI]
    Yáñez Rueda X, Cuadro Mogollón OF. Composición química y actividad antibacteriana del aceite esencial de las especies Eucalyptus globulus y E. camaldulensis de tres zonas de Pamplona (Colombia). Bioagro. 2012;10:5261. Spanish.
    Singa A, Ayoub N, Al-Sayed E, Martiskainen O, Sinkkonen J, Pihlaja K. Phenolic constituents of Eucalyptus camaldulensis Dehnh, with potential antioxidant and cytotoxic activities. Rec Nat Prod. 2011;5:27180.
    González-González GM, Palomo-Ligas L, Nery-Flores SD, Ascacio-Valdés JA, Sáenz-Galindo A, Flores-Gallegos AC, et al. Coffee pulp as a source for polyphenols extraction using ultrasound, microwave, and green solvents. Environ Qual Manag. 2022;32:45161. [DOI]
    Doganlar ZB, Doganlar O, Erdogan S, Onal Y. Heavy metal pollution and physiological changes in the leaves of some shrub, palm and tree species in urban areas of Adana, Turkey. Chem Speciat Bioavailab. 2012;24:6578. [DOI]
    Kanda A, Ncube F, Goronga TK. Trace elements in leaf extracts of Eucalyptus grandis traditionally used to treat common cold and flu. J Heal Pollut. 2019;9:191214. [DOI] [PubMed] [PMC]
    Aljawdah HMA, Abdel-Gaber R, Al-Shaebi EM, Thagfan FA, Al-Quraishy S, Qasem MAA, et al. Hepatoprotective activity of Eucalyptus camaldulensis extract in murine malaria mediated by suppression of oxidative and inflammatory processes. Front Cell Infect Microbiol. 2022;12:955042. [DOI] [PubMed] [PMC]
    Roy A, Khan A, Ahmad I, Alghamdi S, Rajab BS, Babalghith AO, et al. Flavonoids a bioactive compound from medicinal plants and its therapeutic applications. Biomed Res Int. 2022;2022:5445291. [DOI] [PubMed] [PMC]
    Abbas A, Anwar F, Alqahtani SM, Ahmad N, Al-Mijalli SH, Shahid M, et al. Hydro-distilled and supercritical fluid extraction of Eucalyptus camaldulensis essential oil: characterization of bioactives along with antioxidant, antimicrobial and antibiofilm activities. Dose-Response. 2022;20:15593258221125477. [DOI] [PubMed] [PMC]
    Masyita A, Mustika Sari R, Dwi Astuti A, Yasir B, Rahma Rumata N, Emran TB, et al. Terpenes and terpenoids as main bioactive compounds of essential oils, their roles in human health and potential application as natural food preservatives. Food Chem X. 2022;13:100217. [DOI] [PubMed] [PMC]
    Conde E, Cadahía E, García-Vallejo MC. Low molecular weight polyphenols in leaves of Eucalyptus camaldulensis, E. globulusandE. rudis. Phytochem Anal. 1997;8:18693. [DOI]
    Cadahía E, Conde E, García-vallejo MC, Fernández de Simón B. High pressure liquid chromatographic analysis of polyphenols in leaves of Eucalyptus camaldulensis, E. globulus and E. rudis:  proanthocyanidins, ellagitannins and flavonol glycosides. Phytochem Anal. 1997;8:7883. [DOI]
    Radwan RA, El-sherif YA, Salama MM. A novel biochemical study of anti-ageing potential of Eucalyptus Camaldulensis bark waste standardized extract and silver nanoparticles. Colloids Surfaces B Biointerfaces. 2020;191:111004. [DOI] [PubMed]
    Conde E, Wood E. Polyphenolic composition of wood extracts from Eucalyptus camaldulensis, E. globulus and E. rudis. Holzforschung. 1995;49:4117. [DOI]
    Banks JCG, Hillis WE. The characterization of populations of Eucalyptus camaldulensis by chemical features. Aust. J. Bot. 1963;17:13346. [DOI]
    Buenrostro-Figueroa J, Ascacio-Valdés A, Sepúlveda L, Prado-Barragán A, Aguilar-González MÁ, Aguilar CN. Ellagic acid production by solid-state fermentation influenced by the inert solid supports. Emirates J Food Agric. 2018;30:7507. [DOI]
    Márquez A, Chavéz C, González J. Aspectos generales sobre los elagitaninos y su conversión a ácido elágico. Ciencia Nicolaita. 2019:3658. Spanish.
    Enomoto H. Unique distribution of ellagitannins in ripe strawberry fruit revealed by mass spectrometry imaging. Curr Res Food Sci. 2021;4:8218. [DOI] [PubMed] [PMC]
    Nandasiri R, Eskin NAM, Thiyam-Höllander U. Antioxidative polyphenols of canola meal extracted by high pressure: impact of temperature and solvents. J Food Sci. 2019;84:311728. [DOI] [PubMed]
    El Achkar T, Fourmentin S, Greige-Gerges H. Deep eutectic solvents: an overview on their interactions with water and biochemical compounds. J Mol Liq. 2019;288:15:111028. [DOI]
    Hernandez-Trejo A, Rodríguez-Herrera R, Sáenz-Galindo A, López-Badillo CM, Flores-Gallegos AC, Ascacio-Valdez JA, et al. Insecticidal capacity of polyphenolic seed compounds from neem (Azadirachta indica) on Spodoptera frugiperda (J. E. Smith) larvae. J Environ Sci Health Bi. 2021;56:102330. [DOI] [PubMed]
    Sugimoto K, Nakagawa K, Hayashi S, Amakura Y, Yoshimura M, Yoshida T, et al. Hydrolyzable tannins as antioxidants in the leaf extract of eucalyptus globulus possessing tyrosinase and hyaluronidase inhibitory activities. Food Sci Technol Res. 2009;15:3316. [DOI]
    Santos SC, Fortes, Gilmara ACF, Camargo LTFM, Camargo AJ, Ferri PH. Antioxidant effects of polyphenolic compounds and structure-activity relationship predicted by multivariate regression tree. LWT. 2020;137:110366. [DOI]
    Barry KM, Davies NW, Mohammed CL. Identification of hydrolysable tannins in the reaction zone of Eucalyptus nitens wood by high performance liquid chromatography–electrospray ionisation mass spectrometry. Phytochem Anal. 2001;12:1207. [DOI] [PubMed]
    Al-Sayed E, Michel HE, Khattab MA, El-Shazly M, Singab AN. Protective role of casuarinin from melaleuca leucadendra against ethanol-induced gastric ulcer in rats. Planta Med. 2020;86:3244. [DOI] [PubMed]
    Zhang Y, Zhu L, Zhang Y, He P, Wang Q. Simultaneous detection of three foodborne pathogenic bacteria in food samples by microchip capillary electrophoresis in combination with polymerase chain reaction. J Chromatogr A. 2018;1555:1005. [DOI] [PubMed]
    Bintsis T. Foodborne pathogens. AIMS Microbiol. 2017;3:52963. [DOI]
    Gourama H. Foodborne pathogens. In: Barbosa-Cánovas GV, editor. Food engineering series. New York: Springer; 2020. pp. 25–49.
    Adebowale OO, Kassim IO. Food safety and health: a survey of rural and urban household consumer practices, knowledge to food safety and food related illnesses in Ogun state. Epidemiol Biostat Public Heal. 2017;14:e12568. [DOI]
    Araújo AR, Araújo AC, Reis RL, Pires RA. Vescalagin and castalagin present bactericidal activity toward methicillin-resistant bacteria. ACS Biomater Sci Eng. 2021;7:102230. [DOI] [PubMed]
    Ghalem BR, Mohamed B. Antibacterial activity of leaf essential oils of Eucalyptus globulus and Eucalyptus camaldulensis. African J Pharm Pharmacol. 2008;2:2115.
    Quideau S. Chemistry and biology of ellagitannins. In: Quideau S, editor. An underestimated class of bioactive plant polyohenols. Hackensack: World Scientific; 2009. p. 396.
    Zheng S, Laraia L, O’Connor CJ, Sorrell D, Tan YS, Xu Z, et al. Synthesis and biological profiling of tellimagrandin I and analogues reveals that the medium ring can significantly modulate biological activity. Org Biomol Chem. 2012;10:25903. [DOI] [PubMed]
    Salih EYA, Julkunen-Tiitto R, Luukkanen O, Fahmi MKM, Fyhrquist P. Hydrolyzable tannins (ellagitannins), flavonoids, pentacyclic triterpenes and their glycosides in antimycobacterial extracts of the ethnopharmacologically selected Sudanese medicinal plant Combretum hartmannianum schweinf. Biomed Pharmacother. 2021;144:112264. [DOI] [PubMed]
    Puljula E, Walton G, Woodward MJ, Karonen M. Antimicrobial activities of ellagitannins against clostridiales perfringens, Escherichia coli, Lactobacillus plantarum and Staphylococcus aureus. Molecules. 2020;25:3714. [DOI] [PubMed] [PMC]
    Shiota S, Shimizu M, Mizusima T, Ito H, Hatano T, Yoshida T, et al. Restoration of effectiveness of β-lactams on methicillin-resistant Staphylococcus aureus by tellimagrandin I from rose red. FEMS Microbiol Lett. 2000;185:1358. [DOI] [PubMed]
    Grace D, Fetsch A. Staphylococcus aureus—a foodborne pathogen: epidemiology, detection, characterization, prevention, and control: an overview. In: Fetsch A, editor. Staphylococcus aureus. Elsevier Inc; 2018. pp. 3–10.
    Zendejas-Manzo GS, Avalos-Flores H, Soto-Padilla MY. Microbiología general de Staphylococcus aureus: generalidades, patogenicidad y métodos de identificación. Rev Biomed. 2014;25:12943.
    Funatogawa K, Hayashi S, Shimomura H, Yoshida T, Hatano T, Ito H, et al. Antibacterial activity of hydrolyzable tannins derived from medicinal plants against Helicobacter pylori. Microbiol Immunol. 2004;48:25161. [DOI] [PubMed]
    Hou AJ, Liu YZ, Yang H, Lin ZW, Sun HD. Hydrolyzable tannins and related polyphenols from Eucalyptus globulus. J Asian Nat Prod Res. 2000;2:20512. [DOI] [PubMed]
    Boulekbache-Makhlouf L, Slimani S, Madani K. Total phenolic content, antioxidant and antibacterial activities of fruits of Eucalyptus globulus cultivated in Algeria. Ind Crops Prod. 2013;41:859. [DOI]
    Shiota S, Shimizu M, Sugiyama J, Morita Y, Mizushima T, Tsuchiya T. Mechanisms of action of corilagin and tellimagrandin I that remarkably potentiate the activity of β-lactams against methicillin-resistant Staphylococcus aureus. Microbiol Immunol. 2004;48:6773. [DOI] [PubMed]
    Lim D, Strynadka NCJ. Structural basis for the β lactam resistance of PBP2a from methicillin-resistant Staphylococcus aureus. Nat Struct Biol. 2002;9:8706. [DOI] [PubMed]
    Virtanen V, Puljula E, Walton G, Woodward MJ, Karonen M. NMR metabolomics and DNA sequencing of Escherichia coli and Staphylococcus aureus cultures treated with hydrolyzable tannins. Metabolites. 2023;13:320. [DOI] [PubMed] [PMC]
    Álvarez-Martínez FJ, Barrajón-Catalán E, Encinar JA, Rodríguez-Díaz JC, Micol V. Antimicrobial capacity of plant polyphenols against gram-positive bacteria: a comprehensive review. Curr Med Chem. 2020;27:2576606. [DOI] [PubMed]
    Xiao SY, Wen BQ, Zhuang HY, Wang JL, Tang J, Chen HZ, et al. Extraction and antitumor activity of pedunculagin from eucalyptus leaves. International Conference on Biomedical Engineering and Biotechnology (iCBEB); 2012 May 28–30; Macau Macao. IEEE; 2012. pp. 280–2.
    Silva Fernandes A, Hollanda Véras J, Silva LS, Puga SC, Luiz Cardoso Bailão EF, de Oliveira MG, et al. Pedunculagin isolated from Plinia cauliflora seeds exhibits genotoxic, antigenotoxic and cytotoxic effects in bacteria and human lymphocytes. J Toxicol Environ Health A. 2022;85:35363. [DOI] [PubMed]
    Zhao M, Bai J, Bu X, Tang Y, Han W, Li D, et al. Microwave-assisted aqueous two-phase extraction of phenolic compounds from Ribes nigrum L. and its antibacterial effect on foodborne pathogens. Food Control. 2021;119:107449. [DOI]
    Al-Harbi R, Al-Wegaisi R, Moharram FA, Shaaban M, El-Rahman OA. Antibacterial and anti-hemolytic activity of tannins from Pimenta dioica against methicillin resistant Staphylococcus aureus. Bangladesh J Pharmacol. 2017;12:638. [DOI]
    Abdellaoui SE, Destandau E, Krolikiewicz-Renimel I, Cancellieri P, Toribio A, Jeronimo-Monteiro V, et al. Centrifugal partition chromatography for antibacterial bio-guided fractionation of Clidemia hirta roots. Sep Purif Technol. 2014;123:2218. [DOI]
    Orlova A, Kysil E, Tsvetkova E, Meshalkina D, Whaley A, Whaley AO, et al. Phytochemical characterization of water avens (Geum rivale L.) extracts: structure assignment and biological activity of the major phenolic constituents. Plants (Basel). 2022;11:2859. [DOI] [PubMed] [PMC]
    Zheng J, Shang Y, Wu Y, Wu J, Chen J, Wang Z, et al. Diclazuril inhibits biofilm formation and hemolysis of Staphylococcus aureus. ACS Infect Dis. 2021;7:1690701. [DOI] [PubMed]
    Sanhueza L, Melo R, Montero R, Maisey K, Mendoza L, Wilkens M. Synergistic interactions between phenolic compounds identified in grape pomace extract with antibiotics of different classes against Staphylococcus aureus and Escherichia coli. PLoS One. 2017;12:e0172273. [DOI] [PubMed] [PMC]
    Pizzi A. Tannins medical/pharmacological and related applications: a critical review. Sustain Chem Pharm. 2021;22:100481. [DOI]
    Fidelis M, Araújo Vieira do Carmo M, Azevedo L, Mendanha Cruz T, Boscacci Marques M, Myoda T, et al. Response surface optimization of phenolic compounds from jabuticaba (Myrciaria cauliflora [Mart.] O.Berg) seeds: antioxidant, antimicrobial, antihyperglycemic, antihypertensive and cytotoxic assessments. Food Chem Toxicol. 2020;142:111439. [DOI] [PubMed]
    Fidelis M, do Carmo MAV, da Cruz TM, Azevedo L, Myoda T, Miranda Furtado M et al. Camu-camu seed (Myrciaria dubia)—from side stream to an antioxidant, antihyperglycemic, antiproliferative, antimicrobial, antihemolytic, anti-inflammatory, and antihypertensive ingredient. Food Chem. 2020;310:125909. [DOI] [PubMed]
    Fujita A, Sarkar D, Wu S, Kennelly E, Shetty K, Genovese MI. Evaluation of phenolic-linked bioactives of camu-camu (Myrciaria dubia Mc. Vaugh) for antihyperglycemia, antihypertension, antimicrobial properties and cellular rejuvenation. Food Res Int. 2015;77:194203. [DOI]
    Srećković N, Katanić Stanković JS, Matić S, Mihailović NR, Imbimbo P, Monti DM, et al. Lythrum salicaria L. (Lythraceae) as a promising source of phenolic compounds in the modulation of oxidative stress: comparison between aerial parts and root extracts. Ind Crops Prod. 2020;155:112781. [DOI]
    Nohynek LJ, Alakomi HL, Kähkönen MP, Heinonen M, Helander IM, Oksman-Caldentey KM, et al. Berry phenolics: antimicrobial properties and mechanisms of action against severe human pathogens. Nutr Cancer. 2006;54:1832. [DOI] [PubMed]
    Przybylska D, Kucharska AZ, Cybulska I, Sozański T, Piórecki N, Fecka I. Cornus mas L. Stones: a valuable by-product as an ellagitannin source with high antioxidant potential. Molecules. 2020;25:4646. [DOI] [PubMed] [PMC]
    Moilanen J, Karonen M, Tähtinen P, Jacquet R, Quideau S, Salminen JP. Biological activity of ellagitannins: effects as anti-oxidants, pro-oxidants and metal chelators. Phytochemistry. 2016;125:6572. [DOI] [PubMed]
    Boulekbache-Makhlouf L, Meudec E, Mazauric JP, Madani K, Cheynier V. Qualitative and semi-quantitative analysis of phenolics in Eucalyptus globulus leaves by high-performance liquid chromatography coupled with diode array detection and electrospray ionisation mass spectrometry. Phytochem Anal. 2013;24:16270. [DOI] [PubMed]
    de Lima Paula P, de Oliveira Lemos AS, Campos LM, Ferreira TG, Freitas de Souza T, Queiroz LS, et al. Pharmacological investigation of antioxidant and anti-inflammatory activities of leaves and branches extracts from Plinia cauliflora (Jaboticaba). J Ethnopharmacol. 2021;280:114463. [DOI] [PubMed]
    Moon JH, Kim JM, Lee U, Kang JY, Kim MJ, Lee HL, et al. Walnut prevents cognitive impairment by regulating the synaptic and mitochondrial dysfunction via JNK signaling and apoptosis pathway in high-fat diet-induced C57BL/6 mice. Molecules. 2022;27:5316. [DOI] [PubMed] [PMC]
    Chen Y, Wang J, Ou Y, Chen H, Xiao S, Liu G, et al. Cellular antioxidant activities of polyphenols isolated from Eucalyptus leaves (Eucalyptus grandis × Eucalyptus urophylla GL9). J Funct Foods. 2014;7:73745. [DOI]
    de Oliveira Schmidt H, Rockett FC, André Vinícus Bazzan K, Schmidt L, Rodrigues E, et al. New insights into the phenolic compounds and antioxidant capacity of feijoa and cherry fruits cultivated in Brazil. Food Res Int. 2020;136:109564. [DOI] [PubMed]
    Kim M, Yin J, Hwang IH, Park DH, Lee EK, Kim MJ, et al. Anti-acne vulgaris effects of pedunculagin from the leaves of Quercus mongolica by anti-inflammatory activity and 5α-reductase inhibition. Molecules. 2020;25:2154. [DOI] [PubMed] [PMC]
    de Andrade Neves N, César Stringheta P, Ferreira da Silva I, García-Romero E, Gómez-Alonso S, Hermosín-Gutiérrez I. Identification and quantification of phenolic composition from different species of Jabuticaba (Plinia spp.) by HPLC-DAD-ESI/MSn. Food Chem. 2021;355:129605. [DOI] [PubMed]
    Li W, Zhang X, He Z, Chen Y, Li Z, Meng T, et al. In vitro and in vivo antioxidant activity of eucalyptus leaf polyphenols extract and its effect on chicken meat quality and cecum microbiota. Food Res Int. 2020;136:109302. [DOI] [PubMed]
    Almeida C, Murta D, Nunes R, Baby AR, Fernandes Â, Barros L, et al. Characterization of lipid extracts from the Hermetia illucens larvae and their bioactivities for potential use as pharmaceutical and cosmetic ingredients. Heliyon. 2022;8:e09455. [DOI] [PubMed] [PMC]
    Vega J, Bonomi-Barufi J, Gómez-Pinchetti JL, Figueroa FL. Cyanobacteria and red macroalgae as potential sources of antioxidants and UV radiation-absorbing compounds for cosmeceutical applications. Mar Drugs. 2020;18:659. [DOI] [PubMed] [PMC]
    Aires A, Carvalho R, Saavedra MJ. Valorization of solid wastes from chestnut industry processing: extraction and optimization of polyphenols, tannins and ellagitannins and its potential for adhesives, cosmetic and pharmaceutical industry. Waste Manag. 2016;48:45764. [DOI] [PubMed]
    Okumus E, Bakkalbas E, Javidipour I, Raciye M, Ceylan Z. A novel coating material: ellagitannins-loaded maltodextrin and lecithin-based nanomaterials. Food Biosci. 2021;42:101158. [DOI]
    Torgbo S, Rugthaworn P, Sukatta U, Sukyai P. Biological characterization and quantification of rambutan (Nephelium lappaceum L.) peel extract as a potential source of valuable minerals and ellagitannins for industrial applications. ACS Omega. 2022;7:3464756. [DOI] [PubMed] [PMC]
    Li Z, Summanen PH, Komoriya T, Henning SM, Lee RP, Carlson E, et al. Pomegranate ellagitannins stimulate growth of gut bacteria in vitro: implications for prebiotic and metabolic effects. Anaerobe. 2015;34:1648. [DOI] [PubMed]
    Fan N, Fusco JL, Rosenberg DW. Antioxidant and Anti-inflammatory properties of walnut constituents: focus on personalized cancer prevention and the microbiome. Antioxidants (Basel). 2023;12:982. [DOI] [PubMed] [PMC]
    Cegiełka A, Hać-Szymańczuk E, Piwowarek K, Dasiewicz K, Słowiński M, Wrońska K. The use of bioactive properties of sage preparations to improve the storage stability of low-pressure mechanically separated meat from chickens2. Poult Sci. 2019;98:504553. [DOI] [PubMed]
    Firuzi MR, Niakousari M, Eskandari MH, Keramat M, Gahruie HH, Mousavi Khaneghah A. Incorporation of pomegranate juice concentrate and pomegranate rind powder extract to improve the oxidative stability of frankfurter during refrigerated storage. LWT. 2019;102:23745. [DOI]
    Mantzourani I, Daoutidou M, Dasenaki M, Nikolaou A, Alexopoulos A, Terpou A, et al. Plant extract and essential oil application against food-borne pathogens in raw pork meat. Foods. 2022;11:861. [DOI] [PubMed] [PMC]
    Stojanović-Radić Z, Pejčić MG, Joković N, Jokanović M, Ivić M, Šojić B, et al. Inhibition of Salmonella enteritidis growth and storage stability in chicken meat treated with basil and rosemary essential oils alone or in combination. Food Control. 2018;90:33243. [DOI]
    Moghadam M, Salami M, Mohammadian M, Khodadadi M, Emam-Djomeh Z. Development of antioxidant edible films based on mung bean protein enriched with pomegranate peel. Food Hydrocoll. 2020;104:105735. [DOI]