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 [7–9] 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].

Display full size

Figure 1. 

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].

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.

Display full size

Figure 2. 

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).

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

Antioxidant activity

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.