Nanodelivery of essential oils as efficient tools against antimicrobial resistance: a review of the type and physical-chemical properties of the delivery systems and applications

Figures & data

Figure 1. The dynamics of publications for biodegradable and eco-friendly NPs (the ISI Web of Science Core Collection Clarivate Analytics was searched with the following keywords: ‘chitosan’ or ‘cellulose’ or ‘zein’ or ‘sodium alginate’ or ‘PLGA’ or ‘lipid’ and ‘nanoparticles’ (searches carried out on 29/05/2021).

Table 1. CS-EOs NPs characteristics and potential applications.

Characteristics of CS used	EOs loaded into CS NPs	NPs size (nm)	NPs polydispersity index	NPs zeta potential (mV)	Methods used	Functionality	Type of study	Medical or veterinary applications	References
Medium molecular weight (mw) chitosan	Mint (Mentha piperita), Thyme (Thymus vulgaris), Cinnamon (Cinnamomum verum)	40–100	Not reported	Not reported	Ionic gelation	Nanoencapsulation improves body weight gain, feed conversion ratio and feed intake on broiler chickens	In vitro and in vivo	A suitable alternative to synthetic antibiotic growth promoter used as in-feed in poultry production thanks to antibacterial activity against pathogenic bacteria (Escherichia coli), while preserving the bacteria of the intestinal flora, such as Lactobacillus spp.	(Nouri, 2019)
Medium mw chitosan, 75–85% degree of deacetylation	Cardamom (Elettaria cardamomum)	50–100	Not reported	> +50	Ionic gelation	Encapsulation efficiency of more than 90%. Long term stability. Extension of antimicrobial potential up to 7 days compared to 2 days with CSNPs alone	In vitro	Antimicrobial potential against extended-spectrum β-lactamase producing Escherichia coli and methicillin-resistant Staphylococcus aureus	(Jamil et al., 2016)
Medium mw chitosan	Homalomena pineodora	70	0.176	> +24	Ionic gelation	High encapsulation efficiency and loading capacity. Initial burst release followed by a slower release, up to complete release at 72 h. Release profile controlled by the first order kinetic model. Concentration-dependent killing behavior on time–kill assay	In vitro	Antimicrobial activity broad-spectrum against diabetic wound pathogens: Bacillus cereus, Bacillus subtilis, Staphylococcus aureus, and methicillin-resistant Staphylococcus aureus (Gram+). Escherichia coli, Proteus mirabilis, Yersinia spp., Klebsiella pneumoniae, Shigella boydii, Salmonella typhimurium, Acinetobacter anitratus and Pseudomonas aeruginosa (Gram-)	(Rozman et al., 2020)
Not reported	Garlic (Allium sativum)	Not reported	Not reported	Not reported	Ionic gelation	Nanoencapsulation improves body weight gain, feed conversion ratio and feed intake on broiler chickens	In vitro and in vivo	A suitable alternative to synthetic antibiotic growth promoter used as in-feed in broiler production thanks to antibacterial activity against Escherichia coli	(Amiri et al., 2020)
Medium mw chitosan (684 kDa), Roughly 85 % degree of deacetylation	Cinnamon (Cinnamomum zeylanicum)	100–200	<1	> +38	Ionic gelation	Initial burst release in the first 9 days, followed by a slow release. Release faster at low pH. Release profile follows a Fickian behavior	In vitro	Antibacterial activity against Escherichia coli, Erwinia carotovora, and Pseudomonas fluorescens (Gram-)	(Mohammadi et al., 2020)
Medium mw chitosan	Thyme (Thymus vulgaris)	30–100	Not reported	Not reported	Ionotropic gelation	Nanoencapsulation improves body weight gain and feed conversion ratio on broiler chickens. Initial burst release (97%) in the first 96 hours, followed by a slower release	In vitro and in vivo	A suitable alternative to synthetic antibiotic growth promoter used as in-feed in poultry production thanks to antibacterial activity against pathogenic bacteria (coliforms, aerobes), while preserving the bacteria of the intestinal flora, such as Lactobacillus spp.	(Hosseini and Meimandipour, 2018)
Medium mw chitosan 75–85% degree of deacetylation	Rosemary (Rosmarinus officinalis) Oregano (Origanum vulgare subsp. hirtum) Lavender (Lavandula angustifolia) Marine criste (Crithmum maritimum) White fir (Abies alba) Wild chamomile (Matricaria chamomilla) Pennyroyal (Mentha pulegium) Sage (Salvia officinalis) Anise (Pimpinella anisum)	250–300 and 500–600	Not reported	Not reported	Ionotropic gelation	Initial burst release followed by a slower release reaching a plateau	In vitro	Antibacterial activity against Staphylococcus aureus, Bacillus subtilis, Bacillus cereus (Gram+) and Escherichia coli, Xanthomonas campestris (Gram)	(Halevas et al., 2017)
Medium mw chitosan, 84.8% degree of dealkylation	Peppermint (Mentha piperita) Green Tea (Camellia sinensis)	20–60	Not reported	+20–+23and +24–+29	Emulsification/ionic gelation	Thermal stability of EOs-CS NPs reaching 350 °C. Initial burst release in the first 12 h, followed by a slower release up to 72 h. Release faster at low pH. Release profile follows a Fickian behavior	In vitro	Antibacterial activity against Staphyloccocus aureus (Gram+) and Escherichia coli (Gram-)	(Shetta et al., 2019)
Low mw chitosan (50–190 kDa), 80% degree of deacetylation	Nettle (Urtica dioica L)	208–369	0.153–0.412	+14–+30	Emulsion-ionic gelation in two stages: oil-in-water emulsification and then, ionic gelation	Not reported	Not reported	Antibacterial activity against Staphylococcus aureus, Bacillus cereus, Listeria monocytogenes (Gram+) and Escherichia coli, Salmonella typhi (Gram-)	(Bagheri et al., 2021)
Low mw chitosan (50–190 kDa), 75–85 % degree of deacetylation	Clove (Eugenia caryophyllata)	223–445	0.117–0.337	+10–+34	Emulsion-ionic gelation in two stages: oil-in-water emulsification and then, ionic gelation	Not reported	In vitro	Antibacterial activity against Staphylococcus aureus, Listeria monocytogenes (Gram+) and Escherichia coli, Salmonella typhi (Gram-)	(Hadidi et al., 2020)
Medium mw chitosan 75–85% degree of deacetylation	Oregano (Origanum vulgare)	282–402	Not reported	Not reported	Oil-in-water emulsion and ionic gelation	Initial burst release followed by a slower release	In vitro	Not reported	(Hosseini et al., 2013)
Medium mw chitosan 75–85% degree of deacetylation	Ajwain (Carum copticum)	236–721	Not reported	Not reported	Emulsion-ionic gelation	Initial burst effect for the first 24 h, followed by a steady release for 72 h, before decreasing and reaching a plateau. Release faster at low pH	In vitro	Antibacterial activity against Staphylococcus aureus, Staphylococcus epidermidis, Bacillus cereus (Gram+) and Escherichia coli, Salmonella typhimurium, Proteus vulgaris (Gram-)	(Esmaeili and Asgari 2015)
Medium mw chitosan 75–85% degree of deacetylation	Thyme (Thymus vulgaris)	6	Not reported	Not reported	Nanoprecipitation	Release time between 360 and 390 min	In vitro	Antibacterial activity against Staphylococcus aureus, Bacillus cereus, Listeria monocytogenes (Gram+) and Escherichia coli, Salmonella typhi, Shigella dysenteriae (Gram-)	(Sotelo-Boyás et al., 2017)

Table 2. Cellulose-EOs nanomaterials characteristics and potential applications.

Characteristics of cellulose used	EOs loaded into cellulose nanomaterials	Nanomaterials size (nm)	NPs polydispersity index	NPs zeta potential (mV)	Methods used	Functionality	Type of study	Medical or veterinary applications	References
Cellulose nanocrystals (CNCs)	Thyme white (Thymus vulgaris)	Width of 10 and length of 274	Not reported	Not reported	CNCs are produced by hydrolysis of sulfonic acid and used for the formation of the Pickering emulsion with EOs	Not reported	In vitro	Antibacterial activity against Staphylococcus aureus (Gram+), and Escherichia coli (Gram-)	(Shin et al., 2019)
Cellulose nanofibers (CNFs)	Thyme (Thymus vulgaris)	Not reported	Not reported	Not reported	CNFs are prepared by enzymatic hydrolysis pretreatment and TEMPO (2, 2, 6, 6-tetram-ethylpiperidine-1-oxide)-mediated oxidation pretreatment	Not reported	In vitro	Antibacterial properties were tested through fresh beef experiments, to preserve fresh food from contamination by bacteria	(Zhang et al., 2020)
Cellulose nanofibers (CNFs)	Thyme (Thymus vulgaris)	Not reported	Not reported	Not reported	Supercritical impregnation of active molecules, such as EOs, onto nanocellulose three-dimensional (3 D) structures	Not reported	In vitro	Antibacterial activity against Staphylococcus epidermidis (Gram+), and Escherichia coli (Gram-)	(Darpentigny et al., 2020)
Carboxymethyl cellulose (CMC) films	Santolina (Santolina chamaecyparissus), Pepper tree (Schinus molle), Eucalyptus (Eucalyptus globulus)	Not reported	Not reported	Not reported	Preparation of CMC-based films containing EOs	Not reported	In vitro	Antibacterial activity against Staphylococcus aureus, Bacillus subtilis, Enterococcus faecalis (Gram+), and Escherichia coli, Pseudomonas aeruginosa, Salmonella typhi (Gram-)	(Simsek et al., 2020)

Table 3. Zein-EOs NPs characteristics and potential applications.

Characteristics of zein used	EOs loaded into zein NPs	NPs size (nm)	NPs polydispersity index	NPs zeta potential (mV)	Methods used	Type of study	Functionality	Medical or veterinary applications	References
Zein from maize, Strongly hydrophobic because of a high proportion of cationic amino acids.	Clove (Eugenia caryophyllata) Garlic (Allium sativum)	150	<0.2	+30	Antisolvent precipitation, which consists of a hydro-ethanolic zein solution injection into an aqueous solution	In vitro	Encapsulation efficiency of more than 90%, stability in storage for 90 days	Applications in aquaculture, thanks to its bactericidal activity against Streptococcus iniae (Gram+), Aeromonas hydrophila, Edwardsiella tarda (Gram-).	(Luis et al., 2020)
Zein from maize	Oregano (Origanum vulgare) Thyme (Thymus vulgaris)	138–162	0.165–0.191	+20.9–+23.2	Nanoprecipitation with a nonionic Pluronic surfactant	In situ	Physical and chemical stability in storage for 90 days at 4 °C and 20 °C, release profile controlled by the Korsmeyer-Peppas kinetic model	Greater antimicrobial activity against Gram + bacteria, such as Listeria monocytogenes ATCC 7644 and Staphylococcus aureus ATCC 2593 than Gram – bacteria, such as Escherichia coli ATCC 25922 and Salmonella enterica serovar Typhimurium ATCC 14028 (because of their external lipopolysaccharide layer in their membrane which avoids the diffusion of hydrophobic compounds)	(Gonçalves da Rosa et al., 2020)
Zein from maize	Phenolic monoterpenes: Thymol and Carvacrol. There are components of several EOs extracted from Thyme (Thymus vulgaris) or Oregano (Origanum vulgare)	108–122	0.223 − 0.277	+9–+30	Nanoprecipitation	In vitro	Stability in storage for 90 days at 6 °C and 20 °C, release profile controlled by the Korsmeyer-Peppas kinetic model (50% in 72 h without burst effects)	Greater antimicrobial activity against Gram + bacteria, such as Listeria monocytogenes ATCC 7644 and Staphylococcus aureus ATCC 2593 than Gram– bacteria, such as Escherichia coli ATCC 25922 and Salmonella enterica serovar Typhimurium ATCC 14028	(da Rosa et al., 2015)
Zein from maize	Ocimum gratissimum Pimenta racemosa	150	<0.3	+16–+32	Nanoprecipitation	In vitro	High encapsulation efficiency, physical and chemical stability in storage for 180 days at 6 °C and 20 °C	Promising potential to application in a food system. Can act as natural preservative due to good physicochemical stability during 180 days of storage at 6 and 20 °C	(Paula Zapelini de Melo et al., 2019)
Zein from maize	Thyme (Thymus capitatus)	<180	0.250	Not reported	Self-assembly	In vitro	Not reported	Bacteriostatic activity improved against Gram + bacteria: Listeria monocytogenes, andGram – bacteria: Escherichia coli O157:H7	(Merino et al., 2019)
Zein with a minimum protein content of 97 g/100g	Thymol and Carvacrol, essentially found in Thyme (Thymus vulgaris) or Oregano (Origanum vulgare)	<800	<0.3	Not reported	Liquid-liquid dispersion	In vitro	Not reported	Antimicrobial activity against nonpathogenic Escherichia coli ATCC 53323 (Gram-). The nonpathogenic bacteria have been chosen because of their similarity to well-known pathogenic bacteria responsible for several foodborne illness outbreaks	(Wu et al., 2012)

Table 4. NaAlg-EOs films characteristics and potential applications.

Characteristics of NaAlg used	EOs loaded intoNaAlg films	NPs size (nm)	NPs polydispersity index	NPs zeta potential (mV)	Methods used	Functionality	Type of study	Medical or veterinary applications	References
Alginic acid sodium salt with viscosity 15000–20000 cps	Elicriso italic Chamomile (Chamomile blue) Cinnamon (Cannella corteccia) Lavender (Lavandula angustifolia) Tea tree (Melaleuca alternifolia) Peppermint (Mentha piperita) Eucalyptus(Eucalyptus globulus) Lemongrass (Cymbopogon flexuosus) Lemon (Citrus limon)	-	-	-	Films made of EOs dispersed in NaAlg matrix. With the addition of glycerol to induce plasticity and surfactants to improve the dispersion of the EOs through the NaAlg matrix	Progressive release of the EO from the film for long periods (1–17 days) in a very moist environment	In vitro	Antimicrobial activity against Escherichia coli (Gram-)	(Liakos et al., 2014)
Sodium alginate salt with viscosity 15000–20000 cps	Pepper tree (Schinus terebinthifolius) Allspice (Pimenta dioica) Black pepper (Piper nigrum)	-	-	-	Films made of EOs dispersed in NaAlg matrix	Release of the EO from the film in a very moist environment	In vitro	Antimicrobial activity against Staphylococcus aureus ATCC 29213, Bacillus cereus ATCC 11778 (Gram+), and Escherichia coli ATCC 35218 (Gram-)	(Rosa et al., 2018)

Table 5. PLGA-based-EOs NPs characteristics and potential applications.

Characteristics of PLGA used	EOs loaded into PLGA-based NPs	NPs size (nm)	NPs polydispersity index	NPs zeta potential (mV)	Methods used	Functionality	Type of study	Medical or veterinary applications	References
PLGA with a copolymer ratio of DL-lactide to glycolide of 50: 50. PLGA with a molecular weight between 5000–15000 Da	Black caraway (Nigella sativa)	148	0.2	−24.8	Solid-in-oil-in-water solvent evaporation	In the 1st 10 h, release of 25% with a burst effect, followed by a sustained release up to 54% for gastric juice and 75% for intestinal juice at 7 days. Better release rate in acidic pH. Physical properties (size, ZP,) of the NPs slightly modified due to heat treatments(60 °C, 80 °C and 100 °C)	In vitro	Antimicrobial activity against Staphylococcus aureus (Gram+) and Salmonella typhi, Escherichia coli (Gram-)	(Nallamuthu et al., 2013)
PLGA with a copolymer ratio of DL-lactide to glycolide of 65: 35	Clove (Eugenia caryophyllata) Cinnamon (Cinnamomum spp.)	200	>0.1	Not reported	Emulsion evaporation	Release with an initial burst effect, followed by a slower and sustained rate. Entrapment efficiency between 92–98%. Release profile controlled by the 2-term exponential kinetic model	In vitro	Antimicrobial activity against Listeria spp. (Gram+) and Salmonella spp. (Gram-)	(Gomes et al., 2011)
PLGA with a copolymer ratio of DL-lactide to glycolide of 50: 50. PLGA with a molecular weight between 38000–54000 Da	Anise (Pimpinella anisum) Star anise (Illicium verum) Fennel (Foeniculum vulgare) Caraway (Carum carvi) Dill (Anethum graveolens)	126 and 158	0.08–0.2	Not reported	Emulsification solvent evaporation and nanoprecipitation	Release with an initial burst effect during the first 6 h. Controlled release during more than 4 days	In vitro	Antimicrobial activity against Staphylococcus aureus (Gram+) and Salmonella typhi, Enterococcus coli (Gram-)	(Esfandyari- Manesh et al., 2013)
PLGA with a copolymer ratio of DL-lactide to glycolide of 65: 35 and 50:50	Cinnamon (Cinnamomum spp.)	145–167	0.18–0.26	Not reported	Emulsion evaporation	Release with an initial burst effect during the 1st h but reaching a steady plateau quickly	In vitro	Antimicrobial activity against Listeria monocytogenes (Gram+) and Salmonella enterica serovar Typhimurium (Gram-)	(Hill et al., 2013)
PLGA with a copolymer ratio of DL-lactide to glycolide of 85: 15. PLGA with a molecular weight between 50000–75000 Da	Lemongrass (Cymbopogon citratus)	277	0.18	−16	Emulsification/solvent diffusion with Box-Behnken design	Release with an initial burst effect (25% release after 3 h), followed by a sustained release until 84% release after 8 days. Release profile controlled by the Korsmeyer-Peppas model	In vitro	Promising potential for pharmaceutical uses, in controlling the release and in reducing the toxicity of the EO	(Almeida et al., 2019)
PLGA with a copolymer ratio of DL-lactide to glycolide of 50: 50	Phenolic monoterpene: Carvacrol. It is a component of several EOs extracted from Thyme (Thymus vulgaris) or Oregano (Origanum vulgare)	210	0.26	−18.99	Solvent displacement	Release with an initial burst effect (60% release after 3 h), followed by a slower rate until 95% release after 24 h	In vitro	Alter the properties of preformed staphylococcal biofilms (Staphylococcus epidermidis ATCC 35984)	(Iannitelli et al., 2011)

Figure 2. The characteristics, advantages, drawbacks, and applications of polymeric NPs as delivery systems for essential oils.

Table 6. Lipid-based-EOs NPs characteristics and potential applications.

Characteristics of lipids used	EOs loaded into lipid-based NPs	NPs size (nm)	NPs polydispersity index	NPs zeta potential (mV)	Methods used	Functionality	Type of study	Medical or veterinary applications	References
Solid lipid NPs and nanostructured lipid carriers (cocoa butter as solid lipid, olive or sesame oil as liquid lipids)	Eucalyptus (Eucalyptus globulus) Rosemary (Rosmarinus officinalis)	200–300	0.5	−22.07 0.29	High shear homogenization followed by ultrasound application	Physical stability up to 3 months at 2–8 °C	In vitro and in vivo	Antibacterial activity against Staphylococcus aureus ATCC 6538 and Streptococcus pyogenes ATCC 19615 (Gram+)	(Saporito et al., 2018)
Solid lipid NPs	Clove (Eugenia caryophyllata)	397–1231	0.215–0.680	−15–0.6 to 21.70.2	High-shear homogenization and ultrasound	Physical stability up to 3 months at 2–8 °C	In vitro	Antibacterial activity against Staphylococcus aureus (Gram+), and against Salmonella typhi, Pseudomonas aeruginosa (Gram-)	(Fazly Bazzaz et al., 2018)
Nanostructured lipid carriers	Tea tree (Melaleuca alternifolia)	150	0.213	−8.69	High pressure homogenization	Improved therapeutic efficacy in Rhamdia quelen	In vivo	Antibacterial activity against Pseudomonas aeruginosa PA01 (Gram-)	(Souza et al., 2017)
Nanostructured lipid carriers	Peppermint (Mentha piperita)	40–250	0.4	−10 to −15	Hot melt homogenization	Imporve the healing process of infected wounds in mice by decreasing the tissue bacterial count and edema score	In vitro and in vivo	In-vitro antibacterial activity against Staphylococcus aureus, Staphylococcus epidermidis, Bacillus anthracis, Staphylococcus pneumonia, and Listeria monocytogenes (Gram+). And against Escherichia coli, Salmonella typhimurium, Pseudomonas aeruginosa (Gram-). In-vivo antibacterial activity against Staphylococcus aureus (Gram+). And against Pseudomonas aeruginosa (Gram-)	(Ghodrati et al., 2019)
Nanostructured lipid carriers	Pennyroyal (Mentha pulegium)	40–250	0.4	−10 to −15	Hot melt homogenization	Topical application in mice reduced bacterial count and provoke proliferative phase	In vitro and in vivo	Antibacterial activity against Staphylococcus epidermidis ATCC 12228, Staphylococcus aureus ATCC 25923, Streptococcus pneumoniae ATCC 49819, Listeria monocytogenes ATCC 19133, and Bacillus anthracis ATCC 14578 (Gram+). And against Pseudomonas aeruginosa ATCC 27853, Escherichia coli ATCC 25922 and Salmonella typhimurium ATCC 14028 (Gram-)	(Khezri et al., 2020)
Nanoemulsions	Lemongrass (Cymbopogon flexuosus) EO	< 200	<0.3	−10.2	Homogenization under high agitation	Greater ability to reduce the adhesion of pathogenic bacteria to the surfaces, inhibiting the biofilm formation	In vitro	Antibacterial activity against Staphylococcus aureus ATCC 29213 (Gram+). And against Pseudomonas aeruginosa PA01 (Gram-)	(da Silva Gündel et al., 2018)
Nanoemulsions	Eucalyptus (Eucalyptus globulus) EO	32–142	0.153–0.278	−34.25 to −38.25	Aqueous phase titration	Rapid absorption, improved oral bioavailability, better therapeutic efficacy	In vivo	Not reported	(Alam et al., 2018)
Nanoemulsions	Winter savory (Satureja montana)	20–200	Not reported	Not reported	Sonication	Improved stability between 32 and 20 °C	In vitro	Antimicrobial activity against avian Escherichia coli strains (Gram-)	(Rinaldi et al., 2021)
Nanoemulsions	Thyme (Thymus vulgaris)	Not reported	Not reported	−25	Sonication	Positive transcriptional modifications of broiler’s digestive enzymes	In vivo	Antimicrobial activity against avian Salmonella enterica serovar Typhimurium strains (Gram-)	(Ibrahim et al., 2021)
Liposomes Hydrogenated (Phospholipon 80H, Phospholipon 90H) and non-hydrogenated (Lipoid S100) soybean phospholipids were used	Clove (Eugenia caryophyllata)	204–380	0.09–0.58	−3 to −38	Ethanol injection, saturated and unsaturated soybean phospholipids, in combination with cholesterol, were used to prepare liposomes	Stability up to 2 months at 4 °C	In vitro	Not reported	(Sebaaly et al.,, 2015)

Figure 3. The characteristics, advantages, drawbacks, and applications of lipidic NPs as delivery systems for essential oils.

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