Antifungal Activity of Citrus Essential Oils.

Review pubs.acs.org/JAFC

Antifungal Activity of Citrus Essential Oils Li Jing,†,§,# Zhentian Lei,# Ligai Li,†,§ Rangjin Xie,⊥ Wanpeng Xi,†,§ Yu Guan,⊗ Lloyd W Sumner,*,# and Zhiqin Zhou*,†,§ †

College of Horticulture and Landscape Architecture, Southwest University, Chongqing 400716, China Key Laboratory of Horticulture Science for Southern Mountainous Regions, Ministry of Education, Chongqing 400715, China # Plant Biology Division, The Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway, Ardmore, Oklahoma 73401, United States ⊥ Citrus Research Institute, Chinese Academy of Agricultural Sciences/Southwest University, Chongqing 400712, China ⊗ Shanghai Municipal Hospital of Traditional Chinese Medicine affiliated TCM University, Shanghai 200071, China §

ABSTRACT: Citrus essential oils (CEOs) are a mixture of volatile compounds consisting mainly of monoterpene hydrocarbons and are widely used in the food and pharmaceutical industries because of their antifungal activities. To face the challenge of growing public awareness and concern about food and health safety, studies concerning natural biopreservatives have become the focus of multidisciplinary research efforts. In the past decades, a large amount of literature has been published on the antifungal activity of CEOs. This paper reviews the advances of research on CEOs and focuses on their in vitro and food antifungal activities, chemical compositions of CEOs, and the methods used in antifungal assessment. Furthermore, the antifungal bioactive components in CEOs and their potential mechanism of action are summarized. Finally, the applications of CEOs in the food industry are discussed in an attempt to provide new information for future utilization of CEOs in modern industries. KEYWORDS: citrus essential oils (CEOs), antifungal activities, mechanism of action, applications

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INTRODUCTION Food safety is a fundamental concern of both consumers and the food industry, especially due to the increasing awareness of food and health. Fungus growth has been demonstrated to be responsible for food spoilage and plant disease, which leads to significant economic losses.1 Molds are a large group of taxonomically diverse fungal species, which are able to opportunistically colonize a wide array of habitats including foods, especially fresh fruits, vegetables, and grains. Because of the high activity of their hydrolytic enzymes and the production of toxic metabolites such as mycotoxins, molds are responsible for the decay or deterioration of a wide variety of foods and cause quantitative and qualitative losses.1−3 To extend the shelf life and maintain freshness of foods, chemical preservatives and additives such as sorbic acid, benzoic acid, propionic acid, and their salts have been widely used in the food industry. Although chemical treatments have been considered to be the cheapest and most effective way to prevent or control food pathogens, their uses are greatly limited by the emergence of new resistant fungal strains, their toxicity, poor solubility, and low potency.1,4 Recently, plant-derived natural antimycotics have been reported as ideal alternatives to traditional chemical preservatives for improving food quality and have become a focus of multidisciplinary studies.5−14 Among the plant essential oils, citrus essential oils (CEOs) have attracted more attention as antifungal agents owing to their antimicrobial properties, high yields, aromas, and flavors.2,15−18 In the past years, more and more in vitro and on food assessments have been performed to explore the antifungal activity of CEOs and their active components.19−22 Therefore, a thorough review of the recent research advances in CEOs and their antifungal activities would be useful. In this review, we summarize the in vitro and on food © 2014 American Chemical Society

antifungal activities of CEOs and their chemical components in an attempt to provide new information for the utilization of CEOs in the future.

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CITRUS ESSENTIAL OILS, THEIR CHEMICAL COMPOSITION AND VARIATION, AND BIOLOGICAL ACTIVITIES Citrus fruits are widely cultivated and consumed throughout the world. CEOs are a mixture of volatile compounds consisting mainly of monoterpene hydrocarbons and exist especially in citrus peels, leaves, and flowers. CEOs are generally recognized as safe (GRAS)23 and have been used as flavoring agents in foods, beverages, liqueurs, and confections in the current food industry. CEOs have also been widely used as aromatic agents in soaps, perfumes, and household products. In the past decades, numerous investigations have been performed to identify the chemical composition of CEOs from different species and/or cultivars.24−30 The extraction procedures and the chromatography-based analysis methods of the CEOs, as well as the advantages and shortcomings of each method, have been summarized in detail by Tranchida et al.31 CEOs usually consist of 85−99% volatile and 1−15% nonvolatile constituents.31 The volatile constituents are a mixture of monoterpene (mainly limonene) and sesquiterpene hydrocarbons and their oxygenated derivatives including aldehydes, ketones, acids, alcohols, and esters. Among these components, limonene is the major compound, and its content Received: October 17, 2013 Accepted: March 14, 2014 Published: March 14, 2014 3011

dx.doi.org/10.1021/jf5006148 | J. Agric. Food Chem. 2014, 62, 3011−3033

Journal of Agricultural and Food Chemistry

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Table 1. Chemical Composition of CEOs

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Table 1. continued

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Table 1. continued

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varies significantly among the Citrus species and/or varieties. For example, sweet orange contains 83−97%, lemon, 54−80%, and bergamot, 25−32% limonene. 32 The nonvolatile residue, which forms about 1−15% of the oil, contains hydrocarbons, sterols, fatty acids, waxes, carotenoids, coumarins, psoralens, and flavonoids,31 among which flavonoids are a group of components useful in differentiating between species.17 By the end of 1970, approximately 200 different compounds had been described from orange oil, among which around 100 have been identified. In the review by Shaw,32 the quantitative values for individual components of cold-pressed oils of different citrus species and varieties were presented, which gave us a general idea of the oil compositions of different citrus types. On the basis of previous studies,28−30,33−36 the 75 most-reported monoterpenes and sesquiterpenes in CEOs extracted from different organs (flowers, leaves, and peels), species, and/or varieties are summarized in Table 1. The chemical compositions of CEOs are influenced by both internal and external factors.37,38 The genetic factors, including species, cultivars, and different parts of the fruits, are the major determinant of the composition and contents of essential oils. A comparison study of essential oils from the peels of four selected Tunisian citrus species showed that δ-cadinene, a sesquiterpene in CEOs, was found only in pummelo and αcalacorene, another sesquiterpene, was observed only in mandarin.30 Furthermore, cultivars also influence the citrus oil profiles.28,39 Lota et al.28 reported that the composition and content of CEOs were different among 58 mandarin cultivars belonging to 15 different species, and the contents of the major components of these essential oils varied considerably from sample to sample. In addition, the chemical compositions of CEOs also vary significantly depending on the organs extracted. For example, terpineol-4 was one of the major compounds in the leaf oils of lemon, whereas it was not detected in peel oils.29 Environmental factors such as soil, cultural practices, insects, ripening stage, and weather can contribute to the quantitative variations of essential oils.38 Azizi et al.40 compared the response of oregano (Origanum vulgare L.) populations to soil moisture regimens (optimal, consistent water deficiency, and water deficiency from the beginning of flowering) and nitrogen application, and they found that water deficiency after the beginning of blooming could induce an increase in essential oil

content, whereas higher nitrogen levels caused a decrease. Besides soil and cultural practice factors, weather differences such as seasonal variations can also induce a difference in the composition and content of essential oils. For example, Vekiari et al.34 measured the components of essential oil from Zambetakis (Citrus limon Burm.f.) at six different time intervals over a period of greater than a year. They found significant differences between the aroma profiles and quantitative variations between lemon leaves and peels and attributed those variations to the different harvest periods of citrus leaves and fruits. Their study suggested that the ripening effect influenced significantly the chemical compositions of the essential oil. Genetic and environmental factors not only influence the oil compositions and contents but also affect the bioactivity of the oils. For example, Fisher and Phillips41 investigated the antibacterial activity of oils from lemon, sweet orange, and bergamot. They found that bergamot was the most effective among the tested oils due to its high linalool content. CEOs and their chemical compositions possess a wide spectrum of biological activities, including antimicrobial,34,42−49 antioxidant,50,51 anticancer,52−55 anti-inflammatory,56−60 insecticidal,61−67 embryo-fetotoxicity, 68 and metabolism disorder regulating activity.69−76 All of the bioactivities mentioned above are summarized in Table 1. The biological activity of monocyclic monoterpene D-limonene has been evaluated by a number of studies, such as antioxidant,77−79 anti-inflammatory, 38 anticancer,80,81 and metabolic disorder alleviating activities.75,82 In addition, geraniol, a terpene alcohol in CEOs, represents a new class of chemoprevention agents for cancer and other biological activities such as antimicrobial, antioxidant, anti-inflammatory, and some vascular effects.50 Taken together, CEOs and their chemical compositions may be of great importance in many fields, from food chemistry to pharmacology and pharmaceutics.

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METHODS USED IN THE ASSESSMENT OF ANTIFUNGAL ACTIVITY OF CEOS The major methods used for the assessment of antimicrobial activity of essential oils have been summarized in several recent reviews, which include the agar diffusion test, the agar or broth dilution test, and the vapor phase test.17,83 The particular advantages and disadvantages of these different methods are 3016



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Table 2. In Vitro Antifungal Activity of CEOs Reported in Current Literature effective against Aspergillus niger

test CEOs lemon (C. limon Burm.f.) lemon (C. limon Burm.f.)

major component

inhibition zone =6 mm

poisoned food assay; volatile activity assay modified agar dilution

MIC = 600 ppm (PFa) MIC = 500 ppm (VAb) MIC = 0.94% (v/v)

mandarin (C. reticulata Blanco) orange (C. sinensis Osb.)

modified agar dilution

MIC = 0.94% (v/v)


MIC = 0.94% (v/v)

grapefruit (C. paradisi Macf.) Citri-Vc


MIC = 0.94% (v/v)

vapor phase test

67% reduction at 15 mg/L air


MIC = 0.94% (v/v)

agar diffusion method modified agar dilution

inhibition halo =13 mm MIC = 0.94% (v/v)


MIC = 0.94% (v/v)

poisoned food assay

100% inhibition at 750 ppm

agar dilution method

MIC = 0.5% (v/v)


MIC = 0.94% (v/v)

limonene


MIC = 0.5% (v/v)

limonene (31.83%), citral (31.0%) limonene, citronellol, linalool limonene, p-cymene

poisoned food assay

100% inhibition at 750 ppm MIC = 1%, 4% (v/v) MIC = 1%, 4% (v/v)

limonene (96.62%)

agar diffusion method; broth microdilution agar diffusion method; broth microdilution vapor phase test

limonene (96.62%)


MIC = 16000 mg/L

limonene (31.83%), citral (31.0%) limonene (31.83%), citral (31.0%)

poisoned food assay


Singh et al. (2010)

poisoned food assay


Singh et al. (2010)


poisoned food assay


Singh et al. (2010)

poisoned food assay


Singh et al. (2010)

limonene, citronellol, linalool limonene, p-cymene

agar diffusion method; broth microdilution agar diffusion method; broth microdilution

MIC = 1%, 4% (v/v)

Rammance and Hongpattarakere (2011) Rammance and Hongpattarakere (2011)

limonene (84.2%)

lemon (C. limon Burm.f.) mandarin (C. reticulata Blanco) orange (C. sinensis Osb.)

citral, eugenol

orange (C. sinensis Osb.)

limonene (31.83%), citral (31.0%) limonene

acid lime (C. aurantifolia) orange (C. sinensis Osb.) vapor orange (C. sinensis Osb.) orange (C. sinensis Osb.) pummelo (C. maxima Burm.) orange (C. sinensis Osb.) pummelo (C. maxima Burm.) Aspergillus parasiticus

lime (C. hystrix DC) acid lime (C. aurantifolia)

Penicillium chrysogenum

limonene (603.99 mg/mL)

lemon (C. limon Burm.f.)

grapefruit (C. paradisi Macf.) pummelo (C. maxima Burm.) pummelo (C. maxima Burm.) lime (C. hystrix DC)

Aspergillus terreus

references

agar diffusion test


Aspergillus f umigatu

effects inhibition halo =10 mm inhibition zone =7 mm


Aspergillus f lavus

test method agar diffusion method agar diffusion test

sour orange (C. aurantium L.) orange (C. sinensis Osb.)

citral, eugenol

MIC = 8000 EO/air

MIC = 1%, 4% (v/v)



MIC = 0.94% (v/v)



MIC = 0.94% (v/v)


MIC = 0.94% (v/v)

agar diffusion method; broth microdilution modified agar dilution

inhibition zone = 18.99 mm; MIC = 9.33 μL/mL MIC = 0.94% (v/v)

vapor phase test

43.8% reduction at 14 mg/L air

orange (C. sinensis Osb.) grapefruit (C. paradisi Macf.) Citri-V

limonene (77.49%); myrcene (6.27%)

limonene (603.99 mg/mL)

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Souza et al. (2005) Pawar and Thaker (2006) Pawar and Thaker (2006) Sharma and Tripathi (2008) Viuda-Martos et al. (2008) Viuda-Martos et al. (2008) Viuda-Martos et al. (2008) Viuda-Martos et al. (2008) Phillips et al. (2012)

Viuda-Martos et al. (2008) Souza et al. (2005) Viuda-Martos et al. (2008) Viuda-Martos et al. (2008) Singh et al. (2010) Bosquez-Molina et al. (2010) Viuda-Martos et al. (2008) Bosquez-Molina et al. (2010) Singh et al. (2010) Rammance and Hongpattarakere (2011) Rammance and Hongpattarakere (2011) Velázquez-Nuñez et al. (2013)

Viuda-Martos et al. (2008) Viuda-Martos et al. (2008) Viuda-Martos et al. (2008) Tao et al. (2009) Viuda-Martos et al. (2008) Phillips et al. (2012)



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Table 2. continued effective against

test CEOs

Penicillium chrysogenum MPPLU 27


Penicillium verrucosum

major component limonene (84.2%), linalool (4.4%)

test method

effects

references

poisoned food technique; volatile activity assay

MIC = 600 ppm (PF), MIC = 500 ppm (VA)

Sharma and Tripathi (2006)



MIC = 0.94% (v/v)



MIC = 0.94% (v/v)


MIC = 0.94% (v/v)

grapefruit (C. paradisi Macf.)


MIC = 0.94% (v/v)

Viuda-Martos (2008) Viuda-Martos (2008) Viuda-Martos (2008) Viuda-Martos (2008)

et al. et al. et al. et al.

Penicillium spp.


citral, eugenol

agar diffusion method

not effective

Souza et al. (2005)

Penicillium digitatum

orange (C. sinensis Osb.) sour orange (C. aurantium L.) mandarin (C. reticulata Blanco) grapefruit (C. paradisi Macf.) lemon (C. limon Burm.f.) mandarin (C. reticulata Blanco)

limonene, myrcene limonene, myrcene

dry weight determination dry weight determination

ED50 = 2180.2 ppm (A1) ED50 = 1015.4 ppm

Caccioni et al. (1998) Caccioni et al. (1998)

limonene, α-pinene

dry weight determination

ED50 = 713.3 ppm

Caccioni et al. (1998)

limonene, myrcene


ED50 = 910.3 ppm (P1)


limonene, α-pinene limonene (60.74%), γ-terpinene (0.04%)

dry weight determination poisoned food technique

ED50 = 1056.4 ppm (L1) 100% inhibition at 10.0 μL/mL

Caccioni et al. (1998) Tao et al. (2013)

orange (C. sinensis Osb.) sour orange (C. aurantium L.) mandarin (C. reticulata Blanco) grapefruit (C. paradisi Macf.) lemon (C. limon Burm.f.) mandarin (C. reticulata Blanco)

limonene, myrcene limonene, myrcene

dry weight determination dry weight determination

ED50 = 5407.5 ppm (A1) ED50 = 1490.6 ppm


limonene, α-pinene


ED50 = 1977.0 ppm


limonene, myrcene


ED50 = 1498.4 ppm (P1)


limonene, α-pinene limonene (60.74%), γ-terpinene (0.04%)

dry weight determination poisoned food technique

ED50 = 2505.4 ppm (L1) 100% inhibition at 2.5 μL/mL

Caccioni et al. (1998) Tao et al. (2013)


limonene (90.42%), myrcene (2.81%) limonene (91.58%), myrcene (2.79%) limonene (41.4%), β-pinene (18.54%) limonene(70.46%),γ-terpinene (11.09%)


34.9% inhibition at 2000 ppm

Van Hung et al. (2013)










Penicillium italicum

Penicillium expansum

mandarin (C. reticulata Blanco) lime (C. autantifolia) pummelo (C. grandis Osb.)

Penicillium expansum MPPLU 24


limonene (84.2%), linalool (4.4%)

poisoned food assay; volatile activity assay

MIC = 600 ppm (PF) MIC = 500 ppm (VA)


Fusarium spp.


citral, eugenol

plate diffusion procedure

not effective

Souza et al. (2005)

Fusarium oxysporum


limonene (31.83%), citral (31.0%) limonene (31.83%), citral (31.0%) limonene (46.7%), geranial (19.0%)

poisoned food assay


Singh et al. (2010)

poisoned food assay


Singh et al. (2010)


MIC> 0.2% (v/v)

Chutia et al. (2009)

limonene (90.42%), myrcene (2.81%) limonene (91.58%), myrcene (2.79%) limonene (41.4%), β-pinene (18.54%) limonene (70.46%), γ-terpinene (11.09%)













limonene (46.7%), geranial (19.0%)


MIC = 0.2% (v/v)


pummelo (C. maxima Burm.) mandarin (C. reticulata Blanco) Fusarium proliferatum

orange (C. sinensis Osb.) mandarin (C. reticulata Blanco) lime (C. autantifolia) pummelo (C. grandis Osb.)

Alternaria alternata

mandarin (C. reticulata Blanco)

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Table 2. continued effective against

test CEOs Citri-V orange (C. sinensis Osb.) pummelo (C. maxima Burm.) orange (C. sinensis Osb.)

major component limonene (31.83%), citral (31.0%) limonene (31.83%), citral (31.0%) limonene (84.2%), linalool (4.4%)

test method

effects

references

vapor phase test poisoned food assay

34% reduction at 15 mg/L air 100% inhibition at 750 ppm

Phillips et al. (2012) Singh et al. (2010)

poisoned food assay


Singh et al. (2010)


MIC = 600 ppm (PF) MIC = 500 ppm (VA)


Rhizoctonia solani




MIC = 0.2% (v/v)


Curvularia lunata




MIC = 0.2% (v/v)


Colletotrichum gloeosporioides

lime (C. aurantifolia)


MIC = 0.5% (v/v)

Bosquez-Molina et al. (2010)

Rhizopus spp.


agar diffusion method

inhibition halo =12 mm

Souza et al. (2005)

Rhizopus stolonifer

lime (C. autantifolia)


MIC = 0.5% (v/v)

Bosquez-Molina et al. (2010)

Helminthosporium oryzae



MIC > 0.2% (v/v)


Phaeoramularia angolensis

pummelo (C. maxima Burm.) grapefruit (C. paradisi Macf.)

poisoned food assay

>87% inhibition at 2500 ppm

Kuate et al. (2006)

poisoned food assay

>64% inhibition at 2500 ppm

Kuate et al. (2006)

citral, eugenol


Botryodiplodia theobromae




MIC = 600 ppm (VA)


Cladosporium f ulvum




MIC = 700 ppm (PF); MIC = 500 ppm (VA)


Botrytis cinerea



poisoned food assay; volatile activity assay agar dilution method

MIC = 500 ppm (PF); MIC = 400 ppm (VA) MIC = 17 or 22 μL/mL; ED 50 = 11 or 13 μL/mL

Sharma and Tripathi (2006) Vitoratos et al. (2013)


Cladosporium cladosporioides




MIC = 500 ppm (PF); MIC = 400 ppm (VA)


Myrothecium roridum




MIC = 700 ppm (VA)


Mucor hiemalis


limonene (90.42%), myrcene (2.81%) limonene (91.58%), myrcene (2.79%) limonene (41.4%), β-pinene (18.54%) limonene (70.46%), γ-terpinene (11.09%)














poisoned food assay


Singh et al. (2010)

poisoned food assay


Singh et al. (2010)


poisoned food assay


Singh et al. (2010)

poisoned food assay


Singh et al. (2010)

limonene (77.49%), myrcene (6.27%)

agar diffusion method; broth microdilution

inhibition zone = 14.57 mm; MIC = 18.75 μL/mL

Tao et al. (2009)

mandarin (C. reticulata Blanco) lime (C. aurantifolia) pummelo (C. grandis Osb.)

Helminthosporium oryzae

orange (C. sinensis Osb.) pummelo (C. maxima Burm.)

Trichoderma viride

orange (C. sinensis Osb.) pummelo (C. maxima Burm.)

Saccharomyces cerevisiae a


Citri-V, a 50:50 mix of orange/bergamot essential oils (AMPHORA, Bristol, UK). bPF, poisoned food technique. cVA, volatile activity assay. 3019



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extensively discussed in the book by Pauli et al.84 and the reviews mentioned above. In this review, we summarize several of the most commonly used in vitro testing methods for the antifungal assessment of CEOs, especially the agar diffusion, the broth/agar dilution test, the broth microdilution method, and the poisoned food technique. Agar Diffusion Test. This method was described and utilized as a standardized method for the screening of essential oils in the past decades and has been adapted in numerous ways based on the same principle.85 The agar diffusion test is performed by placing an essential oil impregnated filter disk on the surface of agar containing the microbe to be tested, and the antifungal activity of tested essential oils is evaluated by measuring the inhibition zones. The agar diffusion method seems to be the most popular method for examining antimicrobial activity as it allows for the simultaneous testing of a large number of antimicrobials in a relatively easy and flexible manner.86 As shown in Table 2, the agar diffusion test has been widely used in the assessment of antifungal activity of CEOs. However, it is noteworthy to point out that the size of inhibition zones is difficult to be interpreted due to the unknown diffusion coefficients, the different volatilities of single constituents, and other factors such as agar type, agar−agar content, pH, and volume of agar.83 In particular, the results obtained from this method have shown misleadingly low antifungal activity when the components have low water solubility. 83 Broth/Agar Dilution Test. The dilution test is another in vitro method widely used for assessing the antifungal activity of CEOs (Table 2). In the broth dilution test, a concentration series of the antifungal substance is established using a broth medium, which is seeded with fungal strains, whereas in the agar dilution test, a concentration gradient of the tested substance is placed onto an agar plate.83 For both methods, a minimum inhibition concentration (MIC) is used to evaluate the antifungal activity of the tested substance(s), which presents the lowest concentration of tested substance(s) that prevents the growth of seeded fungal strains. The advantages and disadvantages of these two dilution test methods have been summarized in detail by Jiang.86 Generally, in the agar dilution method, the agar with supplements is able to adequately support fungus growth, whereas in the broth dilution method, lack of or poor growth of many anaerobic microorganisms was observed because of insufficient supplements. The agar dilution test has been declared to be the “gold standard” as it overcomes some limitations of the agar diffusion method, primarily the capability to draw a quantitative conclusion by determining the MIC value of the tested substance(s).86−88 This method can also be used to test the susceptibility of a number of substance(s) in one plate simultaneously, as well as to test fastidious organisms due to the agar being able to adequately support microorganism growth.86 However, it is not used frequently due to its high-cost, labor-intensive, and timeconsuming properties. 83 Broth Microdilution Method. Broth microdilution is another quantitative reference method for the fungitoxicity test of CEOs, which allows for the simultaneous testing of multiple antimicrobials with ease, particularly when commercially prepared microtiter trays are used.16,86,89 In the study by Jiang,86 the agar diffusion, the broth/agar dilution test, and the broth microdilution method have been compared on several bacterial strains. Jiang suggested that the broth microdilution be used for MIC determination, compared to other methods, due

to its time and labor savings, as well as its capability of quantitative determination. However, inconsistent and unreliable results can occur when some fastidious anaerobes are tested because of their poor growth due to excessive exposure to oxygen during the setup procedure. Poisoned Food Technique. The poisoned food technique has been used widely in the antifungal assessment of CEOs (Table 2). In this method, the fungitoxicity was expressed in terms of percentage of mycelia growth inhibition and calculated as follows: percentage of mycelial growth inhibition = (dc − dt)/dc × 100, where dc = average diameter of fungal colony in control and dt = average diameter of fungal colony in treatment.90,91 As shown in Table 2, there are other methods that have been used for the antifungal activity test of CEOs, such as mycelium dry weight determination test20,91,92 and volatile activity assay.20,93 As for the vapor phase test of CEOs, the related methodology has been discussed and summarized in the reviews by Cavanagh94 and Laid and Phillips;95 however, there is no standardized method available. In general, a seeded agar plate is placed upside down onto a reservoir, which comprises a certain amount of volatile oil. In this case the generated inhibition zone is considered to be a criterion for the antimicrobial activity.83 In general, each method has its own advantages and disadvantages. Antifungal tests of essential oils are difficult to perform because of their high volatility, which can result in distorted results. Another problem is the hydrophobicity of the essential oils, which sometimes demands the use of surfactants that might lead to noteworthy differences between outcomes.

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IN VITRO ANTIFUNGAL EFFECTS OF CEOS The antimicrobial property of CEOs was recognized a long time ago.17 In the past decades, the antifungal activity of CEOs has attracted the attention of many researchers.19,21,22,96−98 Table 2 summarizes the in vitro antifungal effects of CEOs reported in the current literature. In vitro experiments are valuable precursors to more costly food trials and enable the identification of effective essential oils and determination of the concentrations required for inhibition of a specific pathogen or a spectrum of pathogens.99 The following part of this review will focus on the antifungal activity of CEOs against some food spoilage or phytopathogenic fungal species, especially Aspergillus and Penicillium species. Aspergillus is a genus consisting of several hundred species, which are highly aerobic and found in almost all oxygen-rich environments. Aspergillus species are common contaminants of starchy foods such as bread and potatoes. The current literature has shown that CEOs have a broad anti-Aspergillus spectrum including A. niger, A. flavus, A. fumigatus, A. terreus, and A. parasiticus (Table 2). Among these species, A. niger and A. f lavus are the most commonly used strains in the antifungal test of CEOs (Table 2).2,10,16,19,21,22,89,93,100 The first anti-Aspergillus research of CEOs can be traced back to 1985, when Karapinar101 found that CEOs could inhibit the growth and aflatoxin formation of A. parasiticus. In 2006, Pawar and Thaker100 compared the effects of 75 plant essential oils on the hyphal growth and spore formation of A. niger, among which the essential oils of sour orange (Citrus aurantium L.), bergamot (Citrus bergamia Risso and Poit), lemon (Citrus limon Burm.f.), and Citrus bigaradia Hook.f. exhibited inhibitory effects. In agreement with this, Viuda-Martos et al.21 reported that lemon, mandarin, grapefruit, and sweet orange essential 3020



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oils could reduce or inhibit the growth of A. niger and A. f lavus in a dose-dependent manner, with sweet orange essential oil being the most effective against A. niger and mandarin being the best inhibitor of A. f lavus. Sharma and Tripathi91 found that the sweet orange essential oil treatment resulted in the flattening and ultimate death of A. niger hyphae, and limonene was the major component (84.2%) of the oil. The study conducted by Singh et al.19 found that pummelo (Citrus maxima Burm.) and sweet orange (Citrus sinensis Osb.) essential oils and their combination were all effective against A. f lavus, with the essential oil of pummelo being the most effective. In the study by Rammanee and Hongpattarakere,16 the essential oils prepared from citrus epicarps exhibited stronger antifungal activity to all Aspergillus strains than their ethyl acetate extracts. In particular, the essential oils from kaffir lime (Citrus hystrix DC) and acid lime (Citrus aurantifolia Swingle) were most inhibitory to mold growth as well as aflatoxin production among all of the tested citrus cultivars. On the basis of the studies mentioned above, it can be concluded that the CEOs are effective against Aspergillus species. The genus Penicillium is another prevalent airborne fungus, which belongs to the same family as Aspergillus. There are over 300 different species described in the genus. P. digitatum, P. italicum, and P. chrysogenum are among the most reported Penicillium species that have been used for the fungitoxicity test of CEOs. In 1995, Caccioni and his colleagues102 found that CEOs could exert an important bioregulatory action on the fungal spores of P. digitatum (Pers.) Sacc. and P. italicum Wehm, which are the two most dangerous postharvest pathogens of citrus fruit. Viuda-Martos et al.21 found that lemon, mandarin, grapefruit, and sweet orange essential oils had the capacity to reduce or inhibit the growth of P. chrysogenum in a dose−response manner, and grapefruit was the best inhibitor among those four CEOs, followed by lemon essential oil. Tao et al.89 reported that Bingtang sweet orange essential oil exhibited high antifungal activity against P. chrysogenum ATCC 10106, with an inhibition zone of 18.99 mm. In a study by Sharma and Tripathi,93 sweet orange essential oil completely inhibited the radial growth and spore germination of P. chrysogenum and P. expansum, as well as other postharvest pathogens. Van Hung et al.103 compared the antifungal activity of the essential oils from four citrus species and found that pummelo essential oil was the most effective against P. expansum. In addition, CEOs have been reported to have antifungal activity against Penicillium spp.2 and P. verrucosum (Table 2).21 Besides these most studied Aspergillus and Penicillium species, CEOs have also been reported to have antifungal activity against Fusarium,2,19,20,103 Alternaria19,20,93 (Table 2), and other fungal strains.97,98 Furthermore, the vapor phase of CEOs has also been assessed for their antifungal activity, and they exhibited antifungal activity against several fungal strains, such as A. f lavus10 and Alternaria alternata.22 The study performed by Velázquez-Nuñez et al.10 showed that the vapor state was more effective than the liquid state of orange peel essential oil in antifungal activity, and lower concentrations were required to achieve the same antifungal effect. The advantages of vapor phase of essential oils over the direct application of the oils themselves have been summarized in the review by Cavanagh,94 such as reduced toxicity and ease of application. The author also suggested that the vapor phase of essential oils had great potential for use in fungal control and/or treatment.

On the basis of the reports mentioned above, we may conclude that CEOs are effective in inhibiting the growth of mycelia and spores and in reducing the production of mycotoxins against different fungal species. The essential oils from the same citrus species have about the same antifungal activity, but it also varies from cultivar to cultivar. On the basis of GC-MS analysis data, different chemical compositions have been identified in different CEOs, among which limonene was found to be the major component (Table 2). Table 2 shows the concentrations of limonene varied from 31.83 to 96.62% in the essential oil samples used for the antifungal experiments. From this information, the fungitoxicity of CEOs can be attributed to their chemical composition and the concentration of active compounds. This conclusion is in agreement with the reports that the antifungal activity of CEOs relied on their chemical composition.1,17 However, the exact active compounds that contribute to the fungitoxicity of CEOs still need to be further clarified in future studies. Antifungal Activity of CEOs on Food. To explore the potential of CEOs as alternative additives or fungicides on food, their antimicrobial effectiveness, especially antibacterial activity, has been investigated by using several common foodborne pathogens. CEOs have been reported to be effective against a number of bacteria that cause food spoilage or poisoning, but their antibacterial activities on the strains tested were less effective in food systems than in vitro.41,104 The antifungal assessments of CEOs on food, however, have not been performed until recently. For example, Bosquez-Molina et al.3 reported that the Mexican lime essential oils had inhibitory effects against Colletotrichum gloeosporioides and Rhizopus stolonifer growth of storage rots in papaya fruit. Vitoratos et al.98 found that lemon essential oils were very effective against the fungus Botrytis cinerea in tomatoes, strawberries, and cucumbers. The fungitoxicity assessment on food is necessary and essential for the screening and confirmation of the antifungal activity of CEOs before they are applied in the food industry, as the efficacy of bioactive compounds might decay due to possible interactions of these compounds with the food matrix. For example, Phillips et al.22 assessed the antifungal effects of CEOs both in vitro and on food, including tomatoes and grain, against three fungal strains (A. niger, P. chrysogenum. and Alternaria alternata). They found that citrus essential oil vapors completely inhibited the mycelial growth and spore germination of those three fungi in in vitro tests; however, similar results were not observed on tomatoes or grain. It is important to point out that higher concentrations of CEOs or their chemical components should be used in food products to obtain the same effect observed in in vitro experiments, as highly hydrophobic and volatile active substances are often bound by food surfaces.1 Unfortunately, Dusan and his colleagues105 demonstrated that higher dose of essential oils showed detrimental effects on intestinal cells. Therefore, animal and human toxicity studies of CEOs should be carried out before their commercial use. Antifungal Components of CEOs and Their Mechanism of Action. CEOs are a complex mixture of volatile compounds. The antifungal activity of CEOs has been attributed to a single major compound or to the synergistic or antagonistic effect of different compounds.106 Some authors suggested that the flavonoids likely play a contributing role in the antifungal activity of CEOs.107 However, more and more authors tend to attribute the antifungal function to the presence 3021



Review

Table 3. Antifungal Effects of CEOs on Food Reported in Current Literature test CEO

effective against

test food

effect

reference

lime (C. aurantifolia) lime (C. aurantifolia) bergamot 50:50 mix of orange/bergamot 50:50 mix of orange/bergamot 50:50 mix of orange/bergamot lemon (C. limon Burm.f.) lemon (C. limon Burm.f.)

Rhizopus stolonifer Colletotrichum gloeosporioides

papaya fruits papaya fruits grapes grain grain tomatoes strawberries cucumber

reduction of up to 40% of decay reduction of up to 50% of decay log UFC value for molds reduced reduction of 70.8% of growth reduction of 57.8% of growth not effective 100% inhibition at 0.05 μL/mL 39% inhibition at 0.05 μL/mL

Bosquez-Molina et al. (2010) Bosquez-Molina et al. (2010) Sánchez-González et al. (2011) Phillips et al. (2012) Phillips et al. (2012) Phillips et al. (2012) Vitoratos et al. (2013) Vitoratos et al. (2013)

Aspergillus niger Penicillium chrysogenum Alternaria alternata Botrytis cinerea Botrytis cinerea

monoterpene content of the essential oils from various citrus species and the pathogen fungus inhibition. More recently, an increasing body of research has found that the terpenoids in CEOs, including citral, geranial, eugenol, γ-terpinene, pcymene, myrcene, thymol, and carvacrol, had a wide spectrum of fungitoxicity.2,11,125−130 Among these compounds, citral and limonene have been suggested as the most significant antifungal candidates of CEOs. Citral is an acyclic α,β-unsaturated monoterpene aldehyde with two isomers, geranial and neral. The antifungal activity of citral has been demonstrated by several authors, either in CEOs or in other plant essential oils.131,132 In the works carried out by Caccioni and his colleagues,92,102 citral proved to have the best antifungal activity against P. digitatum and P. italicum, among the tested components including nonanal, citral, α-pinene, myrcene, α-phellandrene, and D-limonene. Souza et al.2 determined the antifungal activity of different phytochemicals from lemon essential oils and found that citral, eugenol, and myrcene were fungitoxic. Overall, citral showed the best fungitoxicity. Wuryatmo et al.133 examined the inhibitory effects of vapor citral, its isomers geranial and neral, and related compounds (such as R-citronellal, S-citronellol, and citronellic acid) on P. digitatum, P. italicum, and Geotrichum candidum, the major fungi responsible for postharvest spoilage of citrus. They found that the inhibitory effect of citral and its isomers differed among the three fungi, and citral was the most effective one even at lower concentrations. The above studies showed that citral and its isomers likely played important roles in the antifungal activities of CEOs, with citral having the most significant role. Recently, more and more studies have suggested that limonene played an important role in the antifungal activity of CEOs.3,16,20,89,92,93,103 Singh et al.19 studied both CEOs and their major component limonene for their antifungal activity and found that limonene showed a better effect against A. f lavus compared to the whole oils, even at lower concentrations. Mahdavi et al.134 compared the antifungal effects of limonene and orange peel extract and found that limonene (S)-(−) isomer had better antifungal effect than its (R)-(−) isomer, whereas orange peel extract did not show any antifungal activity against the tested fungi. In addition, several studies have showed that limonene also had inhibitory activity against a wide range of fungi, including A. niger, P. digitatum, Rhizoctonia solani, Fusarium oxysporum, and Fusarium verticillioides, compared to other monoterpenes.135,136 On the basis of the studies mentioned above, we can conclude that limonene has a higher antifungal activity against a wide range of fungi than other terpenoids and it is most likely one of the major contributors to the fungitoxicity of the CEOs. The fungitoxicity of CEOs may be determined by their complex chemical compositions and the concentration profiles

of the volatile compounds of CEOs, mainly terpenoids, especially monoterpenes and sesquiterpenes.108−113 In the following, the antifungal effective components in CEOs (Tables 3 and 4) and their suggested mechanisms of action are reviewed. Antifungal Activity of Flavonoids in CEOs. Flavonoids are a group of polyphenolic compounds that include flavanone, flavone and polymethoxy flavone aglycones, flavanone- and flavone-O-glycosides, and flavone-C-glycosides.114 Citrus flavonoids have been reported to have many biological activities, such as antioxidant, antimicrobial, and anti-inflammatory properties.114−119 The antifungal activity of citrus flavonoids has been investigated by many authors in the past decades. To our knowledge, citrus flavanones including naringin, hesperidin, neohesperidin, eriodictyol, prunin, and hesperitin glucoside116,120,121 and polymethoxylated flavones such as sinensetin, nobiletin, heptamethoxy flavone, quercetogetin, and tangeretin107,120,122 have been reported to have antifungal activity. The research conducted by Ortuño et al.120 found that polymethoxylated flavones were more active than the flavanones, with nobiletin being the most effective one. The polymethoxylated flavones in CEOs have also been examined for their antifungal activity. Del Rı ́o et al.107 reported that sinensetin, nobiletin, heptamethoxyflavone, quercetogetin, and tangeretin could confer resistance against Phytophthora citrophthora, P. digitatum, and Geotrichum species. Almada-Ruiz et al. 123 found that 3,5,6,7,3′,4′-hexamethoxyflavone, 3,5,6,7,8,3′,4′-heptamethoxyflavone, 5,6,7,8,4′-pentamethoxyflavone, and 5,6,7,8,3′,4′-hexamethoxyflavone were effective in inhibiting mycelial growth of Colletotrichum gloeosporioides (Penz) Penz & Sacc, a major plant pathogen of fruits that causes significant damage to crops in tropical, subtropical, and temperate regions. These studies suggested that the polymethoxylated flavones in CEOs could be involved in the antifungal activity; however, this postulation was not convincing as polymethoxylated flavones occurred at low levels in CEOs. Another reason that polymethoxylated flavones were not suggested as the major antifungal component is that the citrus essential oil vapors have been reported to have antifungal activity,95 and polymethoxylated flavones were not detected in the vapor state of CEOs. The antifungal activity of the flavonoids in CEOs still needs to be clarified. Antifungal Activity of Terpenoids in CEOs. Terpenoids are a group of secondary metabolites in higher plants and are believed to have evolved in defense against herbivores and pathogens. Terpenoids, especially sesquiterpenes and monoterpenes, have been considered to be the most possible antifungal candidates in CEOs.92,124 Caccioni and Guizzardi124 found citrus oxygenated monoterpenes exhibited the highest antifungal activity among examined compounds. Caccioni et al.92 reported that there was a positive correlation between the 3022


3023

monoterpene

(S)-(+)-limonene

monoterpene

monoterpene

monoterpene

monoterpene

citral

citral

citral

citral vapor

monoterpene

monoterpene

(R)-(+)-limonene

D-limonene

monoterpene

limonene

monoterpene

monoterpene

limonene

DL-limonene

monoterpene

terpenes limonene

phytochemicals in CEO

type

agar well diffusion, paper disc diffusion agar well diffusion, paper disc diffusion

agar well diffusion, paper disc diffusion agar well diffusion, paper disc diffusion agar well diffusion, paper disc diffusion agar well diffusion, paper disc diffusion

poisoned food assay poisoned food technique poisoned food technique agar diffusion test agar diffusion test plate plate plate plate plate

AFST-EUCASTb AFST-EUCAST agar diffusion test agar diffusion test agar diffusion test

Aspergillus sp. Candida albicans

Aspergillus niger Penicillium sp. Aspergillus sp. Candida albicans

Aspergillus f lavus Penicillium italicum Penicillium digitatum Penicillium digitatum Penicillium italicum Aspergillus niger Aspergillus f lavus Fusarium spp. Penicillium spp. Rhizopus spp. Aspergillus f umigatus Candida krusei Penicillium digitatum Penicillium italicum Geotrichum candidum

procedure procedure procedure procedure procedure

agar well diffusion, paper disc diffusion

Penicillium sp.

diffusion diffusion diffusion diffusion diffusion

agar well diffusion, paper disc diffusion

Aspergillus parasiticus

Aspergillus f lavus

Aspergillus niger

test method modified semisolid agar antifungal susceptibility method agar diffusion method; broth microdilution agar diffusion method; broth microdilution

effective against Fusarium verticillioides

Table 4. Antifungal Activity of Citrus-Derived Compounds

Souza Souza Souza Souza Souza

et et et et et

al. al. al. al. al.

(2005) (2005) (2005) (2005) (2005)

Wuryatmo et al. (2003) Wuryatmo et al. (2003) Wuryatmo et al. (2003)

(v/v) (v/v) (v/v) (v/v) (v/v)

effective at 15 μL/L effective at 2−6 μL/L effective at 15 μL/L

0.5% 0.5% 0.5% 2.0% 8.0%

Mesa-Arango et al. (2009) Mesa-Arango et al. (2009)

= = = = =

MIC = 78 μg/mL MIC = 270.8 μg/mL

MIC MIC MIC MIC MIC

Tao et al. (2013) Tao et al. (2013)

42.84% inhibition at 1.519 μL/mL 53.2% inhibition at 24.296 μL/mL


Singh et al. (2010)

Mahdavi et al. (2011)





inhibition zone = 5.5 mm (30 μL) for agar well diffusion method inhibition zone = 3.5 mm (30 μL) for paper disc diffusion method inhibition zone = 15 mm (30 μL) for agar well diffusion method inhibition zone = 9.5 mm (30 μL) for agar well diffusion method





MIC = 3.15 mg/mL MFC = 3.60 mg/mL

inhibition zone = 9 mm (30 μL) for agar well diffusion method inhibition zone = 3 mm (30 μL) for agar well diffusion method inhibition zone = 7.5 mm (30 μL) for agar well diffusion method inhibition zone = 4 mm (30 μL) for agar well diffusion method

Dambolena et al. (2008) Rammance and Hongpattarakere (2011) Rammance and Hongpattarakere (2011)

a

reference

MIC = 2.70 mg/mL MFC = 3.15mg/mL

MIC = 1000 mL/L

effect

Journal of Agricultural and Food Chemistry Review


3024

monoterpenoid

monoterpenoid

monoterpenoid alcohol monoterpenoid alcohol

citronellal

citronellal

terpinen-4-ol

from clementine oil

monoterpene monoterpene

β-citronellal

flavonoids polymethoxylated flavones

monoterpenoid

citronellal

monoterpene

myrcene

monoterpenoid

monoterpene phenol

thymol

citronellal

monoterpene

eugenol

monoterpene monoterpene

monoterpene

neral vapor

β-myrcene

monoterpene

type

geranial vapor


Table 4. continued

plate plate plate plate modified semisolid agar antifungal susceptibility plate diffusion procedure plate diffusion procedure

Aspergillus f lavus Penicillium spp. Fusarium spp. Rhizopus spp. Fusarium verticillioides

Fusarium spp. Rhizopus spp.

poisoned food technique poisoned food technique

Penicillium italicum Penicillium digitatum

agar diffusion test



Phytophthora citrophthora


Aspergillus f lavus





Aspergillus f lavus




procedure procedure procedure procedure

agar diffusion test agar diffusion test agar diffusion test

Penicillium digitatum Penicillium italicum Geotrichum candidum diffusion diffusion diffusion diffusion

agar diffusion test agar diffusion test agar diffusion test

test method

Penicillium digitatum Penicillium italicum Geotrichum candidum

effective against

2.0% 4.0% 4.0% 4.0%

(v/v) (v/v) (v/v) (v/v)

et et et et

al. al. al. al.

(2005) (2005) (2005) (2005)

Del Rı ́o et al. (1998)



72% inhibition

Rammance and Hongpattarakere (2011)






Souza et al. (2005) Souza et al. (2005)

Dambolena et al. (2008)

Souza Souza Souza Souza

MIC = 3.60 mg/mL; MFC = 4.05 mg/mL



MIC = 4.05 mg/ML; MFC = 4.05 mg/mL



inhibition halo =12 mm inhibition halo =11 mm

MIC = 1000 mL/L

= = = =


effective at 15 μL/L effective at 15 μL/L effective at 15 μL/L MIC MIC MIC MIC


reference

effective at 15 μL/L effective at 15 μL/L effective at 15 μL/L

effect



3025

flavanone glucoside

polymethoxylated flavone

hesperidin

neohesperidin

polymethoxylated flavone

nobiletin

flavanone

polymethoxylated flavones (from orange essential oil)

5,6,7,8,3′,4′hexamethoxyflavone

naringin


5,6,7,8,4′pentamethoxyflavone

flavanone


3,5,6,7,8,3′,4′heptamethoxyflavone

naringin


3,5,6,7,3′,4′hexamethoxyflavone

flavanone

from sour orange oil

polymethoxylated flavones

hesperidin

from sweet orange oil

type

polymethoxylated flavones


Table 4. continued

agar diffusion test agar agar agar agar

agar dilution method agar dilution method agar dilution method

Penicillium digitatum Fusarium semitectum Penicillium expansum Aspergillus parasiticus Aspergillus f lavus Fusarium semitectum Penicillium expansum Aspergillus parasiticus

dilution dilution dilution dilution

method method method method

method method method method

agar diffusion test



agar diffusion test

Colletotrichum gloeosporioides (Penz) Penz & Sacc

agar agar agar agar

agar diffusion test


Fusarium semitectum Penicillium expansum Aspergillus parasiticus Aspergillus f lavus

agar diffusion test


agar diffusion test

agar diffusion test agar diffusion test

Penicillium digitatum Geotrichum sp.


agar diffusion test


agar diffusion test

agar diffusion test agar diffusion test

Penicillium digitatum Geotrichum sp.


agar diffusion test


test method agar diffusion test agar diffusion test

effective against Penicillium digitatum Geotrichum sp.

reference

Almada-Ruiz et al. (2003)

100% inhibition at 100 μL/mL

inhibition inhibition inhibition inhibition

at at at at

0.25 0.25 0.25 0.25

mM mM mM mM

inhibition inhibition inhibition inhibition

at at at at

0.25 0.25 0.25 0.25

mM mM mM mM 50% inhibition at 0.25 mM 44% inhibition at 0.25 mM 38% inhibition at 0.25 mM

29% 22% 41% 41%

25% inhibition after 100 h


39% 11% 33% 33%


et et et et

al. al. al. al.

(2011) (2011) (2011) (2011)

et et et et

al. al. al. al.

(2011) (2011) (2011) (2011) Salas et al. (2011) Salas et al. (2011) Salas et al. (2011)

Salas Salas Salas Salas

Ortuño et al. (2006)


Salas Salas Salas Salas




effective at 100 μL/mL

100% inhibition at 100 μL/mL


effective at 100 μL/mL


Del Rı ́o et al. (1998) Del Rı ́o et al. (1998)




effect

77% inhibition 57% inhibition

100% inhibition


14% inhibition




Review

al. al. al. al.

(2011) (2011) (2011) (2011)

of their constituents. The terpenoids, especially citral and limonene, most likely play an important role in the antifungal activity of the CEOs. However, the total number of compounds in CEOs that have antifungal activity has not been defined yet. Furthermore, the antagonistic, synergistic, or additive antifungal activities of different components in CEOs on fungal species and/or strains have not yet been explored. Mechanism of Action of Antifungal Compounds in CEOs. The antifungal activities of CEOs against a wide range of fungal species and their potential active compounds have been clearly demonstrated, as can be seen from the studies mentioned above. However, the antifungal mechanism of the compounds in CEOs remains poorly understood. The difficulties for exploring the mechanism of action of the natural bioactive compounds have been summarized in detail in a previous review.137 Generally speaking, the antifungal effects of the natural products can be influenced by a wide variety of factors, such as the different quantitative and qualitative ratios of the compounds in essential oils, their target microorganisms, and the minimum inhibitory concentrations. In addition, the methods used to test the antifungal activities, including the procedures adopted for the extraction, diffusion, and dilution of the substances, can also have an effect. In addition, the different components of an essential oil can have antagonistic, synergistic, or additive effects on microbial cells, which can influence their overall antifungal activity. To solve these problems, Caccioni et al.92 proposed a holistic approach to explore the antifungal mechanism of CEOs, and found that the antifungal performances of CEOs could be the result of a certain quantitative balance of various components. Many papers have suggested that the cell membrane is the possible target of bioactive volatile compounds because of the fact that essential oils are mixtures of molecules characterized by their poor solubility in water and high hydrophobicity.1,17,83,95 Several studies have showed that terpenes and phenolic compounds can disrupt the membrane of both fungi and bacteria.138,139 Terpenes have been suggested to have the ability to disrupt and penetrate the bacterial cell wall, which can lead to the denaturing of proteins and destruction of the cell membrane.17 The antimicrobial activity of the active compounds in essential oils can be explained by the lipophilic character of the monoterpenes contained in the oils. Monoterpenes act by disrupting the microbial cytoplasmic membrane, resulting in the loss of membrane impermeability. If the disturbance of membrane integrity occurs, then its functions are compromised not only as a barrier but also as a matrix for enzymes and as an energy transducer.137,139−142 In a more recent study by Tao et al.,143 the antifungal activity of mandarin essential oils against P. italicum and P. digitatum was attributed to the monoterpenes in the oils, such as limonene, octanal, and citral. They also suggested that mandarin essential oils generated cytotoxicity by disrupting cell membrane integrity, causing the leakage of cell components. Generally, the antimicrobial mechanism of action of the bioactive compounds of essential oils can be explained by the degradation of the cell wall, the disruption of cytoplasmic membrane, or membrane proteins (Figure 1).17,144 This leads to cytoplasmic leakage, cell lysis, and eventually cell death. However, the exact mechanism of the antimicrobial action of the compounds in essential oils remains poorly characterized, and further studies on the antifungal mechanism of the active compounds in CEOs are especially needed.

a

MFC, minimum fungicidal concentration. bAFST-EUCAST, Antifungal Susceptibility Testing Subcommittee of the European Committee on Antibiotic Susceptibility Testing.

et et et et Salas Salas Salas Salas mM mM mM mM 0.25 0.25 0.25 0.25 at at at at inhibition inhibition inhibition inhibition flavanone glucoside prunin


method method method method agar agar agar agar Fusarium semitectum Penicillium expansum Aspergillus parasiticus Aspergillus f lavus

29% 44% 38% 41%

(2011) (2011) (2011) (2011)

reference

al. al. al. al. et et et et Salas Salas Salas Salas mM mM mM mM 0.25 0.25 0.25 0.25 at at at at inhibition inhibition inhibition inhibition 43% 33% 38% 41% flavanone glucoside hesperetin glucoside


method method method method agar agar agar agar Fusarium semitectum Penicillium expansum Aspergillus parasiticus Aspergillus f lavus

41% inhibition at 0.25 mM

effect test method

agar dilution method Aspergillus f lavus

effective against type phytochemicals in CEO

Table 4. continued

Salas et al. (2011)


3026



Review

Use of CEOs in Fresh or Fresh-Cut Food Production. Food spoilage fungi can produce mycotoxins and cause food decay, which causes considerable economic losses and constitutes a health risk for consumers. Following the natural food preservation trends, research has been focused on the effect of essential oils on microbial inhibition of fresh and freshcut products in recent years. Plant essential oils stand out as an excellent alternative to chemical preservatives to extend the foodstuffs’ shelf life, owing to their antimicrobial properties against both food pathogens and food spoilage organisms, as well as their aromas and flavors. In a previous review by Fisher and Phillips,17 the applications of CEOs in different kinds of food including fish, meat, dairy products, fruits, and vegetables to control fungi spoilage and mycotoxin production were summarized. They concluded that CEOs could fulfill the requirements of both the food industry and the consumer for natural antimicrobials. With fresh-cut fruit and vegetable salads becoming more and more popular among consumers, the fresh-cut industry has become one of the most successful businesses within the foodprocessing industry in recent years. However, fruit decay and loss of quality caused by microbial growth, including Pseudomonas spp., E. herbicola, E. agglomerans, lactic acid bacteria, molds, and yeasts, seriously limit the safety and shelf life of fresh-cut fruits and vegetables.151 In addition, the sensorial appeal of fresh-cut fruits and vegetables, such as flavor and aroma, is another major indicator of shelf life and freshness from the view of consumers. The studies mentioned above showed that essential oils can serve as candidates to solve these problems owing to their antimicrobial activity and aroma nature. Ayala-Zavala and his colleagues151 summarized the successful and unsuccessful uses of essential oils and their combinations for enhancing safety, aroma, and appearance of fresh-cut fruits and vegetables. For example, oregano and thyme essential oils exhibited excellent antimicrobial and sensorial efficacy in fresh-cut lettuce and carrots.152 However, and according to their study, most of the present research has focused on the antibacterial effects of plant essential oils in fresh-cut fruits and vegetables, whereas the antifungal efficacy of plant essential oils, especially CEOs, have not been well investigated in the current literature. Although plant essential oils including CEOs can be used as alternative food preservatives for improving the quality and sensorial appeal of fresh-cut fruits and vegetables, it needs to be pointed out that the antifungal compounds derived from plants may impart a strong flavor to the food they applied to, thus restricting their applicability to only those products with compatible flavor. In view of this problem, researchers have proposed different ideas, such as using the plant extract not only as a preservative but also as a flavor component or applying only some of the most active components rather than the whole extracts.1 In a word, in this field there is still a lot of work that needs to be done. Use of CEOs in Edible Coatings of Fruits during Storage. Recently, the use of essential oils in edible coatings has become one of the most important practices in preserving fruit quality during storage.1,153 More and more research has shown that bioactive edible coatings enriched with essential oils exhibited excellent antimicrobial effects while maintaining fruit qualities.154−156 The advantages and limitations of this promising technology were discussed in the review by Sánchez-González et al.153 According to their research, the major advantage of this technology was that the edible coatings

Figure 1. Possible targets or mechanisms of action of antimicrobial compounds of essential oils. The antimicrobial mechanism of the bioactive compounds of essential oils can be explained by the degradation of the cell wall or the disruption of cytoplasmic membrane or membrane proteins, which lead to cytoplasmic leakage, cell lysis, and eventually cell death.

■

APPLICATIONS OF CEOS IN THE FOOD INDUSTRY Use of CEOs for Postharvest Disease Control. Alternative measures have been developed for crop protection, including biological agents, mineral salts, and plant extracts, as the use of synthetic fungicides in crops and trees can result in problems such as environmental pollution, phytotoxicity, and selection of resistant pathogen populations.145 Of various biological approaches, the use of plant essential oils as fungicides for postharvest disease control is becoming popular throughout the world.146,147 Several plant essential oils, such as thyme and lemongrass oils, have been demonstrated to be effective in stopping disease development caused by plant pathogens.99,148−150 For example, Plotto et al.149 explored the potential of several plant essential oils as natural postharvest disease control of tomato (Lycopersicon esculentum) and found that emulsions of oils of thyme and oregano at 5000 and 10000 ppm when used as dip treatments reduced disease development in tomatoes inoculated with Botrytis cinerea and Alternaria arborescens. Both in vitro and on food assessments of CEOs have been performed to explore their potential as alternative fungicides to prevent or control postharvest disease.3,22,96,97,103 Kuate and his colleagues97 studied the effects of 22 varieties of citrus essential oils on in vitro growth and sporulation of Phaeoramularia angolensis, causing citrus leaf and fruit spot disease, and found that both pummelo and grapefruit oils were very effective against it. Lazar-Baker et al.96 found lemon essential oils exhibited the strongest antifungal activity among tested oil samples in controlling brown rot caused by postharvest pathogen Monilinia fructicola in nectarines. In addition, in a recent study performed by Vitoratos et al.,98 lemon essential oils were found to be very effective in controlling disease severity of infected fruits by Botrytis cinerea in tomatoes, strawberries, and cucumbers. Taken together, these studies suggested that CEOs have the potential to replace synthetic fungicides in the management of postharvest diseases of fruits and vegetables. 3027



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synergistic, or additive effects of different components of CEOs will be likely the focus of future studies. Moreover, the antifungal mechanism of action of CEOs and their active components need further investigation. Finally, more on food studies in combination with commercial application trials would be necessary before CEOs can be applied fully as natural fungicides in the future food industry.

can gradually release those antimicrobial compounds in essential oils over time, maintaining a proper concentration of antimicrobial components on the product surface during the storage period. CEOs have been applied in the edible films of oranges and papaya fruits during storage to extend their shelf life.3,157 In addition, Sánchez-González et al.156 applied bergamot essential oil to biodegradable coatings based on hydroxypropylmethylcellulose or chitosan for cold-stored grapes as an environmentally friendly, healthy treatment to better preserve fresh fruit quality and safety during postharvest cold storage. In their study, chitosan coatings containing bergamot oil were found to be more effective than pure hydroxypropylmethylcellulose and chitosan coatings owing to their highest antimicrobial activity and the greatest control of respiration rates. Besides the whole essential oils mentioned above, some individual compounds in CEOs have also been applied to food to explore their antifungal potential. In a series of subsequent semicommercial and commercial trials carried out by du Plooy et al.,158 excellent disease control was achieved with the amended essential oil coatings and terpenoid components such as D-limonene and R-(−)-carvone, whereas the overall fruit quality was maintained. More recently, Vu and his colleagues159 observed that coatings with limonene reduced the decay of strawberries at most time points during the experiment, compared to chitosan alone, peppermint coatings, or uncoated strawberries. They also reported that a limonene coating did not cause any phytotoxicity during the experiment, and the appearance of strawberries was not changed compared to other groups. The application of CEOs or their individual compounds in the edible film of coatings for foods eliminates the need for synthetic food preservatives, thereby complying with consumer preferences and organic requirements and reducing environmental pollution. However, several issues still need to be resolved such as the absorption of aromatic volatile constituents by the food product and altered sensory characteristics. In addition, the reactions of plant essential oils or their active compounds with lipids, proteins, carbohydrates, and other additives may result in an overall decrease in the activity of the antimicrobial compounds.160 Taken together, the efficacy of amended coatings as viable alternatives or supplements to existing fruit protection strategies needs to be demonstrated in more semicommercial and commercial trials taking into consideration all factors such as costs and legal and safety issues. In conclusion, CEOs have obvious in vitro and on food antifungal activities against a wide array of fungal species, and their fungitoxicity may be attributed to the chemical compositions, molecular structure, and concentrations of the bioactive compounds. Compared with the traditional food preservative, the application of CEOs can reduce environmental pollution, eliminate the need for synthetic fungicides, and make good use of the byproducts of the citrus-processing industry. In view of their good fungitoxic function, natural aromas and flavors, as well as their environmentally friendly property, CEOs are potentially an excellent alternative to traditional preservatives in developing highly efficient, safe, and economic fungicides for the future food industry. The fungitoxicity research of CEOs will be of great utility for the utilization of citrus byproducts and for postharvest disease control of fruits and vegetables in the agricultural industry. For a better application of the antifungal activity of CEOs, the antagonistic,

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AUTHOR INFORMATION

Corresponding Authors

*(L.W.S.) Mail: Plant Biology Division, The Samuel Roberts Noble Foundation, 2510 Sam Noble Parkway, Ardmore, OK 73401, USA. Phone: 1 (580) 224-6710. Fax: 1 (580) 224-6692. E-mail: [email protected]. *(Z.Z.) Mail: College of Horticulture and Landscape Architecture, Southwest University, Chongqing 400716, China. Phone: 86-23-68250229. Fax: 86-23-68251274. E-mail: [email protected]. Author Contributions

All authors reviewed the final manuscript. Funding

This work was supported by the Fundamental Research Funds for the Central Universities (XDJK2013A014), the China Scholarship Council (CSC), the National Natural Science Foundation of China (31171930), the Graduate Student Innovation Fund of Southwest University to L.J. (kb2011005), the Program for Chongqing Innovation Team of University (KJTD201333), and the “111” Project (B12006). L.J. and L.W.S. were supported by the Samuel Roberts Noble Foundation. L.W.S. was supported in part by National Science Foundation awards (1139489, 1024974, and 1124719). Notes

The authors declare no competing financial interest.

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ABBREVIATIONS USED CEOs, citrus essential oils; MIC, minimum inhibition concentration

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REFERENCES

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Activity antifungal of the essential oils; aqueous and ethanol extracts from Citrus aurantium L.

Antimicrobial and Antifungal Activity of Pelargonium roseum Essential Oils.

Antimutagenic and antioxidant activity of the essential oils of Citrus sinensis and Citrus latifolia.

Antimycotic Activity and Genotoxic Evaluation of Citrus sinensis and Citrus latifolia Essential Oils.

Essential Oils from the Malaysian Citrus (Rutaceae) Medicinal Plants.

Antifungal Effect of Plant Essential Oils on Controlling Phytophthora Species.

The antibacterial and antifungal activity of essential oils extracted from Guatemalan medicinal plants.

Antifungal activity of essential oils from Iranian plants against fluconazole-resistant and fluconazole-susceptible Candida albicans.

Antifungal activity of various essential oils against Rhizoctonia solani and Macrophomina phaseolina as major bean pathogens.

Antifungal activity of chemically different essential oils from wild Tunisian Thymus spp.

Screening the antifungal activity of essential oils against decay fungi from palmyrah leaf handicrafts.

In vitro and in vivo activity of essential oils against major postharvest pathogens of Kinnow (Citrus nobilis × C. deliciosa) mandarin.

Chemical composition of the essential oils isolated from peel of three citrus species and their mosquitocidal activity against Culex pipiens.

Chemical Profile, Antibacterial and Antioxidant Activity of Algerian Citrus Essential Oils and Their Application in Sardina pilchardus.

Anti-Inflammatory Properties and Chemical Characterization of the Essential Oils of Four Citrus Species.

Effect of second cooling on the chemical components of essential oils from orange peel (Citrus sinensis).

Antifungal activity and chemical composition of twenty essential oils against significant indoor and outdoor toxigenic and aeroallergenic fungi.

genotoxicity to human HEL 12469 cells.

Fumigant antifungal activity of Corymbia citriodora and Cymbopogon nardus essential oils and citronellal against three fungal species.

Antibacterial and Antifungal Activity of Essential Oils against Pathogens Responsible for Otitis Externa in Dogs and Cats.

Traditional Small-Size Citrus from Taiwan: Essential Oils, Bioactive Compounds and Antioxidant Capacity.

Application of Volatile Antifungal Plant Essential Oils for Controlling Pepper Fruit Anthracnose by Colletotrichum gloeosporioides.

Chemical composition, phytotoxic and antifungal properties of Ruta chalepensis L. essential oils.

Chemical Composition, Antifungal and Antioxidant Activities of Hedyosmum brasiliense Mart. ex Miq. (Chloranthaceae) Essential Oils.