Food Applications of Natural Antimicrobial Compounds

REVIEW ARTICLE
published: 08 August 2012

doi: 10.3389/fmicb.2012.00287
Food applications of natural antimicrobial compounds

Annalisa Lucera , Cristina Costa , Amalia Conte and Matteo A. Del Nobile*
Lab of Food Processing and Packaging, Department of Food Science, Agricultural Faculty, University of Foggia, Foggia, Italy
Edited by: In agreement with the current trend of giving value to natural and renewable resources, the
Mirian A. F. Hayashi, Universidade use of natural antimicrobial compounds, particularly in food and biomedical applications,
Federal de São Paulo, Brazil
becomes very frequent. The direct addition of natural compounds to food is the most
Reviewed by:
common method of application, even if numerous efforts have been made to find
Rikke L. Meyer, Aarhus University,
Denmark alternative solutions to the aim of avoiding undesirable inactivation. Dipping, spraying,
Dmitri Debabov, NovaBay and coating treatment of food with active solutions are currently applied to product prior
Pharmaceuticals, USA to packaging as valid options. The aim of the current work is to give an overview on the
Antonio Bevilacqua, University of
Foggia, Italy
use of natural compounds in food sector. In particular, the review will gather numerous
case-studies of meat, fish, dairy products, minimally processed fruit and vegetables, and
*Correspondence:
Matteo A. Del Nobile, Lab of Food cereal-based products where these compounds found application.
Processing and Packaging,
Department of Food Science, Keywords: antimicrobial compounds, food preservation, natural compounds, essential oils, shelf-life extension
Agricultural Faculty, University of
Foggia, Via Napoli 25, 71122 Foggia,
Italy.
e-mail: ma.delnobile@unifg.it
INTRODUCTION activity for a long period of time (Appendini and Hotchkiss, 2002;
Many food products are perishable by nature and require protec- Hanušová et al., 2009).
tion from spoilage during their preparation, storage, and distri- Main natural compounds are essential oils derived from plants
bution to give them desired shelf life. The demand for minimally (e.g., basil, thyme, oregano, cinnamon, clove, and rosemary),
processed, easily prepared, and ready-to-eat fresh food products, enzymes obtained from animal sources (e.g., lysozyme, lacto-
globalization of food trade, and distribution from centralized ferrin), bacteriocins from microbial sources (nisin, natamycin),
processing pose major challenges for food safety and quality. Food organic acids (e.g., sorbic, propionic, citric acid) and naturally
products can be subjected to contamination by bacteria and fungi. occurring polymers (chitosan). In this context, plant essential
Many of these microorganisms can cause undesirable reactions oils are gaining a wide interest in food industry for their poten-
that deteriorate flavor, odor, color, sensory, and textural prop- tial as decontaminating agents, as they are Generally Recognized
erties of foods. Microbial growth is a major concern because as Safe (GRAS). The active components are commonly found
some microorganisms can potentially cause food-borne illness. in the essential oil fractions and it is well established that most
In packaged foods, growth and survival of common spoilage of them have a wide spectrum of antimicrobial activity, against
and pathogenic microorganisms such as Listeria monocytogenes, food-borne pathogens and spoilage bacteria (Gutierrez et al.,
Escherichia coli O157, Salmonella, Staphylococcus aureus, Bacillus 2008, 2009). The antimicrobial activity of plant essential oils is
cereus, Campylobacter, Clostridium perfringens, Aspergillus niger, due to their chemical structure, in particular to the presence of
and Saccharomyces cerevisiae are affected by a variety of intrinsic hydrophilic functional groups, such as hydroxyl groups of pheno-
factors, such as pH and presence of oxygen or by extrinsic factors lic components and/or lipophilicity of some essential oil compo-
associated with storage conditions, including temperature, time, nents (Dorman and Deans, 2000). Usually, the compounds with
and relative humidity (Singh et al., 2003; Lòpez-Malo et al., 2005; phenolic groups as oils of clove, oregano, rosemary, thyme, sage,
Rydlo et al., 2006). and vanillin are the most effective (Skandamis et al., 2002). They
To prevent growth of spoilage and pathogenic microorganisms are more inhibitory against Gram-positive than Gram-negative
in foods, several preservation techniques, such as heat treatment, bacteria (Mangena and Muyima, 1999; Marino et al., 2001).
salting, acidification, and drying have been used in the food Allyl-isothiocyanate is the major antimicrobial component of
industry (Davidson and Taylor, 2007; Farkas, 2007). Numerous mustard and horseradish oil. It has been found to be more effec-
efforts are conducted to find natural alternatives to prevent bac- tive against Gram-negative bacteria with less or no effect on lactic
terial and fungal growth in foods. In recent years, because of acid bacteria. Although its antimicrobial activity varies widely
the great consumer awareness and concern regarding synthetic (Delaquis and Mazza, 1995), the volatile compound particularly
chemical additives, foods preserved with natural additives have inhibits E. coli (Nadarajah et al., 2002; Muthukumarasamy et al.,
become very popular. To inhibit growth of undesirable microor- 2003).
ganisms in food, the antimicrobials can be directly added into the The use of bacteriocin-producing lactic acid bacteria or
product formulation, coated on its surface or incorporated into their more or less purified bacteriocins has been also receiving
the packaging material. Direct incorporation of active agents into increased interest. Bacteriocins are small bacterial peptides that
food results in an immediate but short-term reduction of bacte- show strong antimicrobial activity against closely related bacteria.
rial populations, while the antimicrobial films can maintain their Nisin is a polypeptide produced by Lactococcus lactis spp. It has
www.frontiersin.org August 2012 | Volume 3 | Article 287 | 1

Lucera et al. Natural antimicrobial compounds
been approved as a food additive with GRAS status in over 50 Chitosan has also been documented to possess a film-forming
countries worldwide. It has a relatively broad spectrum of activity property for use as edible film or coating, to decrease water vapor
against various lactic acid bacteria and other Gram-positive bac- and oxygen transmission, diminish respiration rate and increase
teria. Moreover, it is particularly effective against heat-resistant shelf life of fruit (Jiang and Li, 2001).
bacterial spores of Clostridium botulinum and against food-borne This review focuses on the use of natural compounds to
pathogens such as L. mococytogenes, S. aureus, or B. cereus (Brewer control microbiological and physicochemical shelf life of main
et al., 2002; Lopez-Pedemonte et al., 2003; Sobrino-Lopez and food categories, such as meat, fish, dairy products, minimally
Martin-Belloso, 2006). Use of nisin in conjunction with ethylene- processed fruit and vegetables and cereal-based goods. The infor-
diamine tetra-acetic acid (EDTA) may increase the effectiveness. mation is mostly based on case-studies dealing with application
Moreover, the effect of nisin can be enhanced by using exposure of active compounds to prevent microbial proliferation occurring
to chelating agents, sub-lethal heat, osmotic shock and freezing, in packaged food during storage.
because these treatments make the cell wall of Gram-negative
microorganisms more permeable and therefore more susceptible MINIMALLY PROCESSED FOOD AND VEGETABLES
to the nisin (Gálvez et al., 2007). JUICES
The enzymes represent another group of natural com- Minimally processed products are one of the major growing seg-
pounds that found application in food as valid preservatives. ments in food retail establishments. However, fresh-cut fruit and
Lysozyme for example, is a lytic enzyme found in foods, such vegetables are widely studied because of the difficulties in preserv-
as milk and eggs, which can hydrolyze β-1,4 linkages between ing their fresh-like quality during prolonged periods. The goal
N-acetylmuramic acid and N-acetylglucosamin (Cunningham of fresh-cut products is to deliver convenience and high quality.
et al., 1991). Commercially, lysozyme has been used primarily to Taking into account the pressure of consumers about the use of
prevent late blowing in semi-hard cheeses, caused by Clostridium synthetic chemicals, natural compounds have been suggested as
tyrobutyricum. It is well known that lysozyme is bactericidal a valid preservation technique (Table 1). Dipping, impregnation,
against Gram-positive bacteria, whereas it is essentially ineffec- coating, and spraying are the different ways of applications of
tive against Gram-negative bacteria, owing to the presence of active agents to fresh-cut fruit and vegetables but among them,
a lipopolysaccharide layer in the outer membrane. It has been the most recent results on the application of active compounds to
recognized since the 1960’s that susceptibility of Gram nega- ready-to-eat fruit and vegetables deal with coating systems. In the
tive bacteria to lysis by lysozyme can be increased by the use follow, some relevant examples are reported.
of membrane disrupting agents, such as detergents and chela- Malic acid in combination with various stabilizing compounds
tors (EDTA) (Vaara, 1992; Shelef and Seiter, 1993; Branen and was used by Raybaudi-Massilia et al. (2009) for fresh-cut apples.
Davidson, 2004). As reported by Bico et al. (2009), the combined effect of chemi-
Organic acids and their salts are widely used as chemical cal dip and/or edible coating and/or controlled atmosphere (CA)
antimicrobial agents because their efficacy is generally well under- on quality of fresh-cut banana was investigated. Banana slices
stood and cost effective. The most effective organic compounds were dipped into a solution containing 1% (w/v) calcium chlo-
are acetic, lactic, propionic, sorbic, and benzoic acid. Their ride, 0.75% (w/v) ascorbic acid, and 0.75% (w/v) cysteine and/or
antimicrobial effect is based on the increase in proton concentra- combined with a carrageenan coating and/or combined with CA
tion thereby lowering the external pH. Organic acids may affect (3% O2 + 10% CO2 ). Dipping combined with CA treatment
the integrity of microbial cell membrane or cell macromolecules prevented product weight loss and increased polyphenol oxidase
or interfere with nutrient transport and energy metabolism, caus- activity; regarding microbiological quality, the combined strate-
ing bactericidal effect (Ricke, 2003). Production of organic acids gies prevented microbial growth after 5 days of storage at 5◦ C.
had been possible before the discovery of microorganisms, with The antimicrobial effects of propionic, acetic, lactic, malic, and
lactic acid first being commercially produced by fermentation citric acid against E. coli O157:H7, S. Typhimurium, and L. mono-
in 1880, but the majority of the organic acids produced were cytogenes on whole red organic apples and lettuce were also clearly
being chemically extracted or synthesized from other chemicals. demonstrated by Park et al. (2011).
Mixtures of acids could exert a wider antimicrobial activity than Raybaudi-Massilia et al. (2008) investigated the combined
a single organic acid (Theron et al., 2010). effects of malic acid and essential oils of cinnamon, palmarosa,
Among the natural antimicrobials, chitosan also received con- and lemongrass (0.3 and 0.7%) and their main active com-
siderable interest for commercial applications. It has been used pounds (eugenol, geraniol, and citral, 0.5%) on microbiological
in medical, food, agricultural, and chemical industry, mainly due and physicochemical shelf-life of fresh-cut “Piel de Sapo” melon
to its high biodegradability and antimicrobial properties. The (Cucumis melo L.). The active compounds were incorporated into
biological activity of chitosan depends on its molecular weight, an alginate-based edible coating. Melon pieces were inoculated
degree of deacetylation and derivatisation, such as degree of sub- with a S. Enteritidis (108 CFU/ml) culture before applying the
stitution, length, and position of a substitute in glucosamine coating. The incorporation of essential oils or their active com-
units of chitosan, pH of chitosan solution and the target organ- pounds into the edible coating prolonged the microbiological
isms (No et al., 2007). It is commercially produced from crab shelf-life by more than 21 days. Pure citral and citron essen-
and shrimp shell wastes, with different deacetylation grades and tial oil were added in the syrup of industrial ready-to-eat fruit
molecular weights and, hence, it possess different functional salads stored at 9◦ C. Both citral (25–125 ppm) and citron essen-
properties, like emulsification ability, dye binding, and gelation. tial oil (300, 600, 900 ppm) were able to prolong the microbial
Frontiers in Microbiology | Antimicrobials, Resistance and Chemotherapy August 2012 | Volume 3 | Article 287 | 2
Table 1 | Relevant examples of natural active agents applied to minimally processed products.
Products and storage Natural compounds Main results References

conditions
Fresh-cut papaya stored in A microencapsulated beta-cyclodextrin The coating improved the microbiological and Brasil et al., 2012
trays at 4◦ C and trans-cinnamaldehyde complex physicochemical quality of fresh-cut papaya. It
(2 g/100 g) incorporated into a extended the shelf-life up to 15 days compared
multilayered edible coating made of to the control (<7 days)
chitosan and pectin
Cabbage packaged under Dipping treatment with acetic, lactic, Some pathogens inoculated on cabbage were Bae et al., 2011
vacuum, air and two MAP and malic acids (1% and 2%) significantly reduced by treatment with 2%
(100% N2 and 100% CO2 ) acetic, 1% lactic, and 2% malic acids
Minimally processed Edible coating based on chitosan and The coatings retard product weight loss, Ansorena et al., 2011
broccoli packaged in carboxymethyl-cellulose browning, and yellowing, reduced stem
multilayered polyolefin bags hardening, microbial growth, and improved
and stored at 5◦ C for total chlorophyll and ascorbic acid retention
18 days
Ready-to-eat lettuce and Dipping treatment with oregano and The solution containing oregano recorded a Gutierrez et al., 2009
carrots packaged in oriented thyme significantly lower initial total viable count level
polypropylene bags and than the water treatment on carrots. The
stored at 4◦ C sensory panel found essential oil treatments
acceptable for carrots throughout storage, but
no for lettuce rejected for overall appreciation
by day 7
Strawberries packaged Solution of 1% chitosan The chitosan coating inhibited growth of Campaniello et al., 2008
under passive and active microorganisms and significantly affected the
MAP with high (80% O2 , microbiological stability of the strawberries,
20% CO2 ) and low (65% N2 , above all when the samples were packaged
30% CO2 , 5% O2 ) under active MAP
percentage of oxygen
Fresh-cut mushrooms Coating containing 5, 10, and 20 g of At 4◦ C for 15 days, 20 g/L chitosan coating Hesham, 2008
packed in polyethylene bags chitosan/L inhibited growth of total bacteria, yeasts, and
and then stored at 4◦ C moulds
shelf-life. Citron essential oil doubled the time needed for the “Fuji” apples. During 21 days of storage at 4◦ C, the coating with
wild microflora to reach concentrations able to produce a per- vanillin (0.3% w/w) was the most effective in terms of sensory
ceivable spoilage in condition of thermal abuse (9◦ C). The same quality. All the other studied antimicrobial coatings significantly
essential oil showed a strong inhibition against L. monocytogenes, inhibited growth of psychrophilic aerobes, yeasts, and moulds.
but exerted limited effects on the survival of S. Enteritidis and The antimicrobial effect of essential oils against L. innocua inoc-
E. coli (Belletti et al., 2008). Generally, when applying bioactive ulated into apple pieces before coating was also tested. A release
coatings containing essential oils to fruits and vegetables, one of system of antimicrobial volatiles was adopted by encapsulation of
the limiting factors is the impact of such components on the sen- garlic oil in β-cyclodextrin and tested on microbial growth and
sory characteristics of the coated products, mainly due to the great sensory quality of fresh-cut tomato (Ayala-Zavala and González-
amount of volatile compounds which mask the natural flavor of Aguilar, 2010). Grape-fruit seed extract was used as antimicrobial
fruits and vegetables. The use of compatible essential oil-foodstuff compound into a coating of sodium alginate to prolong the shelf-
could also be a good alternative. life of minimally processed kiwifruits. The combination of an
Natural volatile compounds such as methyl jasmonate, active compound to an alginate-based coating delayed micro-
ethanol, tea tree oil, and garlic oil were applied on fresh-cut bial growth, whereas the sole dipping treatment was inefficient.
tomato stored at 5◦ C for 15 days. Ethanol combined with methyl The combined use of modified atmosphere packaging (MAP) and
jasmonate was more effective in suppressing microbial prolifera- coating treatments further prolonged the shelf-life up to 13 days
tion than each single compound. In addition, this combination (Mastromatteo et al., 2011a).
preserved firmness and color better than the other antimicro- As reported by Krasaekoopt and Mabumrung (2008), the
bial preservatives. Moreover, methyl jasmonate let keep higher effectiveness of chitosan incorporated in the edible methyl
content of lycopene, ascorbic acid and phenolic compounds cellulose coating on the microbiological quality of fresh-cut can-
(Ayala-Zavala et al., 2008). Rojas-Graü et al. (2007) investigated taloupe was evaluated. During storage at 10◦ C for 15 days, appli-
the effect of lemongrass, oregano oil, and vanillin incorporated in cations of 1.5 and 2% chitosan in the coating reduced growth of
apple puree-alginate edible coating, on the shelf-life of fresh-cut some pathogens, mesophilic aerobic bacteria (3.3 log cfu g−1 ),

psychrotrophs (3.9 log cfu g−1 ), lactic acid bacteria (3.1 log One solution to the above-mentioned problem may be the use of
cfu g−1 ), yeasts and molds (1.1 log cfu g−1 ), and total col- combinations of different food preservation systems that would
iforms (3.8 log cfu g−1 ). An edible coating containing chitosan give the benefits of each of them while at the same time appre-
was also applied on carrot sticks to maintain quality and pro- ciably reducing the amount of antimicrobial required. For this
long the shelf-life (Simões et al., 2009). The coating application reason, the application of moderate heat treatments and/or the
preserved the overall visual quality, the microbial proliferation preservation of the foodstuff in cold, refrigerated temperatures
and reduced surface whiteness during storage. While the con- may play a key role. By using this method, a stable and, from
tent of total phenolics markedly increased in coated carrot sticks a microbiological viewpoint, safe food can be produced with-
stored under moderate gas levels, it was controlled under low O2 out any loss in sensory quality. In this context various aroma
and high CO2 levels. Film based on methyl cellulose incorpo- compounds and citron essential oils containing citral, β-pinene,
rating chitosan and chitosan/methyl cellulose film incorporating limonene, linalool, and α-pinene, combined with mild heat
vanillin were applied to fresh-cut cantaloupe and pineapple to treatment, were used to inhibit the growth of S. cerevisiae in
control microbial quality during storage at 10◦ C (Sangsuwan non-carbonated soft drinks (Belletti et al., 2007).
et al., 2008). Chitosan/methyl cellulose film and vanillin films
provided an inhibitory effect against E. coli in fresh-cut can- DAIRY PRODUCTS
taloupe. The chitosan/methyl cellulose film rapidly reduced the Fresh dairy products are ready-to-eat foods easily contami-
number of S. cerevisiae inoculated on the products. For fresh-cut nated by undesirable microorganisms. Some of them are spoilage
pineapples coating with vanillin was more efficient than chi- microorganisms which may produce unwanted visual appearance
tosan/methyl cellulose in reducing the number of yeasts by 4 logs and diminish the commercial value of cheese, other ones are
in six days. An edible coating with soy or wheat gluten protein as a pathogens that affect product safety. Moreover, fungal spoilage
carrier of thymol and calcium chloride was applied on strawberry can also occur. Recently, some studies have recorded the effi-
by Atress et al. (2010). Treating fruits did not exhibit any change cacy of natural compounds, alone or in combination with other
in fruit appearance until 9 days of storage. All treatments main- preservation methods, when directly applied to milk (Cava et al.,
tained ascorbic acid content, firmness, total sugar and reduced 2007) or to cheese by spraying, immersing, or dusting the prod-
the total colony, moulds and yeasts compared to the control. ucts. Antimicrobials may also be spread onto the packaging
The effect of sodium hypochlorite, peroxiacetic acid, acidified materials that come in contact with the cheese or incorporated
sodium chlorite and carvacrol on microbiological, sensory, and into the plastic films used for packaging (Conte et al., 2007). A
nutritional quality of fresh-cut jalapeno peppers stored at 5◦ C brief overview of some recent examples of natural active agents
during 27 days was evaluated (Ruiz-Cruz et al., 2010). All sani- applied to cheese is reported.
tizers (except carvacrol) maintained microbiological and overall The effectiveness of lysozyme and EDTA on microbiolog-
quality of jalapeno peppers during 27 days. Carvacrol, active ical shelf life of mozzarella cheese was studied by Sinigaglia
ingredient of oregano essential oil, maintained shelf life for only et al. (2008). Mozzarella was packaged in a brine that con-
17 days and reduced sensory acceptability of fresh-cut produce. tained lysozyme (0.25 mg mL−1 ) and different amounts of EDTA
However, carvacrol-treated samples retained the highest levels of (10, 20, and 50 mmol L−1 ), and stored at 4 ± 1◦ C for 8 days. The
photochemical and antioxidant capacity. packaging system significantly inhibited growth of coliforms and
Juices are food very susceptible to yeasts attack. Pichia Pseudomonadaceae, without affecting the typical lactic acid bacte-
anomala, S. cerevisiae, and Schizosaccharomyces pombe caused ria. Conte et al. (2011) also evaluated the effects of lysozyme and
the most diffuse problems. Generally, heat treatment (pasteur- EDTA in burrata cheese packaged under MAP (95:5 CO2 :N2 ),
ization), aseptic packaging or use of weak acids exclude yeast thus demonstrating that these compounds were valid to prolong
spoilage. As alternative to these traditional artificial preservatives cheese shelf life, especially at high lysozyme concentrations.
the use of natural compounds was proposed in the literature Different release systems containing nisin and natamycin were
(Valero and Salmerón, 2003; Belletti et al., 2010). Clary, sage, also used in various works to create an additional hurdle for
juniper, lemon, and majoram essential oil were chosen to pre- spoilage microorganisms in dairy products. For example, edi-
serve apple juice, as being efficient in in vitro test and not ble coatings made of galactomannans incorporating nisin were
containing phenolics but alcohol terpenoids, linalool (clary sage), tested against L. monocytogenes in Ricotta cheese. The system
and terpinen-4-ol (marjoram), the cyclic monoterpenes α-pinene not only help in retarding the growth of L. monocytogenes but
(juniper) and limonene (lemon) (Tserennadmid et al., 2011). The also help in the maintenance of water content, therefore reduc-
anti-yeast effects of these essential oils were good in the acidic ing cheese weight loss (Martins et al., 2010). Cao-Hoang et al.
pH range optimal for yeasts growth. Synergism or additive effects (2010) used sodium caseinate-based films for incorporating nisin
were recorded by combining the different active compounds. to be active in mini red Babybel cheese. The active films affected
The most interesting result of the study of Tserennadmid et al. L. innocua inoculated on cheese surface. As reported by Ture et al.
(2011) was recorded with lemon essential oil. In fact, experiments (2011) natamycin was incorporated into wheat gluten and methyl
with lemon given to apple juices showed that the “open” stor- cellulose biopolymers and tested against A. niger and P. roque-
age time at ambient temperature could be prolonged and a novel, fortii inoculated on surface of fresh kashar cheese. In a study
refreshing taste could be achieved. conducted by Fajardo et al. (2010) natamycin was also used in
Although the influence of smell-taste of some active agents combination with chitosan. In particular, the effects of the chi-
is known, it has not often been evaluated to a sufficient degree. tosan coating containing natamycin (0.50 mg/mL) on semi-hard
cheese were assessed. The natamycin coated samples presented to yogurt (prepared from buffalo’s milk) (stored up to 20 days
a decrease of moulds and yeasts compared to the control after at 4 ± 1◦ C) at various concentrations (0.1–1.0 g L−1 ) were
27 days of storage. The effects of nisin, natamycin, and their effective in controlling spoilage microorganisms. Eleven essen-
combination into a cellulose polymer matrix were also studied tial oils were evaluated in vitro for their antibacterial properties
by dos Santos Pires et al. (2008). Films efficacy was first evalu- against Vancomycin-resistant Enterococci and E. coli O157:H7
ated in vitro and then on sliced mozzarella cheese. Best effects (Selim, 2011). The most active essential oils against bacteria were
were found when the two compounds were applied together on thyme oil, eucalyptus, juniper, and clove oils. Furthermore, their
cheese. effects were evaluated against the same microbial groups exper-
As regards the applications of essential oils, numerous exam- imentally inoculated in Feta soft cheese and stored at 7◦ C for
ples are reported in the literature (Table 2). The addition of 14 days. The addition of thyme oil at concentrations of 0.5
different concentrations of lemon extract in the brine of moz- and 1% caused a significant reduction in microbial growth. On
zarella and in a gel solution made up of sodium alginate was Feta cheese inoculated with E. coli O157:H7 and L. monocyto-
evaluated by Conte et al. (2007). Shelf-life tests were run at genes oregano and thyme (0.1 or 0.2 and 0.1 ml/100 g) com-
15◦ C to simulate thermal abuse. An increase in shelf-life of bined with MAP were also tested by Govaris et al. (2011). In
all active packaged mozzarella cheese was observed, confirm- the control Feta microbial strains survived up to 1 month of
ing that the investigated substance may exert an inhibitory storage. On the contrary, in Feta cheese treated with oils a
effect on the microorganisms responsible for spoilage, without significant reduction of microbial growth was found. The use
affecting the typical dairy microbial population. As reported by of chitosan, lemon, and sage extract in Fior di latte cheese
Otaibi et al. (2008), three essential oils, thyme, marjoram and was assessed by Gammariello et al. (2010). Different concentra-
sage, were added to concentrated yoghurt (labneh) at concen- tions of active substances were added during processing cow’s
trations of 0.2, 0.5, and 1.0 ppm. The better concentration of milk. Lemon extract and chitosan showed a good compromise
each essential oil was 0.2 ppm that allowed obtaining a shelf- between the antimicrobial effectiveness and the sensory impact
life up to 21 days. Singh et al. (2011) also added essential caused by their addition, thus promoting a satisfactory shelf
oils in yogurt. The anise volatile oil and its oleoresin added life increase (129%). In contrast, the addition of sage extract
Table 2 | Relevant examples of natural active compounds applied to dairy products.

conditions
West African soft cheese Treatment with eucalyptus oil and The treatment of eucalyptus oil 75% plus 25% Belewu et al., 2012
lemongrass oil lemon grass exerted a positive impact on the
nutritional, sensory, and microbial values of
West African soft cheese
Ricotta cheese stored under Coating with a chitosan/whey protein The chitosan/whey protein film slowed Di Pierro et al., 2011
modified atmosphere at 4◦ C edible film detrimental phenomena. The viable numbers of
lactic acid bacteria and mesophilic and
psychrotrophic microorganisms were
significantly lower in the chitosan/whey protein
coated cheese, compared to the control
Traditional Minas Serro Nisin Nisin was effective in reducing S. aureus count Pinto et al., 2011
cheese in Serro cheese. A reduction of 1.2 and 2.0 log
cycles in S. aureus count was observed from
the 7th day of ripening for cheese containing
100 IU mL−1 and 500 IU mL−1 of nisin,
respectively, compared with control sample
Fresh cheese Tosèla Antimicrobial compounds produced by Cheese showed higher concentrations of Settanni et al., 2011
six strains of non-starter lactic acid lactobacilli (7.90 log CFU/g) and streptococci
bacteria. In particular, Lactobacillus (6.10 log CFU/g), lower development of
paracasei NdP78 was also found to coliforms and staphylococci than control cheese
produce a bacteriocin
Caprese salad packaged Dipping with thymol (400 ppm) The combined use of thymol and MAP Bevilacqua et al., 2007
under MAP (65% N2 , decreased the coliform populations from 5.65 to
30% CO2 , and 5% O2 ) 4.23 log CFU/g and extended the microbiological
shelf-life from 3.77 to 12 days. It also decreased
the concentration of Pseudomonadaceae
Gorgonzola cheese Natamycin-incorporated film in the Films with 2 and 4% natamycin presented de Oliveira et al., 2007
production process of cheese satisfactory results for P. roquefortii inhibition

negatively affected the sensory properties, thus making the cheese MEAT-BASED PRODUCTS
unacceptable. Spoilage of meat products contributes to deterioration of texture
Pires et al. (2009) developed a microbial sachet incorporated and change in flavor and color. The use of natural antibacterial
with allyl-isothiocyanate. Its efficiency was tested against yeasts, compounds, such as extracts of spices and herbs, essential oils,
molds, Staphylococcus sp. and psychrotrophic bacteria in sliced organic acids, salts, and bacteriocins is reported in the literature
mozzarella cheese stored at 12◦ C ± 2◦ C. A reduction of 3.6 log to improve the shelf life of meat (Jamilah et al., 2008; Jałosńska
cycles was observed in yeasts and molds counts in the mozzarella and Wilczak, 2009). Some applications are reported in Table 3.
packed with the antimicrobial sachet over 15 days of storage time. Mastromatteo et al. (2011b) suggested the combined use of
The sachet also showed an antibacterial effect on Staphylococcus natural antimicrobials, such as lemon and thymol, and MAP to
sp.; however, psychrotrophic bacteria were very resistant. A new improve the shelf life of reduced pork back-fat content sausages.
dairy product “Karishcum” obtained by adding Curcuma Longa In particular, the application of thymol and thymol-MAP limited
(Curcumin or Turmeric) to classic Karish cheese at a rate of 0.3% the development of Pseudomonas spp., responsible for sausages’
(w/v) was realized in a study conducted by Hosny et al. (2011). unacceptability. The use of bay essential oil combined to MAP
A primary experiment was done to determine the correct per- without oxygen (20% CO2 —80%N2 ) was suggested to control
centage of Curcumin addition to cheese milk to get a good taste L. monocytogenes and E. coli growth and also to extend the
and a long shelf life. The behavior of pathogenic bacteria in the shelf life of naturally contaminated ground chicken meat (Irkin
artificially contaminated product during cold storage for 14 days, and Esmer, 2010). Moreover, the addition of essential oils of
revealed that addition of the extract (0.3%) determined a reduc- marjoram and rosemary to beef patties formulated with mechan-
tion of bacterial counts of about 1 log of S. Typhimurium and two ically deboned poultry meat at a concentration of 200 mg/kg
log of P. aeurogenosa and E. coli 0157:H7. reduced lipid oxidation and improved the sensory characteristics
Table 3 | Relevant examples of natural active agents applied to meat-based products.

conditions
Fresh minced beef Thymol (250, 500, 750 mg/Kg) Better effects on product quality were Del Nobile et al., 2009a
patties packaged under obtained for sample with increased amount of
MAP thymol, under MAP conditions (shelf life
about 7 days)
Minced beef mixed Sage essential oil (0.1, 0.3, and 0.5%) The highest concentration of essential oil Ahmed and Ismail, 2010
with soy-protein stored controlled development of main
at 4◦ C microorganisms
Meat-balls stored at 0.2% of cranberry, rosemary, and lovage Rosemary extract was the most effective on Jałosńska and Wilczak, 2009
10◦ C extracts product shelf life (13.3 days)
Sausages stored at Sodium lactate (0%, 0.6%, 1.2%, 1.8%) as Sodium lactate improved the microbiological Bingöl and Bostan, 2007
4◦ C under vacuum alternative to nitrite quality, extended shelf life, and exhibited a
conditions better antimicrobial effect than nitrite
Fresh sausage Oregano and marjoram essential oil Addition of oregano and marjoram essential Busatta et al., 2007, 2008
oil exerted a bacteriostatic effect
Broiler chicken wings Dipping treatment for 10 min with chlorine Samples treated with lactic acid alone Hecer and Guldas, 2011
stored at 4◦ C dioxide, lactic acid, and fumaric acid showed the most effective reduction on
E. coli and mesophylic bacteria
Fresh chicken meat Treatments with nisin and EDTA, alone or Chicken was better preserved under Economou et al., 2009
stored under MAP at in combination treatments with 500 IU/g of nisin and 50 mM
4◦ C of EDTA, even up to 24 days
Fresh beef Organic acids (citric, lactic, acetic, and Organic acids promoted a significant shelf life Jamilah et al., 2008
tartaric) extension
Fresh chicken sausage Rosemary or Chinese mahogany (500, Chinese mahogany and rosemary improved Liu et al., 2009
stored at 4◦ C 1000, 1500 ppm) meat quality
Turkey-bologna stored Coating with gelatin containing Nisaplin Both Nisaplin film and Guardian film Min et al., 2010
at 4◦ C and Guardian effectively inhibited L. monocytogenes
Meat pieces Combined application of oregano essential Combination of essential oils and organic de Souza et al., 2009
oil and acetic acid acids inhibited microbial growth and
proliferation of pathogens such as S. aureus
(Mohamed and Mansour, 2012). To reduce microbial growth acids improved lipid stability. The obtained results were enhanced
and to preserve the oxidative stability of mortadella, a Bologna- by packaging under MAP conditions.
type sausage, the addition of orange dietary fiber (1%), rosemary As regards bacteriocins, the combined use of lactoferrin and
essential oil (0.02%) and thyme essential oil (0.02%), combined nisin on naturally contaminated Turkish-style meat-balls was
with specific storage conditions, showed very desirable effects proposed. Treatment with lactoferrin alone and in combination
(Viuda-Martos et al., 2010, 2011). Antioxidant and antibacterial with nisin significantly reduced spoilage bacterial counts (total
effects of rosemary, orange, and lemon extracts was also investi- aerobic bacteria, coliform, E. coli, total psychrophilic bacteria,
gated in cooked Swedish-style meat-balls. Results indicated that Pseudomonas spp., yeast and molds) and extended shelf life to
significant advantages were obtained using rosemary and citrus 10 days (Colak et al., 2008). The synergistic antimicrobial activ-
extracts in rancidity-susceptible meat products; however, only ity of lysozyme, nisin, and EDTA against L. monocytogenes and
rosemary slightly reduced lactic acid bacteria (Fernàndez-Lòpez meat-borne spoilage bacteria in ostrich patties packaged in air
et al., 2005). Ayachi et al. (2007) reported that the addition of and vacuum was observed by Mastromatteo et al. (2010a). In par-
a mixture of organic acids (sodium lactate 90% and sodium ticular, the antimicrobial treatment was effective for controlling
acetate 10%) at different concentrations (from 0 to 20 g/Kg) growth of lactic acid bacteria even if it was not effective against
on Marguez sausages, made with lamb and beef, significantly Gram-negative bacteria.
reduced microbial cell loads during storage at 8◦ C.
Chitosan (0.5% and 1%) added individually or in combina- FISH-BASED PRODUCTS
tion with nitrites (150 ppm) as ingredients was tested to protect Fresh fish is a highly perishable product due to its biological
fresh pork sausages from microbial spoilage. Its application as composition. The main cause of deterioration is the activity of
active coating was demonstrated (Bostan and Isin-Mahan, 2011). spoilage seafood microorganisms that provoke loss of essential
Soultos et al. (2008) found chitosan active against total viable fatty acids, fat-soluble vitamins and protein functionality, pro-
count, lactic acid bacteria, Pseudomonas spp., B. thermosphacta, duction of biogenic amines, and formation of off-odors (Gram
Enterobacteriaceae, yeasts, and moulds. and Dalgaard, 2002).
Krisch et al. (2010) compared the antimicrobial effect of com- Literature widely demonstrates that treatments with natural
mercial herbs, spices and essential oils (fresh and dried garlic, compounds are effective preservation methods for fish prod-
onion, thyme, marjoram, and oregano) in minced pork. While ucts (Table 4). Different effects are generally exerted depending
fresh spices showed weak or no inhibition on viable cells of on the active agent used and on the characteristics of the raw
minced pork, some effects of essential oils were observed. Best material. Some examples are provided hereinafter. Erkan et al.
shelf life values were obtained for pork meat added with garlic (2011) proposed the use of thyme (1%) and laurel essential oil
and marjoram oil. Dipping of thyme and oregano oil in concen- (1%) to extend the shelf life of bluefish by about 3–4 days. The
trations of 0.1 and 0.3% were carried out to improve the shelf life quality of hot smoked rainbow trout packaged under vacuum
of meat-based products (Karabagias et al., 2011). The combina- and treated with thymol and garlic oil (1%) was also improved
tion of dipping and MAP extended the shelf life to about 22 days, (Erkan, 2012). Kykkidou et al. (2009) demonstrated that com-
against 7 days of the control sample packaged in air. bination of MAP and thyme essential oil (0.1%) resulted in a
A relevant preservation effect for fresh chicken breast meat, significant shelf life extension of fresh Mediterranean swordfish
stored at 4◦ C, was obtained by dipping meat in oregano oil, fillets. In particular, the addition of thyme essential oil extended
prior to packaging under MAP (Chouliara et al., 2007). Fratianni product shelf life (13 days) if compared to the control (8 days),
et al. (2010) also proposed use of thyme and balm essential whereas its combination to MAP conditions further prolonged
oils to decrease the natural microflora of chicken breast meat. product shelf life (about 20.5 days). Goulas and Kontominas
In particular, balm essential oil significantly limited growth of (2007) also showed that oregano essential oil (0.8 %) extended
Salmonella sp., whereas thyme essential oil effectively inhibited shelf life of sea bream fillet by more than 17 days. Similar
growth of E. coli. It was also widely demonstrated that dip- results were also reported by Pyrgotou et al. (2010) on rain-
ping with lactic acid, clove oil and vitamin C can exert signifi- bow trout where the similar combined strategies reduced the
cant advantages over dipping with lactic acid alone to improve cell load of main spoilage microorganisms. Corbo et al. (2008)
shelf life of buffalo meat steaks. In particular, use of clove highlighted the possibility to extend the microbial acceptability
oil along with lactic acid provided synergistic antioxidant and limit of fresh fish burgers by using a mix of thymol, grape-
antimicrobial effects; the inclusion of vitamin C also stabilized fruit seed extract, and lemon extract. The mixture of the three
product color (Naveena et al., 2006). Ntzimani et al. (2010) high- natural compounds prolonged the sensory quality without com-
lighted that combined use of EDTA, lysozyme, rosemary, and promising the flavor of fish. Each antimicrobial compound was
oregano oil extended shelf life of semi-cooked coated chicken first tested in vitro against the main fish spoilage microor-
fillets stored under vacuum packaging at 4◦ C to more than ganisms (Corbo et al., 2009). In a subsequent work, thymol,
2 weeks. grapefruit seed extract, and lemon extract were used in com-
Effects of pork chops dipped in organic acids, such as ascor- bination to MAP to demonstrate that MAP further enhanced
bic acid (500 ppm) and citric acid (250 ppm) individually or in the effects of the natural active compounds. (Del Nobile et al.,
combination, packaged under MAP and vacuum and stored at 2009b). Min et al. (2009) demonstrated the antimicrobial and
1◦ C were studied by Huang et al. (2005). Ascorbic acid dipping antioxidant activity of purple rice bran extract against catfish
reduced psychrotrophic microbial count, while ascorbic and citric patties.

Table 4 | Relevant examples of natural active agents applied to fish-based products.
Products and storage Natural compounds Results References

conditions
Rainbow trout fillets Oregano essential oil (0.2, 0.4%) The combination of oregano (0.2%) and Frangos et al., 2010
packaged under vacuum resulted in a significant shelf life
vacuum extension of trout fillets (11–12 days) if
compared to the control packaged in air
(5 days)
Rainbow trout fillets Oregano essential oil (0.4%) The antimicrobial compound improved the Mexis et al., 2009
packaged with oxygen sensory shelf life
absorber
Fish burgers packaged Rosemary extract 0.4% and 0.8% Rosemary extract, in combination with Uçak et al., 2011
under vacuum vacuum packaging was effective in
controlling microbial growth and
biochemical changes
Fried mullet fish fillets Edible coating solution mixed with Thyme and marjoram have strong effects Yasin and Abou-Taleb, 2007
thyme (2.5, 5%) and marjoram against Enterobacteriaceae
(2.5, 5%)
Sea bass fillets Thyme essential oil (0.2%) Essential oil improve the quality of sea Kostaki et al., 2009
packaged under bass fillets when used in combination with
different MAP 60% CO2 -30% N2 -10% O2 , providing a
shelf life of 17 days as compared to 6 days
of the control samples
Cooked blue Sodium acetate dipping treatments Shelf life of product dipped in 2% for 2 min Lohalaksanadech and Sujarit,
swimming crab meat (1, 1.5, and 2%) was 12 days compared to the control 2011
(6 days)
Peeled shrimps Coating with thymol (500, 1000, Shelf life of about 14 days for the active Mastromatteo et al., 2010b
packaged under MAP 1500 ppm) coating (1000 ppm) packaged under MAP
compared to the sample in air (5 days) was
obtained.
Coatings enriched with essential oils were also proposed in lit- CEREAL-BASED PRODUCTS
erature as valid technique to improve quality of fish products. Shelf life of bread is generally limited due to the staling phe-
As example, Ojagh et al. (2010) reported that the use of a coat- nomenon and fungi spoilage, in particular moulds. Among
ing with chitosan and cinnamon essential oil improved trout strategies aimed to improve quality of bread, some effects were
fillet shelf life (16 days vs. 10 days of the control) and in par- reported by using different natural compounds. In particular, it
ticular it enhanced texture, odor, and color. Similar results were was reported that chitosan coating improved bread quality by
also obtained for trout fresh fillets coated with gelatin enriched inhibiting microbial growth and retarding oxidation and staling.
with cinnamon oil (1%, 1.5%, and 2%). In particular, experi- A reduced microbial proliferation was obtained for bread coated
mental data indicated that the active coating can be suitable for with chitosan during storage at room temperature (No et al.,
preserving the fillets and maintain quality to an acceptable level 2007).
(Andevari and Rezaei, 2011). Rehman et al. (2007) reported different applications of cit-
To control quality of northern snakehead fish fillets at refrig- rus peel essential oils in bread. Results demonstrated that the
eration temperature cinnamon, coatings with nisin and EDTA, oils influenced sensory characteristics and delayed microbial
alone and in combination were used (Lu et al., 2010). growth. Maximum inhibitory effect against moulds and bacte-
Acetic acid, glucono-delta-lactone and chitosan were tested, ria was achieved by spraying peel essential oil. The combina-
individually and in combination, to inhibit microbial growth tion of MAP and mustard oil was proposed for wheat and rye
in surimi. The results showed that microbial proliferation was bread artificially inoculated with moulds (Suhur and Nielsen,
successfully inhibited by packaging the fish ball in 1% chi- 2005).
tosan dissolved in 1% of acetic acid (Kok and Park, 2007). Breads prepared from wheat flour by adding different addi-
Shirazinejad et al. (2010) evaluated the use of lactic acid alone tives were also evaluated by Latif et al. (2005). The studies on
and in combination with nisin for reducing microorganisms colony count in bread at different storage time showed that treat-
on chilled shrimp. Best results against Pseudomonas spp. were ment containing 0.32% of suhanjna, 3% of lecithin, and 0.1%
obtained for samples treated with the mixture of lactic acid of ascorbic acid proved to be most effective. The different com-
and nisin. bination of the three selected natural additives improved bread
shelf life. In particular, lower cell loads of yeasts and moulds utilization of natural active agents promotes the accepted criteria
were observed for bread with lecithin and ascorbic acid (Latif of food sustainability. The numerous experimental applications
and Masud, 2006). An active packaging with cinnamon essen- of essential oils, enzymes, bacteriocins, chitosans, and organic
tial oil combined with MAP was tested to increase the shelf acids to various fresh perishable foods demonstrate that they are
life of gluten-free sliced bread. Results showed that the active well suited to be utilized as preservatives in foods and could be
packaging is better than MAP to increase product shelf life often valid alternatives to synthetic food additives. However, there
because it inhibited microbial growth while maintaining the is a need to search for new sources of antimicrobial substances,
sensory properties of the gluten-free bread (Gutiérrez et al., including plant metabolites. Natural products have been the most
2011). successful source of drugs ever. Historically, the most important
Natural active compounds were also applied to fresh pasta natural sources have been plants. Research progressed along two
that is a product easily perishable for its high water content. major lines: ethnopharmacology (medicinal herbs, substances of
Del Nobile et al. (2009c) proposed the use of different nat- abuse, ordeal poisons) and toxicology (poisonous plants, ven-
ural antimicrobial compounds such as thymol, lemon extract, omous animals, arrow, and fish poisons). These strategies have
chitosan, and grapefruit seed extract at different concentra- produced many valuable drugs and are likely to continue to pro-
tions (2000 mg/kg and 4000 mg/kg) to improve the microbiolog- duce lead compounds. It must be stated that traditional medicines
ical stability of refrigerated amaranth-based fresh pasta. Results have not been found by systematic research but by a combina-
pointed out that chitosan were the most successful among the tion of coincidence and observation, and at best by trial and
investigated compounds in slowing down the spoilage, whereas error. In order to further promote the application of natural
lemon extract was the less effective. In a subsequent work, active compounds at industrial level, some factors are of striking
the antimicrobial activity of chitosan in combination with dif- importance. First of all it is necessary to have a good under-
ferent MAP was tested. It was found that among the tested standing of the mechanism by which antibacterial agents operate.
MAP conditions, the combination of 30:70 N2 :CO2 extended For many natural compounds these information are still lacking.
the shelf life beyond two months (Del Nobile et al., 2009d). Better understanding of the modes by which antimicrobials can
The antimicrobial activity of chitosan against the main microor- control microorganisms should provide solid grounds for engi-
ganisms of fresh pasta was also reported by Costa et al. neering new and upgraded derivatives with optimized potency
(2010). In particular, statistically significant differences were and stability. Further research is still necessary for specific case-
found between the shelf life of pasta with chitosan pack- study because it is well demonstrated that the combination of
aged under MAP conditions in a low barrier film made up more than one active agent not always amplifies the antimicrobial
of polypropylene and in a multilayer high barrier film made effects. Very often, the combined use of some natural essen-
up of polyethylene terephthalate, ethylene-vinyl alcohol, and tial oils did not induce synergistic effects. So, generally specking
polyethylene. some considerations must be taken into account before using
To improve the shelf life of yellow alkaline noodle Rosyid antimicrobials in food preservation. One of them is the possible
et al. (2011) tested the antibacterial activity of ethanol and water existence of interactions between compounds and food compo-
extracts of six types of leaves against the principal spoilage micro- nents. Moreover, also the adoption of active compounds under
bial groups of this product. Results highlighted that ethanol MAP conditions could exert different effects depending on the
extracts of aromatic leaf, Murraya koenigii L., added in yellow product.
alkaline noodle contributed to improve shelf life better than In the specific case of essential oils, despite their great poten-
the other extracts. Budka and Khan (2010) demonstrated that tial, their use in food preservation remains limited mainly due
essential oils from basil, thyme and oregano exhibit bactericidal to their intense aroma and toxicity problems. Several authors
properties against B. cereus in rice-based foods. The antioxidant have reported changes in the organoleptic properties of the
and antimicrobial activity of different natural compounds (anise, food when these oils are used. To minimize the required doses
black cumin, rosemary and sage) were also tested to increase shelf and improve the effectiveness of active coatings enriched with
life of some bakery products. Preliminary results showed that essential oils, interesting options would be micro- and nanoen-
both Gram-positive and Gram-negative bacteria were sensitive to capsulation of active compounds. In addition, the use of com-
all tested essential oils and phenolic compounds (Basuny et al., binations of different food preservation systems, such as the use
2012). of proper temperature, could represent another solution to the
above-mentioned problem. As regards toxicity, the ingestion of
CONCLUDING REMARKS AND FUTURE PERSPECTIVES high doses of essential oils can induce serious problems. Thus,
Most food products require protection against microbial spoilage it is necessary to find a balance between the effective compound
during storage. Consumers demand safe natural products. This dose and the risk of toxicity. It is also worth noting that the use
drives the search of food authorities and researchers for mild of essential oils remains expensive, so from an economic point
preservation techniques to improve microbial quality and safety of view this preservation strategy needs further enhancement.
without causing nutritional and organoleptic losses. In this con- Moreover, more specific ISO standards are also necessary to assess
text natural compounds are gaining a great interest from research the legal aspects to set out the definition, the general rules for
and industry, due to the potential to provide quality and safety their use, the requirements for labeling and the maximum levels
benefits, with a reduced impact on human health. In addition, authorized.

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published: 08 August 2012

Food applications of natural antimicrobial compounds

www.frontiersin.org August 2012 | Volume 3 | Article 287 | 1

Products and storage Natural compounds Main results References

www.frontiersin.org August 2012 | Volume 3 | Article 287 | 3

Table 2 | Relevant examples of natural active compounds applied to dairy products.

Products and storage Natural compounds Main results References

www.frontiersin.org August 2012 | Volume 3 | Article 287 | 5

Table 3 | Relevant examples of natural active agents applied to meat-based products.

Products and storage Natural compounds Main results References

www.frontiersin.org August 2012 | Volume 3 | Article 287 | 7

Table 4 | Relevant examples of natural active agents applied to fish-based products.

Products and storage Natural compounds Results References

www.frontiersin.org August 2012 | Volume 3 | Article 287 | 9

www.frontiersin.org August 2012 | Volume 3 | Article 287 | 11

www.frontiersin.org August 2012 | Volume 3 | Article 287 | 13

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