Application of essential oils as antimicrobial agents against spoilage and pathogenic microorganisms in meat products

https://doi.org/10.1016/j.ijfoodmicro.2020.108966Get rights and content

Highlights

  • A wide variety of valuable compounds can be obtained from essential oils (EOs).

  • The application of EOs allows to inhibit the growth of several pathogenic bacteria.

  • Phenolic compounds are the main responsible for their microbial activity of essential oils.

  • The application of EOs is conditioned by their suitability and their potential toxicological effects.

Abstract

Meat and meat products are perishable products that require the use additives to prevent the spoilage by foodborne microorganisms and pathogenic bacteria. Current trends for products without synthetic preservatives have led to the search for new sources of antimicrobial compounds. Essential oils (EOs), which has been used since ancient times, meet these goals since their effectiveness as antimicrobial agents in meat and meat products have been demonstrated. Cinnamon, clove, coriander, oregano, rosemary, sage, thyme, among others, have shown a greater potential to control and inhibit the growth of microorganisms. Although EOs are natural products, their quality must be evaluated before being used, allowing to grant the Generally Recognized as Safe (GRAS) classification.

The bioactive compounds (BAC) present in their composition are linked to their activity, being the concentration and the quality of these compounds very important characteristics. Therefore, a single mechanism of action cannot be attributed to them. Extraction technique plays an important role, which has led to improve conventional techniques in favour of green emerging technologies that allow to preserve better target bioactive components, operating at lower temperatures and avoiding as much as possible the use of solvents, with more sustainable processing and reduced energy use and environmental pollution. Once extracted, these compounds display greater inhibition of gram-positive than gram-negative bacteria. Membrane disruption is the main mechanism of action involved.

Their intense characteristics and the possible interaction with meat components make that their application combined with other EOs, encapsulated and being part of active film, increase their bioactivity without modifying the quality of the final product.

Introduction

Recently, the harmful effects associated with synthetic preservatives have led to the search new alternatives in natural products (Alirezalu et al., 2020; Aminzare et al., 2016). A wide variety of valuable compounds can be obtained from plants (Munekata et al., 2020). Essential oils (EOs) are secondary metabolites obtained from plants of Asteraceae, Lamiaceae, Lauraceae, Myrtaceae, Rutaceae, Umbelliferae, Zingiberaceae families, among others (Wińska et al., 2019), which are composed by a complex mixtures of volatile compounds of low molecular weight. These valuable substances can be obtained from different parts of the plants like bark, flowers and fruits, leaves, roots and stems (Nikmaram et al., 2018). Most are characterized by being liquid at room temperature, while some could have a solid or resinous appearance. Regarding their colour, this varies greatly, from pale yellow to emerald green and from blue to dark brownish red (Saranraj and Devi, 2018).

Their beneficial effects are mainly attributed to the presence of bioactive compounds (BAC), which are accountable for their anticarcinogenic, anti-diabetic, anti-inflammatory, antimutagenic, antioxidant and antiproliferative properties (Giacometti et al., 2018; Leyva-López et al., 2017). A huge number of preclinical studies have demonstrated these activities, showing their mechanism of action and pharmacological effects (Costa et al., 2020; de Lima et al., 2020). In contrast, there exists a paucity of human clinical trials, which would limit the potential of some essential oils as effective and safe phytotherapeutic agents (Sharifi-Rad et al., 2017).

There are many valuable compounds that are part of their composition, terpenoids and phenylpropanoids are the main, but fatty acids, oxides and sulfur derivatives are also part of their composition. The antimicrobial properties of EOs derived from many plants have been recognized, what becomes in an interesting strategy to extend the shelf life of meat and meat products. The application of EOs allows inhibiting the growth of several pathogenic bacteria and spoilage microorganisms that synthetic compounds are sometimes unable to eliminate. Moreover, they confer beneficial properties with fewer side effects and functional properties. Although EOs have been used since ancient times, their natural origin does not necessarily imply that their use are safe. To ensure this it is necessary to check their efficacy, safety, toxicity, and mechanism of action (Žuntar et al., 2018). The results of these strict quality controls have recognized them as Generally Recognized as Safe (GRAS), allowing their use in food products as safe additives (FDA, 2020). However, sometimes it is necessary to use them in higher concentrations to achieve the same effect as commercial additives, which could cause undesirable effects on the product or even toxicity problems (Ju et al., 2019). This makes necessary to consider their use combined with other preservatives, looking for a synergistic effect that allows achieving a better activity at a lower concentration but sufficient to avoid the appearance of undesirable effects (Pateiro et al., 2018).

The most common extraction techniques involve in the obtaining of EOs are decoction, digestion, drying, hydro and steam distillation, infusion, maceration, percolation, and solvent extraction. However, several disadvantages are associated with these conventional methods. Therefore, using emerging green technologies such as microwave-assisted extraction, supercritical fluid extraction, and ultrasound-assisted extraction, higher quality compounds are achieved, since these technologies allow to preserve BAC of EOs, since they operate at lower temperatures and avoid as much as possible the use of solvents (Chemat et al., 2020; Dima and Dima, 2015; Pateiro et al., 2018; Putnik et al., 2017, Putnik et al., 2018).

However, the possible application of EOs as antimicrobials in meat and meat products has not been studied much yet, since it is necessary to carry out more studies that allow to deepen in their technological and organoleptic effects, their synergistic behaviour and their functionality (bioavailability and bioaccessibility studies). The aim of this review focuses on evaluating the antimicrobial effect of EOs against major meat spoilage microorganisms and pathogenic bacteria, as well as their implication in the sensory characteristics of the product.

Section snippets

Bioactive compounds present in essential oils and mechanism of action linked to their antimicrobial activity

There are many EOs with antimicrobial properties, but not all have the same activity. In fact, based on the results found in the bibliography, a range of activity could be established. In this way, oregano, clove, coriander and cinnamon would be among the most effective. Below in importance would appear thyme with higher activity than mint, rosemary, mustard and cilantro; the latter with an activity similar to sage.

The composition of the essential oils determines their properties, and therefore

Essential oils as antimicrobials in meat and meat products

Meat and meat products are important sources of nutrients to the human diet because of their high-quality protein content, essential amino acids, and an excellent source of B-group vitamins, minerals, and other nutrients. However, chemical composition of meat makes it a perishable product from the processing of meat products to their distribution and storage.

Among the bacteria responsible for the deterioration of meat and meat products are Acinetobacter, Brochothrix thermosphacta, Enterobacter,

Stabilization of essential oils as antimicrobials in meat products

The use of EOs as antimicrobials is a promising strategy to avoid the use of synthetic additives. However, to get the same effect than those achieved through conventional preservatives, it is necessary to use much higher doses that could lead to harmful effects in meat products. Among these effects, the appearance of intense flavours stands out. Several alternatives could be used to reduce their negative effects and to increase their efficacy, such as the combined effect with other EOs or their

Conclusion and future perspectives

The effectiveness of essential oils in meat products is conditioned by the stability of their BAC, so that EOs should be selected based on meat product and its properties, thus optimizing their effect on microbial counts and reducing the impact on product quality. In addition, understanding the mechanisms of action of essential oils in active films or encapsulated would achieve better results.

Moreover, the application of EOs as antimicrobial agents in meat products is conditioned by their

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgments

The authors thank GAIN (Axencia Galega de Innovación) for supporting this review (grant number IN607A2019/01). Paulo E. S. Munekata acknowledges postdoctoral fellowship support from the Ministry of Economy and Competitiveness (MINECO, Spain) “Juan de la Cierva” program (FJCI-2016-29486). Mirian Pateiro, Paulo E.S. Munekata, Rubén Domínguez, José M. Lorenzo and Anderson S. Sant'Ana are members of the HealthyMeat network, funded by CYTED (ref. 119RT0568). Anderson S. Sant'Ana thanks to Conselho

References (143)

  • K. Das

    Turmeric (Curcuma longa) oils

  • T.L.C. De Oliveira et al.

    Antimicrobial activity of Satureja montana L. essential oil against Clostridium perfringens type A inoculated in mortadella-type sausages formulated with different levels of sodium nitrite. Int. J

    Food Microbiol.

    (2011)
  • K.Á.R. de Oliveira et al.

    Synergistic inhibition of bacteria associated with minimally processed vegetables in mixed culture by carvacrol and 1,8-cineole

    Food Control

    (2015)
  • C. Dima et al.

    Essential oils in foods: extraction, stabilization, and toxicity

    Curr. Opin. Food Sci.

    (2015)
  • D. Djenane et al.

    Antioxidant and antibacterial effects of Lavandula and Mentha essential oils in minced beef inoculated with E. coli O157:H7 and S. aureus during storage at abuse refrigeration temperature

    Meat Sci.

    (2012)
  • R. Domínguez et al.

    Active packaging films with natural antioxidants to be used in meat industry: a review

    Food Res. Int.

    (2018)
  • F. Donsì et al.

    Nanoencapsulation of essential oils to enhance their antimicrobial activity in foods

    LWT - Food Sci. Technol.

    (2011)
  • M.A.M. El-hamahmy et al.

    Physiological effects of hot water dipping, chitosan coating and gibberellic acid on shelf-life and quality assurance of sugar snap peas (Pisum sativum L. var. macrocarpon). Food Packag

    Shelf Life

    (2017)
  • H. Falleh et al.

    Essential oils: a promising eco-friendly food preservative

    Food Chem.

    (2020)
  • R.P.P. Fernandes et al.

    Effects of oregano extract on oxidative, microbiological and sensory stability of sheep burgers packed in modified atmosphere

    Food Control

    (2016)
  • R.P.P. Fernandes et al.

    Evaluation of oxidative stability of lamb burger with Origanum vulgare extract

    Food Chem.

    (2017)
  • R.P.P. Fernandes et al.

    Assessment of the stability of sheep sausages with the addition of different concentrations of Origanum vulgare extract during storage

    Meat Sci.

    (2018)
  • D. Georgantelis et al.

    Effect of rosemary extract, chitosan and α-tocopherol on lipid oxidation and colour stability during frozen storage of beef burgers

    Meat Sci.

    (2007)
  • M. Ghaderi-Ghahfarokhi et al.

    Chitosan-cinnamon essential oil nano-formulation: application as a novel additive for controlled release and shelf life extension of beef patties

    Int. J. Biol. Macromol.

    (2017)
  • J. Giacometti et al.

    Extraction of bioactive compounds and essential oils from mediterranean herbs by conventional and green innovative techniques: a review

    Food Res. Int.

    (2018)
  • A.O. Gill et al.

    Evaluation of antilisterial action of cilantro oil on vacuum packed ham

    Int. J. Food Microbiol.

    (2002)
  • B. Gómez et al.

    Microencapsulation of antioxidant compounds through innovative technologies and its specific application in meat processing

    Trends Food Sci. Technol.

    (2018)
  • A. Guarda et al.

    The antimicrobial activity of microencapsulated thymol and carvacrol

    Int. J. Food Microbiol.

    (2011)
  • A.D. Gupta et al.

    Chemistry, antioxidant and antimicrobial potential of nutmeg (Myristica fragrans Houtt)

    J. Genet. Eng. Biotechnol.

    (2013)
  • M. Hadian et al.

    Encapsulation of Rosmarinus officinalis essential oils in chitosan-benzoic acid nanogel with enhanced antibacterial activity in beef cutlet against Salmonella typhimurium during refrigerated storage

    LWT - Food Sci. Technol.

    (2017)
  • D.D. Jayasena et al.

    Essential oils as potential antimicrobial agents in meat and meat products: a review

    Trends Food Sci. Technol.

    (2013)
  • Y. Jiang et al.

    Chemical composition and antimicrobial activity of the essential oil of rosemary

    Environ. Toxicol. Pharmacol.

    (2011)
  • J. Ju et al.

    Application of essential oil as a sustained release preparation in food packaging

    Trends Food Sci. Technol.

    (2019)
  • M. Kaleem et al.

    Flavonoids as nutraceuticals

  • S.R. Kanatt et al.

    Effects of chitosan coating on shelf-life of ready-to-cook meat products during chilled storage

    LWT-Food Sci. Technol.

    (2013)
  • M.A. Khaleque et al.

    Use of cloves and cinnamon essential oil to inactivate Listeria monocytogenes in ground beef at freezing and refrigeration temperatures

    LWT - Food Sci. Technol.

    (2016)
  • S.T. Khalili et al.

    Encapsulation of thyme essential oils in chitosan-benzoic acid nanogel with enhanced antimicrobial activity against Aspergillus flavus

    LWT - Food Sci. Technol.

    (2015)
  • A.K. Khare et al.

    Comparison study of chitosan, EDTA, eugenol and peppermint oil for antioxidant and antimicrobial potentials in chicken noodles and their effect on colour and oxidative stability at ambient temperature storage

    LWT - Food Sci. Technol.

    (2014)
  • S. Lekjing

    A chitosan-based coating with or without clove oil extends the shelf life of cooked pork sausages in refrigerated storage

    Meat Sci.

    (2016)
  • L. Lin et al.

    Electrospun thyme essential oil/gelatin nanofibers for active packaging against Campylobacter jejuni in chicken

    LWT

    (2018)
  • C.C. Liolios et al.

    Liposomal incorporation of carvacrol and thymol isolated from the essential oil of Origanum dictamnus L. and in vitro antimicrobial activity

    Food Chem.

    (2009)
  • J.M. Lorenzo et al.

    Extension of the shelf-life of foal meat with two antioxidant active packaging systems

    LWT-Food Sci. Techn.

    (2014)
  • A. Luna et al.

    Thymol as natural antioxidant additive for poultry feed: oxidative stability improvement

    Poult. Sci.

    (2017)
  • S. Mandal et al.

    Coriander (Coriandrum sativum L.) essential oil: chemistry and biological activity. Asian Pac

    J. Trop. Biomed.

    (2015)
  • A. Marques et al.

    Bay laurel (Laurus nobilis) oils

  • M. Moraes-Lovison et al.

    Nanoemulsions encapsulating oregano essential oil: production, stability, antibacterial activity and incorporation in chicken pâté

    LWT - Food Sci. Technol.

    (2017)
  • P.E.S. Munekata et al.

    Addition of plant extracts to meat and meat products to extend shelf-life and health-promoting attributes: an overview

    Curr. Opin. Food Sci.

    (2020)
  • A.I. Nazer et al.

    Combinations of food antimicrobials at low levels to inhibit the growth of Salmonella sv. Typhimurium: a synergistic effect?

    Food Microbiol.

    (2005)
  • N. Nikmaram et al.

    Application of plant extracts to improve the shelf-life, nutritional and health-related properties of ready-to-eat meat products

    Meat Sci.

    (2018)
  • S. Noori et al.

    Antimicrobial and antioxidant efficiency of nanoemulsion-based edible coating containing ginger (Zingiber officinale) essential oil and its effect on safety and quality attributes of chicken breast fillets

    Food Control

    (2018)
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