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Research Article | Open Access
  • Available online freely | Peer Reviewed
  • Oregano (Origanium Vulgare) Extract for Food Preservation and Improving Gastrointestinal Health

    Jacob P. Veenstra 1     Jeremy J. Johnson 1      

    1University of Illinois at Chicago, College of Pharmacy, Department of Pharmacy Practice.

    Abstract

    The Mediterranean diet has long been known to provide a variety of health benefits including cardiovascular protection, cancer prevention, and lowering gastrointestinal inflammation. Oregano (Origanium vulgare) is an herb prominent in the Mediterranean diet, and has been shown to possess several bioactive properties including anti-oxidant, anti-microbial, anti-inflammatory, and analgesic properties. The anti-oxidant and anti-microbial properties of oregano also make it a strong candidate as a natural food preservative. Because of the recent public concern with synthetic food preservatives, natural alternatives are increasingly being evaluated for effective food preservation. Oregano extract (OE) and essential oil (OEO) are two such agents that have shown promise as natural food preservatives. Additionally, oregano is being evaluated for its positive effect on gastrointestinal health, suggesting an additional benefit of food preservation with oregano. This review will describe in vitro studies related to the anti-microbial and anti-oxidant properties of oregano along with food preservation studies with oregano in various model food matrices. The major phytochemical content reported for OE and OEO will also be outlined to highlight the importance of characterizing the extract that is used, since the extraction process can have a significant effect on the phytochemicals therein. Finally, in vivo studies that investigate the gastrointestinal health benefits of oregano, specifically against inflammation, will be addressed to describe the role of oregano on gastrointestinal health.

    Received 07 Mar 2019; Accepted 24 Mar 2019; Published 09 Apr 2019;

    Academic Editor:Yue Sheng, University of Florida and University of Illinois at Chicago, United States.

    Checked for plagiarism: Yes

    Review by: Single-blind

    Copyright©  2019 Jacob P. Veenstra, et al.

    License
    Creative Commons License    This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

    Competing interests

    The authors have declared that no competing interest exists.

    Citation:

    Jacob P. Veenstra, Jeremy J. Johnson (2019) Oregano (Origanium Vulgare) Extract for Food Preservation and Improving Gastrointestinal Health . International Journal of Nutrition - 3(4):43-52.
    Download as RIS, BibTeX, Text (Include abstract )
    DOI10.14302/issn.2379-7835.ijn-19-2703

    Introduction

    Approximately 60 plant species and 17 genera share a similar flavor and color often being labelled as “oregano”1. In traditional medicine, oregano has been used for respiratory conditions (i.e. asthma, bronchitis, cough), gastrointestinal (i.e. diarrhea, indigestions, stomachache), anti-bacterial, anti-inflammatory, menstrual disorders, and diabetes2,3,4. Greek oregano (Origanum vulgare) throughout the world is the most recognized herb as being authentic or original “oregano”5. This variety is often reported to be elevated in rosmarinic acid, a phytochemical first isolated from rosemary (Rosmarinus officinalis) in 1958 by the Italian Chemists Scarpati and Oreinte6. The benefits of oregano on human health have been associated and attributed to the phytochemicals found therein. Phytochemicals isolated from oregano represent a heterogeneous class of compounds generated during secondary metabolism with most not appearing to participate in essential metabolic functions7.

    The Mediterranean diet has been recognized for its health-promoting benefits related to cardiovascular disease, stroke reduction, and cancer reduction8,9,10,11. In the Mediterranean region the diet can vary, however, it typically consists of fruits, vegetables, nuts, legumes, moderate fish and poultry consumption, high polyunsaturated fats, and low consumption of red meat12,13. Another important component of the Mediterranean diet includes the herb oregano (Origanium vulgare). This perennial herb has been suggested to have a variety of health promoting properties ranging from anti-oxidant, anti-inflammatory, analgesic, and anti-microbial14,15,16. Interestingly, two attributes that have received significant attention include the antioxidant activity and anti-microbial activity of oregano with regard to enhancing food stability17, 18.

    There is growing public concern among consumers regarding the addition of chemical additives to foods19. Specific examples include the use of synthetic antioxidants that have been routinely used to enhance shelf life of various foods. In the USA, the meat and poultry industry has relied heavily on synthetic antioxidants including butylated hydroxyanisole, butylated hydroxytoluene, tert-butylhydroquinone, and propyl gallate, as well as tocopherols to prevent lipid and protein oxidation20,21,22. Consequently, researchers and food manufacturers are starting to shift from synthetic antioxidants to natural antioxidants. Oregano is one such herb that has been approved in the United States as a spice and natural flavor that can reduce oxidation. A recent study reported that oregano extract can maintain the physicochemical, sensory acceptance, reduce lipid and protein oxidation of lamb meat after frozen storage after 120 days23. In addition to maintaining the physical and chemical properties of the meat there was also good sensory acceptance by consumers. These results suggest that that oregano prepared using a variety of extraction methods may be a promising alternative to the synthetic food preservatives.

    In addition to the food preservation properties of oregano, there is compelling evidence that these phytochemicals display health promoting properties related to the gastrointestinal tract1. Different extraction methods and solvents for each plant are detailed and the most abundant phytochemicals from each extract are outlined in this report. The anti-oxidant and anti-microbial properties of each herb are described along with specific food preservation studies. Finally, in vivo studies that show the impact of herb extracts on gastrointestinal health are outlined with significant findings. The goal of this review is to highlight oregano as a natural food preservative and to describe the potential benefits related to gastrointestinal health.

    Oregano (Origanium Vulgare)

    Phytochemicals

    Oregano extract (OE) and oregano essential oil (OEO) have been studied for their bioactive properties, and an important step to understanding their mechanisms of action is identification of major components (Table 1). The volatile aroma compounds in oregano OEO has been well characterized, with the majority of published articles on oregano focusing on the essential oil. The most abundant compounds present in OEO include the diterpenes carvacrol and thymol, which have been extensively studied for their anti-bacterial and anti-oxidant properties. Studies have identified these compounds as comprising up to 92% of the total essential oil content24,25,26. Oregano has been extracted various methods creating a variety of extracts that can vary in phytochemical composition (Figure 1). In a hydroalcoholic (80:20 methanol:water) extract, Martins et al. reported the major components to be luteolin 7-O-glucoside (20.88%), rosmarinic acid (14.62%), luteolin O-glucuronide (12.48%), and apigenin-7-O-glucuronide (5.78%)27. In sub- and supercritical CO2 extraction, the major phytochemicals identified include carvacrol, linalyl acetate, thymol, and cis-sabinene hydrate28. Other compounds identified in an ethanolic extract of oregano are 4-hydroxy-4-methyl-2-pentanone, rosmarinic acid, thymol, luteolin 7-O-glucoside, and caffeic acid29.

    Table 1. Most abundant phytochemicals characterized in oregano extract prepared by different extraction methods
    Extraction method or essential oil Major phytochemicals Citation
    Essential oil Carvacrol (14.5% total oil composition)β-fenchyl alcohol (12.8%)Thymol (12.6%)γ-terpinene (11.6%)δ-terpineol (7.5%) 14
    Essential oil Carvacrol (61.3% total oil composition)Thymol (13.9%)γ-terpinene (3.1%)1,8-cineole (1.6%)Borneol (1.3%) 25
    Essential oil Carvacrol (not quantified)γ-terpineneCamphene1-octen-3-olβ-caryophyllene 28
    Supercritical CO2 Carvacrol (not quantified)Cis-sabinene hydrateLinalyl acetateTrans-sabinene hydrateThymol 28
    Hydroalcoholic(methanol:water 80:20) Luteolin 7-O-glucoside (20.88 mg/g extract)Rosmarinic acid (14.62 mg/g)Luteolin O-glucuronide (12.48 mg/g)Apigenin 7-O-glucuronide (5.78 mg/g)Quercetin 3-O-rutinoside (3.71 mg/g) 27
    Infusion (aqueous) Luteolin O-glucuronide (26.50 mg/g extract)Luteolin 7-O-glucoside (22.93 mg/g)Rosmarinic acid (15.91 mg/g)Apigenin 7-O-glucuronide (8.24 mg/g)Kaempferide O-glucuronide (3.99 mg/g) 27
    Decoction (aqueous) Luteolin O-glucuronide (28.27 mg/g extract)Luteolin 7-O-glucoside (25.26 mg/g)Rosmarinic acid (15.42 mg/g)Apigenin 7-O-glucuronide (8.63 mg/g)Kaempferide O-glucuronide (3.97 mg/g) 27
    Ethanol (70%) Diacetone alcohol (32.18 mg/g dry weight)Rosmarinic acid (25.02 mg/g)Thymol (24.36 mg/g)n-heptanoic acid (17.06 mg/g)Luteolin 7-O-glucoside (10.08 mg/g) 29
    Methanol (70%) Diacetone alcohol (28.87 mg/g dry weight)Rosmarinic acid (28.42 mg/g)Thymol (16.29 mg/g)Nitro-L-argnine (15.93 mg/g)Luteolin 7-O-glucoside (13.53 mg/g) 29

    Figure 1. Several compounds found in OE or OEO that have been reported in the literature
    Figure 1.

    Applications of Oregano as a Food Preservative

    Anti-oxidant activity: Teixeira et al. compared the anti-oxidant activities of OEO and three types of OE (i.e. hot water, cold water, and ethanolic) using three different assays – ferric reducing anti-oxidant power (FRAP), reducing power of Fe3+ to Fe2+, and DPPH assay14. The chemical constituents of the OEO were characterized by GC-MS and reported the most abundant compounds being carvacrol (14.5%), β-fenchyl alcohol (12.8%), and thymol (12.6%). However, the chemical compositions of the extracts were not reported. FRAP analysis showed OEO (38.5 µmol Fe2+/g) and cold water OE (37.7 µmol Fe2+/g) having the highest anti-oxidant power, followed by hot water (27.9 µmol Fe2+/g) and ethanolic (12.6 µmol Fe2+/g). In terms of reducing power, hot water OE (621.7 µmol ascorbic acid/g) was the highest, followed by ethanolic (232.7 µmol ascorbic acid/g), cold water (203.3 µmol ascorbic acid/g), and OEO (74.5 µmol ascorbic acid/g). DPPH assay followed the same trend as the reducing power analysis with EC50 being 25.1 µg/mL for hot water, 64.1 µg/mL for ethanolic, 144.3 µg/mL for cold water, and 1509.1 µg/mL for OEO. The researchers concluded that hot water OE had the highest anti-oxidant activity, followed by ethanolic, cold water, and OEO, respectively. Interestingly, the results of this study did not correlate total phenolic content with anti-oxidant activity, suggesting that other phytochemicals were contributing to the anti-oxidant activity of oregano.

    Anti-microbial activity: In the same study, Teixeira et al. also tested the anti-bacterial activity of hot water, cold water, and ethanolic OE and OEO against Brochothrixthermosphacta, Escherichia coli, L. innocua, Listeria monocytogenes, Pseudomonas putida, Salmonella typhimurium, and Shewanellaputrefaciens14. Anti-bacterial activity was tested by paper disc diffusion test and growth in liquid medium. Neither the hot or cold water extracts had any significant inhibitory properties against the growth of any bacteria. Ethanolic OE demonstrated moderate activity against S. typhimurium, E. coli, L. innocua, and L. monocytogenes, resulting in MICs of 13.9 mg/mL, 6.9 mg/mL, 13.9 mg/mL, and 6.9 mg/mL, respectively. OEO displayed strong activity against all bacterial strains, with the strongest against P. putida at 0.4 mg/mL and the weakest against S. putrefaciens. Ethanolic OE and OEO at the calculated MICs reduced bacterial growth in liquid broth dilution of the species susceptible to treatment in the disc diffusion experiment. Coccimiglio et al. tested the anti-bacterial activity of an ethanolic OE against a panel of various gram-negative and gram-positive bacteria using the agar dilution method30. The researchers calculated MICs for OE against all strains of bacteria, and the study noted that OE had the strongest effect against non-mucoid isolates of Pseudomonas aeruginosa (MIC = 6.3 µg/mL), that are more susceptible to immune responses and drug treatment than mucoid isolates. Hernández-Hernández et al. tested the anti-bacterial activity of both free and microencapsulated OEO by disc diffusion method31. Microencapsulation was performed by adding OEO to a modified starch dispersion and homogenizing by ultra-centrifugation. The oils were tested against Bronchothrixthermosphacta, Lactobacillus plantarum, Pseudomonas fragi, Salmonella sp., and Micrococcus luteus. The study showed that free OEO at 25% w/v possessed activity against all species except for L. plantarum, while microencapsulated OEO showed no activity against L. plantarum and Salmonella sp. and was less effective than free OEO against all other species.

    Food Preservation

    Oregano has been evaluated for its anti-oxidant and anti-microbial properties with special application to food preservation. One application of oregano in food preservation is Cypriot pastrami, a type of sun-dried meat product, also known as samarella32. The more modern way of making samarella is to take the meat of a goat or sheep and dry the meat using the sun. Once dry, the meat is washed and sprinkled with oregano. A second application of OEO as a food preservative includes that use of additive-free meats that have been dried and cured. This approach has been recognized in the European Union where essential oils are considered safe food additives at concentrations <2 mg/kg body weight/day33.

    Several studies evaluated the effectiveness of food preservation using OE and OEO. Aqueous OE was shown to significantly reduce microbial growth and TBARS values in raw beef samples over a 15 day period compared to controls, although the strongest effect was observed in both experiments when combined with cinnamon and clove extracts34. In a study of anti-oxidant herbs added to animal fat, methanolic OE was determined to have anti-oxidant capacity of 13.59 ± 0.87 nmol equivalent of Vitamin E per gram of fat at a concentration of 5 µg extract per g fat, which was more than double the control group35. The major phytochemicals detected in this study were rosmarinic acid (30.03 mg/g) and carvacrol (16.29 mg/g). OEO prepared by an oil-in-water nanoemulsion inhibited growth of L. monocytogenes, S. Typhimurium, and E. coli on commercial iceberg and romaine lettuce leaves at concentrations of 0.05% and 0.1%, with the latter being the most effective36.

    Another strategy of food preservation is to incorporate a combination of extracts to enhance preservation capabilities. Oregano tested in combination with other natural extracts has been reported to enhance its preservative qualities. Chitosan (1%) was found to be effective with OEO (2-4%) in pork meat at inhibiting bacterial growth, protecting from lipid oxidation, and extending shelf-life with minimal effect on sensory qualities37. OEO was tested with caprylic acid at 0.2% and 0.5%, respectively, and found to have a greater anti-microbial effect than either compound alone in minced beef38. A combination of OEO and REO inhibited growth of naturally occurring fungi in table grapes and preserved the sensory and physical (appearance, firmness) qualities during storage39. In a study using cooked chicken, OEO in combination with sage essential oil and honey reduced the amount of lipid oxidation after 48 and 96h as measured by TBARS40. These studies suggest that oregano can be used alone, however, some evidence suggests a combination of other herbs may enhanced food preservation properties.

    In vivo GI Health Benefits

    Another benefit of phytochemicals in food preservation is that they may also improve gastrointestinal health (Table 2). Both OE and OEO have been shown to exhibit anti-inflammatory effects in vivo by suppression of TNF-α expression15, 41. In mice with streptozotocin-induced diabetes, an ethyl acetate OE compared to control mice. This study found that OE reduced the number of TH1 and TH17 cells and activity measured by expression of the cytokines IFN-γ and IL-17, and both of these results reached statistical significance (P < 0.05)4. Treated mice also had a lower population of pro-inflammatory macrophage F4/80+ cells in the peritoneum while also decreasing the expression of IL-6 and IL-1β (P < 0.05), further suggesting that the ethyl acetate OE has anti-inflammatory properties in vivo.

    Table 2. In vivo models evaluating oregano extracts and essential oil.
    Model Experimental conditions Significant findings Citation
    P. acnes-induced mouse ear edema 8-week old ICR miceGroups (5 mice each):Ethanolic OE (2 mg/10 μL) in 5% DMSOVehicle control (5% DMSO)Propionibacterium acnes (6 x 107 CFU/10 μL PBS) was inoculated in right ear by intradermal injection and PBS (10 μL) was injected in right earEthanolic OE or vehicle (5% DMSO) was injected in both ears directly after P. acnes24 hours after P. acnes injection, mouse ear swelling was measured and mice were euthanized P. acnes injection increased ear thickness by 2.5-fold and ear weight by 2.3-foldOEO reduced P. acnes-induced ear thickness by 32% and ear weight by 37%  41
    Streptozotocin-induced type 1 diabetes mice 8-12 week old C57BL/6 miceGroups (≥7 mice each):Streptozotocin (40 mg/kg/day) + OE (2 mg/day)Streptozotocin onlyStreptozotocin (40 mg/kg/d) was administered through intraperitoneal (IP) injection at multiple low doses (MLDS) for 5 consecutive daysEthyl acetate OE administered by IP at 2 mg doses for 10 consecutive days, starting on same day as Streptozotocin dosing Streptozotocin administration alone resulted in 80% development of hyperglycemia in mice, and ethyl acetate OE administration reduced hyperglycemic development to 15% of miceEthyl acetate OE reduced the number of F4/80* macrophages and concentrations of IL-1β and IL-6, while also increasing concentrations of TNF and IL-10Th1 and Th17 cell counts decreased with ethyl acetate administration, along with concentrations of associated cytokines IFN-γ and IL-17 4
    TNBS-induced colitis mice 7-week old Balb/c miceGroups (16 mice each):Group A: TNBS + 0.4% thyme oil + 0.2% oregano oilGroup B: TNBS + 0.2% thyme oil + 0.1% oregano oilGroup C: TNBS + 0.1% thyme oil + 0.05% oregano oilGroup D: TNBS onlyGroup E: ShamColitis induced by intrarectal administration of 120 mg/kg TNBS in 50% ethanolThyme and oregano oil combinations were administered for 7 consecutive days Mice in Group B recovered body weight significantly compared to TNBS-only miceMice in Group B had a significantly lower colonic damage score compared to TNBS-only miceThe mRNA and protein levels of IL-1β and IL-6 cytokines was significantly reduced in Group B mice 42

    A study by Bukovská et al. investigated the effects combined oregano and thyme essential oils in a colitis mouse model induced by trinitrobenzene sulphonic acid (TNBS) (120 mg/kg in 50% ethanol)42. The oregano and thyme oils were combined at different concentrations and given in the feed for 6 days prior to TNBS administration. The 0.1% oregano and 0.2% thyme combination treatment also had the highest prevention of macroscopic colonic damage (P < 0.05) and also the most recovery in body weight (not statistically significant). This dose also decreased both the mRNA and protein the expression of pro-inflammatory cytokines IL-6 and IL-1β (P < 0.01). The investigators found that oregano and thyme at 0.1% and 0.2%, respectively, had the highest decrease of mortality rate at 33.3% compared to 53.3% in the TNBS-only group, although this result was not statistically significant. These studies suggest that oregano may decrease inflammatory markers in vivo while improving gastrointestinal health.

    Conclusion

    This review summarizes the biological activities of different oregano extracts related to their natural food preservation properties and health promoting properties related to gastrointestinal health. The public interest for clean-labeling of food products and alternatives to synthetic food preservatives provide the demand natural alternatives. Oregano extract and essential oil present promising methods of natural food preservation due to their bioactivities that prevent many types of food spoilage and microbial growth. Defining the phytochemical content is essential in understanding the advantages of different forms tested for anti-oxidant and anti-microbial properties.  In addition to using a single herb such as oregano, a combination of multiple extracts or essential oils may produce an even greater effect on food preservation. Beyond food preservation, however, these herbs have also been shown to promote GI health. Studies performed in mice have shown positive effects of lowering GI inflammation and lessening the symptoms of TNBS exposure.  Future studies will be needed to determine the full potential and health benefits of oregano extract as an alternative to synthetic food preservatives.

    Acknowledgements

    Johnson JJ is supported by the National Institutes of Health (R37 CA227101) and USDA National Institute of Food and Agriculture (67017-26364)

    References

    1.Gutierrez-Grijalva E P, Picos-Salas M A, Leyva-Lopez N, Criollo-Mendoza M S, Vazquez-Olivo G et al. (2017) Flavonoids and Phenolic Acids from Oregano: Occurrence, Biological Activity and Health Benefits. Plants. , (Basel, Switzerland) 7-1.
    2.Morshedloo M R, Craker L E, Salami A, Nazeri V, Sang H et al. (2017) Effect of prolonged water stress on essential oil content, compositions and gene expression patterns of mono- and sesquiterpene synthesis in two oregano (Origanum vulgare L.) subspecies. Plant physiology and biochemistry:. , PPB 111, 119-28.
    3.Han F, Ma G Q, Yang M, Yan L, Xiong W et al. (2017) Chemical composition and antioxidant activities of essential oils from different parts of the oregano. , Journal of Zhejiang University Science B 18(1), 79-84.
    4.Vujicic M, Nikolic I, Kontogianni V G, Saksida T, Charisiadis P et al. (2016) . Ethyl Acetate Extract of Origanum vulgare L. ssp. hirtum Prevents Streptozotocin-Induced Diabetes in C57BL/6 Mice. Journal of food science 81(7), 1846-53.
    5.Mastro G, Tarraf W, Verdini L, Brunetti G, Ruta C. (2017) Essential oil diversity of Origanum vulgare L. populations from Southern Italy. Food chemistry. 235, 1-6.
    6.Al-Dhabi N A, Arasu M V, Park C H, Park S U. (2014) Recent studies on rosmarinic acid and its biological and pharmacological activities. , EXCLI journal 13, 1192-5.
    7.Oniga I, Puscas C, Silaghi-Dumitrescu R, Olah N K, Sevastre B et al. (2018) Origanum vulgare ssp. vulgare: Chemical Composition and Biological Studies. Molecules. , (Basel, Switzerland) 23-8.
    8.Widmer R J, Flammer A J, Lerman L O, Lerman A. (2015) The Mediterranean diet, its components, and cardiovascular disease. The American journal of medicine. 128(3), 229-38.
    9.N Di Daniele, Noce A, Vidiri M F, Moriconi E, Marrone G et al. (2017) . Impact of Mediterranean diet on metabolic syndrome, cancer and longevity. Oncotarget 8(5), 8947-79.
    10.Lakkur S, Judd S E. (2015) Diet and Stroke: Recent Evidence Supporting a Mediterranean-Style Diet and Food in the Primary Prevention of Stroke. , Stroke 46(7), 2007-11.
    11.Tektonidis T G, Akesson A, Gigante B, Wolk A, Larsson S C. (2015) A Mediterranean diet and risk of myocardial infarction, heart failure and stroke: A population-based cohort study. , Atherosclerosis 243(1), 93-8.
    12.Panagiotakos D B, Pitsavos C, Stefanadis C. (2006) Dietary patterns: a Mediterranean diet score and its relation to clinical and biological markers of cardiovascular disease risk. Nutrition, metabolism, and cardiovascular diseases:. , NMCD 16(8), 559-68.
    13.Keys A, Menotti A, Karvonen M J, Aravanis C, Blackburn H et al. (1986) The diet and 15-year death rate in the seven countries study. , American journal of epidemiology 124(6), 903-15.
    14.Teixeira B, Marques A, Ramos C, Serrano C, Matos O et al. (2013) Chemical composition and bioactivity of different oregano (Origanum vulgare) extracts and essential oil. , Journal of the science of food and agriculture 93(11), 2707-14.
    15.Grondona E, Gatti G, Lopez A G, Sanchez L R, Rivero V et al. (2014) Bio-efficacy of the essential oil of oregano (Origanum vulgare Lamiaceae. Ssp. Hirtum). Plant foods for human nutrition. , (Dordrecht, Netherlands) 69(4), 351-7.
    16.Vujicic M, Nikolic I, Kontogianni V G, Saksida T, Charisiadis P et al. (2015) Methanolic extract of Origanum vulgare ameliorates type 1 diabetes through antioxidant, anti-inflammatory and anti-apoptotic activity. The British journal of nutrition. 113(5), 770-82.
    17.Garcia-Diez J, Alheiro J, Pinto A L, Soares L, Falco V et al. (2017) . Influence of Food Characteristics and Food Additives on the Antimicrobial Effect of Garlic and Oregano Essential Oils. Foods , (Basel, Switzerland) 6-6.
    18.Silva N, Alves S, Goncalves A, Amaral J S, Poeta P. (2013) Antimicrobial activity of essential oils from Mediterranean aromatic plants against several foodborne and spoilage bacteria. Food science and technology international = Ciencia y tecnologia de los alimentos internacional. 19(6), 503-10.
    19.Oswell N J, Thippareddi H, Pegg R B. (2018) Practical use of natural antioxidants in meat products in the U.S.: A review. , Meat science 145, 469-79.
    20.Brul S, Coote P. (1999) Preservative agents in foods. Mode of action and microbial resistance mechanisms. International journal of food microbiology. 50(12), 1-17.
    21.Pandey H, Kumar V, Roy B K. (2014) Assessment of genotoxicity of some common food preservatives using Allium cepa L. as a test plant. Toxicology reports. 1, 300-8.
    22.Parke D V, Lewis D F. (1992) Safety aspects of food preservatives. Food additives and contaminants. 9(5), 561-77.
    23.RPP Fernandes, Trindade M A, Tonin F G, SMP Pugine, Lima C G et al. (2017) Evaluation of oxidative stability of lamb burger with Origanum vulgare extract. Food chemistry. 233, 101-9.
    24.Mueller K, Blum N M, Mueller A S. (2013) Examination of the Anti-Inflammatory, Antioxidant, and Xenobiotic-Inducing Potential of Broccoli Extract and Various Essential Oils during a Mild DSS-Induced Colitis in Rats. ISRN gastroenterology. 2013-710856.
    25.Bozin B, Mimica-Dukic N, Simin N, Anackov G. (2006) Characterization of the volatile composition of essential oils of some lamiaceae spices and the antimicrobial and antioxidant activities of the entire oils. Journal of agricultural and food chemistry. 54(5), 1822-8.
    26.Mancini E, Camele I, Elshafie H S, L De Martino, Pellegrino C et al. (2014) Chemical composition and biological activity of the essential oil of Origanum vulgare ssp. hirtum from different areas in the Southern Apennines (Italy). Chemistry & biodiversity. 11(4), 639-51.
    27.Martins N, Barros L, Santos-Buelga C, Henriques M, Silva S et al. (2014) Decoction, infusion and hydroalcoholic extract of Origanum vulgare L.: different performances regarding bioactivity and phenolic compounds. Food chemistry. 158, 73-80.
    28.Rodrigues M R, Krause L C, Caramao E B, dos Santos JG, Dariva C et al. (2014) Chemical composition and extraction yield of the extract of Origanum vulgare obtained from sub- and supercritical CO2. Journal of agricultural and food chemistry. 52(10), 3042-7.
    29.Kozlowska M, Laudy A E, Przybyl J, Ziarno M, Majewska E. (2015) . Epub 2015/12/10. PubMed PMID: , CHEMICAL COMPOSITION AND ANTIBACTERIAL ACTIVITY OF SOME MEDICINAL PLANTS FROM LAMIACEAE FAMILY. Acta poloniae pharmaceutica 72(4), 757-67.
    30.Coccimiglio J, Alipour M, Jiang Z H, Gottardo C, Suntres Z. (2016) Antioxidant, Antibacterial, and Cytotoxic Activities of the Ethanolic Origanum vulgare Extract and Its Major Constituents. Oxidative medicine and cellular longevity. 2016-1404505.
    31.Hernandez-Hernandez E, Regalado-Gonzalez C, Vazquez-Landaverde P, Guerrero-Legarreta I, Garcia-Almendarez B E. (2014) Microencapsulation, chemical characterization, and antimicrobial activity of Mexican (Lippia graveolens H.B.K.) and European (Origanum vulgare L.) oregano essential oils. , TheScientificWorldJournal 2014-641814.
    32.Ulusoy B, Hecer C, Kaynarca D, Berkan S. (2018) Effect of Oregano Essential Oil and Aqueous Oregano Infusion Application on Microbiological Properties of Samarella (Tsamarella), a Traditional Meat Product of Cyprus. Foods. , (Basel, Switzerland) 7-4.
    33.Aguilar F, Autrup H, Barlow S, Castle L, Crebelli R et al. (2008) Use of Rosemary Extracts as a food additive - Scientific opinion of the panel on food additives, flavourings, processing aids and materials in contact with food. , The EFSA 8(7), 1-29.
    34.Krishnan K R, Babuskin S, Babu P A, Fayidh M A, Sabina K et al. (2014) Bio protection and preservation of raw beef meat using pungent aromatic plant substances. , Journal of the science of food and agriculture 94(12), 2456-63.
    35.Vichi S, Zitterl-Eglseer K, Jugl M, Franz C. (2001) Determination of the presence of antioxidants deriving from sage and oregano extracts added to animal fat by means of assessment of the radical scavenging capacity by photochemiluminescence analysis. , Die Nahrung 45(2), 101-4.
    36.Bhargava K, Conti D S, da Rocha SR, Zhang Y. (2015) Application of an oregano oil nanoemulsion to the control of foodborne bacteria on fresh lettuce. Food microbiology. 47, 69-73.
    37.Paparella A, Mazzarrino G, Chaves-Lopez C, Rossi C, Sacchetti G et al. (2016) Chitosan boosts the antimicrobial activity of Origanum vulgare essential oil in modified atmosphere packaged pork. Food microbiology. 59, 23-31.
    38.Hulankova R, Borilova G, Steinhauserova I. (2013) Combined antimicrobial effect of oregano essential oil and caprylic acid in minced beef. , Meat science 95(2).
    39.de Sousa LL, de Andra, Athayde A J, de Oliveira CE, de Sales CV et al. (2013) Efficacy of Origanum vulgare L. and Rosmarinus officinalis L. essential oils in combination to control postharvest pathogenic Aspergilli and autochthonous mycoflora in Vitis labrusca L. (table grapes). International journal of food microbiology. 165(3), 312-8.
    40.Sampaio G R, Saldanha T, Soares R A, Torres E A. (2012) Effect of natural antioxidant combinations on lipid oxidation in cooked chicken meat during refrigerated storage. Food chemistry. 135(3), 1383-90.
    41.Chuang L T, Tsai T H, Lien T J, Huang W C, Liu J J et al. (2018) Ethanolic Extract of Origanum vulgare Suppresses Propionibacterium acnes-Induced Inflammatory Responses in Human Monocyte and Mouse Ear Edema Models. Molecules. , (Basel, Switzerland) 23(8), 10-3390.
    42.Bukovska A, Cikos S, Juhas S, Il'kova G, Rehak P et al. (2007) Effects of a combination of thyme and oregano essential oils on TNBS-induced colitis in mice. Mediators Inflamm,2007-23296.

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    1.Camacho Santiago, 2019, Research in Basic Sciences Is Essential for Creating New Ideas for Practice and Learning of Surgery, Journal of Investigative Surgery, (), 1, 10.1080/08941939.2019.1651923