Salvia officinalis L. and Salvia sclarea Essential Oils: Chemical Composition, Biological Activities and Preservative Effects against Listeria monocytogenes Inoculated into Minced Beef Meat
Abstract
:1. Introduction
2. Results and Discussion
2.1. GC-MS Analyses
2.2. Antioxidant Capacities of SOEO and SCEO
2.3. Antibacterial Properties of SCEO and SOEO
2.4. Application of SOEO, SCEO Alone and in Combination for Preservation of Minced Beef Meat during 14 Days of Refrigerated Storage
2.4.1. Chemical Stability Changes
2.4.2. Microbiological Evaluation
2.4.3. Effective Action of Essential Oils on Listeria monocytogenes Inoculated into Minced Beef Meat
2.4.4. Sensory Evaluation of Beef Minced Meat
2.4.5. Chemometric Approaches
3. Materials and Methods
3.1. Materials
3.2. GC-MS Analyses of EOs
3.3. Antioxidant Activity
3.3.1. Phosphomolybdenum Assay
3.3.2. DPPH Radical Scavenging Activity
3.4. Antibacterial Activity
3.4.1. Microbial Strains
3.4.2. Agar Diffusion Sensitivity Test
3.5. Determination of Minimum Inhibitory and Bactericidal Concentrations of the EOs
3.6. Analysis of Beef Meat Samples
3.6.1. Physiochemical Analysis
pH Analysis
Evaluation of Protein and Lipid Oxidation
3.7. Microbiological Analysis
Inhibitory Effect of SCEO, SOEO Alone and in Combination against Listeria Monocytogenes Inoculated into Minced Beef Meat
3.8. Sensory Evaluation
3.9. Statistical Evaluation
4. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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N° | Component 1 | LRI 2 | LRI 3 | SOEO 4 (%) | SCEO 5 (%) |
---|---|---|---|---|---|
1 | α-pinene | 938 | 943 | 4.8 ± 0.03 | Tr |
2 | camphene | 941 | 946 | 6.9 ± 0.03 | - |
3 | 1-octen-3-ol | 960 | 964 | 0.2 ± 0.01 | - |
4 | β-pinene | 973 | 980 | 14.5 ± 0.08 | - |
5 | β-myrcene | 982 | 987 | - | 0.5 ± 0.02 |
6 | α-terpinene | 1018 | 1020 | 0.1 ± 0.00 | - |
7 | p-cymene | 1028 | 1026 | 0.2 ± 0.01 | - |
8 | trans-β-ocimene | 1051 | 1048 | 0.2 ± 0.02 | 0.1 ± 0.00 |
9 | limonene | 1031 | 1029 | 2.4 ± 0.02 | 0.1 ± 0.01 |
10 | 1,8-cineole | 1035 | 1033 | 2.6 ± 0.02 | - |
11 | γ-terpinene | 1051 | 1048 | 0.4 ± 0.01 | - |
12 | trans-sabinene hydrate | 1055 | 1053 | 0.2 ± 0.02 | - |
13 | α-ocimene | 1060 | 1057 | - | 0.4 ± 0.02 |
14 | terpinolene | 1090 | 1087 | 0.3 ± 0.01 | - |
15 | linalool | 1095 | 1092 | 0.3 ± 0.01 | 11.3 ± 0.05 |
16 | α-thujone | 1105 | 1097 | 12.9 ± 0.06 | - |
17 | camphor | 1141 | 1139 | 19.0 ± 0.07 | 0.1 ± 0.01 |
18 | trans-3-pinanone | 1145 | 1141 | 0.8 ± 0.01 | - |
19 | L-borneol | 1150 | 1152 | 3.4 ± 0.03 | - |
20 | terpinen-4-ol | 1178 | 1182 | 0.4 ± 0.02 | 2.0 ± 0.02 |
21 | linalyl formate | 1201 | 1206 | - | 0.1 ± 0.01 |
22 | cis-geraniol | 1230 | 1227 | - | 0.4 ± 0.02 |
23 | linalyl acetate | 1255 | 1252 | - | 59.3 ± 1.14 |
24 | bornyl acetate | 1287 | 1290 | 5.6 ± 0.02 | 0.2 ± 0.01 |
25 | nerol acetate | 1322 | 1326 | - | 1.5 ± 0.02 |
26 | α-cubebene | 1352 | 1350 | 0.3 ± 0.01 | - |
27 | geranyl acetate | 1371 | 1366 | - | 2.5 ± 0.02 |
28 | α-copaene | 1381 | 1379 | 0.8 ± 0.02 | 1.2 ± 0.02 |
29 | (-)-β-bourbonene | 1390 | 1388 | 0.1 ± 0.00 | - |
30 | β-caryophyllene | 1445 | 1440 | 1.2 ± 0.04 | 3.7 ± 0.02 |
31 | γ-gurjunene | 1447 | 1444 | - | 0.8 ± 0.02 |
32 | aromadendrene | 1463 | 1460 | 3.3 ± 0.06 | 0.4 ± 0.01 |
33 | humulene | 1477 | 1473 | 11.9 ± 0.08 | 1.7 ± 0.03 |
34 | γ-muurolene | 1490 | 1486 | 1.6 ± 0.03 | - |
35 | germacrene D | 1492 | 1489 | 0.3 ± 0.02 | 10.5 ± 0.04 |
36 | ledene | 1498 | 1496 | 1.6 ± 0.03 | - |
37 | bicyclogermacrene | 1506 | 1504 * | - | 0.8 ± 0.03 |
38 | δ-cadinene | 1511 | 1509 * | 1.6 ± 0.02 | 0.7 ± 0.02 |
39 | α-calacorene | 1531 | 1528 | Tr | - |
40 | spathulenol | 1567 | 1563 | 0.7 ± 0.03 | 0.3 ± 0.02 |
41 | globulol | 1581 | 1576 | 0.1 ± 0.02 | - |
42 | caryophyllene oxide | 1583 | 1580 | 0.2 ± 0.02 | 0.2 ± 0.02 |
43 | humulene epoxide II | 1615 | 1611 | 0.6 ± 0.02 | 0.3 ± 0.02 |
44 | α-eudesmol | 1655 | 1650 | - | 0.1 ± 0.01 |
45 | β-eudesmol | 1657 | 1652 | - | 0.1 ± 0.00 |
46 | α-cadinol | 1682 | 1676 | Tr | - |
47 | geranyl-p-cymene | 1996 | 1993 | - | 0.6 ± 0.03 |
SUM | 99.5 | 99.9 | |||
Monoterpene hydrocarbons | 54.9 | 71.9 | |||
Oxygenated monoterpenes | 20.3 | 6.4 | |||
Sesquiterpene hydrocarbons | 21.1 | 19.8 | |||
Oxygenated sesquiterpene | 1.6 | 1.0 | |||
Others | 0.6 | 0.8 |
Diameter of Inhibition Zones (mm) | ||||
---|---|---|---|---|
SOEO | SCEO | |||
Concentration (µg/mL) | 25.0 | 50.0 | 25.0 | 50.0 |
Gram positive | ||||
Bacillus cereus ATCC 14579 | - | - | 17.0 ± 0.71 | 23.0 ± 0.02 |
Staphylococcus aureus ATCC 25923 | 12.0 ± 0.04 | 14.0 ± 0.12 | 17.0 ± 0.01 | 21.0 ± 0.45 |
Enterococcus faecalis ATCC 29212 | 8.0 ± 0.14 | 9.0 ± 0.23 | 14.0 ± 0.24 | 17.0 ± 0.22 |
Micrococcus luteus ATCC 1880 | 12.0 ± 0.12 | 14.0 ± 0.75 | 19.0 ± 0.14 | 25.0 ± 0.21 |
Listeria monocytogenes ATCC 1911 | - | - | 17.0 ± 0.12 | 20.0 ± 0.42 |
Gram negative | ||||
Pseudomonas aeruginosa ATCC 9027 | - | - | - | - |
Escherichia coli ATCC 25922 | - | - | - | - |
Salmonella enterica ATCC 43972 | - | 15.0 ± 0.01 | - | - |
Bacterial Strains | MIC | MBC | MBC/MIC | Interpretation |
---|---|---|---|---|
Salvia officinalis | ||||
Gram positive | ||||
Bacillus cereus ATCC 14579 Staphylococcus aureus ATCC 25923 | 5.6 ± 0.68 5.6 ± 0.68 | 11.2 ± 0.3 11.2 ± 0.3 | 2 2 | Bactericidal Bactericidal |
Enterococcus faecalis ATCC 29212 Micrococcus luteus ATCC 1880 | 5.6 ± 0.68 4.6 ± 0.03 | 22.5 ± 0.6 11.5 ± 0.3 | 4 2 | Bacteriostatic Bactericidal |
Listeria monocytogenes ATCC 1911 | 4.6 ± 0.03 | 15 ± 0.0 | 3 | Bacteriostatic |
Gram negative | ||||
Pseudomonas aeruginosa ATCC 9027 | 7.5 ± 0.00 | 11.2 ± 0.3 | 0.5 | Bactericidal |
Escherichia coli ATCC 25922 | 7.5 ± 0.31 | 11.2 ± 0.3 | 1 | Bactericidal |
Salmonella enterica ATCC 43972 | 4.6 ± 0.03 | 11.2 ± 0.3 | 0.7 | Bactericidal |
Salvia sclarea | ||||
Gram positive | ||||
Bacillus cereus ATCC 14579 Staphylococcus aureus ATCC 25923 | 7.5 ± 0.00 5.6 ± 0.68 | 15 ± 0.0 15 ± 0.0 | 2 2 | Bactericidal Bactericidal |
Enterococcus faecalis ATCC 29212 Micrococcus luteus ATCC 1880 | 7.5 ± 0.00 7.5 ± 0.00 | 18.7 ± 0.9 15 ± 0.0 | 2 2 | Bactericidal Bactericidal |
Listeria monocytogenes ATCC 1911 | 4.6 ± 0.31 | 18.7 ± 0.9 | 4 | Bacteriostatic |
Gram negative | ||||
Pseudomonas aeruginosa ATCC 9027 | 11.2 ± 0.31 | 15 ± 0.0 | 1 | Bactericidal |
Escherichia coli ATCC 25922 | 3.7 ± 0.00 | 22.5 ± 0.6 | 6 | Bacteriostatic |
Salmonella enterica ATCC 43972 | 7.5 ± 0.00 | 22.5 ± 0.6 | 3 | Bacteriostatic |
Samples | pH Trend During the Days of Refrigerated Storage at 4 °C | ||||
---|---|---|---|---|---|
0 | 3 | 7 | 10 | 14 | |
Control | 5.15 ± 0.07 aA | 5.58 ± 0.00 bC | 5.89 ± 0.04 cC | 6.62 ± 0.05 Dd | 7.85 ± 0.05 eD |
BHT | 5.25 ± 0.06 aA | 5.32 ± 0.14 bB | 5.72 ± 0.08 bcBC | 6.29 ± 0.05 cC | 6.96 ± 0.08 cC |
SCEO | 5.10 ± 0.13 aA | 5.32 ± 0.14 bB | 5.65 ± 0.03 bB | 6.09 ± 0.01 cB | 6.52 ± 0.02 cB |
SOEO | 5.30 ± 0.014 aA | 5.41 ± 0.28 aB | 5.63 ± 0.01 bB | 6.01 ± 0.02 bB | 6.46 ± 0.02 bB |
SCEO + SOEO | 5.19 ± 0.07 aA | 5.25 ± 0.07 aA | 5.43 ± 0.08 aA | 5.67 ± 0.02 aA | 5.94 ± 0.05 bA |
Samples | Days of Refrigerated Storage | ||||
---|---|---|---|---|---|
0 | 3 | 7 | 10 | 14 | |
Enterobacteriaceae Counts (log CFU/g) | |||||
Control | <1 aA | 1.25 ± 0.02 bAB | 2.25 ± 0.06 bB | 2.79 ± 0.24 dBC | 3.36 ± 0.07 aC |
BHT | <1 aA | 1.06 ± 0.06 bAB | 1.99 ± 0.01 abB | 2.52 ± 0.18 cBC | 2.84 ± 0.15 aC |
SCEO | <1 aA | <1 aA | 1.33 ± 0.91 bAB | 1.70 ± 0.10 cB | 2.11 ± 0.02 cC |
SOEO | <1 aA | 1.24 ± 0.19 aAB | 1.92 ± 0.14 abAB | 2.01 ± 0.03 bBC | 2.26 ± 0.1 bC |
SCEO + SOEO | <1 aA | <1 aA | <1 aA | <1 aA | 1.68 ± 0.29 aB |
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Ben Akacha, B.; Ben Hsouna, A.; Generalić Mekinić, I.; Ben Belgacem, A.; Ben Saad, R.; Mnif, W.; Kačániová, M.; Garzoli, S. Salvia officinalis L. and Salvia sclarea Essential Oils: Chemical Composition, Biological Activities and Preservative Effects against Listeria monocytogenes Inoculated into Minced Beef Meat. Plants 2023, 12, 3385. https://doi.org/10.3390/plants12193385
Ben Akacha B, Ben Hsouna A, Generalić Mekinić I, Ben Belgacem A, Ben Saad R, Mnif W, Kačániová M, Garzoli S. Salvia officinalis L. and Salvia sclarea Essential Oils: Chemical Composition, Biological Activities and Preservative Effects against Listeria monocytogenes Inoculated into Minced Beef Meat. Plants. 2023; 12(19):3385. https://doi.org/10.3390/plants12193385
Chicago/Turabian StyleBen Akacha, Boutheina, Anis Ben Hsouna, Ivana Generalić Mekinić, Améni Ben Belgacem, Rania Ben Saad, Wissem Mnif, Miroslava Kačániová, and Stefania Garzoli. 2023. "Salvia officinalis L. and Salvia sclarea Essential Oils: Chemical Composition, Biological Activities and Preservative Effects against Listeria monocytogenes Inoculated into Minced Beef Meat" Plants 12, no. 19: 3385. https://doi.org/10.3390/plants12193385