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Antibacterial and Antifungal Activities of Spices

Infectious diseases caused by pathogens and food poisoning caused by spoilage microorganisms are threatening human health all over the world. The efficacies of some antimicrobial agents, which are currently used to extend shelf-life and increase the safety of food products in food industry and to inhibit disease-causing microorganisms in medicine, have been weakened by microbial resistance. Therefore, new antimicrobial agents that could overcome this resistance need to be discovered. Many spices—such as clove, oregano, thyme, cinnamon, and cumin—possessed significant antibacterial and antifungal activities against food spoilage bacteria like Bacillus subtilis and Pseudomonas fluorescens, pathogens like Staphylococcus aureus and Vibrio parahaemolyticus, harmful fungi like Aspergillus flavus, even antibiotic resistant microorganisms such as methicillin resistant Staphylococcus aureus. Therefore, spices have a great potential to be developed as new and safe antimicrobial agents. This review summarizes scientific studies on the antibacterial and antifungal activities of several spices and their derivatives.


Introduction
Microbial pathogens in food may cause spoilage and contribute to foodborne disease incidence, and the emergence of multidrug resistant and disinfectant resistant bacteria-such as Staphylococcus aureus (S. aureus), Escherichia coli (E. coli), and Pseudomonas aeruginosa (P. aeruginosa)-has increased rapidly, causing the increase of morbidity and mortality [1]. Weak acids such as benzoic and sorbic acids [2], which are commonly applied in food industry as chemical preservatives to increase the safety and stability of manufactured foods on its whole shelf-life by controlling pathogenic and spoilage food-related microorganisms [3], can result in the development of microbiological resistance [4]. Moreover, chemical preservatives cannot completely eliminate several pathogenic bacteria like Listeria monocytogenes (L. monocytogenes) in food products or delay the growth of spoilage microorganisms [5]. Natural products, as substitutes of synthetic chemical preservatives, are increasingly accepted because they are innately better tolerated in human body and have inherent superiorities for food industry [4]. The antimicrobial activities of natural products are necessary to be studied and applied in food industry.
Morbidity and mortality are mainly caused by infectious diseases all over the world. The World Health Organization reported that 55 million people died worldwide in 2011, with one-third of the deaths owing to infectious diseases [6]. Antibiotic resistant microorganisms can increase mortality rates because they can survive and recover through their ability to acquire and transmit resistance S. aureus, B. cereus, and L. monocytogenes. The films prepared by low molecular mass chitosan with 2% EO and ethyl heptanoate extract from clove showed antimicrobial activities against a majority of the tested strains. In another study, the researchers tested the antimicrobial activities of EOs and functional extracts of cumin, clove, and elecampane against E. coli, S. typhimurium, B. cereus, S. aureus, and L. monocytogenes by determining the MICs and MBCs [31]. They also evaluated the antibacterial activities of edible films prepared by EOs and functional extracts of spices based on chitosan polymeric structure against the same bacteria by determining the DIZs. Clove EO showed the best inhibitory effects with the MIC of 500 mg/L on all the bacteria tested, clove extracts showed very similar MICs to those of EO, except ethyl caproate extract of clove against L. monocytogenes (MIC of 750 mg/L) and ethyl heptanoate extract of clove against B. cereus (MIC of 250 mg/L). Among the chitosan films added with EOs, only clove showed inhibition zones of all tested bacteria except L. monocytogenes. The ethyl heptanoate extract of clove film also possessed antibacterial activities against all tested bacteria, weaker than those of clove EO though. Liu et al. [32] evaluated the antimicrobial activities of spice EOs against microbial populations in chilled pork stored in PE film antimicrobial package using the disk diffusion method to determine the DIZs and serial dilution assay to determine the MICs. Clove EO was the most effective against microorganisms tested among all the spice EOs tested. The MICs of clove EO were 0.10%, 0.10%, and 0.30% v/v against Enterobacteriaceae, S. aureus, and Pseudomonas sp., respectively. Spice EOs possessed the ability to decrease the number of spoilage populations, but not the species diversity of spoilage microbiota.
Collectively, clove EO and extracts could prevent against some food spoilage and foodborne pathogens (Table 1), especially Gram-positive bacteria. The MICs of clove were less than 2.5% against tested microorganisms like P. fluorescens, S. typhimurium, E. coli, B. cereus, and L. innocua. Generally speaking, the qualities of the papers cited are good and the results are reliable. Table 1. Antibacterial and antifungal activities of clove.

Type of Samples Bacteria and Fungi Main Results Reference
Clove and cinnamon water extracts Staphylococcus aureus and Escherichia coli Both in vivo and in vitro results confirmed the efficacy of clove extract as natural antimicrobials. [18]

Oregano
Oregano (Origanum vulgare), belonging to family Lamiaceae, has been used as food seasoning and flavoring for a long time. The major components associated with antimicrobial activities in oregano EO were proved to be carvacrol and thymol [33].

Antimicrobial Activities of Oregano
Babacan et al. [34] evaluated the antimicrobial activities of oregano extract against various Salmonella serotypes by evaluating the bacterial growth with disc diffusion method. The results showed that DIZs of oregano were 15, 19, and 16 mm for Salmonella gallinarum (S. gallinarum), Salmonella enteritidis (S. enteritidis), and S. typhimurium, respectively. Santoyo et al. [35] observed the antimicrobial activities of EO-rich fractions of oregano which were selectively precipitated in the second separator in different conditions against six microorganism strains (S. aureus, Bacillus subtilis (B. subtilis), E. coli, P. aeruginosa, C. albicans, and Aspergillus niger (A. niger)), using the disk diffusion and broth dilution methods. The results showed that all of the supercritical fluid extraction fractions exhibited antimicrobial effects on tested microorganisms, and the most efficient fraction was obtained with 7% ethanol at 150 bar and 40 • C. De Souza et al. [36] evaluated the effects of heating (at the temperatures of 60, 80, 100, and 120 • C, at a duration of 1 h for each) on the antimicrobial activities of oregano EO against 9 microorganism strains (C. albicans, Candida krusei (C. krusei), Candida tropicalis (C. tropicalis), B. cereus, E. coli, S. aureus, Yersinia enterocolitica (Y. enterocolitica), S. enterica, and Serratia marcescens (S. marcescens)), using the solid medium diffusion procedure. The results indicated that heating treatment showed no significant effects on the antimicrobial activities of EO, with the DIZs and MICs of heated EO close to those of EO kept at room temperature (MICs ranging from 10 to 40 µL/mL).
Oregano could bind to sterols in the fungal membranes of C. albicans strains [37], but the exact mechanisms of action on other microorganisms are to be further studied. Carvacrol, one of the major components of oregano, could interact with cell membranes through changing the permeability for small cations [38]. As the chemical compounds in EO and extracts of oregano are complex, they could inhibit microorganisms through different cell targets.

Comparison of Antimicrobial Activities of Oregano and Other Spices
Ozcan et al. [39] investigated the antifungal activities of four spice decoctions against six molds (Fusarium oxysporum f. sp. phaseoli, Macrophomina phaseoli (M. phaseoli), Botrytis cinerea (B. cinerea), Rhizoctonia solani (R. solani), Alternaria solani (A. solani), and Alternaria parasiticus (A. parasiticus)). The results showed that the mycelial growth were 100% inhibited by 10% oregano decoction in culture medium. Ai-Turki et al. [40] tested the antimicrobial activities of aqueous extracts of four plants against E. coli and B. subtilis using the disc diffusion method. Oregano extract showed the best antibacterial effects on two bacteria compared with three other spice extracts, and B. subtilis showed more sensitivity than E. coli. Marques et al. [41] assessed the antimicrobial activities of the EOs of oregano and marjoram against S. aureus isolated from poultry meat using the disk diffusion method, and the MICs and MBCs were tested using the microdilution technique. All the S. aureus strains were susceptible to oregano EO with the MICs ranging from 6.25 to 25 µL/mL, but four of the isolates were resistant to ampicillin and one was resistant to tetracycline. Bozin et al. [42] investigated the antimicrobial activities of 3 spice EOs against 13 bacterial strains using the hole-plate agar diffusion method and 6 fungi by the microdilution technique. The results indicated that the most effective antibacterial activities were expressed by oregano EO, even on multiresistant strains of P. aeruginosa and E. coli. Viuda-Martos et al. [43] studied the antimicrobial activities of EOs from six spices against six bacteria (Lactobacillus curvatus (L. curvatus), Lactobacillus sakei (L. sakei), Staphylococcus carnosus (S. carnosus), Staphylococcus xylosus (S. xylosus), Enterobacter gergoviae (E. gergoviae) and Enterobacter amnigenus (E. amnigenus)), using the disc diffusion method. Oregano EO was the most effective against bacteria tested, with DIZs ranging from 35.29 mm (S. xylosus) to 57.90 mm (E. amnigenus). Santurio et al. [44] reported the antimicrobial activities of EOs of eight spices against E. coli strains isolated from poultry and cattle faeces by determining the MICs using the broth microdilution technique. The results showed that the most effective against all E. coli strains in the study was oregano EO. Khosravi et al. [45] investigated the antifungal activities of Artemisia sieberi and oregano EOs against Candida glabrata (C. glabrata) isolated from patients with vulvovaginal candidiasis by determining the MICs and minimal fungicidal concentrations (MFCs), using the broth macrodilution method. The results indicated that the EOs inhibited all tested C. glabrata isolates concentration-dependently, with the MICs ranging from 0.5 to 1100 µg/mL (mean: 340.2 µg/mL) for oregano. Dal Pozzo et al. [46] studied the antimicrobial activities of 7 spice EOs, and some majority constituents of these spices such as carvacrol, thymol, cinnamaldehyde, and cineole against 33 Staphylococcus spp. isolates from herds of dairy goats, by determining the MICs and MBCs using the broth microdilution method. Oregano and thyme possessed equally strong antimicrobial activities among EOs. Santos et al. [47] evaluated the antimicrobial activities of four spices against several bacteria like S. aureus and E. coli isolated from vongole and bacteria standard ATCC (American Type Culture Collection): E. coli, S. aureus, and Salmonella choleraesuis (S. choleraesuis), by determining the MICs using diffusion test. Oregano and clove EOs presented antimicrobial activities against all tested bacteria, but oregano presented larger DIZs of 26.7 mm (E. coli) and 29.3 mm (S. aureus). Hyun et al. [48] tested the antibacterial effects of various spice EOs including oregano on total mesophilic microorganisms in products (fresh leaf lettuce and radish sprouts) using the dipping method. One species of oregano (in the USA) EO showed the best effects on maintaining reduced levels of total mesophilic microorganisms in fresh leaf lettuce and radish sprouts compared with the control.

The Application of Oregano as Antimicrobial Agents in Food Packaging
The antimicrobial effects of pure EOs of four spices and chitosan-EOs films on L. monocytogenes and E. coli were evaluated in vitro by agar diffusion test [49]. The antimicrobial activities of EOs alone and incorporated in the films were similar following the order: oregano >> coriander > basil > anise. When used in inoculated bologna samples at 10 • C and stored for five days, pure chitosan films led to 2 log reduction of L. monocytogenes, 3.6-4 log reduction of L. monocytogenes, and 3 log reduction of E. coli were observed in films incorporated with 1% and 2% oregano EO.
All the above studies are of good quality, and oregano showed strong antimicrobial activities against microorganism strains such as Staphylococcus spp. and S. aureus isolates with larger DIZs and lower MICs, MBCs, and MFCs compared with several other spices (Table 2). Future studies could focus on the application of oregano and its EO in food industry, and also the possible mode of action. Various spice EOs Microorganisms in fresh leaf lettuce and radish sprouts. Oregano-2 (in the USA) oil was the most effective at maintaining the reduced levels of total mesophilic microorganisms. [48] Pure EOs of 4 spices and chitosan-EOs films L. monocytogenes and E. coli Both oregano EO alone and incorporated in the films possessed the best antimicrobial activities. [49]

Thyme
Thyme (Thymus vulgaris), belonging to family Lamiaceae, is a subshrub native to the western Mediterranean region. Thyme is widely used as a spice to add special flavor to foods. In recent studies, thyme was found to possess efficient antimicrobial activities and was used in some foods to extend the shelf-life [50].

Antimicrobial Activities of Thyme
A study evaluated the antimicrobial activities of thyme EO against bacteria (B. subtilis, S. aureus, Staphylococcus epidermidis (S. epidermidis), P. aeruginosa, E. coli, and Mycobacterium smegmatis (M. smegmatis)) and fungal strains (C. albicans and Candida vaginalis) [51]. Thyme EO showed effective bactericidal and antifungal activities against tested microorganism strains with MICs ranging from 75 to 1100 µg/mL for bacteria, and from 80 to 97 µg/mL for fungi. In another study, EOs obtained from thyme harvested at four ontogenetic stages were tested for their antibacterial activities against nine strains of Gram-negative bacteria and six strains of Gram-positive bacteria using the bioimpedance method to test the bacteriostatic activities and plate counting technique to study the inhibitory effects by direct contact [52]. The results indicated that all the thyme EOs had significant bacteriostatic activities against the microorganisms tested. Furthermore, the antimicrobial activities of EOs of four Thymus species (T. vulgaris, T. serpyllum, T. pulegioides, and T. glabrescens) were determined by agar diffusion method [53]. T. vulgaris and T. serpyllum EOs were the most efficient as they inhibited all the tested bacteria (P. aeruginosa, Cronobacter sakazakii (C. sakazakii), L. innocua, and Streptococcus pyogenes (S. pyogenes)) and yeasts (C. albicans and Saccharomyces cerevisiae (S. cerevisiae)) both at original and half-diluted concentrations. P. aeruginosa, L. innocua, and S. pyogenes were highly and equally sensitive to the Thymus oils, while C. sakazakii exhibited limited sensitivity, and the sensitivity of the two yeast strains were similar to that of C. sakazakii, but S. cerevisiae was a little more sensitive than C. albicans.
The major active compound of thyme is thymol, which exerted its antimicrobial action through binding to membrane proteins by hydrophobic bonding and hydrogen bonding, and then changing the permeability of the membranes [20]. Thymol also decreased intracellular adenosine triphosphate (ATP) content of E. coli and increased extracellular ATP, which could disrupt the function of plasma membranes [54]. As thymol was proved to act differently against Gram-positive and Gram-negative bacteria [20], the exact mechanisms of antimicrobial action should be further studied.

Comparison of Antimicrobial Activities of Thyme and Other Spices
Al-Turki et al. [55] reported the antibacterial activities of thyme, peppermint, sage, black pepper and garlic hydrosols against B. subtilis and S. enteritidis, using the agar disk diffusion method. Thyme hydrosol demonstrated more significant inhibitory effects on B. subtilis and S. enteritidis than sage, peppermint, and black pepper hydrosols, with the mean DIZs 20 mm for B. subtilis and 15 mm for S. enteritidis. According to another study, the antimicrobial effects of the six plant hydrosols on S. aureus, E. coli, S. typhimurium, P. aerugenosa, and C. albicans were tested by determining the microbial growth zones on hydrosol agar plates and control agar plates [56]. The results showed that at 15% thyme hydrosol completely inhibited E. coli and S. typhimurium, but C. albicans was inactive to the tested hydrosols. Girova et al. [57] assessed the antimicrobial activities of five plant EOs against psychrotrophic microorganisms (P. fluorescens, Pseudomonas putida (P. putida), P. fragi, B. thermosphacta, and C. albicans) isolated from spoiled chilled meat products and some reference strains (P. fluorescens ATCC 17397, P. putida NBIMCC (National Bank for Industrial Microorganisms and Cell Cultures) 561, P. aeruginosa ATCC 9027, and C. albicans ATCC 10231) using the method of disc diffusion and serial broth dilution. The results indicated that the antimicrobial effects of the EOs were equal at 37 • C and 4 • C. Thyme EO exhibited the highest antimicrobial activities with the MICs ranging from 0.05% to 0.8% w/v. Hajlaoui et al. [58] observed the anti-Vibrio alginolyticus (V. alginolyticus) activities of five aromatic plant EOs using agar well diffusion test, and the MICs and MBCs were examined using the broth microdilution susceptibility method. Thyme EO was proved to be the most efficient against 13 V. alginolyticus strains compared with 4 other EOs, with the MICs ranges of 0.078-0.31 mg/mL and MBCs ranges of 0.31-1.25 mg/mL. Also, Viuda-Martos et al. [59] assessed the growth inhibition of some indicators of spoilage bacteria strains (L. innocua, S. marcescens, and P. fluorescens) and the concentration effects of five spice EOs using the agar disc diffusion method. Only the EO of thyme showed inhibitive effects on all tested bacteria at all added doses (100%, 50%, 25%, 12.5%, and 5%). Aliakbarlu et al. [60] evaluated the antibacterial activities of EOs from thyme, Thymus kotschyanus, Ziziphora tenuior, and Ziziphora clinopodioides, against two Gram-positive bacteria (B. cereus and L. monocytogenes) and two Gram-negative bacteria (S. typhimurium and E. coli), using the agar disc diffusion and micro-well dilution assay. The EO of thyme showed the highest antibacterial activities, with the widest inhibition zones and the lowest MICs (0.312-1.25 µL/mL), and B. cereus was the most sensitive bacterium tested. Hyun et al. [48] investigated the antibacterial effects of several EOs on 18 pathogenic bacteria and 15 spoilage bacteria by agar disc diffusion test. The results showed that thyme-1 (T. vulgaris) EO and thyme-2 (T. vulgaris ct linalool) EO exerted the highest antibacterial activities against 18 pathogenic bacteria strains compared with other spices, except for P. aeruginosa. Thyme-1 EO also demonstrated the best antibacterial effects on spoilage bacteria. In addition, the antimicrobial effects of 17 spices and herbs against Shigella strains were tested in another study [61]. The MICs were determined by the agar dilution method with dried ground spices and herbs added to the broth and agar, and the results showed that MICs of thyme were 0.5-1% w/v for the Shigella strains. The study also used various combinations of temperatures (12,22, and 37 • C), pH values (5.0, 5.5, and 6.0), and NaCl concentrations (1%, 2%, 3%, and 4% w/v), and the inclusion or exclusion of thyme or basil at 1% w/v in a Mueller-Hinton agar model system to test the inhibitory effects of thyme and basil. In the presence of thyme, Shigella flexneri (S. flexneri) did not develop Colony-Forming Units (CFU) during the seven-day incubation period for 16 of the 18 tested combinations.
Some studies compared the antimicrobial activities of different extracts of thyme. Martins et al. [62] evaluated and compared the antimicrobial activities of the infusion, decoction, and hydroalcoholic extracts prepared from thyme against S. aureus, S. epidermidis, E. coli, Klebsiella spp., P. aeruginosa, Enterobacter aerogenes (E. aerogenes), Proteus vulgaris (P. vulgaris), and Enterobacter sakazakii (E. sakazakii) using the disc diffusion halo test. For Gram-positive species, thyme extracts only presented activity against S. epidermidis, and hydroalcoholic extract showed a lower antibacterial activity than decoction and infusion extracts, which showed the similar activities. For Gram-negative species, thyme extracts showed antimicrobial activities in the order of E. coli > P. vulgaris, P. aeruginosa > E. aerogenes = E. sakazakii; decoction and hydroalcoholic extracts had similar effects against the bacteria except P. aeruginosa, while the lowest activity was observed in infusion extracts. Moreover, the antifungal effects of thyme EO, hydrosol and propolis extracts on natural mycobiota on the surface of sucuk were evaluated [63]. The results showed that potassium sorbate (15% w/v, in water), thyme EO (10 mg/mL, in dimethyl sulfoxide), and propolis extract (50 mg/mL, in dimethyl sulfoxide) reduced by 4.88, 2.45, and 2.05 log CFU/g in yeast-mold counting compared with sterile water, respectively.
Aman et al. [64] analyzed the polyphenolic fractions and oil fractions of oilseeds from 4 spices, including thyme, for their antimicrobial activities against 35 bacterial strains. The results showed that oil fractions of all spice oilseeds were more active than their polyphenolic fractions, and thyme oil fraction had the highest antibacterial activities compared with other spice oilseeds. Aznar et al. [65] studied the growth of Candida lusitaniae (C. lusitaniae) on different concentrations of nisin (0.1-3 mmol/L), thymol (0.02-1.5 mmol/L), carvacrol (0.02-1 mmol/L), or cymene (0.02-3 mmol/L) in broths (pH = 5, 25 • C), and also evaluated the inhibitory activity of thymol against C. lusitaniae in tomato juice. Thymol, carvacrol, and cymene totally inhibited the yeast growth for more than 21 days at 25 • C when the concentrations were higher than 1 mmol/L. Compared with the control without thymol, the activity of thymol against C. lusitaniae in tomato juice was significant.
In conclusion, the results obtained from a number of investigations with good quality indicated that thyme possessed effective antimicrobial activities against several pathogenic and spoilage bacteria and fungi, like S. aureus and E. coli, with low MICs (≤1100 µL/mL) ( Table 3).

Cinnamon
Cinnamon (Cinnamomum zeylanicum), belonging to family Lauraceae, is widely applied in savory dishes, pickles, and soups [66]. Cinnamaldehyde, cinnamyl acetate, and cinnamyl alcohol are the three main compounds of cinnamon [67]. Due to its antimicrobial activities, cinnamon is also used in cosmetics or food products [11], and also used as health-promoting agents to treat diseases like inflammation, gastrointestinal disorders, and urinary infections [68,69].

Antimicrobial Activities of Cinnamon
The antimicrobial activities of cinnamon were evaluated in some studies. Gupta et al. [70] compared the antimicrobial activities of cinnamon extract (50% ethanol) and EO against 10 bacteria and 7 fungi by the agar well diffusion method. Cinnamon EO was more effective than cinnamon extract against tested microorganisms, with the MICs ranging from 1.25% to 5% v/v. Cinnamon EO exerted the strongest effect on B. cereus among bacteria, and Rhizomucor sp. among fungi. Cinnamon extract showed the highest activities against B. cereus among bacteria, and Penicillium sp. among fungi. Ceylan et al. [71] tested the antibacterial effects of cinnamon, sodium benzoate, potassium sorbate, and their combinations on E. coli at 8 and 25 • C in apple juice. The results showed that 0.3% w/v cinnamon provided 1.6 log CFU/mL reduction on E. coli at 8 • C and 2.0 log CFU/mL reduction at 25 • C. Cinnamon had synergistic effects with sodium benzoate and potassium sorbate on E. coli at 8 and 25 • C. Recently, the anti-biofilm effects of cinnamon EO and liposome-encapsulated cinnamon EO on methicillin resistant S. aureus (MRSA) were evaluated in a study by scanning electron microscopy and laser scanning confocal microscopy analyses [72]. Cinnamon EO possessed effective antibacterial activity and prominent anti-biofilm activity against MRSA. In the presence of liposomes, the stability and the acting time of cinnamon EO were further improved.
The major component of cinnamon, cinnamaldehyde, possesses antimicrobial effects on microorganisms, as it inhibited cell wall biosynthesis, membrane function, and specific enzyme activities. More specific cellular targets of cinnamaldehyde are still required to be studied in detail [73].

Comparison of Antimicrobial Activities of Cinnamon and Other Spices
Mvuemba et al. [74] evaluated the inhibitory effects of aqueous extracts of four spices (cinnamon, ginger, nutmeg, and horseradish) on the growth of mycelial of various spoilage pathogens (A. niger, Fusarium sambucinum (F. sambucinum), Pythium sulcatum (P. sulcatum), and Rhizopus stolonifera (R. stolonifera)). At the concentration of 0.05 g/mL, cinnamon extract totally inhibited A. niger and P. sulcatum, while at the level of 0.10 and 0.15 g/mL F. sambucinum and R. stolonifer were completely inhibited, respectively. Another study conducted by Wang et al. [75] tested the antibacterial effects of five plant aqueous extracts on five bacteria (S. aureus, Lactobacillus sp., B. thermosphacta, Pseudomonas spp., and E. coli) by the aerobic plate count method and disc diffusion. Cinnamon aqueous extract was the only one to inhibit all the tested microorganisms at the concentration of 1% w/v. The inhibitory effects were stronger with the increase of extract concentrations from 1% to 5% w/v. In the same way, the antimicrobial activities of the hydrosols of six spices (basil, clove, cardamom, cinnamon, mustard, and thyme) against five microorganisms (S. aureus, E. coli, S. typhimurium, P. aeruginosa, and C. albicans) were tested [56]. The inhibition percentage of cinnamon hydrosol was 10-33.8% at 5% v/v hydrosol, 10-66.5% at 10% v/v hydrosol, and 10-100% at 15% v/v hydrosol against microorganisms tested except C. albicans. Moreover, S. aureus was the most sensitive strain to cinnamon hydrosol, while P. aeruginosa was the least sensitive strain. Agaoglu et al. [76] examined the antimicrobial activities of diethyl ether extracts of six spices used in meat products against eight strains of bacteria (S. aureus, K. pneumoniae, P. aeruginosa, E. coli, Enterococcus faecalis (E. faecalis), M. smegmatis, Micrococcus luteus (M. luteus), and C. albicans), by the disc diffusion. Among all the spices tested, only cinnamon exerted inhibitory activities against all the tested microorganisms. S. aureus and C. albicans were the most sensitive to cinnamon, while E. coli was the least. Keskin et al. [27] investigated the antimicrobial effects of the ethyl acetate, acetone, and methanol extracts of 12 plant species on 8 bacterial and 2 fungi species using the disc assay. Cinnamon methanol extract exerted antimicrobial effects on all tested microorganisms, while the ethyl acetate extract showed inhibition against tested microorganisms except P. aeruginosa and R. rubra, and the acetone extract showed inhibition against tested microorganisms except R. rubra. Revati et al. [77] explored the antimicrobial activities of seven Indian spice ethanol extracts against Enterococci (including 215 enterococcal strains) isolated from human clinical samples with the agar well diffusion method. Crude ethanol extract of cinnamon was the most effective against all the clinical isolates of Enterococci, with the DIZs ranging from 31 to 34 mm. Moreover, the antimicrobial activities of 8 spice EOs against 6 bacterial species and 10 fungal species were tested in a study using the disk diffusion assay and MICs were determined using the agar dilution test [78]. Cinnamon EO possessed the strongest inhibition effects on all tested microorganisms among all spices examined with the MICs ranges of 0.015-2.0 mg/mL. Compared with bacteria, fungi were more sensitive to cinnamon EO.
Collectively, all the mentioned studies with good quality demonstrated that cinnamon showed antimicrobial activities covering a wide range of species, such as MRSA and A. niger, at low MICs (Table 4), indicating that cinnamon had great potential to provide health benefits through application in food industry. Table 4. Antibacterial and antifungal activities of cinnamon.

Type of Samples Tested Bacteria and Fungi Mian Results Reference
Cinnamon extract and oil 7 Gram-positive bacteria, 3 Gram-negative bacteria, and 7 fungi Cinnamon oil was more effective than cinnamon extract with MICs ranging from 1.25% to 5% v/v. [70] Cinnamon, sodium benzoate, potassium sorbate E. coli E. coli was reduced by 1.6 log CFU/mL at 8 • C and 2.0 log CFU/mL at 25 • C by 0.3% cinnamon. [71] Cinnamon oil and liposome-encapsulated cinnamon oil Methicillin resistant Staphylococcus aureus (MRSA) Cinnamon oil possessed effective antibacterial activity and prominent anti-biofilm activity against MRSA. [72] 4 spice aqueous extracts A. niger, Fusarium sambucinum, Pythium sulcatum, Rhizopus stolonifer 0.05 g/mL of cinnamon extract completely inhibited A. niger and P. sulcatum, 0.10 g/mL of cinnamon extract completely inhibited F. sambucinum. [

Cumin
Cumin (Cuminum cyminum) is an aromatic plant belonging to the Apiaceae family. Cumin has been used since ancient time as an ingredient in foods in Middle East, and cumin seeds have long been used as antiseptic and disinfectant in India [80]. Cuminaldehyde, cymene, and terpenoids are the major bioactive constituents of cumin EOs [81].

Antimicrobial Activities of Cumin
In a study, the antimicrobial activities of cumin EO against E. coli, S. aureus, S. faecalis, P. aeruginosa, and K. pneumoniae were investigated by agar diffusion and dilution methods [81]. E. coli, S. aureus, and S. faecalis were susceptive to various cumin EO dilutions while P. aeruginosa and K. pneumoniae were resistant. In another study, the antifungal activities of cumin seeds EO against 1230 fungi isolated from food samples were tested [82]. The EO was fungicidal to most of the fungal species, and exerted a broad spectrum of fungal toxicity at MIC (0.6 µL/mL) against all 19 foodborne fungi strains except R. stolonifer. Furthermore, Abd El Mageed et al. [83] explored the effects of microwaves on EO of cumin seeds on its antimicrobial activities against E. coli, S. aureus, P. aeruginosa, A. niger, A. parasiticus, and C. albicans using the disk diffusion method. Both microwave and conventionally (oven) roasted cumin oils had similar antimicrobial effects on microorganisms tested and were more effective than those of raw oils. Reza et al. [80] studied the effects of ã-irradiation (10 and 25 kGy) on the antibacterial activities of cumin against E. coli, P. aeruginosa, B. cereus, and S. aureus, by the agar well diffusion method and disk diffusion method. The results indicated that cumin EO exerted antibacterial effects on bacteria tested, and ã-irradiation (10 and 25 kGy) to cumin seeds had no significant effects on the antimicrobial activities of cumin.

Comparison of Antimicrobial Activities of Cumin and Other Spices
Chaudhry et al. [84] determined the antibacterial effects of aqueous infusions and aqueous decoctions of 3 spices on 188 bacteria from 11 genera isolated from oral cavity of apparently healthy individuals, by the disc diffusion test. Aqueous decoction of cumin possessed the highest antimicrobial activities for it showed inhibitory effects on 73% of the bacteria strains tested. Cumin EO was also more effective than some spice EOs as reported. Iacobellis et al. [85] evaluated the antimicrobial activities of EOs of cumin and Carum carvi L. against E. coli and the genera Pseudomonas, Clavibacter, Curtobacterium, Rhodococcus, Erwinia, Xanthomonas, Ralstonia, and Agrobacterium using the agar diffusion test. Cumin EO showed antibacterial effects on both Gram-positive and Gram-negative bacteria except Pseudomonas viridiflava, which was resistant to 8 µL EO, the highest level tested. Ozcan et al. [86] examined the antimicrobial activities of nine spice EOs at three concentrations (1%, 10%, and 15% v/v) against S. typhimurium, B. cereus, S. aureus, E. faecalis, E. coli. Y. enterocolitica, S. cerevisiae, Candida rugosa, Rhizopus oryzae, and A. niger. The results showed that cumin EO was effective against all tested bacterial species as well as S. cerevisiae and Candida rugosa among fungi. Stefanini et al. [87] analyzed the antimicrobial activities of EOs of spices (fennel seeds, dill, cumin, and coriander) by determining the DIZs. The results indicated that cumin was effective against E. coli, P. aeruginosa, and Salmonella sp. with DIZs of 18, 10, and 23 mm, respectively. In another study, the antimicrobial activities of EOs of six spices against L. curvatus, L. sakei, S. carnosus, S. xylosus, E. gergoviae, and E. amnigenus were assessed using the agar disc diffusion method [43]. Cumin EO was the second effective against bacteria tested with DIZs ranging from 31.23 mm (L. sakei) to 38.17 mm (E. gergoviae). Moreover, another study evaluated the antimicrobial activities of EOs of five spices against different microorganism species by the disc diffusion method and discussed the possible effects in vitro between plants and antibiotics [88]. Cumin inhibited all tested bacteria and fungi. The application of cumin with gentamicin, cephalothin, and ceftriaxone showed synergistic effects against Pseudomonas pyocyaneus (P. pyocyaneus) and Aeromonas hydrophila (A. hydrophila), but showed antagonistic effects against other bacteria tested. Similarly, the possible synergistic interactions of some spice EOs on antibacterial activities against six foodborne bacteria-B. cereus, L. monocytogenes, M. luteus, S. aureus, E. coli, and S. typhimurium-were evaluated by micro broth dilution, checkerboard titration, and time-kill methods [89]. The results showed that coriander and cumin seed oil combination exhibited synergistic interactions on antibacterial activities.
Consequently, cumin had antimicrobial effects on several microorganisms like E. coli, S. aureus, and S. faecalis at low concentrations (Table 5). In the future, the mechanisms of antimicrobial action of cumin and its major components-cuminaldehyde and cymene-on other microorganisms should be further studied.

Rosemary
Rosemary (Rosmarinus officinalis), belonging to the Lamiaceae family, is a perennial shrub with pleasant smell and grows all over the world. Rosemary has been used in pharmaceutical products and traditional medicine, and also used as a flavoring agent in food products due to its desirable flavor, antioxidant activities, and antimicrobial activities [90,91].

Antimicrobial Activities of Rosemary
Tavassoli et al. [91] reported rosemary EO suppressed Leuconostoc mesenteroides, Lactobacillus delbruekii, S. cerevisia, and C. krusei. The results indicated that rosemary EO showed higher inhibitory effects on bacteria (MICs: 0.5-1.5 mg/mL) tested than on yeasts. Bozin et al. [92] identified the antimicrobial activities of EOs of rosemary and sage against 13 bacterial strains and 6 fungi by the microdilution technique. Compared with bifonazole, rosemary EO showed better antifungal activities especially against C. albicans, Trichophyton tonsurans (T. tonsurans), and Trichophyton rubrum at lower MICs (15.0-30.2 µL). Rosemary EO also expressed important antibacterial activities on E. coli, S. typhimurium, S. enteritidis, and Shigella sonei. Weerakkody et al. [93] compared the antibacterial effects of extracts from seven spices and herbs on E. coli, S. typhimurium, L. monocytogenes, and S. aureus by the agar disc diffusion and broth dilution assay. The results of both methods indicated that hexane extract of rosemary exhibited significantly higher antibacterial activities than ethanol and water extracts against all bacteria tested except S. typhimurium with the MICs ranging from 1.25 to 5.0 mg/mL.

Comparison of Antimicrobial Activities of Rosemary and Other Spices
Additionally, Krajcova et al. [94] observed the antimicrobial activities of five plant ethanol extracts against B. cereus, E. coli, P. aeruginosa, S. aureus, and L. monocytogenes using the dilution method and the description of growth curves of the tested bacteria. Rosemary extract was proved to be the most effective at all concentrations (0.1%, 0.05%, 0.02%, and 0.01% w/w). At the concentration of 0.01% w/w, rosemary extract only inhibited P. aeruginosa and E. coli, while the higher extract concentrations were effective against all other bacteria. Zhang et al. [95] examined the antimicrobial effects of 14 spice ethanol extracts and their mixtures on L. monocytogenes, E. coli, P. fluorescens, and L. sake using the well diffusion test. Individual extract of rosemary showed strong antimicrobial activities, and the combination of rosemary and liquorice extracts showed the best inhibitory effects on all tested microorganisms. Kozlowska et al. [96] tested the antimicrobial activities of aqueous extracts from 5 spices against 8 Gram-positive bacteria and 12 Gram-negative bacteria by the disc diffusion assay. Rosemary exhibited its inhibitory effects with a broader spectrum than the other four spices, as the MICs were 0.125-0.5 mg/mL for all the tested Gram-positive bacteria and 0.25-0.5 mg/mL for four Gram-negative bacteria. Weerakkody et al. [97] studied the antimicrobial activities of two extract combinations against L. monocytogenes and S. aureus and naturally spoilage microflora on instant shrimp stored for 16 days at 4 or 8 • C. Both combinations (galangal, rosemary, and lemon; galangal and rosemary) significantly decreased the levels of aerobic bacteria and lactic acid bacteria, but showed no effects on L. monocytogenes or S. aureus. Azizkhani et al. [90] evaluated the antimicrobial effects of rosemary, mint, and a mixture of tocopherols against microorganisms from the sausages. The application of rosemary significantly inhibited the growth of microorganisms and the lowest microbial counts were obtained in samples containing both rosemary and mint, indicating the possible synergistic effects. Toroglu [88] evaluated the antimicrobial activities of five spice EOs by the disc diffusion method and discussed possible effects of plants and antibiotics. Rosemary had antimicrobial effects on all tested fungi and bacteria. The combination of rosemary EO and cephalothin antibiotics showed synergic effects on S. aureus, while the combination of rosemary EO and ceftriaxone antibiotics showed no effect.
Above all, the papers cited are of good quality and indicated that rosemary EO and extracts were found antimicrobial at low MICs against some bacteria and fungi, especially Gram-positive bacteria such as S. aureus (Table 6). Some studies indicated that rosemary showed synergic effects with some spices and antibiotics such as galangal and cephalothin. The mechanisms of antimicrobial action of both rosemary and its major components should be further studied.

Antimicrobial Activities of Garlic
In a study, Sallam et al. [100] examined the antimicrobial effects of fresh garlic, garlic powder, and garlic oil on microorganisms in raw chicken sausage by aerobic plate count. Garlic materials showed antimicrobial activities in such an order: fresh garlic > garlic powder > garlic oil > butylated hydroxyanisole. Another study also assessed the antimicrobial activities of dried garlic powders made by different drying methods against S. aureus, E. coli, S. typhimurium, B. cereus and a mixed lactic culture containing Lactobacillus delbrueckii subsp. bulgaricus and Streptococcus thermophilus [99]. Fresh garlic exhibited the highest activities followed by freeze-dried powder. The retaining of active components responsible for antimicrobial activities was mainly affected by both drying temperature and time.
Chopped garlic at concentrations from 0% to 10% were investigated for the antimicrobial effects in ground beef (stored at refrigerator and ambient temperatures) and raw meatballs (stored at room temperature) by determining the colony counts of total aerobic mesophilic bacteria, yeast, and molds at 2, 6, 12, and 24 h after storage [101]. The results indicated that chopped garlic delayed the growth of microorganisms in ground meat, which depended on the garlic concentrations. The addition of garlic (5% or 10%) to the raw meatball mix reduced the microorganism counting, in terms of total aerobic mesophilic bacteria, yeast, and mold counts.
Garlic EO penetrated the cellular membranes and even the menbranes of organelles like mitochondria, damaged organelles, and resulted in the death of C. albicans [102]. Furthermore, garlic EO induced differential expression of several critical genes including those involved in oxidation-reduction processes, and cellular response to drugs and starvation.

Comparison of Antimicrobial Activities of Garlic and Other Spices
Some studies compared the antimicrobial activities of different spices. Indu et al. [103] studied the antimicrobial effects of 5 spice extracts on 20 serogroups of E. coli, 8 serotypes of Salmonella, L. monocytogenes and A. hydrophila using the agar well method and filter paper method. Garlic extract exhibited significant antibacterial activities at all concentrations (100%, 75%, 50%, and 25%) against all test microorganisms except L. monocytogenes, and the activity against E. coli was linearly dependent with concentration. Joe et al. [104] reported the antimicrobial effects of garlic, ginger, and pepper ethanol extracts on K. pneumoniae, S. aureus, M. morgani, C. albicans, E. coli, and P. vulgaris using the filter paper assay. Garlic extract exerted superior antibacterial activities at all concentrations (1000, 1500, and 2000 ppm), especially against P. vulgaris and M. morgani, and the activities were a linear function of concentrations. Geremew et al. [105] examined the antimicrobial activities of six spice crude extracts (acetone, ethanol, and hexane extracts) against E. coli, S. aureus, S. flexneri, and Streptococcus pneumoniae by the agar well diffusion method. Garlic was the most effective against all tested pathogens except S. flexneri. Among different solvent extracts used, garlic acetone extract exhibited the highest antibacterial activities. Touba et al. [106] tested the antimicrobial activities of crude extracts of seven spices against three Roselle pathogens by poisoned food technique. The results indicated that the cold water extract of garlic exhibited good antifungal activities against all three tested fungi, and hot water extract of garlic showed the best antifungal activities. Nejad et al. [98] reported the antibacterial effect of garlic aqueous extract on S. aureus in hamburger. Samples treated with garlic aqueous extract were kept in refrigerator for one and two weeks, and were frozen for one, two, and three months, before being tested by the microbial counts. The first-and second-week samples were significantly reduced by all the 1, 2, and 3-mL extracts, which were added to 100 g hamburger samples, respectively, showing 2 and 3-mL extracts were more effective. In treatment of one, two, and three-month samples, the growth of S. aureus was significantly decreased by the 2 and 3-mL extracts. Al-Turki [55] explored the antimicrobial activities of five spice hydrosols (thyme, peppermint, sage, black pepper, and garlic) against B. subtilis and S. enteritidis using the agar disk diffusion method. Garlic hydrosol exhibited stronger antibacterial activities against B. subtilis and S. enteritidis compared with thyme, peppermint, sage, and black pepper hydrosols.
In conclusion, garlic showed great antimicrobial activities at low concentrations against several pathogenic microorganisms like E. coli and S. aureus (Table 7). Fresh garlic was found to possess higher antimicrobial activities than garlic powder and oil.

Ginger
Ginger (Zingiber officinale), belonging to the family of Zingiberaceae [107], is widely used as an ingredient in food, pharmaceutical, cosmetic, and other industries. Some volatile compounds which are responsible for antimicrobial activities in ginger were á-pinene, borneol, camphene, and linalool [108].

Antimicrobial Activities of Ginger
Ginger was proved to possess antimicrobial activities in several studies. Singh et al. [109] determined the antifungal activities of EO and oleoresin of ginger against Aspergillus terrus, A. niger, Aspergillus flavus (A. flavus), Trichothecium roseum (T. roseum), Fusarium graminearum (F. graminearum), F. oxysporum, Fusarium oxysporum (F. monoliforme), and Curvularia palliscens, by food poison and inverted petri-plate technique. The results showed that the EO 100% inhibited F. oxysporum, while the oleoresin 100% inhibited A. niger. Park et al. [107] compared the ethanol and n-hexane extracts of ginger and five ginger constituents against three anaerobic Gram-negative bacteria, Porphyromonas gingivalis (P. gingivalis), Porphyromonas endodontalis, and Prevotella intermedia. The results indicated that ginger extracts exhibited antibacterial activities against three tested bacteria. Two highly alkylated gingerols showed significant inhibition against the growth of these oral pathogens with the MICs ranging from 6 to 30 µg/mL, and also killed the oral pathogens at a MBC range of 4-20 µg/mL. Sa-Nguanpuag et al. [108] evaluated the in vitro and in vivo antimicrobial activities of ginger oils which were obtained by hydrodistillation and solvent extraction method. The results showed that the oils extracted by both methods possessed antimicrobial activities against B. subtilis, Bacillus nutto, P. aerugenosa, Rhodoturola sp., Samonella newport, S. enteritidis, and Fusarium sp.; except E. coli, Campylobactor coli, and Campylobactor jejuni (C. jejuni) in vitro. In the case of shredded green papaya, when the package was added with 5 and 10 µL ginger oils the growth of microorganisms was inhibited well, while with 15 µL ginger oil a reduction in growth rate was observed.

Comparison of Antimicrobial Activities of Ginger and Other Spices
Yoo et al. [110] investigated the antibacterial activities of EOs from ginger and mustard against Vibrio species at various temperatures. The results indicated that EOs from ginger and mustard could inhibit the growth of Vibrio parahaemolyticus and Vibrio vulnificus at 5 • C of storage. Indu et al. [103] tested the antibacterial activities of 5 spice extracts against 20 serogroups of E. coli, 8 serotypes of Salmonella, L. monocytogenes, and A. hydrophila by the agar well method and filter paper method. The results indicated that ginger extract possessed inhibitory effects on two serogroups of E. coli. Mvuemba et al. [74] assessed the antimicrobial activities of four spice water extracts against the mycelial growth of A. niger, F. sambucinum, P. sulcatum, or R. stolonifera. The results demonstrated that ginger extract significantly suppressed the mycelial growth of tested microorganisms, and P. sulcatum was 100% inhibited by 0.05 g/mL of ginger extract. Touba et al. [106] tested the antifungal activities of crude extracts of seven spices made by cold water and hot water against Phoma exigua (P. exigua), Fusarium nygamai (F. nygamai), and R. solani by poisoned food technique. The results showed that hot water extracts from garlic and ginger possessed the best antifungal activities. Cold water extracts were commonly more effective than hot water extracts on tested pathogens. In another study, the antibacterial activities of 7 ethanol extracts of spices against 215 high levels gentamicin resistant enterococcal strains isolated from clinical samples were evaluated by the well diffusion method [77]. The results indicated that only cinnamon and ginger extracts were found to have activities against all the isolates, with the DIZs of ginger ranged from 27 to 30 mm.
Collectively, ginger was proved to possess significant antimicrobial activities against some common microorganisms such as P. aerugenosa both in vivo and in vitro at low concentrations (Table 8). Ginger could also inhibit pathgens like P. gingivalis and enterococcal isolates with low MICs and MBCs. The exact mechanisms of action of ginger on bacteria and fungi were rarely studied and need futher exploration.

Basil
Basil (Ocimum basilicum) is one of the oldest spices, which is widely used in the flavoring of confectionary, baked goods, condiments, etc. Basil oil was also used in perfumery, as well as in dental and oral products [112]. Basil is a natural spice which possesses antimicrobial activities as many studies have reported.

Antimicrobial Activities of Basil
In a study, the antimicrobial activities of EOs from aerial parts of basil (collected at full flowering stage during summer, autumn, winter, and spring) against S. aureus, E. coli, B. subtilis, and Pasteurella multocida, as well as pathogenic fungi A. niger, Mucor mucedo, Fusarium solani (F. solani), Botryodiplodia theobromae, and R. solani were assessed by the disc diffusion method and the MICs were determined by a microdilution broth susceptibility assay [113]. The results indicated that basil EOs possessed antimicrobial activities against all tested microorganisms. Antimicrobial activities of the EOs varied significantly as seasons changed, and EOs from winter and autumn crops exhibited greater antimicrobial activities. In another study, the antimicrobial activities of chloroform, acetone and 2 different concentrations of methanol extracts of basil against 10 bacteria and 4 yeasts were determined by the disc diffusion assay [114]. Methanol extracts provided inhibition zones on P. aeruginosa, Shigella sp., L. monocytogenes, S. aureus, and two strains of E. coli, but the chloroform and acetone extracts exhibited no effects. Kocic-Tanackov et al. [115] reported the antifungal effects of basil extract on Fusarium species (Fusarium oxysporum, Fusarium proliferatum, Fusarium subglutinans, and Fusarium verticillioides isolated from cakes), by the agar plate test. Basil extract showed significant activities against F. proliferatum and F. subglutinans at the concentration of 0.35 and 0.70% v/v, but showed lower activities against other tested Fusarium species. Basil extract 100% inhibited aerial mycelium of all tested Fusarium spp. at 1.50% v/v. Beatovic et al. [116] investigated the antimicrobial activities of EOs of 12 basil cultivars against 8 bacterial species (B. cereus, Micrococcus flavus, S. aureus and E. faecalis, E. coli, P. aeruginosa, S. typhimurium, and L. monocytogenes) and 7 fungi (Aspergillus fumigatus (A. fumigatus), A. niger, Aspergillus versicolor (A. versicolor), Aspergillus ochraceus (A. ochraceus), Penicillium funiculosum, Penicillium ochrochloron, and Trichoderma viride) by a modified microdilution technique. All basil EOs tested showed significant antimicrobial activities, with MICs ranging from 0.009 to 23.48 µg/mL for bacteria and 0.08-5.00 µg/mL for fungi. All the EOs showed 100-fold higher antibacterial activities than ampicillin for some bacteria, and 10-to 100-fold higher antifungal activities than the commercial antifungal agents, e.g., ketoconazole and bifonazole.

Comparison of Antimicrobial Activities of Basil and Other Spices
El-Habib [117] investigated the antifungal activities of seven spice EOs against A. flavus and aflatoxin producted by A. flavus strain. The results showed that basil EO delayed the growth of A. flavus. At 150 µL/100 mL, basil EO completely inhibited A. flavus, and effectively controlled the aflatoxin B1 production. Lomarat et al. [17] tested the antibacterial activities of eight EOs against M. morganii, a histidine decarboxylase producing bacteria, by microdilution assay. Basil EO possessed the antibacterial activity against M. morganii (MIC: 2.39 mg/mL, MBC: 4.77 mg/mL), and the active compound of basil oil was methyl chavicol.
Generally, basil has been proved to possess effects of inhibiting some microorganisms at low MICs especially fungi like A. flavus (Table 9), but the mechanisms of action have been rarely explored. Therefore, future studies are needed.

Fennel
Fennel (Foeniculum vulgare), belonging to family Umbellifarae [118], is widely planted in temperate zones and the tropical belt for its aromatic fruits, and is used as an ingredient in the cooking [119]. The EO of fennel seeds has been reported with significant antifungal activities and antibacterial activities.

Antimicrobial Activities of Fennel
In a study, the antibacterial activities of fennel seeds EO against Streptococcus mutans (S. mutans) strains were tested [120]. The results showed that growths of all S. mutans strains tested were completely inhibited by fennel seeds EOs at concentrations higher than 80 ppm. Diao et al. [119] also determined the antibacterial activities of EO from fennel seeds against several foodborne pathogens by the kill-time curve assay method. The results showed that fennel seeds EO exerted antibacterial effects on Streptomyces albus (S. albus), B. subtilis, S. typhimurium, Shigella dysenteriae (S. dysenteriae). and E. coli, among which S. dysenteriae was the most sensitive with the lowest MIC (0.125 mg/mL) and MBC (0.25 mg/mL). In another study, the antimicrobial activities of crude extract of fennel was determined using the agar diffusion method against E. coli, S. blanc, P. merabilis, P. vulgaris, S. epidemidis, S. saprophyticus, A. versicolor, A. fumigates, and Penicilium camemberti [121]. The results indicated that the crude extract of fennel had a great potential as an antimicrobial material against all the nine microorganisms tested, especially fungal strains. Some studies also tested the methanol, ethanol, and acetone extracts of fennel. In a study, the antifungal activities of EO and acetone extract of fennel against 10 fungi were assessed by the inverted petriplate method [118]. The results showed that fennel EO completely inhibited A. niger, A. flavus, F. graminearum, and Fusarium moniliforme (F. moniliforme) at 6 µL (in 20 mL culture medium), and it was effective on A. niger even at 4 µL.
Fennel seed EO could break the permeability of cell membrane of S. dysenteriae and result in the leakage of electrolytes, losses of proteins, reducing sugars, etc., and eventually lead to the decomposition and death of cells [119].

Comparison of Antimicrobial Activities of Fennel and Other Spices
The antimicrobial activities of cumin and fennel EOs on S. typhimurium and E. coli were compared by the disc diffusion method and dilution method [122]. Fennel EO was more effective than cumin EO, with the lowest MICs of 0.031% and 0.062% v/v against S. typhimurium and E. coli, respectively. Nguyen et al. [123] evaluated the antimicrobial activities of methanol and ethanol extracts of eight spices against B. subtilis, E. faecalis, L. innocua, E. coli, P. putida, Providencia stuartii, and Acetobacter calcoaceticus (A. calcoaceticus) by the Kirby-Bauer disc diffusion method. Methanol and ethanol extracts from fennel seeds exhibited the best antimicrobial effects with the largest DIZs on six out of the seven bacteria except E. coli.
Fennel EO and extracts were effective against several foodborne pathogens with low MICs and MBCs such as S. dysenteriae, S. typhimurium, and E. coli (Table 10). The mechanisms of fennel and its major components need further studies. Fennel seeds extracts showed the largest zones of inhibitions in six out of the seven bacteria. [123]

Coriander
Coriander (Coriandrum sativum), belonging to family Umbelliferae, is a native plant of the Mediterranean region and is widely cultivated in India, Russia, Central Europe, Asia, and Morocco. Coriander was widely applied in producing chutneys and sauces, flavoring pastry, cookies, buns, and tobacco products, and extensively employed for preparation of curry powder, pickling spices, sausages, seasonings, and food preservatives [4,118].

Antimicrobial Activities of Coriander
Duarte et al. [124] investigated the antimicrobial activities of coriander EO and its major compound, linalool, against C. jejuni and C. coli strains by the disc diffusion test, vapor-phase method and microdilution method. The MICs of coriander EO and linalool against C. jejuni and C. coli strains ranged between 0.5 and 1 µL/mL. Coriander EO also showed inhibitory effects on the biofilim formation of Campylobacter spp. Also, the antimicrobial activities of coriander EO against multidrug resistant pathogen, Acinetobacter baumannii (A. baumannii), were tested [125]. The MICs and MBCs were determined by a microdilution broth susceptibility assay. The MICs and MBCs of coriander EO against A. baumannii strains both ranged between 1 and 4 µL/mL. Another study investigated the synergistic antibacterial effects of coriander EO and six antibacterial drugs (cefoperazone, chloramphenicol, ciprofloxacin, gentamicin, tetracycline, and piperacillin) against two A. baumannii strains [126]. The results indicated that coriander EO showed synergistic action with chloramphenicol, ciprofloxacin, and tetracycline, and contributed to resensitizing A. baumannii to the action of chloramphenicol. Freires et al. [127] investigated the antifungal activities of EO from coriander leaves against Candida spp. The results showed that the MICs ranged from 15.6 to 31.2 µg/mL, and MFCs ranged from 31.2 to 62.5 µg/mL against Candida spp. for coriander EO. Sliva et al. [128] assessed the bacterial activities of coriander EO against 12 bacterial strains by microdilution broth susceptibility assay. The results indicated that coriander EO showed antimicrobial activities against all tested bacteria and showed bactericidal activities against bacteria except B. cereus and E. faecalis. The MICs of coriander against all tested bacteria ranged from 0.1% to 1.6% v/v, and MBCs ranged from 0.1% to 3.2% v/v except B. cereus and E. faecalis. Acimovic et al. [129] assessed the antifungal activities of EOs of six coriander accessions of different origins against Colletotrichum acutatum and Colletotrichum gloeosporioides using the inverted petriplate method. The results indicated that coriander EOs could inhibit Colletotrichum genus at higher application rates (≥0.16 µL/mL of air).
Singh et al. [130] reported the antifungal effects of coriander EO and oleoresin on eight fungi by the inverted petriplate and food poison techniques. The results of the former method showed that EO was highly active against Curpularia palliscens, F. oxysporum, Fusarium monitiforme, and Aspergillus terreus (A. terreus), and the oleoresin inhibited more than 50% mycelial zones for F. oxysporum, A. niger, and A. terreus. The results of the latter method indicated that EO 100% inhibited the growth of A. terreus, A. niger, F. graminearum, and F. oxysporum, but the oleoresin exhibited weaker fungitoxic activities, which only 100% inhibited the growth of F. oxysporum. In another study, the antimicrobial activities of ethanol and aqueous-ethanol extracts of coriander were investigated against B. subtilis, S. aureus, P. vulgaris, E. coil, P. aeruginosa, K. peunomonia, L. monocytogenes, and C. albicans [131]. Ethanol extract revealed the elevated antimicrobial activities against P. vulgaris and C. albicans, and was more potent against tested microorganisms. Besides, aqueous-ethanol extract exhibited the highest activities against B. subtilis and L. monocytogenes. Furthermore, the effect of microwaves on EO of coriander on its antimicrobial activities was also tested [83]. The antimicrobial effects against microorganisms of both microwave and conventionally roasted oils were similar and more effective than those of raw oils.
Coriander EO permeated the cell membranes, resulting in the loss of all cellular functions [4]. The mechanisms of antibacterial action of coriander EO on Gram-positive and Gram-negative bacteria are different and need further exploring. Coriander EO was found to bind to membrane ergosterol and increase ionic permeability, ultimately causing cell death of C. albicans [127].

Comparison of Antimicrobial Activities of Coriander and Other Spices
The antimicrobial activities of four spice EOs against isolated clinical specimens were compared using the diffusion method [87], and the results showed that coriander oil was active only against Salmonella sp. Dimic et al. [132] tested the antifungal activities of lemon EO, coriander extract and cinnamon extract against five molds (A. parasiticus, Cladosporium cladosporioides (C. cladosporioides), Eurotium herbariorum, Penicillium chrysogenum, and Aspergillus carbonarius) by the agar dilution method and vapor phase method. The results indicated that coriander extract had the best antifungal activities in the vapor phase as it completely inhibited A. parasiticus, C. cladosporioides, E. herbariorum, and P. chrysogenum at 4.17 µL/mL.
The papers cited are of high quality and indicated that coriander possessed significant antimicrobial activities at low concentrations against several pathogens such as A. baumannii, Campylobacter spp. at low MICs, MBCs, and MFCs (Table 11).

Galangal
Galangal (Alpinia galangal) (Table 12) has been used as a food additive in Thailand and other Asian countries since ancient time [133]. In a study, the antimicrobial activities of extracts of seven spices and herbs against E. coli, S. typhimurium, L. monocytogenes, and S. aureus were compared by the agar disc diffusion and broth dilution assays [93]. The hexane and ethanol extracts of galangal had strong antimicrobial activities against S. aureus (MIC < 0.625 mg/mL) and L. monocytogenes (MIC < 0.625 mg/mL at 24 h and 1.25 mg/mL at 48 h). Moreover, the synergistic antimicrobial effects of extract combination (galangal, rosemary, and lemon iron bark) on S. aureus, L. monocytogenes, E. coli, S. typhimurium, and Clostridium perfringens were evaluated [134]. Galangal and rosemary showed synergistic activities against S. aureus and L. monocytogenes, while galangal and lemon iron bark showed synergistic activities against E. coli and S. typhimurium. Additionally, Rao et al. [133] tested the antibacterial activities of galangal methanol, acetone, and diethyl ether extracts against B. subtilis, E. aerogenes, E. cloacae, E. faecalis, E. coli, K. pneumoniae, P. aeruginosa, S. typhimurium, S. aureus, and S. epidermis using agar well diffusion method and macrodilution method. Among the three solvents used, the activities of methanol extract at pH 5.5 were excellent against all the pathogens (MIC: 0.04-1.28 mg/mL, MBCs: 0.08-2.56 mg/mL). Another study also evaluated the antimicrobial activities of methanol extracts of four Alpinia strains against six strains of bacteria and four strains of fungi, using the disc diffusion assay [135]. The results demonstrated that galangal flower possessed the best effects on M. luteus and only the extract from galangal rhizome showed antifungal activity toward A. niger. The mechanisms of action of galangal have been rarely explored up till now. Galangal showed synergistic activities against tested microorganisms with rosemary and lemon iron bark. [134] Galangal methanol, acetone and diethyl ether extracts B. subtilis, E. aerogenes, E. cloacae, E. faecalis, E. coli, K. pneumoniae, P. aeruginosa, S. typhimurium, S. aureus, S. epidermis The activities of methanol extract at pH 5.5 were excellent with MICs ranging from 0.04 to 1.28 mg/mL. [133] 4 Alpinia strains methanol extracts 6 strains of bacteria and 4 strains of fungi Galangal flower possessed the highest activity against M. luteus and only the extract from galangal rhizome showed antifungal activity toward A. niger. [135]

Black Pepper
Black pepper (Piper nigrum) (Table 13) is largely used as a flavoring agent in foods. The antifungal effects of EO and acetone extract of black pepper on various pathogenic fungi were tested by the inverted petriplate technique and food poisoning technique [136]. The results showed that the EO was 100% controlled the mycelial growth of F. graminearum, while the acetone extract 100% inhibited mycelial growth of Penicillium viridcatum and A. ochraceus. In another study, the bacterial effects of EOs and acetone extracts of four spices on S. aureus, B. cereus, B. subtilis, E. coli, S. typhi, and P. aeruginosa were studied using the disk diffusion and poison food assay [137]. The results showed that black pepper extracts completely reduced colonies of S. aureus, B. cereus, and B. subtilis at 5 and 10 µL levels using the poison food method. Zarai et al. [138] evaluated the antimicrobial effects of various solvent extracts, piperine, and piperic acid from pepper against E. coli, K. pneumonia, S. enterica, S. aureus, S. epidermidis, E. faecalis, and B. subtilis by the agar diffusion assay and micro-well dilution assay. The results showed that the ethanol extract was the most effective to the tested bacteria with the MICs ranging from 156.25 µg/mL (S. aureus and B. subtilus) to 1250 µg/mL (E. coli and K. pneumonia). Black pepper EO could cause physical and morphological alterations in the cell walls and membranes of E. coli, and then result in the leakage of electrolytes, ATP, proteins, and DNA materials [139]. Chemical components of black pepper and its mechanisms of antimicrobial action need further exploration.

Other Spices
The antimicrobial activities of the spices mentioned above against several common microorganisms are summarized in Table 14. Other spices-such as Allium roseum L., Cinnamomum verum, Laurus nobilis, Myristica fragrans, and Pimpinella anisum-were also proved to possess significant antifungal and antibacterial activities (Table 15).               Sage extract showed the best antibacterial activities compared with four other plants, especially against Gram-positive bacteria and C. coli. [222]

Conclusions
The antibacterial and antifungal activities of commonly used spices have been summarized. Several spices-such as clove, oregano, thyme, cinnamon, and cumin-have exhibited significant antimicrobial activities against food spoilage bacteria like B. subtilis and P. fluorescens; pathogens like S. aureus, V. parahaemolyticus, and S. typhimurium; harmful fungi like A. flavus and A. niger; and even antibiotic resistant microorganisms such as MRSA. Therefore, these spices could be used to decrease the possibility of food poisoning and spoilage, to increase the food safety and shelf-life of products, and to treat some infectious diseases. In the future, as the combinations of several spices were proven to possess higher inhibitory effects on specific bacteria than those of individual spices, the interactions of more spices should be studied and evaluated to inhibit different microorganisms in different food products. Additionally, spices could be used in food packaging as published, but more studies are required to take the other aspects into consideration, such as how to prevent odor/flavor transferring from packages containing natural spice extracts to the packaged foods. Furthermore, spice products may be considered as an alternative to common antibiotics to treat infectious diseases. As the majority of the studies focused on the in vitro activities of spices against human pathogenic bacteria, in vivo studies and clinical trials are needed to be conducted in future. The mechanisms of antimicrobial action of spices remain to be clarified in order to make the best use of spices. Furthermore, the potential toxicity of spices on humans should be evaluated.