A Review on Antibacterial Effects of Iranian Herbal Medicine on Methicillin-Resistant Staphylococcus aureus

AUTHORS

Masoumeh Baradaran 1 , * , Amir Jalali 2

1 Toxicology Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

2 Department of Pharmacology and Toxicology, Toxicology Research Center, Ahvaz Jundishapur University of Medical Sciences, Ahvaz, Iran

How to Cite: Baradaran M , Jalali A. A Review on Antibacterial Effects of Iranian Herbal Medicine on Methicillin-Resistant Staphylococcus aureus, Jundishapur J Chronic Dis Care. 2019 ; 8(4):e96058. doi: 10.5812/jjcdc.96058.

ARTICLE INFORMATION

Jundishapur Journal of Chronic Disease Care: 8 (4); e96058
Published Online: October 23, 2019
Article Type: Review Article
Received: July 6, 2019
Revised: September 28, 2019
Accepted: October 4, 2019
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Abstract

Context: Staphylococcus aureus (S. aureus) is an opportunistic pathogen that is able to cause different types of life-threatening infections from acute bacteremia to often chronic osteomyelitis, endocarditis, infections of indwelling devices and wound infections. These chronic infections are highly recalcitrant to antibiotic treatment. Owing to the increasing incidence of S. aureus infections and resistance with long-term treatment with available antibiotics, S. aureus is notorious. Research for new drugs, especially from natural sources is ongoing. Plants were commonly used in the treatment of diseases by a primary human from ancient times. Exhibiting minimum side effects, ease of use, availability, and commonly cost-effective are the advantages of plants. So in the last few decades, research on herbal medicine is getting popularized.

Evidence Acquisition: In this systematic review, we aimed to review antimicrobial potential of essential oil and different extracts (methanolic, ethanolic, ethyl acetate, ether or aqueous extracts) from 31 genera of medical plants, including 83 species against S. aureus and its most frequent resistant strain, methicillin-resistant S. aureus (MRSA) for introducing them as potent therapeutic agents. To find intended articles, we searched in several databases using a list of suitable keywords.

Results: The essential oil of T. caucasicus has the best inhibitory effect on S. aureus. However, extract of 8 plant species has also the acceptable inhibitory effect. Surprisingly, essential oil of some plants showed better anti-staphylococcal effect than standard antibiotics. Moreover, twelve plant species have effective inhibitory effect against MRSA.

Conclusions: Some of the evaluated Iranian plants such as T. parthenium, T. vulgaris, T. eriocalyx, T. persicus, A. millefollum, P. harmala, H. scabrum, and S. urmiensis with acceptable MIC or inhibition zone have the potency of antimicrobial activity, especially against S. aureus and MRSA. According to the comparison, essential oil of Thymus caucasicus with the MIC value of 0.31 μg/mL for S. aureus and 2.5 μg/mL for MRSA has the best inhibitory effect. So the mentioned natural extract, especially essential oil of T. caucasicus can be a candidate for drug design with the goal of the treatment of S. aureus infections.

Keywords

Herbal Medicine Antimicrobial Susceptibility Staphylococcus aureus Chronic Infections

Copyright © 2019, Jundishapur Journal of Chronic Disease Care. This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial 4.0 International License (http://creativecommons.org/licenses/by-nc/4.0/) which permits copy and redistribute the material just in noncommercial usages, provided the original work is properly cited.

1. Context

Infectious diseases are the second leading cause of death worldwide (1). Staphylococcus aureus (S. aureus) is one of the important and problematical infectious pathogens (2). It is an opportunistic pathogen and is the primary cause of lower respiratory tract and surgical site infections, and the second leading cause of nosocomial bacteremia, pneumonia, and cardiovascular infections (3). Moreover, S. aureus is often found among chronic and recurrent bone infections, and is often the cause of chronic osteomyelitis, endocarditis, infections of indwelling devices and postsurgical wound infections such as chronic biofilm-associated infections in prosthetic devices (4). In recent years, the emergence of antibiotic-resistant forms of pathogenic S. aureus is a worldwide problem in clinical medicine (5). Methicillin-resistant S. aureus (MRSA) is the most common antibiotic-resistant of all antibiotic-resistant threats. The MRSA was first identified five decades ago (6). Hereafter, MRSA infections have spread in Europe, the Americas, and the Asia-Pacific region (7). Hence the search for newer, safer and more potent antimicrobials with less susceptibility to the resistance is a pressing need (8). Evidence currently shows that improved quality of life is considerably important in the treatment of chronic diseases (9). The negative effects of chronic infection induced by MRSA on the quality of life increase the need to search for newer, safer, and more potent antimicrobial agents with less susceptibility to resistance is a pressing need (8).

Plants were commonly used in the treatment of diseases by a primary human from ancient times. (9). Over the years, the World Health Organization (WHO) advocated traditional medicine as safe remedies for both microbial and non-microbial diseases. According to the WHO in 2008, above 80% of the world’s population rely on traditional medicine for their primary healthcare needs (10). On the other hand, almost one-third of all medical products have a plant origin (11). Plants contain a variety of compounds against a variety of pathogens. It means that plants have wide-spreading effects against a different variety of infectious agents, including antibiotic-resistant bacteria. Thus recently, the research is growing on medical plants as safe, cheap, accessible, and more acceptable for peoples than synthetic antibiotics (12).

The diversity of the climate has resulted in a high diversity of plant flora in Iran. So it is possible to identify effective substances in different native plants of the country and to extract these substances in order to produce these materials in large quantities at the industrial level. Evaluation of these capabilities, especially in the case of plants native to Iran is of special importance (13). A considerable number of articles are published annually on the antimicrobial effect of various Iranian plants. Given the growing problem of antibiotic resistance, analyzing and summarizing the results of these articles will be important for their practical use. Moreover, the comparison between pharmaceutical effects of different parts of a medical plant can give a good vision for accomplishing further study with more efficiency.

2. Objectives

The aim of the present systematic review was to deliberate on whether plants, found commonly in Iran, could be used as an alternative for infection therapy. This review would describe some of the Iranian plant species as potent therapeutic agents specifically against S. aureus and its frequent resistant strain, MRSA. It also compared the antimicrobial potential of different Iranian herbs to highlight the most functional of them.

3. Data Sources

The present systematic review study was conducted after obtaining prior permission from the Research Ethics Committee (code: IR.AJUMS.REC.1396.150). This review involves searching for available literature about plants and herbal compounds effective against S. aureus and MRSA. To find related articles, we searched several databases, including PubMed, Science Direct, Scopus, Springer Link, Wiley Online Library, and Google Scholar databases and Persian databases, including Iran Medex (indexing articles published in Iran biomedical journals), Magiran (Iranian magazines database), and SID (scientific information database) using a list of keywords in MeSH such as medical plant, healing plants, pharmaceutical plants, medical herbs, healing plants, plant extracts, plant drug, Iranian medical plants, antimicrobial susceptibility, Staphylococcus aureus, plant antimicrobial extract, microbial sensitivity tests, plant biologically active compounds, methicillin-resistant Staphylococcus aureus, as well as a combination of them. We studied all related articles, collected, and classified all relevant data published from January 1, 1974 to January 2017.

4. Study Selection and Data Extraction

All research articles that focused on the antimicrobial assay of essential oil or at least one of the different extracts (methanolic, ethanolic, ethyl acetate, ether or aqueous) from plants, growing in Iran, by Microdilution method and Kirby-Bauer test (zone of inhibition test) against S. aureus, published from January 1, 1974 to January 2017 were included in this study. All other relevant research articles that used other antimicrobial assays did not investigate the antimicrobial effect against S. aureus or were out of desired time range were excluded from the study. A flow diagram depicts the flow of information through the different phases of this review (Figure 1).

The flow of information through the different phases of the current review is shown
Figure 1. The flow of information through the different phases of the current review is shown

5. Results

This systematic review compared the result of research articles that determined the antimicrobial activity of essential oil and different extracts (methanolic, ethanolic, ethyl acetate, ether or aqueous extracts) from different parts of 31 genera of medical plants, including 83 species, especially against S. aureus. All described herbal medicine with the details of using part of the plant, types of extracts, maximum inhibitory concentration (MIC) and inhibition zone against S. aureus, location of harvesting, and the references are summarized in Table 1. The map of Iran along with the provinces is shown in Figure 2 so that the harvesting areas of the plants can be traced back to the map.

Geographical position of provinces in Iran is shown
Figure 2. Geographical position of provinces in Iran is shown
Table 1. The Name of the Plant Species with Their Related Characterization are Listed in the
PlantReferencesUsing PartExtractionInhibition Zone (IZ)MIC
Dicyclophora persica(19)Aerial partEssential oil20 mm1.2 mg/mL
Nepeta cripsa(20)Aerial partEssential oil19.5 mm (15 μL/disc)
Nepeta menthoid(21)Aerial partEssential oil21 mm (10 μL/disc)3.6 mg/mL
Terminalia chebula(22)Ripe and unripe seedMethanolic extract5 mg/mL for ripe seed 2.5 mg/mL for unripe seed
Myrtus communis(23)Leaves and seedsMethanolic extract26 mm (20 mg/mL), 10 mm (5 mg/mL) for leaves 16 mm(20 mg/mL), 9 mm (0.62 mg/mL) for seeds5 mg/mL (leaves) 0.62 mg/mL (for seed)
Salvia multicaulis(24)Aerial partsEssential oil7.5 mg/mL
Salvia multicaulis(25)Methanolic extract10 mm (S. aureus penicillin-resistant)
Salvia sclarea(24)Aerial partsEssential oil15 mg/mL
Salvia verticillata(24)Aerial partsEssential oil7.5 mg/mL
Salvia limbata(26)Essential oil15 mg/mL
Salvia choloroleuca(26)Essential oil7.5 mg/mL
Salvia officinalis(22)Whole plantMethanolic extract16 mm
Salvia sahendica(27)Aerial partsMethanolic extract14 mm1.2 mg/mL
Salvia reuterana(28)Flower and leavesMethanolic extract0.5 mg/mL for flower, 0.25 mg/mL for leaves
Salvia eremophila(29)Aerial partsMethanolic extract and essential oil7.8 mg/mL for essential oil, 0.5 mg/mL for methanolic extract
Salvia eremophila(30)Aerial partsMethanolic extract10 mm (4 mg/disc)1 mg/mL
Salvia reuterana(30)Aerial partsMethanolic extract8 mm (4 mg/disc)1 mg/mL
Salvia mirzayanii(30)Aerial partsMethanolic extract12.2 mm (4 mg/disc)1 mg/mL
Salvia santolinifolia(30)Aerial partsMethanolic extract12.2mm (4 mg/disc)1 mg/mL
Salvia microsiphon(30)Aerial partsMethanolic extract14.2 mm (4 mg/disc)1 mg/mL
Salvia urmiensis(31)Ethyl acetate extract21.3 μg/mL
Salvia urmiensis(31)Essential oil85.3 μg/mL
Salvia urmiensis(31)Ether extracts37.3 μg/mL
Salvia tomentosa(32)Mature plantAqueous extractNA for MRSAa & S. aureus strains
Salvia tomentosa(32)Mature plantEthanolic extract8.4 mm (4 mg/disc for MRSAa) 6.8 mm(4 mg/disc for S.aureus)
Alhagi maurorum(22)Stem gumMethanolic extract15 mm
Heracleum rechingeri(22)FruitMethanolic extract20 mm
Heracleum transcaucasicum(33)Aerial partsEssential oilNA
Heracleum anisactis(33)Aerial partsEssential oilNA
Foeniculum vulgare(34)Fennel seedsEssential oil2%
Foeniculum vulgare(22)Fennel rootMethanolic extract12 mm
Cuminum cyminum(35)Essential oil10 mm (10 μL/disc)1/8 oil dilution
Cuminum cyminum(22)FruitMethanolic extract12 mm
Cuminum cyminum(23)SeedsMethanolic extract15 mm
Cuminum cyminum(32)SeedsAqueous extractNA for MRSAa and S. aureus
Cuminum cyminum(32)SeedsEthanolic extract11.5 mm (4 mg/disc for MRSAa) 8.5 mm(4 mg/disc for S. aureus)
Artemisia diffusa(36)Aerial partsMethanolic extract18.4 mm (16 mg/cup)10 mg/mL
Artemisia oliveria(36)Aerial partsMethanolic extract12.2 mm (16 mg/cup)10 mg/mL
Artemisia scorpia(36)Aerial partsMethanolic extract13.6 mm (16 mg/cup)10 mg/mL
Artemisia turanica(36)Aerial partsMethanolic extract11.9 mm (16 mg/cup)10 mg/mL
Artemisia dracunulus(34)Essential oil7.0%
Artemisia dracunulus(32)Mature plantEthanolic extract8 mm(4 mg/disc) (for MRSAa) 7 mm(4 mg/disc for S. aureus)
Artemisia dracunulus(32)Mature plantAqueous extractNA (for MRSAa & S. aureus)
Artemisia herbalba(32)Mature plantEthanolic extract22.5 mm(4 mg/disc) (for MRSAa) 11 mm (4 mg/disc for S. aureus)0.39 mg/mL (for clinical MRSAa and S. aureus strains) 0.04 mg/mL (for standard MRSAa strain) 0.02 mg/mL(for standard S. aureus strain)
Artemisia herbalba(32)Mature plantAqueous extract12 mm(4 mg/disc) (for MRSAa) 9 mm(4 mg/disc for S. aureus)
Artemisia absinthium(32)Mature plantEthanolic extract9 mm(4 mg/disc) (for MRSAa) 8 mm(4 mg/disc for S. aureus)
Artemisia absinthium(32)Mature plantAqueous extractNA (for MRSAa & S. aureus)
Pistacia vera(37)FruitExtract32 mm
Pistacia mutica(37)FruitExtract18 mm
Pistacia vera(37)LeavesExtract22 mm
Pistacia mutica(37)LeavesExtract22 mm
P. khinjuk(38)LeavesChloroform0.04 mg/mL
P. khinjuk(38)LeavesEthyl acetate0.13 mg/mL
P. khinjuk(38)LeavesEthyl alcohol0.09 mg/mL
P. khinjuk(38)LeavesDiethyl ether0.42 mg/mL
P. atlantica(39)Mastic gumEssential oil11 mm (10 μL/disc ) 13 mm (20 μL/disc)
Helichrysum armenium(40)Flower, leaf and stemOil12.4 mm, 11.22 mm and 10.8 mm (50 μL/cup)
Helichrysum scabrum(41)FlowerExtract9mm to 19mmMIC value varied from lower than 19 μg/mL to 5000 μg/mL
Scrophulari astriata(42)LeavesEthanolic extract50.6 μg/mL
Thymus persicus(43)LeavesEssential oil0.5 μL/mL
Thymus eriocalyx(43)LeavesEssential oil0.5 μL/mL
Thymus pubescens(44)Pre and flowering stagesEssential oil29 mm for pre and 34 mm for floweringdilution of 1/8
Thymus serpyllum(44)Pre and flowering stagesEssential oil14 mm for pre and 22 mm for floweringdilution of 1/4
Thymus pubescens(45)Aerial partsMethanolic extract8 to 16 mm
Thymus vulgaris(34)LeavesEssential oil0.1%
Thymus vulgaris(22)Whole plantMethanolic extract10 mm5 mg/mL
Thymus vulgaris(46)Essential oil20 - 35 mm (for 14 clinical MRSAa strains) 19 mm (for S. aureus)18.5 µg/ml -37 µg/mL (for 14 clinical MRSAa strains) 18.5 µg/mL (for S. aureus)
Thymus vulgaris(32)Mature plantEthanolic extract10.5 mm (4 mg/disc for MRSAa) 9.4 mg/disc for S. aureus
Thymus vulgaris(32)Mature plantAqueous extractNA (for MRSAa & S. aureus)
Thymus caramanicus(32)Mature plantEthanolic extract11.2 mm (4 mg/disc for MRSAa) 9 (4 mg/disc for S. aureus
Thymus caramanicus(32)Mature plantAqueous extractNA (for MRSAa & S. aureus)
Thymus caucasicus(47)Essential oil0.31 μg/mL for S. aureus 2.5 μg/mL for MRSAa
Mentha pulegium(48)Flowering aerial partsEssential oil21 mm (1 μL of oil)0.5 μL/mL
Mentha pulegium(34)LeavesEssential oil0.5%
Menth apiperita(49)Essential oil2 μL/mL
Mentha piperita(34)LeavesEssential oil0.4%
Mentha piperita(32)LeavesEthanolic extract7.5 mm (4 mg/disc for MRSAa) 8.5 (4 mg/disc for S. aureus
Mentha piperita(32)LeavesAqueous extract7 mm (4 mg/disc for MRSAa) 7.5 mm (4 mg/disc for S. aureus)
Peganum harmala(50)Seed smokeDichloromethane extract15.7 mm(5 mg of smoke condensate)
Peganum harmala(32)Mature plantAqueous extract7.4 mm(4 mg/disc) (for MRSAa) NA (4 mg/disc)
Peganum harmala(32)Mature plantEthanolic extract18 mm(4 mg/disc) (for MRSAa) 20 mm(4 mg/disc)0.02 mg/mL (for clinical and standard MRSAa strains) 0.02 mg/mL(for standard and clinical S. aureus strains)
Peganum harmala(51)SeedMethanolic extract22 mm (in concentration of 400 mg/mL for MRSAa)0.625 mg/mL
Peganum harmala(51)LeavesMethanolic extract10 mm (in concentration of 400 mg/mL for MRSAa)
Peganum harmala(51)StemMethanolic extract11 mm (in concentration of 400 mg/mL for MRSAa)
Peganum harmala(51)RootMethanolic extract24.5 mm (in concentration of 400 mg/mL for MRSAa)0.625 mg/mL
Peganum harmala(51)FlowerMethanolic extract5.5 mm (in concentration of 400 mg/mL for MRSAa)
Grammosciadium platycarpum(52)Aerial partsEssential oil18 mm1.9 mg/mL
Grammosciadium scabridum(53)Aerial partsEssential oil14 mm (10 μg/disc)1.2 mg/mL
Onosmadi chroanthum(54)RootMethanolic and ethanolic extract15 mm (50 μL/well), 15 mm (50 μL/well)0.156 mg/mL for methanolic extract and 0.312 mg/mL for ethanolic extract
Scutellaria litwinowii(55)Aerial partsMethanolic extract6.25 mg/mL
Scutellaria lindbergii(55)Aerial partsMethanolic extract6.25 mg/mL
Oliveria decumbens(56)Aerial partsEthanolic and methanolic exracts20 mg/mL, 20 mg/mL
Teucrium polium(57)Aerial partsAlcoholic extracts40 mg/mL
Teucrium polium(58)Hydroalcholic20 mm
Stachys fruticulosa(27)Aerial partsMethanolic extract12 mm2.5 mg/mL
Stachys schtschegleevii(27)Aerial partsMethanolic extract13 mm1.25 mg/mL
Stachys byzantia(59)Methanolic extract8.4 mm100 μg/mL
Stachys inflate(59)Methanolic extract8.3 mm250 μg/mL
Stachys lavandulifolia(59)Methanolic extract8.6 mm500 μg/mL
Stachys laxa(59)Methanolic extract8.6 mm100 μg/mL
Stachys grandiflora(60)Aerial partsEssential oil12 mm
Stachys obtusicrena(30)Aerial partsMethanolic extract9.2 mm (4 mg/disc)
Hymenocrater longiflorus(61)Polar sub-fractionEssential oil31 mm40 μg/mL
Pistachia vera(62)Green hullPurified extract11.7 mm (at 1200 μg/plate)
Phlomis caucasica(27)Aerial partsMethanolic extract1.25 mg/mL
Phlomis buruguieri(59)Aerial partsMehanolic extract16.7 mm10 mg/mL
Phlomis herbaventi(59)Aerial partsMehanolic extract12.2 mm10 mg/mL
Phlomis oliveri(59)Aerial partsMehanolic extract13.1 mm25 mg/mL
Torilis leptophyla(63)Aerial partsEthanolic extract10 mm0.4 g/mL
Tanacetum balsamita(27)Aerial partsDichloromethane extract2.5 mg/mL
Tanacetum parthenium(11)Whole plantEssential oil18.5 mm (2.5 μL), 34mm (5 μL), 39mm (7.5 μL) and 42 mm (15 μL)1 μg/mL
Tanacetum parthenium(64)Flowering stageEssential oil24 mm8 μg/mL
Tanacetum parthenium(64)Pre-flowering stageEssential oil18 mm8 μg/mL
Tanacetum parthenium(64)Post-flowering stageEssential oil22 mm8 μg/mL
T. pinnatumboiss(65)Aerial partsEssential oil24.2 mm
Achillea millefollum(27)Methanolic extract0.625 mg/mL
Achillea millefollum(66)Essential oil31.4 mm (region 1) 19.8 mm(region 2)15.4 μg/mL (region 1) 27.5 μg/mL (region 2)
Achillea pachycephala(67)FlowersEssential oil12 mm
Achillea pachycephala(67)LeavesEssential oil10.5 mm
Achillea pachycephala(67)StemsEssential oil8 mm
Achillea pachycephala(67)Aerial partsHexan-ether14 mm6.25 mg/mL
Achillea pachycephala(67)Aerial partsMethanolic extract6 mm12.5 mg/mL
Achillea santolina(67)FlowersEssential oil9 mm
Achillea santolina(67)LeavesEssential oil7.5 mm
Achillea santolina(67)StemsEssential oil6.5 mm
Achillea santolina(67)Arial partsHexan-ether7 mm6.25 mg/mL
Achilleas antolina(67)Aerial partsMethanolic extract5 mm12.5 mg/mL
Achillea tenuifolia(68)FlowerVolatile oils14 mm
Achillea tenuifolia(68)LeavesVolatile oils9 mm
Achillea tenuifolia(68)StemsVolatile oils8 mm
Achillea wilhelmsii(69)Essential oil27 mm (200 μL) (for MRSAa) 19 mm (200 μL )( for MRSAa)
Achillea wilhelmsii(70)Methanolic extract19mm(400 mg/mL)
Otostegia persica(71)Aerial partsHexane extract11.4 mm10 mg/mL
Otostegia persica(71)Aerial partsChloroform extract15.4 mm1.25 mg/mL
Otostegia persica(71)Aerial partsMethanolic extract15.6 mm3.12 mg/mL
Otostegia persica(30)Aerial partsMethanolic extract9.7 mm (4 mg/disc)
Berberis vulgaris(32)RootAqueous extract8.4 mm (4 mg/disc) (for MRSAa) 7 mm (4 mg/disc)
Berberis vulgaris(32)RootEthanolic extract12.5 mm (4 mg/disc) (for MRSAa) 15.5 mm (4 mg/disc)0.39 mg/mL (for clinical strain S. aureus & MRSAa) 0.04 mg/mL (for standard strain S. aureus & MRSAa)
Berberis vulgaris(22)FruitMethanolic extract17 mm
Ferulago angulata(38)Aerial partsEssential oil15 µg/mL
Ferula goangulata(38)SeedsEssential oil> 4 × 103 µg/mL
Ferulago Bernardii(72)Aerial partsEssential oil250 µg/mL
Eucalyptus globulus(32)LeavesAqueous extract14 mm (4 mg/disc) (for MRSAa) 11 mm (4 mg/disc)
Eucalyptus globulus(32)LeavesEthanolic extract17 mm(4 mg/disc) (for MRSAa) 15.5 mm(4 mg/disc)0.18 mg/mL (for clinical strain MRSAa) 0.09 mg/mL (for standard MRSAa strain) 0.39 mg/mL(for standard and clinical S. aureus strains)
Eucalyptus globulus(46)Essential oil10 to 30 mm (for 14 clinical MRSAa strains) 17 mm (for S. aureus)34.24 to 85.6 µg/mL (for 14 clinical MRSAa strains) 51.36 µg/mL (for S. aureus)

Abbreviation: NA, no activity.

aPlants that were also evaluated against MRSA.

According to the comparison, essential oil of T. caucasicus with the MIC value of 0.31 μg/mL for S. aureus and 2.5 μg/mL for MRSA has the best inhibitory effect on S. aureus strains (Table 1). However, essential oil of T. parthenium, T. vulgaris, T. eriocalyx, T. persicus, A. millefollum, ethanolic extract of P. harmala, flower extract of H. scabrum, and ethyl acetate extract of S. urmiensis with MIC value lower than 22 μg/mL have also the acceptable inhibitory effect against S. aureus (Table 1). The antimicrobial properties the oil of Thymus species is due to phenol content. The oil of Thymus has been traditionally used as anthelmintic, bacteriostatic, antiseptic and spasmolytic agents (14, 15). Achillea species also contain a complex of different antimicrobial agents such as monoterpens, sesquiterpene lactones, flavonoids, and phenolic acids that are found most often in their oils (16-18). Therefore, displaying acceptable inhibitory effect against S. aureus was predictable in these plants. It seems the best antimicrobial effect of T. caucasicus, may be due to more phenol concentration in this species.

Flower extract of H. scabrum, collected from Charmahal va Bakhtiari was more potent than that collected from Isfahan due to its more thymol and carvacrol content (41). It is consistent with other studies that variation in environmental parameters, such as irradiance, climate, nutrients, and soil-water availability can influence plant compositions, and thus cause variation in the antimicrobial activity (73). In some herbs, variation in the antimicrobial activity was due to the plant parts used for extract preparation. For example, methanolic extract of the root from P. harmala has the best effect rather than other parts of this plant. Moreover, different extracts of herbs showed significant different antimicrobial effects in most cases. In addition, some plants showed different antimicrobial effects at different stages of their growth. In this case, Thymus pubescens, Thymus serpyllum (44), and Tanacetum parthenium (64) should be noted that during flowering stage, they had a better anti-staphylococcal effect than the pre-flowering stage. Unripe seeds of Terminalia chebula was also more active against S. aureus than ripe seeds (22).

The antimicrobial effect of methanolic extract of aerial parts of Salvia sahendica (27) and essential oil and methanolic extract from aerial parts of Salvia eremophila (29) were the same as Gentamicin on S. aureus. Moreover, the antimicrobial effect of hydroalcholic extract of Teucrium polium was higher compared to Amoxicillin, Ciprofloxacin, Vancomycin, and Imipenem (58). Surprisingly, essential oil of M. pulegium (48), Tanacetum parthenium (11), and Tanacetum pinnatum (74) showed better anti-staphylococcal effects than standard antibiotics.

Bahrami et al. determined that the antimicrobial activity of ethanolic extract from S. striata leaves is lower than Doxycyclin and Ofloxacin against S. aureus. However, these antibiotics have synergistic effects in combination with ethanolic extract of S. striata leaves (42).

Among all of the evaluated medical herbs, antimicrobial effect of 12 species, including S. tomentosa, Cuminum cyminum, Artemisia dracunulus, Artemisia herbalba, Artemisia absinthium, Thymus vulgaris, Thymus caramanicus, Mentha piperita, Peganum harmala, Achillea wilhelmsii, Berberis vulgaris, and Eucalyptus globules are also studied against MRSA. In comparison to antibacterial assays against MRSA we found that ethanolic extract of S. tomentosa, seeds of C. cyminum, A. dracunulus, A. herbalba, A. absinthium, T. caramanicus, A. wilhelmsii, ethanolic, and aqueous extract of M. piperita, root of B. vulgaris, essential oil and ethanolic extract of T. vulgaris, methanolic extract of seed, leaves, stem, root, flower and ethanolic extract of P. harmala, ethanolic extract, aqueous extract and essential oil of leaves of E. globulus have effective inhibitory effects against MRSA.

It is noteworthy that S. multicaulis (methanolic extract) was the only plant active against penicillin-resistant S. aureus. More studies concerning the molecular basis of every active extract against clinical S. aureus, especially MRSA must be performed in the future. A limitation was trouble finding the full text of some articles. We had to email the authors. Lack of response or late response of some of them caused to waste a lot of time.

6. Conclusions

Most of the evaluated Iranian plants with acceptable MIC or inhibition zone have the potency of antimicrobial activity, especially against S. aureus and its most frequent resistant strains, MRSA. So the intended natural extract, especially essential oil of Thymus caucasicus can be a candidate for drug design for replacement of conventional antibiotics with the intention treatment of S. aureus infections. However, further clinical and analytical trials of these data are necessary to finding new knowledge such as in vivo effects and side effects of using herbal extracts as antibiotics. It was also understood that extracts derived from the same species can show significant differences in antimicrobial potency when collected at different sites, owing to the influence of soil, climate, and other factors. These differences may also relate to the type of extract, using plant parts, and the stage of plant growth.

Acknowledgements

Footnotes

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