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Potential of Rosemary oil to be used in drug-resistant infections
Article in Alternative Therapies in Health and Medicine · September 2007
Source: PubMed
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ORIGINAL RESEARCH
POTENTIAL OF ROSEMARY OIL TO BE USED IN
DRUG-RESISTANT INFECTIONS
Suaib Luqman, PhD; Gaurav R. Dwivedi, MSc; Mahendra R Darokar, MSc; Alok Kaira, PhD; Sunian P. S. Khanuja, PhD
Objective • To evaluate the antimicrobial acti\ity potential of the
essential oil of rosemary specifically for its efficacy against the
drug-resistant mutants oi Mycobackrium smegmalis, Escheriehia
coli. and Candida alhiians.
Method* Aiuibacterialantifimgal.anddrugresistance-modifying
activity was evaluated both (jualitatively and quantitatively following disc diliiision and broth dilution assay procedures.
Results • The rosemary essential oil was found to be more active
against the gram-positive pathogenic bacteria except Efaccalis
Suaib Luqman, PhD; Gaurav R. Dwivedi, \isc; Mahendra P.
Darokar, MSc; and Suman P. S. Khanuja, PhD, work in the
Genetic Resources and Biotechnology Division and Alok
Kalra, PhD, works in the Field Laboratory and Organic
Farming Division of the Central Institute of Medicinal and
Aromatic Plants (Council of Scientific and Industrial
Research), Lucknow, India.
R
osemary (Rosmarinus officinalis L.) is a very important medicinal and aromatic plant belonging to the
Lamiaceae family and has been cultivated for a long
time. Evidence suggests that rosemary herbs were
used as medicinal, culinary, and cosmetic virtues in
ancient Egypt. Mesopotamia, China and India.' As a result, it is
widely used today as a medicinal plant. Rosemary has a long list
of claims pertaining to its medicinal uses, including antibacterial
and antioxidant properties.^' It is known to be an effective
chemopreventive agent/ an anti-mutagenic," and has been shown
to be non-toxic in animal models."' The essential oil enhances
the blood circulation of the limbs, has antirheumatic effects, and
relieves neuralgic pains. Besides the therapeutical applications,
the essential oil is widely used in the cosmetic industry, producing various colognes, bathing essences, lotions, and shampoos.
Rosemary is a popular spice in many Western countries, but its
use is most popular in the Mediterranean countries, especially
Italy and France. The leaf of rosemary is an indispensable spice
in French, Italian, and Spanish cuisine."'"
Today, rosemary is cultivated in nearly all countries around
the Mediterranean Sea and in England, the United States, and
Mexico. The leaves contain about 1% to 2.5% essential oil. The compounds 1.8-cineole (3% to 89%), camphor (2% to 14%), borneol (16%
54
and drug-resistant mutants off coli. compared to gram-negative
bacteria. Similarly, it was found to be more active toward nonfilamentous, filamentous, dermatophytic pathogenic fiingj and
drug-resistant mutants oiCandida albicaris.
Conclusion • Our findings suggest that characterization and isolation of the active comp()und(s)fi"omthe rosemary oil may be useful
in counteractinggram-positive bacterial, Ringal, and drug-resistant
infections. (A/ffn; TherHmllh Med. 2007;13(5):54-59.}
to 20%), bornyl acetate {0% to 17%), a-pinene (2% to 25%). and others contribute to the complex taste. Rosemary leaf has applications
as an antioxidant both internally and externally. In addition to antioxidant properties, laboratory studies have established the inhibitory effects of rosemary extract on tumor generation and mutagenesis.
The antimicrobial effects of rosemary also have been studied.""
It is well known that the activity of rosemary extracts in the
food industry and in medicine is due to the presence of some
important antioxidant oil and phenolic components""^ to prevent oxidative degradation of oil- and iipid-containing foods."^"
Essential oils are volatile compounds of a plant's secondary
metabolism and may act as phytoprotective agents,'' It has long
been recognized that some essential oils have antimicrobial
properties'*^-' and these have been reviewed in the past.^"'* Besides
antibacterial properties.^''" essential oils also have insecticidal,*"
antiparasitic,"'^ and antifungai activit)', which are important both
for food preservation and the control of human and plant diseases
that are of microbial origin,'" This is particularly relevant, as some
very dangerous microbial mutants have demonstrated an increased
resistance to the most common antibiotics.''^" In the present study.
we report the antimicrobial activity of the essential oils extracted
from Rosmarinus officinalis L. against pathogenic bacteria and ftmgi
and evaluate their efficacy against some of the drug-resistant mutants
ot'Mycobacterium smegmatis, Escheriehia coli. and Candida albicana.
MATERIALS AND METHODS
Collection of Plant Material and Extraction of Essential Oils
The plant material (leaves) of Rosmarinus officinalis L.
(Lamiaceae) was collected fi"om the research farm of the Central
Institute of Medicinal and Aromatic Plants (CIMAP), Lucknow,
India. The leaves were shade-dried and a voucher specimen was
deposited at the CIMAP herbarium (CIMAP-10051) in Lucknow.
ALTERNATIVE THERAPIES. SEP/OCT 2007. VOL, 13. NO. 5
Rosemary Oil for Drug-resistant Infections
Tlie shade-dried leaves were subjected to steam distillation for 3-4 h
using a Clevenger-type apparatus.*" Essential oils were collected after
decantation and tested for antimicrobial activity against pathogenic
bacteria, flmgi. and drug-resistant mutants using disc diffusion and
broth dilution assay.
acid (10 mg/mL), clotrimamle (10 mg/mL). and amphotericin B (10
mg/niL) were used as positive controls, and dimethyl sulfoxide
(DMSO) was used as a negative control.
Disc Difiusion Assay
Antibacterial and antifungal disc difiusion assay was carried out
Microorganisms Used
folknving the method descrilied by Bauer et aL "^ Bacterial and flingal
The pathogenic bacteria, fungi, and drug-resistant mutants
inoculums were prepared ironi culture grown overnight (24 h) in
used in the present study are as follows.
Luria broth and Sabouraud Dextrose broth (Himedia Liboratories,
Bacterial strains: Streptococcus imttans Microhial Type Culture Mumbai, India), respectively, and the turbidity was adjusted equivaCollection (MTCC) 890. Enterococcus faecalis MTCC 439,
lent to 0.5 McFarlaud standards (approximately 1.2 x 10" CFU/niL).
Mycobacterium smegmatis ATCC 10231, Bacillus subtilis MTCC 121,
Aliquots (100 pL) of moculums were spread over the surface of agar
Staphylococciis aiircus MTCC 96. SUiphyhcoccus epidcrmidis MTCC
plate with a sterile glass spreader. Five \.\l. of oil was put on the paper
435, Kleibsella pneunumiac MTCC 109, Pseudomonas aeruginosa
disc (5 mm diameter. Whatman filter paper no. 3). air-dried, and then
MTCC 741. Salmonella typhii MTCC 733, Salmonella typhimurium
placed on the pre-made bacterial and ftingal lawiis. Tlie plates were
MTCC 98, Fscherichhi coli MTCC 723, Enterobacter aewgenes MTCC
then incuhated for 16 to 24 h at 37°C. and the zone of complete
111,and
YminiamterocoUticaMI'CC861.
growth inhibition was measured in millimeters (mm). The values
reported are the mean of 3 experiments in replicate.
Fungal strains: Candida albicans (AH India Institute of
Medical Sciences [MIMS] and MTCC 1637). Aspergilhis nigtr.
Aspergitlus flavus. Sporothrix schenckii. Trichophylon rubrum,
Minimum Inhibitor)' Concentration. Minimum Bactericidal
Microsporum gypseum, Cryptococcus neoformans. and Histoplasma Concentration, and Minimum Fungicidal Concentration
capsulatum {all AllMS, New Delhi).
Determination
Drug-resistant mutants: The wild-type and drug-resistant
The niimmum inhibitory concentration (MIC) ofthe essential
mutants of M smegmatis, E coH, and C albicans used in the present oils extracted from Rosmarinus officinalis L. against pathogenic bactestudy are shown in Table 1.
ria andftingiand also against drug-resistant mutants of M smegmatis,
E coli, and C albicans was detemiined by 2-fbld serial dilution broth
Antibacterial and Antifungal Agents Used
assay as described by Petersdorf and Sherris," Jorgeiison et al,*^ and
Zentz et al.^' The oil was diluted into final concentration of 11 to 1.38
Vancomycin {10 mg/mL), streptomycin (10 mg/mL). nalidixic
TABLE 1 Wild Type and Dnig-resistant Mutants of Msmegmatis, E coli, and Culbkam
Mutants
Drug-resistance Property
References
M smegmatis
MO 155
MSR lOf
CSMC^105
CSLMO205
Wild type (sensitive to quinolones and floroquinolones)
Resistance to ciprofloxacin, lomofloxacin. norfloxacin
Resistance to ciprofloxacin
Resistance to lomofloxaciTi
Snapper etal (1988)''
Sinha (2003),^
Srivastava(2002).""
Luqman et al (2005)™
CA 8000
NK 5819
ET 8000
DH5a
Wild type (sensitive to quinolones and floroquinolones)
Resistance to nalidixic acid
Resistance to nalidixic acid
Resistance to nalidixic acid
Kumar (1976),"
Luqman et al (2005),'"
Santha et al (2000)'^
C albicans
Al and MTCC
Wild type (sensitive to poiyenes and azoles)
E coU
CloGMC128,
CETR Amp
2R. Amp45,
DlR.cAmp
8R, Amp 8R
KGMC 1,
KGMC 3
Kosemary Oil for Drug-resistaiil [nfectioiis
Gupta (2005)"
Resistance to clotrimazole
Resistance to amphotericin B
Clinical isolates, resistance to both amphotericin B and
ciotrimazole
ALTERNATIVE THEIUriES. SEP/OCT 2007. VOL 13. NO. 5
55
mg/mL. The microtitre plates were inoculated with 10 pi, of diluted
24-h grown culture of the test organism with a titre equivalent to 0.5
McFarland standards. The inoculated microtitre plates were then
incubated at 37°C for 16 to 24 h, and the growth was recorded spectrophotometricaliy at 600 nm using spectramax a 190-niicroplate
reader (Molecular Devices, Sunnyvale, Calif). The MIC (IC^,^ value
was detected from the turbJdiinetric data as the lowest concentration
of oil showing growth inhibition equal to or greater than 80% as compared to oil-free control. The minimum bactericidal concentration
(MBC) and minimum ftingicidal concentration (MFC) values also
were detected from tlie turbidimetric data as the lowest concentration
of oil at which 99% of killing was observed. The MIC, MBC, and MFC
values reported are the mean of 3 experiments in replicate.
RESULTS AND DISCUSSION
The essential oil obtained from Rosmarimis offidnalis h. were
tested for the antibacterial, antifungal, and resistance-modifying
activity against pathogenic bacteria, fringi, and drug-resistant
mutants of M smcgmatis. E coli. and C alhicans following disc diffusion and broth dilution assay, respectively. Results are expressed
in terms of zone of inhibition, MIC, MBC, and MFC.
The essential oil from Rosmarinus ojjidrnilis 1,. was active
against all the gram-positive pathogenic bacteria except f faccuhs.
whereas no activity was observed against gram-negative bacteria
(Figure 1). Interestingly, oil was found to be more active against
drug-resistant mutants of E coll (Figure 2, Tables 2 and 3) but less
active against M stnegmatis. Similarly, it was found that essential
oil was active against all the non-filamentous, filamentous, and
dermatophytic pathogenic fungi and drug-resistant mutants of
Calbicans (Figures ^ and 4, Tables 4 and 5).
The observed antibacterial, antiflmgal, and resistance-modifying
activity of essential oil from Rosmarinus ojjkinalis L. against
pathogenic bacteria, fungi, and drug-resistant mutants of M
smegniatis. /;' coli. and C alhicam was quantified using the broth
dilution assay in terms of MIC, MBC, and MFC, respectively. The
MIC of essential oil from Rosmarinus officinaiis L. ranged from 11
mg/ml, to more than 11 mg/ml, against pathogenic bacteria and
drug-resistant mutants of Msmcgmalis and Ecoii, 1.38 ing/niL to
11 mg/mL against pathogenic fungus, and 2.75 mg/mL to 5,5
mg/mL against drug resistant mutants of C alhicam. The MBC
of essential oil necessary to cause an eil^ect is more than 11 mg/
mL di^amsX-M smegmatis zndEcoli, 2.75 mg/mL to more than 11
Bl
B2
m
B4
B5
Bti
Drug-resistant Mutants
a R ojfidiuilis O R officinalis (1:1)
B7
B8
• Streptomycin • Nalidixic acid
FIGURE 2 Growl h-iii hi bitory Activit)' nf Essential Oil From
Rosmarinus ojjkinaiis L. Againsl Drug-resistant Mutants of Bacteria
Assayed by Disc Diflusion
14 n
Bl: CA 8000, B2: FT 8(XM). B.-J: NK 5819, B4: D H 5 a , B5: M C 2 1 5 5 , B6: CSMC2105.
B7: C S L M a 205, B8: MSH 101.
1210-
TABLE 2 Minimum Inhibitory Concentration and Miniintini
Bactericidal Concentration of Essential Oil iToni Rosmarinus
officinalis L. and Antibiotics Against Pathogenic Bacteria
8-
4-
Pathogenic
Bacteria
2-
Saureus
SA SE SM EF MS BS KP PA ST Sim EC EA YE
Pathogenic Bacteria
n R. oiBcinalis D R. officinalis (1:1) • Streptomycin • Vancomycin
FIGURE 1 Growth Inhibitory Activity of Essential Oil From Rosmarinus
officinalis L. Against Pathogenic Bacteria Assayed by Disc Diffiision
S A - StaphyliKiHrm aiimis; SE= StaphylociKriis q)itknmdis\
SM=Stn'ptoi'otras iriiHiiiis;
EF= FMerofnccusfaecalbr. MS= Mycobactcrium smegmalis; V&= Bacillus siibliliy,
KP= Klrilm-llii piieiwmimc
?K~ I'st'udmumm
tifniginaw. ST= Stilmoriclln lyphii;
?iTm=Siiliiioni'll(i lyphimurium; liC= Bclieridiia coli: EA= Enkroi)ader aeragene^.
56
Sepidermidis
S mutans
Efaecalis
Msmcgmalis
B subtilis
Kpneumoniae
P aeruginosa
Styphii
S typhimurium
Eeoli
Eaerogenes
Y enterocolidca
ALTERNATIVE THERAPIES, SEP/OCT 2007. VOL. 13. NO, 5
MIC of R
officinalis
(mg/mL)
>11
>11
>11
—
11
>11
—
—
—
—
—
—
—
MIC and MBC
of Streptomycin
(Mg/mL)
MIC and MBC
of Vancomycin
(MBC pg/mL)
6.25 (6.25)
12.5(50)
1.56(3.125)
25(100)
0.78 (1.56)
0.78(3.125)
12.5(12.5)
25 (50)
25 (100)
25(100)
12.5 (25)
12.5 (50)
12.5 (100)
3.125 (6.25)
3.125 (12.5)
1.78(6.25)
125(125)
15.625(15.62)
7.81 (15.62)
500(>500)
>500 (>500)
500(>500)
250 (>500)
250 (500)
250 (500)
500 (>500)
Rosemary Oil for Drug-resistant In(eclii>iis
mg/mL against pathogenic flmgal strains, and 5.5 mg/mL to 11
mg/mL against drug resistant mutants of Calhicans.
The present study was undertaken with the objective of
evaluating the antimicrobial property of the essential oil of rosemary and testing its efficacy against the drug-resistant mutants
of M sniegmatis, E coli, and C alhicans in view of the emergence of
resistance against the currently available antimicrobial agents."
Our observation showed the essential oil of rosemary was more
active toward gram-positive than gram-negative mutants, which
is in line with the finding of earlier reports.'"'"'' This finding suggests less susceptibility of gram-negative organisms due to the
presence of an outer membrane surrounding the cell walJ^ that
restricts diffusion of hydrophobic compounds through its lipo
polysaccharide covering.^''
In the present global scenario, disease-causing microbes are
acquiring resistance to many of the antimicrobials used for treating bacterial and ftingal infections. The quinolones/ftoroquinolones, azole, and polyene classes of antimicrobials often are the
last resort to treat infections; hence the chances of acquiring
resistance against these antimicrobials are higher. Therefore, it is
imperative to research the structurally different antimicrobial
agent(s) that can kill drug-resistant mutants with fewer side
effects. The usefiil observation in this study, however, is that the
oil was more active toward gram-positive and drug-resistant
mutants as compared to wild-type strains. Similarly, oil was
more effective toward pathogenic fungi, particularly against
drug-resistant mutants of Calbicans (FI to FIO; resistant against
TABLE 3 Minimum inhihitory Concentration and Minimum Bactericidal
Concentrjtion of Essf iitiai Oil Fmm Ra\miirimi\ offidmilis L. and Antibiotic
20-
in Wild Type and l>ug-resistant Mutants of Ecoli and MsmegmatLs
Dnig-resistant
Mutants of
Bacteria
Bl
B2
B3
B4
B5
B6
B7
B8
MIC of «
offidnalis
(mg/mL)
MIC of
Nalidixic acid
(MBC Mg/niL)
MIC of
Streptomycin
(MBC Mg/mL)
>LL
U
>11
>11
>U
>U
>U
12.5 (25)
6.25(12.5)
3.125(6.25)
50 (100)
6.25(12.5)
25 (50)
25 (50)
12.5 (25)
1.56(3.125)
6.25 (6.25)
50 (50)
1.56(3.125)
1.56(3.125)
0.78(3.125)
0.78 (.3.125)
12.5 (25)
>n
I 1
i
\.\
i I
I,.
lo
17
F8
1-9
HIO
Drug-resistant Mutants
B 5: MO 155. B 6:
B1:CA8000.B2 FT 8000, B 3: NK 5819. B 4: DH5a.
CSMeiO5. B 7: CSLMC'205, B 8 MSR 101.
URoffidnalis n R offidnalis (hi)
• Amphotericin B • Clotrimazole
FIGURE 4 Growth lniiibitory Activity of Essential Oil From Rosmarinus
offidnalis L. Against Dnig-resistant Mutants o^Candida albicans
Assayed by Disc Diffusion
I'l: KGMC1.1^: KGMC X V3: C'b 31. [-4: C 6R, 1'5: Oo GMC128, F6: CETR Anip
2R. P7: Amp 45. F8: t> IR, F9: cAmp 8R, HID: Amp 8R.
TABLE 4 Minimum Inhibitory Concentration and Minimum
Eungicidal Concentration of Essential Oil From Rosmarinus offidnalis
L. and,Viitilungal Against Pathogenic Fungal Mutants
AI
MTCC
CN
SS
AF
AN
HC
TK
Pathogenic
MIC and MFC
ofR offidnaTvi
Fungi
(mg/mL)
ofAmpluiU'ricin
B(jig/mL)
Calbicans(M)
5.5 (11)
2.75 (5.5)
5.5 (11)
11 (>11)
11 (>11)
11 (11)
2.75 (2.75)
1.38 (2.75)
2.75 (5.5)
1.56(3.12.'"))
1.56(3.125)
1.56(3.125)
3.125 (6.25)
3.125 (6.25)
1.56(3.125)
0.78(1.56)
12.5 (12.5)
1.56 (3.125)
\U.
Pathogenic Fungi
nRofficinaUs BR officinalis (hi) • Amphotericin B •Qotrimazole
MTCC
Cneoformis
Sschenckii
FIGURE 3 Growth Inhibitory Activity of Essential Oil From Rosmarinus
A flavus
offidnalis I.. Against Pathogenic hungi Assayed by Disc Diftlision
A nigcr
AI= Camiida alhicam (AllMS): MTCC= Candida albirans {MYCC1637);
CN= CrypltHWivs neojonnaiis:. S,S= Sjmrnlhrix sihemkii: M'= AsjKT^illtafla\wi\
AN=Asper^!lus nigtr. 1 IC= I lislopltisrmi lapsutiilum; TR= Trichnphytini rubmm;
M.G= Micnisporum gypsfum.
Rosemary Oil for Drug-resistant Infections
It capsulalum
Trubrum
Mgypseum
MIC and MFC
MIC and MFC
of Clotrimazole
(Mg/mL)
0.39 (0.78)
1.56(3.125)
0.39 (0.78)
1.56(3.125)
3.125(6.25)
0.39(1.56)
0.195(0.39)
6.25 (12.5)
0.195 (0.195)
ALTERNATIVE THERAPIES. S E P / O C T 2007. V O L 13. N O . S
57
TABLE 5 Minimum Inhibitory Concentrarion and Minimum
Fungicidal Concentration of Essential Oil o(Rcsmarinus ojfiiiimlis L.
and Antiftingal Against Drug-resistant Mutants ii{Candida nlbicans
Drug-resistant
Mutants of
CaBmmts
MIC and MFC
oiR officinalis
(mg/mL)
MIC and MFC
of Ainphoteridn
B(pg/mL)
MIC and MFC
ofCIotrimazok
(pg/mL)
Fl
F2
F3
F4
F5
F6
F7
F8
F9
FIO
5.5 (5.5)
5.5 (U)
5.5 (U)
5.5 (5.5)
2.75 (5.5)
5.5 (11)
2.75 (5.5)
2.75 (5.5)
5.5 (U)
2.75 (11)
6.25 (12.5)
6.25 (12.5)
3.125 (6.25)
6.25 (12.5)
6.25 (6.25)
3.125 (3.125)
3.125 (6.25)
6.25 (12.5)
6.25(12.5)
6.25 (6.25)
0.095(0.195)
0.095(0.195)
6.25 (12.5)
3.125(6.25)
3.125(6.25)
6.25 (fi.25)
0.195(0.39)
3.125 (6.25)
3.125 (6.25)
0.195(0.39)
16.
F 1: KGMC 1, F 2: KGMC 3. F 3: Qo 31, F 4: C 6R, F 5: Clo GMC 128, F 6:
CETR Amp 2R, F 7: Amp 45, F 8: D I R , F 9: cAinp 8R, F 10 : AmpSR
17.
18.
the polyene and azole group of antifiingal agents). Although the
mechanism of action of rosemary oil has not been studied in
detail due to the presence of different groups of compounds
present in it. it is thought that the action may be due to any of
the following mechanisms reported in several essential oils'
activity: damage or degradation of the cell wall.""-' disturbances
in the cytoplasmic membrane,''^''•• depletion of proton motive
force, •"'•" electron flow, leakage of cell contents,^''^* •''"^' damage to
membrane proteins,''"' or active transport and coagulation of
cell contents.'"' Earlier published reports have shown that rosemary extract and its fraction inhibit the in vitro efflux of antibacterial agents" in mutants (including methicillin-resistant S
aureus) of 5 aureus.''•"''- Our observation suggests that essential oil
of rosemary is very effective against drug-resistant mutants of
bacteria and fungi and that it has greater efficacy against fungus
than bacteria. The present findings also suggest that characterization and isolation of the active constituent(s) of rosemary oi!
may be useftil in counteracting gram-positive bacteria and fungi
and drug-resistant infections.
Acknowledgments
We ilijiik ilii' l)f[iarlmen[ of Biotechnology. Ministry of Science and Technology,
Governmem of Imlia and Council of Scieniifir and Iniiuslrial Research. New Delhi, for
financial assistance. We are also gratefiil to All India Institute oI Medical Sciences, University
of Delhi (South Campus), New Delhi and Kin^ George's Medical Ciillege. Lucknow. for providing some ol tlie pathogenic bacteria, fungi, and drug-resistanl strains.
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