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Journal of Applied Pharmaceutical Science Vol. 3 (06), pp. 074-078, June, 2013
Available online at http://www.japsonline.com
DOI: 10.7324/JAPS.2013.3611
ISSN 2231-3354
Antimicrobial Activity of Different Aqueous Lemon Extracts
Nada Khazal Kadhim Hindi1*, Zainab Adil Ghani Chabuck2*
1M.Sc., Ph.D. Basic and Medical science Department, College of Nursing, Babylon University, Babylon Province, Iraq.
2M.B.Ch.B., M.Sc. Department of Microbiology, College of Medicine, Babylon University, Babylon Province, Iraq.
ARTICLE INFO
ABSTRACT
Article history:
Received on: 24/04/2013
Revised on: 09/05/2013
Accepted on: 11/05/2013
Available online: 27/06/2013
Over three-quarter of the world’s population is using herbal medicines with an increasing trend globally. Plant
medicines may be beneficial but are not completely harmless. The aim of this study is to evaluate the
antimicrobial activity of different types and part of lemon against different microbial isolates. The antimicrobial
effects of aqueous extracts of peel and juice from fresh and dried citrus and sweet lemon against 6 Gram-positive
and 8 Gram-negative bacterial and one yeast isolates, including Staphylococcus aureus, Staphylococcus
epidermidis, Streptococcus pyogenes, Enterococcus faecalis, Streptococcus pneumoniae, Streptococcus
agalactiae, Pseudomonas aeruginosa, Enterobacter aerogenes, Klebsiella pneumoniae, Escherichia coli,
Salmonella Typhi, Proteus spp., Moraxella catarrhalis, Acinetobacter spp. and Candida albicans, all of them
were studied. The water extracts of all the materials screened showed various inhibitory effects. The juice of
Citrus limon has antimicrobial activities more than other types of extracts. Escherichia coli, Staphylococcus
epidermidis, Streptococcus agalactiae and Candida albicans showed the highest resistance to these extracts.
Lemon species might have antimicrobial activity against different Gram-positive, Gram-negative and yeast
pathogens and could be used for prevention of various diseases caused by these organisms.
Key words:
Plant extracts, Citrus limon,
C.limetta, antimicrobial
activity, aqueous extracts.
INTRODUCTION
For a long period in history, plants have been valuable
and indispensable sources of natural products for the health of
human beings and they have a great potential for producing new
drugs (Nascimento et al., 2000). Bacteria have the genetic ability
to transmit and acquire resistance to drugs, which are utilized as
therapeutic agents (Abeysinghe, 2010). Finding new naturally
active components from plants or plant-based agricultural products
has been of interest to many researchers. Hence, a great deal of
attraction has been paid to the antibacterial activity of citrus as a
potential and promising source of pharmaceutical agents (Jo et al.,
2004; Ortuño et al., 2006). According to World Health
Organization, medicinal plants would be the best source to obtain
a variety of drugs. About 80% of individuals from developed
countries use traditional medicine, which has compounds derived
from medicinal plants. Therefore, such plants should be
investigated to better understand their properties, safety and
efficiency (Nascimento et al., 2000). Lemon is an important
medicinal plant of the family Rutaceae. It is used mainly
for its alkaloids, which are having anticancer activities and the
.
* Corresponding Author
Email: zainabibz@gmail.com
Mob. 009647601102354
antibacterial potential in crude extracts of different parts (leaves,
stem, root, juice, peel and flower) of Lemon against clinically
significant bacterial strains has been reported (Kawaii et al., 2000).
Citrus flavonoids have a broad spectrum of biological activity
including antibacterial, antifungal, anti-diabetic, anticancer and
antiviral activities (Burt, 2004; Ortuño et al., 2006). Antimicrobial
activity of the peel extract is directly concerned with the
components that they contain.
The studies showed that essential oils, protopine and
corydaline alkaloids, lactons, polyacetylene, acyclic sesquiterpenes,
hypericin and pseudohypericin compounds are effective toward
various bacteria (Keles et al., 2001; Maruti et al., 2011).
Furthermore, citrus fruit had been used in traditional Asian
medicines for centuries to treat indigestion and to improve
bronchial and asthmatic conditions (Kalpa et al., 2012). Johann et
al., (2007) and Ghasemi et al., (2009) have shown that citrus
varieties are considered and containing a rich source of secondary
metabolites with the ability to produce a broad spectrum of
biological activities.
Giuseppe et al., (2007) have reported the presence of
limonoids in Citrus species, which can be considered responsible
for activity against many clinically, isolated bacterial strains.
Hindi and Chabuck / Journal of Applied Pharmaceutical Science 3 (06); 2013: 074-078 075
Limonoids obtained from C. limon, showed good
antibacterial and antifungal activity. Extracts of citrus fruit (e.g.
lemon, orange and grape fruit) are among the most studied natural
antimicrobials for food applications), and it has shown to be
effectively decrease the growth of bacteria (Corbo et al., 2008).
There are several Citrus (C.) species, of these C. limon (lemon), C.
aurantium (bitter orange), C. limetta (sweet lemon), C. jambhiri
(Rough lemon) and C. paradise (grape fruit) (Al-Ani et al., 2009).
Due to rapid increase of antibiotic resistance in our
country, plants that have been used as medicines over hundreds of
years, constitute an obvious choice for study. It is interesting to
determine whether their traditional uses are supported by actual
pharmacological effects or merely based on folklore. The aim of
this study is to evaluate the antimicrobial activity of different types
and part of lemon against different bacterial isolates.
MATERIALS AND METHODS
Microbial isolates
Different fifteen clinical microbial isolates (Gram
positive, Gram negative and yeast) (listed at table-1) were isolated
and identified by using conventional biochemical tests and Api
system (Biomeraux, France) (Forbes et al., 2007) and cultivated in
pure culture, at microbiological laboratory/college of Medicine /
Babylon University.
Table. 1: Bacterial isolates used in this study.
Gram positive bacterial
isolates
Gram negative bacterial
isolates
Fungi
Staphylococcus species
Staphylococcus aureus
Staphylococcus
epidermidis
Enterobacteriaceae
Escherichia coli
Enterobacter aerogenes
Klebsiella pneumoniae
Proteus spp.
Salmonella Typhi
Candida
albicans
(yeast)
Streptococcus species
S. agalactiae
Enterococcus faecalis
Streptococcus pneumoniae
Streptococcus pyogenes
Gram negative cocci
Acinetobacter spp.
Moraxella catarrhalis
Pseudomonas aeruginosa
Plants collection
Fresh and dried fruits listed at table (2) used in this study
were obtained from the local market at Hilla City, Iraq, 2013. The
fresh fruits were washed in running tap water in laboratory,
surface sterilized with 70% alcohol, rinsed with sterile distilled
water and cut open with a sterile knife and the juice pressed out
into a sterile universal container separately and then filtered (using
Millipore 0.45 filter paper) into another sterile container to remove
the seeds and other tissues and used freshly as crude without
refrigeration. Extracts of peels were stored at 4 °C until use.
Table. 2: Medicinal plants used to evaluate antibacterial activity.
s.
no
Scientific
name
English
name
Parts of plant
used
Local Arabic
name
1.
Citrus limon L.
Lemon
Fruit (peel)
ضماح يمون
2.
Citrus limon L.
Lemon
Fruit (juice)
3.
Citrus limon L.
Lemon
Fruit(driedfruit)
ةرصب يمون
4.
Citrus limetta
Sweet lemon
Fruit (peel)
ولح يمون
5.
Citrus limetta
Sweet lemon
Fruit (juice)
Antimicrobial activities
The screening of antimicrobial activities of each crude
aqueous lemon extract on the tested bacteria used in this
investigation was determined on Muller Hinton agar media (all
tested organism grow on Muller Hinton agar media), by the using
agar well diffusion method. Wells of 6 mm diameter and 5 mm
depth were made on the solid agar using a sterile glass borer
(CLSI, 2002; Prescott et al., 2002).
Approximately 20μl of each extract was inoculated onto
wells were made in the spread plate culture of each microbial
isolates. (The plates were performed in triplicates). All plate of the
tested organisms was then allowed to incubate at 37°C for
overnight. After 24 h of incubation, each extract was noted for
zone of inhibition for all isolates. The diameters of the zone of
inhibitions were measured by measuring scale in millimeter
(mm).
Statistical analysis
Bonferroni test recommended by Danial (1988) was used for
statistical analysis (P ≤ 0.05) to show if there is any significant
differences between lemon extracts.
RESULTS AND DISCUSSION
Results of antimicrobial activity of lemon extracts
against Gram positive and negative isolates by the agar well
diffusion method were shown on Table (3) and (4) respectively.
The microbial susceptibility was collectively summarized in
Figure (1). The water extracts of all the materials screened showed
various inhibitory effects.
Table. 3: Antimicrobial activity of lemon extracts against Gram positive and
yeast isolates measured in (mm).
microbial isolates
Lemon extracts
Citrus
limon
(peel)
Citrus
limon
(juice)
Citrus
limon
(dry)
Citrus
limetta
(peel)
Citrus
limetta
(juice)
S. aureus
30
26
N.I
20
N.I
S. epidermidis
N.I
N.I
25
N.I
N.I
S. agalactiae
N.I
20
N.I
N.I
N.I
Enterococcus faecalis
30
28
28
25
N.I
S. pneumoniae
N.I
29
18
35
N.I
S. pyogenes
N.I
20
N.I
24
N.I
Candida albicans
N.I
30
N.I
N.I
N.I
mm= millimeter (diameter of inhibition zone), N.I= No Inhibition
Table. 4: Antimicrobial activity of lemon extracts against Gram-negative
isolates measured in (mm).
Bacterial isolates
Lemon extracts
Citrus
limon
(peel)
Citrus
limon
(juice)
Citrus
limon
(dry)
Citrus
limetta
(peel)
Citrus
limetta
(juice)
Escherichia coli
N.I
10
N.I
N.I
N.I
E. aerogenes
20
20
20
20
30
K. pneumoniae
20
30
20
N.I
N.I
Proteus spp.
N.I
20
20
N.I
20
S. Typhi
N.I
30
8
20
20
Acinetobacter spp.
N.I
20
N.I
10
10
M. catarrhalis
30
30
N.I
20
N.I
Ps. aeruginosa
N.I
N.I
10
10
10
mm= millimeter (diameter of inhibition zone), N.I= No Inhibition
076
Hindi and Chabuck / Journal of Applied Pharmaceutical Science 3 (06); 2013: 074-078
The extract from the juice of C. limon presented the highest
antimicrobial activities, as it inhibited most 13 isolates (out of 15
isolates used) of the bacteria under the study whether Gram
positive or negative with inhibition zone ranging from (10-30mm)
except S. epidermidis and P. aeruginosa which showed no any
susceptibility to this extract. On the other hand, the extracts from
the peel of C. limon show low antimicrobial activity inhibited only
5/15 isolates ( out of 15 isolates used), while the juice of C. limetta
showed no any activity against Gram-positive bacteria but
inhibited 5 Gram-negative bacteria (out of 8 isolates used).
Drastically, peels of C. limetta produced a good
antimicrobial activity (Out of 15 isolates used) with inhibition
zones rang (10-35mm) whether against Gram-positive or Gram-
negative bacteria with no response against Candida.
E. aerogenes showed the highest susceptibility (out of
Gram-negative bacteria) to all of the extracts, with inhibition zones
(20-30mm). Followed by S. Typhi was susceptibility to 4 extracts
(out of 5 extracts used). Followed by K. pneumoniae, Proteus,
Acinetobacter and M. catarrhalis were resistance to 3 extracts (out
of 5 extracts used).
Among Gram-positive isolates, Enterococcus faecalis
gave the top susceptibility to most of the 4 extracts (out of 5
extracts used). Followed by S. aureus and S. pneumoniae was
susceptibility to 3 extracts (out of 5 extracts used). Last but not
least S. pyogenes was susceptibility to 2 extracts (out of 5 extracts
used). Statistical analysis showed significant differences
between effect of C. limon (peel) and C. limon (juice), extract on
microbial isolates, there were no significant differences between
C. limon (peel) and C. limon (dry) extract on microbial isolates,
and there were no significant differences between C. limon (peel),
and C. limetta (peel) on microbial isolates, and there were no
significant differences between C. limon (peel) and C. limetta
(juice) at level (P≤ 0.05). Statistical analysis showed significant
differences between effect of C. limon (juice), and C. limon
(peel), extract on microbial isolates, there were significant
differences between C. limon (juice) and C. limon (dry) extract on
microbial isolates, and there were significant differences between
C. limon (juice) and C. limetta (peel) on microbial isolates, and
there were significant differences between C. limon (juice) and C.
limetta (juice) at level (P≤ 0.05).
Statistical analysis showed significant differences
between effect of C. limon (dry), and C. limon (juice), extract on
microbial isolates, there were no significant differences between
C. limon (peel) and C. limon (dry) extract on microbial isolates,
and there were no significant differences between C. limon (dry),
and C. limetta (peel) on microbial isolates, and there were no
significant differences between C. limon (dry) and C. limetta
(juice) at level (P≤ 0.05).
Statistical analysis showed no significant differences
between effect of C. limetta (peel), and C. limon (juice) extract on
microbial isolates, there were significant differences between C.
limetta (peel), and C. limon (dry) extract on microbial isolates, and
there were no significant differences between C. limetta (peel), and
C. limon (peel) on microbial isolates, and there were no significant
differences between C. limetta (peel), and C. limetta (juice) at
level (P≤ 0.05). Statistical analysis showed on significant
differences between effect of C. limetta (juice) and C. limon
(juice), extract on microbial isolates, there were significant
differences between C. limetta (juice) and C. limon (dry) extract
on microbial isolates, and there were no significant differences
between C. limetta (juice) and C. limetta (peel) on microbial
isolates, and there were no significant differences between C.
limetta (juice) and C. limon (peel), at level (P≤ 0.05).
Hindi and Chabuck / Journal of Applied Pharmaceutical Science 3 (06); 2013: 074-078 077
The microorganism E.coli, which is already known to be
multi-resistant to drugs, was also resistant to the plant extracts
tested. It was susceptible only to the juice of C. limon. Similar
result was noted with S. epidermidis with vulnerability only to the
extract of dry C. limon, S. agalactiae and C. albicans to the juice
of C. limon.
On the other hand, P. aeruginosa, which is also resistant
to different antibiotics, its growth was inhibited weakly by the
extracts from peel and juice of C. limetta and dry lemon.
The prevalence of antibiotic resistance is a continual
problem due to the evolution of a potent defense mechanism
against antibiotics. Therefore, it is necessary to exploit and
develop a novel inhibitory agent against those bacteria (Cabello,
2006). Plants and plant products have been used extensively
throughout history to treat medical problems. Numerous studies
have been carried out to extract various natural products for
screening antimicrobial activity (Nita et al., 2002).
The results indicated that the extracts of all the sorts
studied showed antibacterial activities towards the Gram-positive,
negative bacteria and yeast, but with variability related to the
bacterial genus and species.
Some significant components are abundantly available in
citrus peel, including ascorbic acid, phenolic acids, polyphenols,
and dietary fiber (Gorinstein et al., 2001). Constituents with
antioxidant, antiviral, antibacterial, antifungal, and anticancer
activities have also been reported in citrus (Matasyoh et al., 2007;
Mahmud et al., 2009). Numerous studies have described the
inhibitory activities of citrus against human pathogens, fungi, and
yeasts and food pathogens (Nannapaneni et al., 2008, Lee and
Najiah, 2009).
The reason for the different sensitivity of the Gram-
negative bacteria compared to that of Gram-positive bacteria could
be due to differences in their cell wall composition. Gram-positive
bacteria contain an outer peptidoglycan layer, which is an effective
permeability barrier, whereas Gram-negative bacteria have an
outer phospholipidic membrane (Samarakoon et al., 2012).
Hayes and Markovic (2002) investigated the
antimicrobial properties of lemon and found that lemon possesses
significant antimicrobial activity against S. aureus, Klebsiella,
Escherichia coli, P. aeruginosa and C. albicans. Nevertheless,
these results unmatched with our results as these organisms
showed resistance to most of these extracts except that of S. aureus
and Klebsiella as it matched with these results with inhibition zone
(20-30mm). Moreover, Al-Ani et al (2009) showed good bacterial
inhibition by C. limon especially against S. aureus, P. aeruginosa
and P. vulgaris.
In addition, Abdullah (2009) found that the juice of C.
limon has significant inhibition against both S. aureus and K.
pneumoniae with inhibition zones 17.4 and13.3 mm respectively,
While the juice of C. limetta gave no any inhibition effect on these
bacteria. These results were agreed with our results as the juice of
C. limon was more effective. This could be due to the acidic pH of
this juice that will affect the charges of the amino acids that
constitute the peptidoglycan, and it may affect the active sites of
enzymes leading to defect in their activity (Abdullah, 2009).
The resistance of Gram-negative bacteria to plant
extracts was not unexpected. In general, this class of bacteria is
more resistant than Gram-positive bacteria. Such resistance could
be due to the permeability barrier provided by the cell wall or to
the membrane accumulation mechanism (Abu-shanab et ai., 2004).
Infections caused by P. aeruginosa, especially those with multi-
drug resistance, are among the most difficult to treat with
conventional antibiotics (CDC, 1999). In this study, the growth of
P. aeruginosa was slightly inhibited by lemon extracts. Such
results are very interesting and with expectation, increasing the
concentration of the extracts may produce more inhibition to this
bacterium. They may inhibit bacteria by a different mechanism
than that of currently used antibiotics and may have therapeutic
value as an antibacterial agent against multi-drug resistant
bacterial strains.
There are clinical studies found that daily usage of pure
hand gel which contain C. limon in its ingredients is associated
with reduction in the microbial load, which is important to prevent
risk of transmitting nosocomial infections by healthcare workers
(Kavathekar et al., 2004; Ravikumar et al., 2005). This result
agreed with our outcome as it showed that S. Typhi murium is
affected with all these extracts except the peel of C. limon.
Dhanavade et al., (Dhanavade et al., 2011) suggest that
different alcoholic extracts of lemon peel give antimicrobial
activity against different bacterial isolates especially P. aeruginosa
and S. Typhi murium better than the aqueous extract that we used
in this study as it gave no effect against most of the study isolates
including the two mentioned above.
Generally, Rahman et al (2011) documented that, during
the detection of microbial susceptibility to different plant extracts,
the size of inhibition zone to indicate relative antibacterial activity
is not adequate. The zone must be affected by the solubility and
rate of diffusion in agar medium or its volatilization; and thus the
results could be affected.
CONCLUSION
Lemon extracts have an important role as antimicrobial
agents against microorganisms. They are natural, cheap, safe, and
due to increase antibiotic resistance among bacteria.
ACKNOWLEDGEMENTS
We are extremely thankful to the College of Medicine
and Nursing, Babylon University for providing all the needed
facilities, which are essential for successful completion of the
present work.
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How to cite this article:
Nada Khazal Kadhim Hindi., Zainab Adil Ghani Chabuck.,
Antimicrobial Activity of Different Aqueous Lemon Extracts. J
App Pharm Sci, 2013; 3 (06): 074-078.