Life Science Journal 2013;10(4) http://www.lifesciencesite.

com

Antimicrobial Activity Of Garlic Juice (Allium Sativum), Honey, And Garlic -Honey Mixture On Some
Sensetive And Multiresistant Microorganisms

Saad B. AL Masaudi and Mona O. AlBureikan

King Abdulaziz University, Faculty of science, Department of Biological Science, division of microbiology, Jeddah,
Saudi Arabia
*Corresponding E-mail: [email protected]

ABSTRACT: Garlic is well known for having strong antimicrobial effects. The antimicrobial effects of Chinese
garlic juice alone, honey alone (Langaneza honey, Black Forest) and honey-garlic mixture (1/1v, 1/4 v, 4/1v) with
different concentrations 100%, 50%, 20%, 10% against 8 microbial species, Streptococcus pyogenes ATCC 19615,
Staphylococcus aureus; (Methicillin- Sensitive Staphylococcus aureus - MSSA) ATCC 25923, (Methicillin-
Resistant Staphylococcus aureus -MRSA) ATCC 10442, Enterococcus faecalis; (Vancomycin -Sensitive
Enterococci-VSE) ATCC 29212, (Vancomycin - Resistant Enterococci-VRE) ATCC 51299, Escherichia coli
ATCC 25922, Pseudomonas aeruginosa ATCC 27853, and Candida albicans ATCC 10291 were examined by broth
Dilution Method. The results showed that garlic juice at 100%, 50%, 20% and 10% concentration have a very strong
effect on the growth of all species of microbes comparing with control, and Staphylococcus aureus, Escherichia
coli, and Pseudomonas aeruginosa were the most sensitive microbes. Moreover, Honey at 100%, 50%, 20% and
10% concentration have a very strong effect on the growth of all species of microbes but significantly less than the
effect of garlic juice. Also when studying the effects of the garlic- honey mixture (1/1v, 1/4v, 4/1v) with different
concentrations, it became clear that the garlic- honey mixture had a very noticeable effect on all kinds of microbes
examined, and when comparing the effect of the honey alone and the garlic alone with the garlic- honey mixture, it
became clear that all honey-garlic mixtures concentrations (1/1 v, 1/4 v, 4/1 v) were significantly the most effective
comparing with garlic or honey alone.
[Saad B. AL Masaudi and Mona O. AlBureikan. Antimicrobial activity of garlic juice (allium sativum), honey,
and garlic -honey mixture on some sensetive and multiresistant microorganisms. Life Sci J 2013;10(4):2429-
2435]. (ISSN:1097-8135). http://www.lifesciencesite.com. 325

Key word: Garlic, Honey, Garlic- Honey mixture, Antimicrobial activity, MRSA, MSSA, VSE, VRE, Escherichia
coli, Pseudomonas aeruginosa, and Candida albicans.

1- Introduction: of nosocomial infections that are so prevalent in

Garlic (Allium sativum) in the family Liliaceae is hospitals (Abubakar,2009).
a perennial bulb-forming plant. It is world-wide The most important chemical compounds of garlic
known, as a dietary and medicinal purposes which was thought to be responsible for antimicrobial
(Palaksha et al.,2010; Daka,2011) Louis Pasteur was activity are the organosulphur compound including
the first to describe the antibacterial effect of onion allicin (Hovana et al., 2011). It showed better
and garlic juices (Penecilla; Magno;2011). Garlic has antibacterial activity than streptomycin and ampicillin
antimicrobial effect which has proved in many (Ilić et al., 2012). Allicin exhibits its antimicrobial
previous studies (Elnima et al., 1983; Ayala-Zavala; activity mainly by immediate and total inhibition of
González-Aguilar,2010;. Goncagul; Ayaz,2010) RNA synthesis, although DNA and protein syntheses
Garlic has been found to exhibit antibacterial activity are also partially inhibited, suggesting that RNA is the
against a wide range of Gram negative and Gram- primary target of allicin action (Durairaj et al., 2009).
positive bacteria (Chehregani et al., 2007; Pundir; Moreover, garlic is known to inhibit cell wall
Jain,2010; Bakht et al.,2011; Bakhshi et al.,2012) synthesis because it inhibits trans-peptidation enzymes
including multidrug-resistant strains (Ham et al., involved in the cross-linking of the polysaccharide
2010; Gull et al., 2012), and also possesses antifungal chains of the bacterial cell wall and also activates lytic
activity (Aala et al., 2010); antiparasitic (Farkhondeh enzymes (Eja et al., 2007). Joe et al (2009) postulated
et al., 2010), and antiviral activity (Guo et al., 1993) that the antibacterial and antifungal properties of
Garlic is a very important natural plant that used as garlic juice are due to the inhibition of succinic
alternative medicine for management of typhoid that dehydrogenase via the inactivation of thiol group. The
caused by sensitive and multi resistance isolates of ability of garlic to inhibit the growth of both gram-
Salmonella typhi.(Hannan et al., 2012), and it can be positive and gram-negative bacteria shows that it has a
used alongside conventional antibiotics to fight agents broad spectrum of activity and can be used for
formulation and development of newer broad

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spectrum antibacterial substances (Penecilla; Fresh garlic (Allium sativum) bulbs were
Magno;2011) and it provides scientific basis for its purchased from local market. The bulbs were peeled,
utilization in traditional and folk medicine (Meriga et weighed (100 g) and cleaned. Cleaned cloves were
al., 2012). Victor and Igeleke(2012) found that garlic surface-sterilized by immersing them into 70% (v/v)
has very strong antimicrobial activity against ethanol for 60s. Residual ethanol on surface was
Staphylococcus aureus, Escherichia coli, evaporated in sterile laminar airflow chamber
Pseudomonas aeruginosa and Salmonella typhi. Joe followed by homogenizing aseptically in sterile mortar
and co-workers evaluated the antimicrobial activity of and pestle. The homogenized mixture was filtered
garlic extract against Klebsiella pneumoniae, through sterile cheesecloth. This extract was
Staphylococcus aureus, Morganella morgani, considered as the 100% concentration of the extract.
Candida albicans, Escherichia coli and Proteus The concentrated mother extract was further diluted to
vulgaris. The results showed excellent antibacterial 50%, 20% and 10% by mixing with sterile Nutrient
activity of garlic extract against P. vulgaris and M. broth (Oxoid) (Palaksha et al.,2010; Durairaj et al.,
morgani and the garlic extracts showed excellent 2009)
antimicrobial activity against almost of all pathogens Media used; Nutrient agar (Oxoid), Nutrient
tested better than ginger and pepper (Joe et al., 2009). broth (Oxoid), and Blood agar (Oxoid) were used in
Al-Masaudi and Al-Bureikan(2012) found that a this study.
combination of onion juice suspended in honey Assay of antibacterial activity:
inhibits the growth of some microbe's showing The antibacterial effect of the garlic, honey and
stronger effect than that observed by honey alone or garlic-honey mixture was determined by broth dilution
onion juice alone. Omoya and Akharaiyi(2011) method (Al-Masaudi; Al-Bureikan, 2010)
proved that there is a synergistic effect of The broth Dilution Method:
antimicrobial activity from the combination of ginger A- All five ml of different concentration (100,
and honey against some clinical isolates. The 50,20and 10%) of (garlic or honey or mixture) were
synergistic effect of antimicrobial activity from the prepared in Nutrient broth in test tubes. All the tubes
combination of garlic and ginger or garlic and lime, were inoculated with 0.1 ml of Over Night culture of
against isolates from carious teeth was noted (Patel et the test organisms 1, 5 × 106 cfu/ml. The tubes were
al., 2011). Allicin has even been noted to act incubated at 37o C for 24 h and serial dilution were
synergistically with antibiotics and enhance the made using sterile Nutrient broth and counts were
antimicrobial Activity of antibiotics against tested determined as cfu/ml using Nutrient agar plate count.
microbes (Cai et al., 2007; Khodavandi et al., 2010). B- Garlic-honey mixture was prepared in
deferent volume (1v/1v), (1v/4v) and (4v/1v). The
2- MATERIALS AND METHODS garlic extract was considered as the 100%
Type of honey: one brand of commercial honey concentration of the extract. The concentrated mother
was obtained available in Saudi Arabia (Jeddah) used extract was further diluted to 50%, 20% and 10% by
in current study called Black Forest honey, mixing with sterile Nutrient broth then, every volume
Langaneza, Germany. prepared with different concentration in Nutrient broth
Type of garlic: The garlic which used in this (100, 50, 20 and 10%) in test tubes (Al-Masaudi and
study was Chinese garlic (Allium sativum) from local Al-Bureikan,2012).
market in Jeddah, KSA.
Microbial strains: six strains of standard 3- RESULTS:
microbes; Escherichia coli ATCC 25922, Table (1) illustrates the antimicrobial activity of
Pseudomonas aeruginosa ATCC 27853, garlic on all tested microorganisms that not shown any
Streptococcus pyogenes ATCC 19615, growth at 100%, 50% and 20% concentration of
Staphylococcus aureus; (Methicillin-Sensitive garlic. While when we use 10% concentration of
Staphylococcus aureus - MSSA) ATCC 25923, garlic the result showed some clear microbial growth
(Methicillin-Resistant Staphylococcus aureus-MRSA) of S. pyogenes ، VSE ، VRE and C. albicans while
ATCC 10442, Enterococcus faecalis; (Vancomycin- MSSA, MRSA, P. aeruginosa and E. coli did not
Sensitive Enterococci - VSE) ATCC 29212, show any growth at this concentration. Despite the
(Vancomycin - Resistant Enterococci - VRE) ATCC appearance of growth at a 10% concentration of garlic
51299 and Candida albicans ATCC 10291. All strains the growth was significantly less than the growth of
are collected from the Microbiology lab at King the control sample for all species.
Khaled National Guard Hospital and King Abdulaziz The table (2) illustrate that Langaneza Black
University in Jeddah, Saudi Arabia. Forest honey has antimicrobial activity against all
Preparation of Allium sativum extract: microorganisms in different concentrations.
Staphylococcus aureus (MSSA) was the most affected

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microbe while E. coli and Enterococcus faecalis tested microorganisms. The results showed that garlic-
(VSE) were significantly the least affected microbes honey mixtures (1v/1 v, 4v/1 v, 1v/4 v) at all
comparing with the growth of the control sample. concentrations of 100%, 50%, 20%, and 10% were
Tables (3, 4, 5) illustrate that garlic - honey significantly have the stronger antimicrobial effect on
mixture (1v/1v, 4v/1v, 1v/4v) at concentrations 100%, all tested organisms comparing to garlic alone or
50%, 20%, and 10% have antimicrobial activity on all honey alone.

Table 1. Effect of garlic on different microbial organisms by dilution method.

Total plate count of organisms with different concentrations of garlic.
Different concentration of garlic
Organism Cfu/ml
100% 50% 20% 10%
S.pyogenes 2,02 × 108 0 0 0 6.1 ×106
MSSA 5,8 × 108 0 0 0 0
MRSA 5,2 × 108 0 0 0 0
VSE 4,8 × 108 0 0 0 9.8 ×105
VRE 2,8 × 108 0 0 0 7.1 ×105
9
E. coli 1,35 × 10 0 0 0 0
P.aeruginos 5,2 × 108 0 0 0 0
C. albicans 1,04 × 107 0 0 0 4.8 ×105
MSSA, (Methicillin- Sensitive Staphylococcus aureus); MRSA, (Methicillin-Resistant Staphylococcus aureus);
VSE, (vancomycin -sensitive enterococci); VRE, (vancomycin - resistant enterococci)

Table 2. Effect of honey on different microbial organisms by dilution method.

Total plate count of organisms with different concentrations of honey.
L.B.F Langaneza Black Forest honey
Organism Cfu/ml
100% 50% 20% 10%
S.pyogenes 2,02 × 108 0 1.04 ×104 2.3 ×105 2.4 ×107
MSSA 5,8 × 108 0 0 0 2.4 ×103
8
MRSA 5,2 × 10 0 0 0 4.8 ×104
8 5 6
VSE 4,8 × 10 0 8.2 ×10 1.83 ×10 1.17 ×108
8 5 6
VRE 2,8 × 10 0 2.3 ×10 1.29 ×10 2.4 ×107
9
E. coli 1,35 × 10 0 0 0 2.35 ×108
8 3
P.aeruginosa 5,2 × 10 0 0 1.6 ×10 4.1 ×107
7 6
C. albicans 1,04 × 10 0 0 2.3 ×10 3.3 ×106
MSSA, (Methicillin- Sensitive Staphylococcus aureus); MRSA, (Methicillin-Resistant Staphylococcus aureus);
VSE, (vancomycin -sensitive enterococci); VRE, (vancomycin - resistant enterococci)

Table 3. Effect of garlic - honey mixture (1/1 v) on different microbial organisms by dilution method.
Total plate count of organisms with different concentrations of garlic - honey mixture (1/1 v).
different concentrations garlic - honey mixture (1/1 v)
Organism Cfu/ml
100% 50% 20% 10%
S.pyogenes 2,02 × 108 0 0 0 0
MSSA 5,8 × 108 0 0 0 0
MRSA 5,2 × 108 0 0 0 0
VSE 4,8 × 108 0 0 0 0
VRE 2,8 × 108 0 0 0 0
E. coli 1,35 × 109 0 0 0 0
P.aeruginosa 5,2 × 108 0 0 0 0
C. albicans 1,04 × 107 0 0 0 0
MSSA, (Methicillin- Sensitive Staphylococcus aureus); MRSA, (Methicillin-Resistant Staphylococcus aureus);
VSE, (vancomycin -sensitive enterococci); VRE, (vancomycin - resistant enterococci)

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Table 4. Effect of garlic - honey mixture (4/1 v) on different microbial organisms by dilution method.
Total plate count of organisms with different concentrations of garlic - honey mixture (4/1 v).
different concentrations garlic - honey mixture (4/1 v)
Organism Cfu/ml
100% 50% 20% 10%
S.pyogenes 2,02 × 108 0 0 0 0
MSSA 5,8 × 108 0 0 0 0
MRSA 5,2 × 108 0 0 0 0
VSE 4,8 × 108 0 0 0 0
VRE 2,8 × 108 0 0 0 0
E. coli 1,35 × 109 0 0 0 0
P. aeruginosa 5,2 × 108 0 0 0 0
C. albicans 1,04 × 107 0 0 0 0
MSSA, (Methicillin- Sensitive Staphylococcus aureus); MRSA, (Methicillin-Resistant Staphylococcus aureus);
VSE, (vancomycin -sensitive enterococci); VRE, (vancomycin - resistant enterococci)

Table 5. Effect of garlic - honey mixture (1/4 v) on different microbial organisms by dilution method.
Total plate count of organisms with different concentrations of garlic - honey mixture (1/4 v).
different concentrations garlic - honey mixture (1/4 v)
Organism Cfu/ml
100% 50% 20% 10%
S.pyogenes 2,02 × 108 0 0 0 0
MSSA 5,8 × 108 0 0 0 0
MRSA 5,2 × 108 0 0 0 0
VSE 4,8 × 108 0 0 0 0
VRE 2,8 × 108 0 0 0 0
E. coli 1,35 × 109 0 0 0 0
P.aeruginosa 5,2 × 108 0 0 0 0
C. albicans 1,04 × 107 0 0 0 0
MSSA, (Methicillin- Sensitive Staphylococcus aureus); MRSA, (Methicillin-Resistant Staphylococcus aureus);
VSE, (vancomycin -sensitive enterococci); VRE, (vancomycin - resistant enterococci)

4- Discussion: MSSA, MRSA, P. aeruginosa and E. coli did not

From our results in table (1) we noted that garlic show any growth at 10% concentration of garlic and
juice has a strong antimicrobial activity on all tested this is not in agreement with (Gull et al., 2012), who
microorganisms at 100%, 50% and 20% concentration found that garlic aqueous extract exhibited highest
of garlic, while when we use 10% concentration of antibacterial activity against all tested bacteria except
garlic the result showed some clear microbial growth E. coli. Also, our results were not in agreement with
with some microbes. Despite the appearance of Kivanc; Kunduhoglu (1997), who found that garlic
growth at a concentration 10% of garlic for some juice did not inhibit B. subtilis and P. aeruginosa.
microbes but that growth is less than the growth of the From table (1) we noted that garlic juice has clear
control sample significantly for all species which is effect on multidrug-resistant strains including MRSA
agree with many previous studies (Goncagul; and VRE, which is totally in agreement with
Ayaz,2010; Victor and Igeleke,2012; Rees et (Palaksha et al.,2010; Gull et al., 2012; Cutler;
al.,1993 ; Onyeagba et al.,2004; Khalid et al.,2011; Wilson,2004) The most important chemical
Rahman et al.,2011). Garlic is very important natural compounds of garlic which was thought to be
plant that used as alternative medicine for responsible for antimicrobial activity are the
management of typhoid that caused by sensitive and organosulphur compound including allicin ((Hovana
multi resistance isolates of Salmonella typhi (Hannan et al., 2011) It showed better antibacterial activity than
et al., 2012), and it can be used alongside streptomycin and ampicillin (Ilić et al., 2012). Allicin
conventional antibiotics to fight agents of nosocomial exhibits its antimicrobial activity mainly by immediate
infections that are so prevalent in hospitals and total inhibition of RNA synthesis, although DNA
(Abubakar,2009). Also, our results proved that garlic and protein syntheses are also partially inhibited,
has been found to exhibit antibacterial activity against suggesting that RNA is the primary target of allicin
a wide range of Gram negative and Gram-positive action (Durairaj et al., 2009). Moreover, garlic is
bacteria and this is agreement with (Bakhshi et known to inhibit cell wall synthesis because it inhibits
al.,2012; Safithri et al.,2011). From our results, transpeptidation enzymes involved in the cross-linking

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of the polysaccharide chains of the bacterial cell wall herbal medicines are believed to be more effective
and also activates lytic enzymes (Eja et al., 2007). when taken in combination (Eja et al., 2011).
This ability of garlic to inhibit the growth of both Our results in tables (1,2,3) showed that garlic-
gram-positive and gram-negative bacteria shows that honey mixtures (1/1 v, 4/1 v, 1/4 v) at all
it has a broad spectrum of activity and can be used for concentrations of 100%, 50%, 20%, and 10% were
formulation and development of newer broad significantly have the best antimicrobial effect on all
spectrum antibacterial substances (Penecilla; tested organisms without any growth and this effect
Magno;2011), and it provides scientific basis for its was significantly has stronger antimicrobial activity
utilization in traditional and folk medicine (Meriga et on all tested organisms than garlic alone and honey
al., 2012). Garlic also has antifungal activity on C. alone which is agree with Al-Masaudi and Al-
albicans which is agreed with (Bakhshi et al.,2012), Bureikan (2012), who found that a combination of
but not agrees with (Pundir; Jain,2010) who found onion juice suspended in honey inhibits the growth of
that the garlic extract was not effective against some microbe's showing stronger effect than that
Penicillium oxalicum. Joe et al(2009) reported that the observed by honey alone or onion juice alone. Also,
antibacterial and antifungal properties of garlic juice agree with Omoya and Akharaiyi (2011) and Patel
are due to the inhibition of succinic dehydrogenase via et al 2011), who proved that there is a synergistic
the inactivation of thiol group. All our results from effect of antimicrobial activity from the combination
fresh garlic juice agree with (Hovana et al., 2011) of ginger and honey against isolates from carious teeth
who proved that garlic when used in its raw form has and on some clinical isolates. Also, our results agree
better antibacterial activity, either directly or as an with Al-Jabri et al (2005) who found that the
adjuvant in a solvent. combination of honey and bovine milk had stronger
Honey is known to contain phenol, fatty acids, antimicrobial effect than honey alone or bovine milk
lipids, amylases, ascorbic acid, peroxidases and alone. Mboto et al. (2009) were found that a
fructose, and has high osmolarity and low pH. These combination of medicinal plants like G. kola and V.
elements acting alone or synergistically may amygdalina extracts suspended in Honey inhibits the
contribute significantly to the antimicrobial activity of growth of some microbe's showing stronger effect
honey. Our results in table (2) demonstrate the activity than that observed by honey alone or medicinal plants
of different concentrations of Langaneza Black Forest alone. On the other hand, the results agree with many
honey against eight microorganisms. The results studies which confirm that garlic act synergistically
showed that honey has antimicrobial effect on all with antibiotics and enhancement the antimicrobial
tested microorganisms at different concentrations Activity of antibiotics by Allicin against tested
which were in full agreement with the study microbes (Bakhshi et al.,2012; Cai et al., 2007).
performed by (Aurongzeb; Azim,2011). Antibacterial Also, agree with Patel et al(2011) who detected the
and antifungal activities of honey are well synergistic effect of antimicrobial activity from the
documented and characterized. These antimicrobial combination of garlic and lime against isolates from
properties have been related to oligosaccharides, carious teeth was noted and agree with the study
glycopeptides and peptides present in honey. Honey which observed the highly antimicrobial activity for
glucose oxidase provides a continuous and slow combination of garlic, onion, ginger, pepper and
release of hydrogen peroxide at a level which is coriander seed on different microbes (Rahman et
antibacterial but not tissue-damaging. Hydrogen al.,2011). On the other hand, these results of mixtures
peroxide produced by glucose oxidase plays important on microbes not agree with Eja et al (2011) who
roles in inflammation, wound healing etc found that the combination of garlic and utazi
(Aurongzeb; Azim,2011). The results of the diffusion (Gongronema latifolium)may not always yield the
method exhibited a contrast in the sensitivity of desired effect on both Gram positive and Gram
microbes. It was recommended to use the dilution negative bacteria and the antagonistic effect is more
method instead of diffusion method because it gave evident when the combination is used on Gram
the real effect at different concentrations of honey (Al- negative organisms, e.g. E.coli. and not agree with
Masaudi and Al-Bureikan,2012). Shaista et al(2009) who evaluated The effect of five
The application of blends was based on the stabilizers on microbes isolates and found that E.coli
concept of the effectiveness of combination therapy and Salmonella typhi showed more resistance in case
(synergism) in the treatment of certain bacterial of citric acid and sodium benzoate mixed in the ginger
infections involving drug resistant organisms (Eja et - garlic paste.
al., 2011). However, synergic treatment of ailments
has been a long aged practice in both orthodox and Conclusion:
traditional medicines. In Sub-saharan Africa, The conclusion of this result could be explained
especially West Africa, including Ghana and Nigeria, in two ways. The first way, as we noted previously in

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our results, garlic has antimicrobial effect against Agent on Fresh-Cut Tomato through a Controlled
tested microbes because it is a rich source of the Release System. Journal of Food Science, 75: 398–405.
organosulphur compound including (allicin) the most 8- Bakhshi, M., J. B.Taheri, S.Basir Shabestari,
important chemical compounds of garlic which was A.Tanik, R.Pahlevan (2012). Comparison of
therapeutic effect of aqueous extract of garlic and
thought to be responsible for garlic medicinal
nystatin mouthwash in denture stomatitis.
properties (Koch,1996). Honey, also, has Gerodontology, 29: 680–684.
antimicrobial effect against tested microbes because it 9- Bakht J., M.Tayyab, H. Ali, A. Islam, M. Shafi
is known to contain phenol, fatty acids, lipids, (2011). Effect of different solvent extracted sample of
amylases, ascorbic acid, peroxidases and fructose and Allium sativum (Linn) on bacteria and fungi. African
has high osmotic potential and low pH. These Journal of Biotechnology, 10: 5910-5915.
elements (either in garlic or in honey) which can 10- Cai Y., R. Wang, F. Pei, B B. Liang (2007).
acting alone or synergistically may be contribute Antibacterial Activity of Allicin Alone and in
significantly to the antibacterial activity of the Combination with b -Lactams against Staphylococcus
spp. and Pseudomonas aeruginosa. J. Antibiot, 60:
combination of honey and garlic which resulting
335–338.
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