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Antibacterial Effect of Origanum majorana L. (Marjoram) and Rosmarinus officinalis L. (Rosemary) Essential Oils on Food Borne Pathogens Isolated from Raw Minced Meat in Egypt

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Bacterial activity is a primary mode of deterioration of many foods and is often responsible for the loss of quality and safety of these foods. In this study, a total of 100 raw refrigerated minced meat samples were collected from retail stores in Egypt and examined for the presence of food borne microorganisms. Antimicrobial susceptibility of the isolates was determined using the disc diffusion assay. Alarming level of resistance was observed to some tested antibiotics reflecting multi-drug resistant strains. The dominant type of resistance was detected to amoxiclav (amoxicillin / clavulanic acid). The effect of Origanum majorana L. (marjoram) and Rosmarinus officinalis L. (rosemary) essential oils in comparison to erythromycin on the growth of Salmonella, E. coli, Shigella, Citrobacter, Proteus and Pseudomonas species isolates was investigated. All the isolates were susceptible to marjoram essential oil. Salmonella was the most sensitive strain tested to the antibacterial action of marjoram essential oil. Finally, marjoram essential oil can play an important role as antimicrobial agent in refrigerated minced meat and potentially it might be used as a natural preservative ingredient for longer periods without the need to use hazardous preservatives in food industry.
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Global Veterinaria 13 (6): 1056-1064, 2014
ISSN 1992-6197
© IDOSI Publications, 2014
DOI: 10.5829/idosi.gv.2014.13.06.9149
Corresponding Author: Shimaa Tawfeeq Abdallha Omara, Department of Microbiology and Immunology, National Research
Centre, Dokki, Giza, Egypt. Postal code 12311. E-mail: shimaa_omara2112@yahoo.com.
1056
Antibacterial Effect of Origanum majorana L. (Marjoram) and
Rosmarinus officinalis L. (Rosemary) Essential Oils on
Food Borne Pathogens Isolated from Raw Minced Meat in Egypt
Shimaa T. Omara, Sherein I. Abd El-Moez and Amany M. Mohamed
11 2
Department of Microbiology and Immunology, National Research Centre, Giza, Egypt
1
Department of Parasitology and Animal Diseases, National Research Centre, Giza, Egypt
2
Abstract: Bacterial activity is a primary mode of deterioration of many foods and is often responsible for the
loss of quality and safety of these foods. In this study, a total of 100 raw refrigerated minced meat samples
were collected from retail stores in Egypt and examined for the presence of food borne microorganisms.
Antimicrobial susceptibility of the isolates was determined using the disc diffusion assay. Alarming level of
resistance was observed to some tested antibiotics reflecting multi-drug resistant strains. The dominant type
of resistance was detected to amoxiclav (amoxicillin / clavulanic acid). The effect of Origanum majorana
L. (marjoram) and Rosmarinus officinalis L. (rosemary) essential oils in comparison to erythromycin on the
growth of Salmonella,E. coli,Shigella, Citrobacter,Proteus and Pseudomonas species isolates was
investigated. All the isolates were susceptible to marjoram essential oil. Salmonella was the most sensitive
strain tested to the antibacterial action of marjoram essential oil. Finally, marjoram essential oil can play an
important role as antimicrobial agent in refrigerated minced meat and potentially it might be used as a natural
preservative ingredient for longer periods without the need to use hazardous preservatives in food industry.
Key words: Minced Meat Antibacterial Resistance Origanum majorana L. (Marjoram) Rosmarinus
officinalis L. (Rosemary) Bacteria
INTRODUCTION Food contamination with antibiotic resistant bacteria
Food borne infections and illnesses have become resistance determinants can be transferred to other
a major international health problem as it is the cause pathogenic bacteria, causing compromise in the treatment
of major illness and deaths worldwide [1]. Outbreaks of of severe infections [5]. The prevalence of antimicrobial
food borne diseases and gastrointestinal illness such resistance among food-borne pathogens has increased
as dysentery and diarrhea have been associated with during recent decades [6]. Natural antimicrobial
the consumption of meat that are contaminated by compounds have several beneficial effects as they
Salmonella,Escherichia coli,Shigella sonnei and reduce the need for antibiotics, control microbial
Listeria monocytogenes through unhygienic practices [2]. contamination in food, improve shelf-life extension
Meat is the main source of food borne diseases in humans technologies to eliminate undesirable pathogens and/or
[3]. The principal pathogens which can be transmitted delay microbial spoilage, decrease the development of
through meat include: Bacillus cereus, Campylobacter antibiotic resistance by pathogenic microorganisms or
species, Clostridium perfringens, Clostridium botulinum, strengthening immune cells in humans [7].
Escherichia coli, Listeria monocytogenes, Salmonella Spices and herbal essential oils (Eos) are used by the
species, Staphylococcus aureus, Yersinia enterocolitis, food industry as natural agents for extending the shelf
Aeromonas, Brucella, Clostridium difficile, Enterobacter life of foods. A variety of plant- and spice-based
and Shigella [4]. antimicrobials is used for reducing or eliminating
could be a major threat to public health as the antibiotic
Global Veterinaria, 13 (6): 1056-1064, 2014
1057
pathogenic bacteria and increasing the overall quality of overnight, then pre-enrichment in maximum recovery
food products. Edible medicinal and herbal plants such as broth and Rappaport vassiliadis broth (Oxoid) then
oregano, rosemary have been successfully used alone or streaked on Salmonella Shigella agar (SS Agar) (Oxoid),
in combination with other preservation methods [7]. Mannitol salt agar (Oxoid), MacConkey’s agar (Oxoid)
Food processing technologies such as chemical and defibrinated sheep blood agar media (Oxoid, Ltd.,
preservatives cannot eliminate food pathogens or delay Hampshire, UK). All plates were incubated at 37°C for
microbial spoilage totally [8]. Cold distribution of 24 hours. Identification was occurred by culture
perishable food can help, but it cannot guarantee the characteristics and bacterial films stained with Gram’s
overall safety and quality of the product. Moreover, technique (BD, Maryland, USA). Identification of the
changes in dietary habits and food processing practices recovered isolates was done according to Forbes et al.
and increasing demand for ready-to-eat products [7]. [12]. API system (20 E and NE) (Biomerieux SA, Marcy
Among several essential oils that may be useful as l'Etoile, France) was used to identify members of family
antimicrobial agents, Origanum majorana L. (marjoram) Enterobacteriaceae using manufacturer’s instructions
essential oil belonging to the family Lamiaceae possesses that inserted within each diagnostic kit. For the isolation
antimicrobial properties against food borne bacteria and of Campylobacter, 1 g of each sample was added to 9 ml
mycotoxigenic fungi and therefore, it may have the of Preston Campylobacter selective enrichment broth
greatest potential for use in industrial applications [9, 10]. (Oxoid) supplement with Campylobacter selective
They are characterized by a wide range of volatile supplement SR 117 (Oxoid), Campylobacter growth
secondary metabolites. It is commercially used as a spice. supplement SR 84 (Oxoid) and 5% defibrenated horse
It is traditionally used to treat asthma, indigestion, blood [13]. The inoculated broth was incubated under
headache, rheumatism, dizziness, gastrointestinal disorder microaerophilic conditions at 42°C for 24 hours. Then the
and migraine [11]. enrichment culture was streaked onto Campylobacter
Rosmarinus officinalis L. essential oil, common name blood-free selective agar base (Oxoid) supplemented with
rosemary, belongs to the family Lamiaceae and it is a very Campylobacter selective supplement SR 155 (Oxoid)
ancient plant of several applications. Some of its and incubated under microaerophilic conditions at 42°C
traditional uses include antispasmodic, analgesic, for (3-5) days. Suspected Campylobacter isolates were
antirheumatic, diuretic and antiepileptic. On the other confirmed using standard biochemical procedure
hand, Rosmarinus officinalis has several applications including catalase, oxidase and hippurate hydrolysis
especially in the food processing and preserving industry tests [14].
because of its natural antioxidant and antimicrobial effect
[11]. Antimicrobial Susceptibility Testing (Ast) of the
The objectives of this study were to determine the Recovered Isolates: The isolates were tested for their
antimicrobial resistance activities of the food borne antibiotic resistance patterns using the disc diffusion
pathogens isolated from raw refrigerated minced meat method. Steps of the test and interpretation were
obtained from retail stores in Egypt and to evaluate the relying on the instructions of the NCCLS [15]. The used
antimicrobial activities of two essential oils (marjoram and antimicrobial discs (Oxoid) were imipenem (IPM10 µg),
rosemary) against the isolated food borne pathogens. gentamicin (CN10 µg), amoxiclav (amoxicillin / clavulanic
Also, this study aimed to investigate the effect of acid) (AMC30 µg), tobramycin (TOB10 µg), ciprofloxacin
marjoram (Origanum majorana L.) essential oil on the (CIP5 µg) and oxytetracycline (OT30 µg). In addition to
quality of meat during cold storage. vancomycin (VA30 µg) was used for Staphylococci
MATERIALS AND METHODS determined. MDR strain is defined as that the pathogen
Sample Collection: Raw refrigerated minced meat samples [16].
(n=100) were randomly collected from local supermarkets
in Cairo and Giza governorates, Egypt and transported on Antimicrobial Activity of Origanum majorana L.
ice to the laboratory.
Isolation and Identification of Bacterial Pathogens:
Twenty five gram of each meat sample was homogenized
in 225 ml of peptone water (PW) and incubated at 37°C
isolates. Multidrug Resistant (MDR) strains were also
which is resistant to 3 groups of antibacterial agents
(Marjoram) and Rosmarinus officinalis (Rosemary)
Essential Oils: The antimicrobial activity of marjoram
and rosemary essential oils was studied using agar
well diffusion method in comparison with
erythromycin [17].
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Extraction of essential oils: The aerial parts of wild Each group was mixed well in polyethylene bags
marjoram (Origanum majorana L.) and rosemary
(Rosmarinus officinalis) were collected from Egypt at full
flowering stage. The collected plants were dried in shade
and ground in a grinder. The dried plant samples (500 g)
were subjected to hydrodistillation (plant material in
boiling water) using a Clevenger-type apparatus for 4h
[18]. Hydrodistillation of plants yielded 2.3% (v/w) of
essential oil. The 2 essential oils preparations were
stored at 4°C in dark glass bottles until used.
Method: The prepared essential oils were tested for their
antimicrobial activities against 62 isolates. Aliquots
(100µl) of each bacterial cell culture suspension matching
with 0.5 McFarland was spread over the surface of
pre-dried Mueller-Hinton agar plates with a sterile glass
spreader. Eighty µl of each type of oil was added into
wells of agar plates directly. Erythromycin discs were
used to assess the susceptibility of tested isolates to
compare with the result of essential oils efficiency.
All Petri dishes were sealed with sterile laboratory
parafilm to avoid eventual evaporation of the essential
oils. The plates were left for 30 min at room temperature to
allow the diffusion of oil. The plates were re-incubated at
37°C for 24 h. After incubation, plates were observed for
antimicrobial activities by measuring the diameters of the
zones of inhibition in millimeter for each of the essential
oil. For an accurate analysis, tests were run in triplicate for
each isolate to avoid any error. Standard reference strains
of S. Typhimurium ATCC 14028 were used as a control.
Microbiological Evaluation of Treated and Untreated
Minced Meat with Origanum majorana L. (Marjoram)
Essential Oil During Cold Storage with and Without
Salmonella Inoculation [19]: Raw minced meat was
divided into 4 groups as following:
Group 1: contained 15 g of raw minced meat.
Group 2: contained 15 g of raw minced meat treated by
1.5 ml marjoram essential oil.
Group 3: contained 15 g of raw minced meat inoculated
by 1.5 ml of Salmonella in concentration of 1.5x108
CFU/ml.
Group 4: contained 15 g of raw minced meat treated by
1.5 ml marjoram essential oil and inoculated by 1.5 ml of
Salmonella in concentration of 1.5x10 CFU/ml.
8
using stomacher, then labeled and stored at -4°C.
The groups were analyzed at each 10 days interval during
the storage period. To evaluate the antimicrobial
potency of marjoram essential oil in the food system
as a preservative, heterotrophic aerobic bacteria
counting on plate count agar and Salmonella
counting on SS agar were carried out on the four
tested groups.
Statistical Analysis: ANOVA was carried out on data of
the sensory evaluation applying the function of two
factors with replicates. “Excel” Software of Microsoft
office 2000. L.S.D. analysis was adapted according to
statistical procedures for agriculture research [20].
Data were expressed as mean ± SE.
RESULTS
Prevalence of Food Borne Pathogenic Microorganisms:
A total of 100 samples of raw refrigerated minced
meat were collected from retail stores in Egypt and
examined for the presence of food borne microorganisms;
Campylobacter was not isolated from any of the
analyzed samples. Meanwhile, the prevalence of
Salmonella species was 19(19%), E. coli was 13(13%),
Shigella species was 12(12%), Staphylococcus species
was 8(8%), Enterobacter species was 8(8%),
Pseudomonas species was 2(2%), Citrobacter species
was 1(1%) and Proteus species was 1(1%) as shown in
Figure (1).
Antimicrobial Susceptibility Testing: Seven different
antibiotics were used against 62 identified bacterial
species isolated from raw minced meat samples.
The results presented in Table (1) showed that the
ciprofloxacin was the most effective antibiotics
against 62 bacterial isolates followed by imipenem,
amoxiclav, gentamicin, tobramycin and oxytetracycline.
Resistance to one or more antimicrobial agents was
found. The dominant type of resistance was detected
to amoxiclav (amoxicillin / clavulanic acid) followed
by oxytetracycline, tobramycin, gentamicin and
imipenem. Results clearly showed that Gram-negative
isolates were more resistant than the Gram-positives;
it was observed that there's marked resistance of Shigella
and Pseudomonas that were 100% for both of them
followed by Salmonella,E. coli and some strains of
staphylococci to amoxiclav (amoxicillin / clavulanic acid)
that were 84.20, 76.92 and 25.00% respectively.
Global Veterinaria, 13 (6): 1056-1064, 2014
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Fig 1: Occurrence of food borne pathogenic bacteria isolated from minced meat in Egypt.
Table 1: Antimicrobial susceptibility testing of meat isolates
Tested isolates (No) Sensitivity type (%) IPM VA CIP TOP AMC CN OT
Salmonella (19) S % 42.11 - 100.00 21.05 0.00 42.10 -
I % 57.89 - - 0.00 15.79 36.84 -
R% 0.00 - - 78.95 84.20 21.05 100.00
ND% - 100.00 - - - - -
E. coli (13) S% 76.92 - 100.00 30.76 - 23.08 -
I% 23.08 - - 46.15 61.54 76.92 23.08
R% 0 - - 23.08 76.92 - 76.92
ND% - 100.00 - - - - -
Shigella (12) S% 66.67 - 100.00 - - - -
I% - - - 33.33 - 66.67 66.67
R% 33.33 - - 66.67 100.00 33.33 33.33
ND% - 100.00 - - - - -
Pseudomonas (2) S% 100.00 - 100.00 - - - -
I% - - - 100.00 - 100.00 100.00
R% - - - - 100.00 - -
ND% - 100.00 - - - - -
Enterobacter (8) S% - - 100.00 50.00 100.00 - 50.00
I% 100.00 100.00 - 50.00 - 50.00 50.00
R% - - - - - 50.00 -
ND% - - - - - - -
S.aureus (8) S% 25.00 37.50 100.00 37.50 62.50 87.50 50.00
I% 50.00 62.50 - 50.00 12.50 - -
R% 25.00 - - 12.50 25.00 12.50 50.00
ND% - - - - - - -
IPM (10) = Imipenem, VA (30 mcg) = Vancomycin, CIP (5mcg) = Ciprofloxacin, TOB (10mcg) = Tobramycin, AMC (30 mcg) = Amoxiclav (Amoxicillin
/ Clavulanic acid), CN (10 mcg) = Gentamicin, OT (30) = Oxytetracycline, ND= Not detectable.
*S=sensitive, I=intermediate, R=resistance
Table 2: Antibacterial activities of Origanum majorana L. (marjoram) and Rosmarinus officinalis L. (rosemary) essential oils in comparison to erythromycin
using disc diffusion method:
Inhibition zone diameter (mm)
---------------------------------------------------------------------------------------------------------------------
Microorganisms (number) Marjoram Rosemary Erythromycin
Shigella (4) 16.75 Resistance Resistance
Salmonella (6) 19.20 Resistance Resistance
Pseudomonas (2) 14.00 Resistance Resistance
Proteus (1) 15.00 Resistance Resistance
E. coli (3) 19.00 Resistance Resistance
Citrobacter (1) 16.00 Resistance Resistance
Reference strain S.TyphimuriumATCC 14028 13.00 Resistance Resistance
Global Veterinaria, 13 (6): 1056-1064, 2014
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Table 3: Inhibitory effect of Origanum majorana L. (marjoram) essential oil as a preservative on total bacterial count and Salmonella either normally present
or inserted in minced meat during storage period at -4 °C for 1 month period with an interval 10 days between each examination:
Bacterial count CFUs/gm
----------------------------------------------------------------------------------------------------------------------------------------------------
Groups Group 1 Group 2 Group 3 Group 4
--------------- ------------------------------ ---------------------------------- --------------------------- ----------------------------------
Storage time SS PCA SS PCA SS PCA SS PCA
Zero day 3×10 TNTC No Growth 3.5×10 3×10 TNTC No Growth 5.6×10
3 37 3
Day 10 10×10 TNTC No Growth 3.5×10 5×10 TNTC No Growth 4.4×10
2363
Day 20 No Growth 8.5×10 No Growth 1×10 3.5×10 7.5×10 No Growth 1.4×10
5 3 56 3
Day 30 No Growth 5.6×10 No Growth No Growth 8×10 1.1×10 No Growth No Growth
5 46
TNTC= Too Numerous to Count.
Group 1: 15 gm of raw minced meat only.
Group 2:15 gm of raw minced meat treated by 1.5 ml 100% Marjoram essential oil.
Group 3: 15 gm of raw minced meat inoculated by 1.5 ml of Salmonella in concentration of 1.5x10 CFU/ml.
8
Group 4: 15 gm of raw minced meat treated by 1.5 ml 100% Marjoram essential oil and inoculated by 1.5 ml of Salmonella in concentration of 1.5x108
CFU/ml.
Antibacterial Activities of Origanum majorana L. E. coli was 13(13%), Shigella species was 12(12%),
(Marjoram) and Rosmarinus officinalis L. (Rosemary)
Essential Oils in Comparison to Erythromycin Using
Disc Diffusion Method: The effect of marjoram and
rosemary essential oils on the growth of Salmonella,
E. coli,Shigella, Citrobacter,Proteus and Pseudomonas
species isolates was illustrated in Table (2). It is clear that
rosemary and erythromycin did not show any inhibitory
effect against the isolates. However, all tested isolates
either Gram negative or Gram positive were susceptible to
the action of 100% marjoram essential oil with a range of
inhibition zone diameter values from 13.00 to 19.20mm.
The results revealed that Salmonella was the most
sensitive strain tested to the antibacterial action of
marjoram essential oil with the strongest inhibition zone
(19.20mm) followed by E. coli (19.00 mm), Shigella
(16.75mm), Citrobacter (16.00mm), Proteus (15.00mm) and
Pseudomonas species(14.00mm).
Effect of Origanum majorana L. (Marjoram) Essential
Oil as a Preservative on the Microbiological Quality of
Cold Stored Minced Meat: Table (3) shows the effect of
marjoram essential oil as a preservative on the
microbiological aspects of minced meat (Salmonella and
total bacterial count) during 4 intervals examination
(day zero, day 10, day 20 and day 30) at -4°C for 1 month.
The data indicated that marjoram showed 100%
bactericidal effect on the end of the storage period.
DISCUSSION
In the present study, Campylobacter was not
isolated from any of the analyzed samples. Meanwhile,
the prevalence of Salmonella species was 19(19%),
Staphylococcus species was 8(8%), Enterobacter species
was 8(8%), Pseudomonas species was 2(2%), Citrobacter
species was 1(1%) and Proteus species was 1(1%) as
shown in Figure (1). It was reported that 69% of cases of
bacterial food borne diseases are caused by Gram
negative bacteria [21]. Enterobacter species (28.6%),
Klebsiella species (5.7%), Escherichia coli (8.6%),
Bacillus species (14.2%) and Pseudomonas species
(42.9%) was recorded from meat samples [22]. A total of
thirty-one bacterial isolates covering six genera from raw
meat was isolated and characterized as Bacillus (9.68%),
Enterobacter (9.68%), Escherichia (25.81%), Klebsiella
(22.58%), Pseudomonas (9.68%) and Staphylococcus
species (22.58%) [23], these microorganisms causes
toxic infection after multiplication in meat foods [24].
Escherichia species are of the most concern in
undercooked meat products, such as beef meat [25].
The presence of E. coli in raw meat might have originated
from animal tissues or contaminated tools used in
slaughtering and related treatment or cutting process.
Escherichia coli is commonly used as surrogate indicator,
its presence in food generally indicate direct and indirect
fecal contamination [21]. Meat may be contaminated with
Salmonellae throughout the slaughtering, dressing and
boning process, starting with the carcass during knife
incision for hide removal [25]. S. aureus has a huge impact
on animals’ health and welfare and causes major economic
losses in livestock’s production [26]. The prevalence of
S. aureus in meat products indicates the presence of
cross contamination, which is usually related to human
skin and clothing and this level of food contamination by
this pathogen might lead to food intoxications [27].
If meat product is temperature abused, this pathogen is
Global Veterinaria, 13 (6): 1056-1064, 2014
1061
able to produce heat-resistant enterotoxins [25]. The data Bacterial gain of antimicrobial resistance is an
concluded that minced meat is considered important
source of bacterial pathogens causing severe
gastroenteritis in human.
Antibiotic resistance levels are elevated among
food borne pathogens. Although, it is difficult to prove a
direct role of drug resistance in bacteria contaminating
food with increased clinical cases of resistant infections,
the presence of such resistant bacteria in food items could
play a role in the spread of antimicrobial resistance
amongst food borne pathogens [28].
Seven different antibiotics were used in the present
study against 62 identified bacterial species isolated
from raw minced meat samples. The results presented in
Table (1) showed that the ciprofloxacin was the most
effective antibiotics against 62 bacterial isolates, followed
by imipenem, amoxiclav, gentamicin, tobramycin and
oxytetracycline. Resistance to one or more antimicrobial
agents was found. The dominant type of resistance was
detected to amoxiclav (amoxicillin / clavulanic acid)
followed by oxytetracycline, tobramycin, gentamicin and
imipenem. Results clearly showed that there’s marked
resistance of Shigella and Pseudomonas that were 100%
for both of them followed by Salmonella,E. coli and
some strains of staphylococci to amoxiclav (amoxicillin /
clavulanic acid) that were 84.20, 76.92 and 25.00%
respectively.
In the present study Gram-negative isolates were
more resistant than the Gram-positives; this is expected
because of intrinsic nature of gram-negative cell wall also
they harbor series of antibiotic resistance genes which
can be transferred horizontally to other bacterial species
[29]. Most of investigated Salmonella isolates were
sensitive to colistine sulphate, ciprofloxacin, amoxicillin,
sulfa-trimethoprim, ampicillin, danofloxacin and
gentamicin; on the other hand, most of the isolates were
multiple drug resistance [30].
In veterinary medicine, antimicrobial agents are
used in therapy, prophylaxis and as growth promoters and
this may be responsible for generation of resistant
bacteria. During the two past decades, the emergence of
antibiotic-resistant bacteria has become a serious problem
worldwide and wide usage of antibiotics in the diet of
domestic animals has made drug resistant bacteria which
could be transferred to human beings. The problem of
resistant strains to multiple drugs (MDR) is increasing
and most studies in different countries have shown high
resistance of strains to several antibiotics [31].
alarming situation where treatment is getting limited to
currently sensitive antibiotics. The prophylactic use of
many antimicrobials in animal feed can also lead to
acquired antibiotic resistance [32]. Plant extracts can be
used in the treatment of infectious disease caused by
resistant microbes [33]. Some herbs are used as meat
effects which have been reported to have bactericidal or
bacteriostatic additives [34]. The inhibitory effects of
herbs are mostly because of their content of volatile oils;
the volatile oils can act as pro-oxidant affecting inner cell
membranes and organelles such as mitochondria in
eukaryotic organisms. Mitochondria like structure and
membranes structure in prokaryotic organisms are also
affected by volatile oil depending on type and
concentration [35].
This investigation was directed to study the effect
of Origanum majorana L. (marjoram) and Rosmarinus
officinalis L. (rosemary) essential oils in comparison to
erythromycin on the growth of Salmonella,E. coli,
Shigella, Citrobacter,Proteus and Pseudomonas isolates
using agar well diffusion method. The results illustrated
that rosemary and erythromycin did not show any
inhibitory effect against the isolates. It was reported that
the weak antimicrobial activities of rosemary essential oils
against pathogenic and nonpathogenic bacteria were
likely due to the lack of verbenone [36]. The antibacterial
activity potential of rosemary essential oil against bacteria
was related to the rate of verbenone, camphor and linalool
rather than to the increased content of 1, 8-cineole. In fact,
major or trace compounds contained in an essential oil
might increase or decrease its antimicrobial activity
because it should be taken into consideration the possible
synergistic and antagonistic effect of compounds in the
oil [37]. The low activity of the essential oil against the
tested isolates suggests either that the crude extracts
held very low concentration of active antibacterial
compounds or that the crude extract contained
compounds that inhibited the antibacterial activity of
the effective compounds.
On the other hand, all tested isolates were
susceptible to the action of 100% Origanum majorana L.
(marjoram) essential oil with a range of inhibition zone
diameter values from 13.00 to 19.20 mm. The results
revealed that Salmonella was the most sensitive strain
tested to the antibacterial action of marjoram essential oil
with the strongest inhibition zone (19.20mm) followed
by E. coli (19.00 mm), Shigella (16.75mm), Citrobacter
(16.00mm), Proteus (15.00mm) and Pseudomonas species
Global Veterinaria, 13 (6): 1056-1064, 2014
1062
(14.00mm). It was reported that marjoram essential oil antimicrobials as a preservatives to control food borne
possesses antimicrobial properties against food borne pathogens. Antimicrobial activities of marjoram
pathogens and spoilage microorganisms when tested in (Origanum majorana L.) essential oils could be used as
vitro and therefore, it may have the greatest potential for natural preservative to control microbial contamination;
use in industrial applications [9, 38]. The main component improve quality of minced meat; and replace synthetic
of marjoram essential oils was carvacrol which preservatives. In-vivo extension studies will be required
represented at 81.5 % in marjoram [39]. It was explained to find appropriate doses of essential oils showing both
that globally, the antimicrobial mode of action of the antimicrobial activity and very low detrimental effect on
marjoram essential oil is considered to arise mainly from eukaryotic cells.
their hydrophobic potential to introduce into the bacterial
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... The last decade has witnessed the emergence of highly virulent and antibiotic-resistant Salmonella isolated from different food matrices causing greater morbidities and mortalities in humans (Parry et al. 2002). In this review, we observed that Salmonella spp. was the most commonly reported bacteria (72 studies), particularly in Egypt (Abdallah et al. 2015(Abdallah et al. , 2018Abd-Elghany et al. 2015;Ahmed et al. 2014Ahmed et al. , 2016Amin et al. 2016;Eid et al. 2020;El Bayomi et al. 2016a, b;Elafify et al. 2019;Elkenany et al. 2019;El-Wehedy et al. 2019;Gharieb et al. 2015;Gwida and El-Gohary 2015;Hakim et al. 2015;Hassanen et al. 2018;Ibrahim 2016;Ibrahim et al. 2014;Mahmoud et al. 2018;Moawad et al. 2017;Morshdy et al. 2018;Omara et al. 2014;Ramadan et al. 2018;Sallam et al. 2014;Sofy et al. 2017;Tarabees et al. 2017;Younis et al. 2019a, b), Iran (Fardsanei et al. 2017;Manafi et al. 2020;Sodagari et al. 2015;Akbarmehr 2012;Besharati et al. 2020;Danesh Ghohar et al. 2017;Doosti et al. 2016Doosti et al. , 2017Enayat et al. 2012;Karimiazar et al. 2019;Mahdavi et al. 2018 Cetin et al. 2020;Demirci et al. 2019;Ertas Onmaz et al. 2014;Goncuoglu et al. 2016;Gunel et al. 2015;Guran et al. 2020;Gurler et al. 2015;Kahraman et al. 2018;Siriken et al. 2015Siriken et al. , 2020Taban et al., 2013;Tellİ et al. 2018;Yüksel et al. 2019;Zafer et al. 2015). In these studies, 4247 isolates of Salmonella spp. ...
... Besides, E. coli has a great capacity to accumulate resistance patterns that can be transferred horizontally with a significant turnover of drug-resistant E. coli every day (Friedman et al. 2002;Poirel et al. 2018). In this review, it was observed that AMR among E. coli isolates was reported in 64 studies from 10 countries: Egypt (Abdelkarim et al. 2020;Ahmed and Shimamoto 2015a, b;Ali Elsayed 2019;Darwish et al. 2015;Elafify et al. 2020;Elmonir et al. 2018;El-Wehedy et al. 2019;Gwida and El-Gohary 2015;Hakim et al. 2015;Hassanen et al. 2018;Mahmoud et al. 2018;Moawad et al. 2017;Omara et al. 2014;Ombarak et al. 2018;Ombarak et al. 2019;Ramadan et al. 2020;Rasmey et al. 2018;Sadek et al. 2019;Sadek et al. 2020;Shawish et al. 2020;Sofy et al. 2017;Younis et al. 2019a, b), Iran Listeriosis is a mainly foodborne illness caused by Listeria monocytogenes (L. monocytogenes) that needs an effective antibiotic treatment because it leads to a high mortality rate, especially in immune-deficient patients, pregnant women, newborns, and the elderly Riviera et al. 1993). ...
... In contrast, few studies focused on AMR among Shigella isolates of food origin (Ahmed and Shimamoto 2015a, b;Shahin et al. 2019). There are just five studies(Ahmed and Shimamoto 2015a, b;Demirci et al. 2019;Obaidat and Bani Salman 2017;Omara et al. 2014;Hassan et al. 2011) that demonstrated AMR among Shigella spp. in the Middle East. Median resistance was calculated for four drugs; tet- ...
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Foodborne pathogens are known as significant public health hazards worldwide, particularly in the Middle East region. Antimicrobial resistance (AMR) among foodborne pathogens becomes one of the top challenges for the environment, public health, and food safety sectors. However, less is known about antimicrobial-resistant foodborne pathogens in the Middle East region. Possibly because of the lack of surveillance, documentation, and reporting. This review focuses on the current status of antimicrobial resistance profiling among foodborne pathogens in the Middle East. Therefore, PubMed and other relevant databases were searched following PRISMA guidelines. Subject heading and texts were searched for “antimicrobial resistances,” “foodborne,” and “Middle East” to identify observational studies on AMR foodborne pathogens published during the last 10 years (2011 to 2020). Article retrieval and screening were done using a structured search string and strict inclusion/exclusion criteria. Median and interquartile ranges of percent resistance were calculated for each antibiotic-bacterium combination. A total of 249 articles were included in the final analysis from ten countries, where only five countries had more than 85% of the included articles. The most commonly reported pathogens were Escherichia coli, Salmonella spp. Staphylococcus aureus, and Listeria spp. An apparent rise in drug resistance among foodborne pathogens was recorded particularly against amoxicillin-clavulanic acid, ampicillin, nalidixic acid, streptomycin, and tetracycline that are commonly prescribed in most countries in the Middle East. Besides, there is a lack of standardization and quality control for microbiological identification and susceptibility testing methods in many of the Middle East countries.
... Marjoram is used in the food sector because of its antioxidant and antibacterial characteristics, which can be used as a preservative and flavoring agent. It is mostly used in dried form to flavor sausages, preserved meats, soups, herb mixes, sauces, beverages and some other foods (Omara and El-Moez, 2014) [40] . The marjoram E.O has recently been used to produce antimicrobial packing film through the nanoencapsulation technique that helps in protecting the food material from microbial spoilage during storage and transportation (Maurya et al., 2021) [35] . ...
... For example, due to climatic conditions and lack of cold storage facilities, it is virtually impossible to keep meat fresh for longer periods in the tropics. Therefore, processing of meat such drying, curing and smoking (by aromatic plants) are the only solution way to keep meatedible for long time (Shimaa et al., 2014 andZeedan et al., 2014).Converting camel meat into products such as burgers and sausages increasing the acceptability to domestics' consumers. Camels are good potential meat producers especially in arid regions where other meat-producing animals do not thrive. ...
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Global demand for foods of animal origin is growing and it is apparent that the livestock sector will need to expand. The detrimental effects of extreme weather adversely affect livestock. Climatic extremes and seasonal fluctuations in herbage quantity and quality will affect the well-being of livestock, and will lead to a decline in production and reproduction efficiency. The overpopulation and the high rate of people density in Nile valley and Delta is a major challenge. Therefore, the Egyptian Government has boosted the agricultural sector during the last seven years by constructing many projects in desert areas of Egypt. According to Egypt vision (2030), we have to exploit the available natural resources under the desert and harsh environmental conditions and to make the livestock production a real sustainable development tool for the Bedouins. Research Staff of Animal and Poultry production Division at the Desert Research Center are investigating their research programme to deal with the ecosystem of the desert which is suffering from a deficiency in fresh water, long draught season, a severe shortage in the conventional feedstuffs, animal diseases at the boarder governorates, etc..For example, In the field of animal breeding, a good program was started to implement the recent techniques of marker-assisted selection to improve local strains of sheep and goats productivity. In the same way, the utilization of agro-industrial by-products, desert shrubs and salt tolerant plants in animal and poultry feeding appeared to decrease the drastic gap in animal feeding under desert condition were taken into consideration. The recent molecular techniques such as next generation sequencing and classical cultivation techniques to identify camel rumen bacteria and fungi and their ability to produce lignocellulolytic enzymes were also investigated. Moreover, sustainable value chain approach for livestock by products (milk, meat, wool, fur) based on livelihood strategies for Bedouin communities for sustainable development strategies were discussed.
... After 18 to 24 h of incubation, the zone of inhibition was measured in mm using a measuring ruler, and the means of three measurements were determined. Any bacterial strains resistant to ≥3 antibiotics were defined as MDR pathogens [49]. ...
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... O. majorana's volatile oil was noticed to have substantial antibacterial, antifungal, antioxidant, and cytotoxic properties [19,20]. Studies revealed that the essential oil of O. majorana is effective against Staphylococcus epidermidis, Salmonella enteritidis, Salmonella typhimurium, Escherichia coli, Klebsiella pneumoniae, Pseudomonas aeruginosa, Citrobacter freundii, Proteus mirabilis, and Candida albicans [18,20,21]. Marjoram essential oil was found to inhibit colon cancer by inducing protective autophagy and apoptotic cell death in vitro [22]. ...
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Citation: Kaskatepe, B.; Aslan Erdem, S.; Ozturk, S.; Safi Oz, Z.; Subasi, E.; Koyuncu, M.; Vlainić, J.; Kosalec, I. Antifungal and Anti-Virulent Activity of Origanum majorana L. Essential Oil on Candida albicans and In Vivo Toxicity in the Galleria mellonella Larval Model.
... The extract showed very weak or no antibacterial activity against selected bacteria. Other publications showed O. majorana methanolic and oil extracts have antibacterial activities (Leeja and Thoppil, 2007;Omara, Abd El-Moez and Mohamed, 2014;Pepa et al., 2019). These differences between our results and others results may be due solvent used in preparation. ...
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... Antibacterial activity Several works showed the antibacterial efficacy of different essential oils and extracts from different plant parts. An investigation of previous researches shows that many studies listed antibacterial potential of O. majorana against Gram-positive and Gram-negative bacteria (Charai et al., 1996;Leeja and Thoppil, 2007;Busatta et al., 2008;Choi and Rhim, 2008;de Oliveira et al., 2009;Ramos et al., 2011;Omara et al., 2014;Adam and Ahmed, 2014;de Lima Marques et al., 2015;Lakhrissi et al., 2015;Ouedrhiri et al., 2016;Partovi et al., 2018;Amor et al., 2019;Al-Fatimi, 2018;Chaves et al., 2019). ...
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... It was also recommended that essential oil and other extracts of marjoram could be used as a potent bio-protective agent for preservation of refrigerated meat. Thus, marjoram essential oil can play an important role as antimicrobial agent in refrigerated minced meat and potentially it might be used as a natural preservative ingredient for longer periods without the need to use hazardous preservatives in food industry (Omara et al., 2014). Extracts of plants specially spices have been traditionally used as an ingredient of food items but essential oil of spices has also been proved to work as preservative due to their antimicrobial activity against various food borne pathogens (Marquesa et al., 2015). ...
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