


































Food Science and Nutrition Studies 

ISSN 2573-1661 (Print) ISSN 2573-167X (Online) 

Vol. 1, No. 1, 2017 

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31 
 

Evaluation the Antimicrobial Activity of Artemisia and 

Portulaca Plant Extracts in Beef Burger 

Marwa Al-Moghazy1, M. S. Ammar2, Mohamed M. Sief3 & Sherif R. Mohamed3* 

1 Dairy Science Department, Food Industries and Nutrition Division, National Research Centre, Dokki, 

Giza, Egypt 

2 Food Science and Technology Department, Faculty of Agriculture, AL-Azhar University, Cairo, Egypt 

3 Food Toxicology and Contaminants Department, Food Industries and Nutrition Division, National 

Research Centre, Dokki, Giza, Egypt 

* Sherif R. Mohamed, E-mail: sheriframzy4@gmail.com 

 

Received: April 9, 2017         Accepted: April 23, 2017        Online Published: May 15, 2017 

doi:10.22158/fsns.v1n1p31        URL: http://dx.doi.org/10.22158/fsns.v1n1p31 

 

Abstract 

Medicinal plants contain substances can alternate the traditional chemical preservatives which used 

for preserving meat products that have negative effects on consumer health. Several biological 

activities have been reported for Artemisia and Portulaca as antimicrobial agents, so the current study 

focused on using Artemisia and Portulaca extracts as antimicrobial agents in beef burger. 

Phytochemical of Artemisia and Portulaca extracts were analyzed, and both extracts contain alkaloids, 

flavonoids, phenols, trepenoids and saponin. The results show that Artemisia extract was inhibited all 

tested microorganisms (Staphylococcus aureus, Pseudomonas aeruginosa, Salmonella Typhimurium, 

Listeria monocytogenes and E.coli O157:H7) while, Portulaca extract affect Staphylococcus aureus 

only. The Minimum Cidal Concentration (MCC) and Minimum Inhibitory Concentration (MIC) were 

carried out for testing microorganisms, since Artemisia extract was very effective against 

Staphylococcus aureus followed by E.coli, Pseudomonas aeruginosa, Salmonella Typhimurium and L. 

monocytogenes. Artemisia and Portulaca extracts were separately applied in beef burger as 

antimicrobials at levels 1% and 1.5%. The sensory evaluation of treated beef burger showed no 

significant differences between control sample and treatments containing Portulaca extract while, the 

addition of Artmesia extract had a detrimental effect on taste of beef burger since it causes formation of 

bitter taste. 

Keywords 

antimicrobial, Artemisia, Portulaca, plant extracts, beef burger 

 

 



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1. Introduction 

Nowadays, new preservation techniques are being developed to extend the storage time with 

maintaining both the natural appearance and safety of fresh meat (Patsias et al., 2008; Zhou et al., 

2010). Synthetic preservatives such as nitrite has been widely used for preserving meat products such 

as sausages and luncheon meats. Nitrite is efficient for inhibition of Clostridium botulinum (Gibson et 

al., 1984). Nitrite may react with secondary amines naturally present in the meat to form 

N-nitrosamines, which are carcinogenic (IARC, 1998). There is an association between consumption of 

processed meat and increase risk of different cancers (Santarelli et al., 2008; Larsson et al., 2006; 

Larsson & Wolk, 2012), which cause death (Rohrmann et al., 2013). Unlike synthetic compounds, 

natural extracts obtained from plants are rich in phenolic compounds which can enhance the overall 

quality of food by decreasing lipid oxidation and microbial growth (Zhang et al., 2016). 

Artemisia vulgaris is used in asthma emmenagogue, anthelmintic, and stomachic (Ambasta, 1994). The 

essential oil of leaves exhibited significant antimicrobial activity (Laxmi & Rao, 1991). The leaves 

have an antibacterial activity on Staphylococcus aureus, Bacillus typhi, Bacillus dysenteriae, 

Streptococci, Escherichia coli, Bacillus subtilis and Pseudomonas.  

Pharmacological studies on Portulaca oleracea showed its activities as antibacterial (Chan et al., 2015), 

hepatoprotective (Al-Sheddi et al., 2015), anti-inflammatory, analgesia (Zhou et al., 2015), antioxidant 

(Liu et al., 2015). So the goal of this work is the evaluation of antimicrobial effect for both Artemisia 

and Portulaca extracts against microorganisms in vitro and as a preservative agent in beef burger. 

 

2. Materials and Methods 

2.1 Materials 

Herbs: Artemisia vulgaris and Portulaca oleracea were obtained from Egyptian herbal market, Dokki, 

Giza.  

Microbial strains: Three Gram negative pathogen bacteria; Salmonella Typhimurium (ATCC 14028), E. 

coli O157:H7 and Pseudomonas aeruginosa and 2 Gram positive pathogens; Staphylococcus aureus 

(25923), and Listeria monocytogenes (ATCC 7644), Microbial strains are generously given by 

Microbiology Department, Faculty of Agriculture, Cairo University. Different microbial strains were 

preserved at -20oC.  

Ingredients of beef burger: 

a. Beef meat: Frozen beef, lean meat was obtained from the local butcher shop in the day before the 

experiment. The meat was cold stored at 5±1ºC overnight. 

b. Soybean flour: Soybean flour was obtained from food Technology Research Institute, Agriculture 

Research Center, Giza, Egypt. 

c. Other ingredients: Spices, Fresh eggs, onion and salt were obtained from the local market. While, 

sodium tripolyphosphate, and sodium ascorbate were obtained from the Adwic Laboratory Chemicals 

Co., Cairo, Egypt. 



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2.2 Methods 

2.2.1 Technological Methods 

Preparation of Artemisia vulgaris and Portulaca oleracea extract: One hundred grams of Artemisia 

vulgaris or Portulaca oleracea leaves were added to excessive distilled water: ethanol (2:8 v/v) and 

incubated at room temperature for 24 h, then the slurry was filtered through filter paper. The water 

extract was concentrated using a rotary evaporator under reduced pressure and the residues were 

dissolved in 50 ml of distilled water.  

Beef burger formulation: Beef burger patties were processed by the method described by (Oroszvári et 

al., 2005; Ou & Mittal, 2006) according to the formula showed in Table 1: 

 

Table 1. Beef Burger Formulation 

Main ingredients (%) 

Treatments 

Control 
Artemisia extract Portulaca extract 

1% 1.5% 1% 1.5% 

Beef meat 62 62 62 62 62 

Soy flour 12 12 12 12 12 

Iced water 10 10 10 10 10 

Fresh eggs 7 7 7 7 7 

Fresh onion  7 7 7 7 7 

Salt 1.5 1.5 1.5 1.5 1.5 

Spices  0.5 0.5 0.5 0.5 0.5 

Total 100 100 100 100 100 

Additives (%)      

Sodium tripolyphosphate 0.3 0.3 0.3 0.3 0.3 

Sodium ascorbate 0.03  0.03  0.03  0.03  0.03  

Artemisia extract  1 1.5 1 1.5 

Portulaca extract  1 1.5 1 1.5 

 

2.2.2 Analytical Methods 

DPPH radical scavenging method: The antioxidant activity of the plant extracts was evaluated using the 

stable 2, 2-diphenyl-1-picrylhydrazyl radical (DPPH) according to a modified method of Bandoniene et 

al. (2002). 

Qualitative Phytochemical Analysis: phytochemical of plant extracts was carried out by standard 

methods described by (Brain & Turner, 1975; Evans, 1996) as follows: 

Detection of Alkaloids: Extracts were dissolved separately in dilute hydrochloric acid and filtered. The 

filtrates were used to detect the alkaloids by using Mayer’s test, since filtrates were treated with 

Mayer’s reagent. Formation of a yellow, cream precipitate indicates the presence of alkaloids. 

Detection of Saponins: About 0.5 mg of the extract was mixed by agitation with five ml of distilled 

water. Formation of frothing (appearance of creamy miss of small bubbles) shows that the presence of 



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saponins. 

Detection of Tannins: A small quantity of extract was mixed with water and heated using water bath. 

Then the mixture was filtered and ferric chloride was added to the filtrate. The formation of dark green 

colour indicates the presence of tannins. 

Detection of Flavonoids: Detection of flavonoids was carried out as follows:  

-Lead acetate test: Extracts were treated with a few drops of lead acetate solution. The formation of 

yellow color indicates the presence of flavonoids. 

-H2SO4 test: Extracts were treated with a few drops of H2SO4. Formation of orange color indicates the 

presence of flavonoids. Precipitate indicates that the presence of flavonoids. 

Detection of Phenols: Detection of phenols was carried out as follows:  

-Ferric chloride test: 10 mg extracts were treated with a few drops of ferric chloride solution. 

Formation of bluish black color indicates the presence of phenol. 

-Lead acetate test: 10 mg extract was treated with a few drops of lead acetate solution. Formation of a 

yellow color precipitate indicates the presence of phenol. 

2.2.3 Quantitative Phytochemical Analysis 

Estimation of Alkaloids was carried out by using the method of (Harborne, 1973) as follows: One gram 

of extract was weighed into a 250 ml beaker and 200 ml of 10% acetic acid in ethanol was added and 

the beaker was covered and allowed to stand for 4 h, then the mixture is filtered and concentrated on a 

water bath to one quarter of the original volume. Concentrated NH4OH was added by drop wise to the 

extract until the precipitation was complete. The whole solution was allowed to settle and the 

precipitate was collected and washed with dilute NH4OH, then filtered. The residue is the alkaloid, 

which was dried and weighed. 

Estimation of Flavonoids was carried out as follows: One gram of plant sample was repeatedly 

extracted with 100ml of 80% aqueous methanol at room temperature. The mixture was filtered through 

a Whatman No.1 filter paper into a pre-weighed 250 ml beaker. The filtrate was transferred into a water 

bath and allowed to evaporate to dryness and weighed (Krishnaiah et al., 2009). 

Estimation of Total Phenols was carried out as follows: The fat free sample was boiled with 50 ml of 

ether for extraction of phenolic compounds for 15 min. Five ml of the extract was pipetted into a 50 ml 

flask, then 10 ml of distilled water was added. Two ml of NH4OH solution and 5 ml of concentrated 

amyl alcohol were also added. The samples were made up to mark and left to react for 30 min for color 

development. This was read spectrophotometry at 505 nm.  

Screening of antimicrobial activity: Screening of antimicrobial activity was performed using the agar 

diffusion method. The Nutrient agar plate was over layered with approximately 2 mL soft agar 

inoculated with 105-106 cfu/mL of overnight activated microbial cultures, then wells of 8 mm diameter 

were holed by cork borer, 60 µL of each tested compounds were injected in every well. Negative 

control was performed using sterile distilled water. Plates were incubated for 24 h at 37oC. Diameters 

of inhibition clear zones were measured using graded ruler.  



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2.2.4 Microbiological Methods  

Determination of Minimum Inhibitory Concentrations (MIC) and Minimum Cidal Concentrations 

(MCC): Determination of Minimum Cidal Concentrations (MCC) of extracts were performed using 

microplate methods, 100 µL of sterile nutrient broth were loaded in each well of 96 wells plate, then 

defferent volumes of extract were added to achieve final concentrations ranged from1 to 15% (v/v), 

then the inoculums of different pathogens were added to have 106 CFU/mL final concentration. After 

incubation for 24 h at 37oC, bacterial count of each sample was determined using the drop plate method 

(Naghili et al., 2013). Drops of 10 µL from each well were pipetted onto surface of solidified nutrient 

agar, and then the plates were incubated for 24 h at 37oC. Minimum inhibitory concentration defined as 

the concentration which shows no increase or decrease of the initial counting after 24 h of incubation, 

while Minimum Cidal Concentration (MCC) defined as the less concentration showed no bacterial 

viability. 

Microbiological assessment of frozen beef burger: Microbiological assay of the different beef burger 

samples was carried out at zero time and after 3 months of frozen storage. Total count of bacteria was 

determined to evaluate the antimicrobial activity of plant extract in a real food system such as beef 

burger and the ability of this extract to prolong the storage period of beef burger. Ten g of each sample 

was added to 90 ml of sterile pepton water and mixed well for 1 min to homogenize. Decimal dilutions 

in sterilized pepton water were prepared and 1 ml was poured in Plate count agar (PCA, CM0325, 

Oxoid) to enumerate total bacterial count after incubation for 24 h at 37oC. 

2.2.5 Statistical Analysis 

One-way analysis of variance (ANOVA) was performed to test for differences between the groups 

mean. Significant differences between the means were determined by Duncan’s multiple range test and 

p<0.05 were regarded as significant (Sokal & Rohlf, 1995). 

 

3. Results 

Table 2 shows the qualitative phytochemical of Artemisia and Portulaca Extracts. From the obtained 

results it cleared that both extracts contain alkaloids, flavonoids, phenols, trepenoids, saponin while the 

tannins was positive in Artemisia and negative in Portulaca extract.  

 

Table 2. Qualitative Phytochemical Analysis of Artemisia and Portulaca Extracts 

Phytochemicals Artemisia extract Portulaca extract 

Alkaloids 

Mayer s test  

 

+ 

 

+ 

Flavonoids  

Lead acetate test  

H2SO4 test  

 

+ 

+ 

 

+ 

+ 

Phenols  

Ferric chloride test 

 

+ 

 

+ 



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Lead acetate test + + 

Terpenoids  + + 

Saponin  + + 

Tannin + - 

Note. (+) Present; (-) Not detected. 

Table 3 shows the quantitative phytochemical of Artemisia and Portulaca Extracts. From the results it 

cleared that both extracts contained Alkaloids, Flavonoids, phenol and antioxidant activity at levels 

4.25-5.34, 14.34-9.46, 9.47-3.85 W/w, 74%-68% respectively. 

 

Table 3. Quantitative Phytochemical Analysis of Artemisia and Portulaca Extracts 

Phytochemicals Artemisia extract (W/w) Portulaca extract (W/w) 

Alkaloids  4.25 5.34 

Flavonoids 14.34 9.46 

Phenol 9.47 3.85 

Antioxidant Activity 74% 68% 

 

Table 4 shows the Artemisia and Portulaca water extract against pathogenic bacteria. The obtained 

results showed that Artemisia extract has a potent antimicrobial effect against all tested microorganisms, 

Staph aureus, Pseudomonas aeruginosa, Salmonella Typhimurium, Listeria monocytogenes and E.coli 

O157:H7. The maximum effect of the Artemisia extract as an antibacterial was against Pseudomonas 

aeruginosa and gave 28 mm Inhibition zone diameter followed by Listeria monocytogenes, Staph 

aureus, Salmonella typhimurium and E.coli O157:H7 since the extract could inhibit the microbial 

growth and the inhibition zones were 26.25, 26, 24 and 15.4 mm respectively. The Portulaca extract 

was also tested as an antimicrobial against the same microorganisms, but it had a potent effect only 

against Staph aureus while, did not have any effect against Pseudomonas aeruginosa, Salmonella 

Typhimurium, Listeria monocytogenes and E.coli O157:H7. 

 

Table 4. Screening of Antimicrobial Activity (Inhibition Zone Diameter in mm) of Artemisia and 

Portulaca against Tested Pathogenic Bacteria 

Microorganism Artemisia extract Portulaca extract 

Staph aureus 26 20 

Pseudomonas aeruginosa 28 Nil 

Salmonella typhimurium 24 Nil 

Listeria monocytogenes 26.25 Nil 

E.coli O157:H7 15.5 Nil 

 

Table 5 shows the Minimum Inhibitory Concentration (MIC) and Minimum Cidal Concentrations 



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(MCC) of Artemisia extract against pathogenic bacteria (Portulaca extract was excluded because that it 

had not antimicrobial activity except against Staph aureus only). The Minimum Cidal Concentration 

(MCC) is the lowest concentration of an antibacterial agent required to kill a particular bacterium. It 

can be determined from broth dilution Minimum Inhibitory Concentration (MIC) tests by subculturing 

to agar plates that do not contain the test agent. The Minimum inhibitory concentration MIC and 

Minimum Cidal Concentration (MCC) were carried out for testing pathogenic bacteria are E. coli, 

Pseudomonas aeruginosa, Staph aureus, Salmonella Typhimurium, L.monocytogenes. The MIC was 

regarded as the lowest concentration of the extracts that prevent the growth of any tested bacterial 

colony on the medium. From the obtained results in Table 4 the Artemisia extract was very effective on 

Staph aureus and the MIC was appeared at 5 µL/100 µL, while MIC for both E.coli and Pseudomonas 

aeruginosa were medium and detected at 7 µL/100 µL, moreover Salmonella Typhimurium and 

L.monocytogenes possess the lowest MIC which recorded at 9 µL/100 µL. Also the minimum cidal 

concentration MCC was carried out and found that the results related and agreed with the results of MIC 

and the MCC at 6 µL/100 µL was for Staph aureus followed by E.coli, Pseudomonas aeruginosa and 

Salmonella Typhimurium, L.monocytogenes at 8, 10 µL/100 µL respectively. 

 

Table 5. Minimum Inhibitory Concentration (MIC) and Minimum Cidal Concentrations (MCC) 

of Artemisia Extract against Pathogenic Bacteria 

Microorganism MIC (µL/100 µL) MCC (µL/100 µL ) 

E.coli  7 8 

Staph aureus 7 8 

Pseudomonas aeruginosa 5 6 

Salmonella typhimurium 9 10 

Listeria monocytogenes 9 10 

 

 

Staph aureus 

 

 

pseudomonas aeruginosa 



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Salmonella typhimurium 

 

Listeria monocytogenes 

 

E.coli O157:H7 

 

Figure 1. The Minimum Inhibitory Concentration (MIC) and Minimum Cidal Concentrations 

(MCC) of Artemisia Extract against Pathogenic Bacteria 

 

Data in Table 6 show changes in the total bacterial count of beef burger during freezing, storage which 

was determined at zero time and after three months of frozen storage. The results show that Portulaca 

extract had a slight effect on beef burger microbial quality, but the rate of growth was slow which may 

be due to the polyphenols content of Artemisia extract which cause reducing the growth rate and 

maximum growth population and/or extending the lag-phase of the target microorganism (Zhou et al., 

2010). The Artemisia extract possesses a potent effect as an antimicrobial agent against all tested 

bacteria opposite the Portulaca extract that had only effect against Staph aureus, but unfortunately based 

on the sensory evaluation of beef burger results the Artemisia extract has a detrimental effect on the taste 

of burger patties which impart bitter taste and were unpalatable. So, more researchers are required to 

remove the bitterness of Artemisia extract until we can be used it in beef burger preservation without its 

affecting the sensory properties. 

 

Table 6. Microbiological Changes in Total Bacterial Count (cfu/g) Analysis of Beef Burger 

Samples during Frozen Storage Period 

Storage time 

Treatments 

Control 
Artemisia extract Portulaca extract 

1% 1.5% 1% 1.5% 

Zero time 2.40 E+06 3.70 E+06 2.10 E+06 2.66 E+06 2.68 E+06 

3 months 3.07 E+06 3.85 E+06 2.86 E+06 3.00 E+06 3.40 E+06 



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Table 7 shows that there is no significant differences (P≤0.05) between control and treatments 

containing Portulaca extract in all sensory properties of beef burger, furthermore addition of Portulaca 

extract with 1.5% was enhanced the taste, tenderness, juiciness and overall acceptability of beef burger. 

On the other hand the addition of Artmesia extract had a detrimental effect on taste of beef burger since 

it impart it bitter taste. Also addition of Artmesia extract was slightly lower the sensory score of beef 

burger for tenderness and juiciness but did not affect color and appearance.  

 

Table 7. Effect of Addition Plant Extracts on Sensory Characteristics of Beef Burger 

Sensory 

characteristics 

Treatments 

Control 
Artemisia extract Portulaca extract 

1% 1.5% 1% 1.5% 

Color 8a 8a 8a 8a 8a 

Taste 8a 1b 1b 8a 9a 

Flavor 8a 1b 1b 8a 8 a 

Tenderness 8ab 7b 7b 8ab 9a 

Juiciness 8ab 7b 7b 8ab 9a 

Appearance 8a 8a 8a 8a 8a 

Overall acceptability 8a 1b 1b 8a 9a 

* Scores ranging from 0-3 = very poor, 4 = poor, 5 = fair, 6-7 = good and 8-10 = very good. 

** In rows means have the same superscript are not significantly different. 

 

4. Discussion 

Our obtained phytochemical analysis of Artemisia and Portulaca extracts in agreement with (Alireza et 

al., 2013) who showed that tannins, saponins, alkaloids, amino acids, phenolic compounds, quinines 

and terpenoids are present in Artemisia extract using mass gas-chromatograph. Also, Okafor (2014) 

studied the water extract of aerial parts of Portulaca and showed that it contain steroids, protein, and 

alkaloids.  

The Artemisia extract had a potent effect as an antimicrobial against all tested microorganisms while, 

Portulaca extract had a potent effect against Staph aureus only. In our respect study (Abdul & Waheeta, 

2010) showed that Artemisia nilagirica extracts had a broad spectrum of antibacterial activity against 

phytopathogens and clinical pathogens except S. aureus, E. faecalis and K. pneumoniae.  

Our results showed that plant extracts contain effective biological compounds such as alkaloids, 

flavonoids, phenols, tannins and terpenoids, which could be alternate the traditional chemicals to 

inhibit phytopathogenic bacteria and decrease the negative effects of synthetic drugs. 

The MIC of Artemisia extract that gave a positive effect against all tested microorganisms was 

analyzed and the results was in agreement agreed with (Abdul & Waheeta, 2010) who studied the 

effects of various Artemisia extracts against bacteria and reported that hexane extract was effective 



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against all phytopathogens with low MIC of 32 μg/ml, while the methanol extract showed higher 

inhibition activity against Escherichia coli, Yersinia enterocolitica, Salmonella typhi, Enterobacter 

aerogenes, Proteus vulgaris, Pseudomonas aeruginosa (32 μg/ml), Bacillus subtilis (64 μg/ml) and 

Shigella flaxneri (128 μg/ml).  

The MIC analyses of clinical pathogens showed an activity against Gram-positive and Gram-negative 

bacteria, which indicate that plant extracts contains several antimicrobials. 

The phytochemical screening of plant menthol extracts showed that it contain flavonoids, terpenoids, 

phenols, amino acids, alkaloids and tannins, which have antimicrobial properties (Fernandez et al., 

1996; Mendoza et al., 1997; Amaral et al., 1998; Cowan, 1999 ; Shaheen et al., 2003; Amarowicz et al., 

2008; Chowdhury et al., 2008).  

Artemisia and Portulaca extracts were incorporated into the beef burger formula as an antimicrobial 

agent and both extracts gave good results as antibacterial, but Artemisia extract was had superior 

antimicrobial activity than Portulaca extract. The sensory quality of the formulated beef burger was 

carried out, beef burgers incorporated with Portulaca extract were having good sensory quality, while 

the beef burgers containing Artemisia extract were having bad sensory quality (bitter taste), although it 

showed good microbiological quality, thus further researches are needed to remove the compounds 

which induce the bitter taste until we can use the Artemisia extract as an antimicrobial in meat 

products. 

 

5. Conclusion 

Finally, Beef burger can be formulated with incorporation of Portulaca extract as antimicrobial without 

any detrimental effect on its sensory properties, whereas more researches are needed to remove the 

compounds of Artemisia extract which cause the bitter taste to make it suitable for using in persevering 

meat products without detrimental effect on its sensory properties. 

 

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