Home Biochemical analysis, antioxidant, and antibacterial efficacy of the bee propolis extract (Hymenoptera: Apis mellifera) against Staphylococcus aureus-induced infection in BALB/c mice: In vitro and in vivo study
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Biochemical analysis, antioxidant, and antibacterial efficacy of the bee propolis extract (Hymenoptera: Apis mellifera) against Staphylococcus aureus-induced infection in BALB/c mice: In vitro and in vivo study

  • Sohail Mahmood , Sumbal Haleem EMAIL logo , Syed Ishtiaq Anjum , Asif Ullah and Amal Alotaibi EMAIL logo
Published/Copyright: May 30, 2023
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Open Chemistry
From the journal Open Chemistry Volume 21 Issue 1

Abstract

Background

Antibiotic resistance to Staphylococcal infections has prompted the pharmaceutical and scientific community to consider alternate treatments. Propolis is a natural substance produced by honey bees (Hymenoptera: Apis mellifera) from the exudates of different plants. The aim of the current study was to evaluate the antibacterial activity of ethanolic extracts of Pakistani bee propolis (PBP) against Staphylococcus aureus in both in vitro and in vivo modeling.

Methods

The propolis sample was collected from the Kohat district and dried in the dark until processing. The antibacterial activity of the propolis extract was examined using the agar well diffusion method. The S. aureus culture was incubated on Mueller–Hinton agar media. Five different concentrations of propolis, 100, 200, 350, 500, and 650 μg/ml, were used. Gentamicin disc was used as a positive control. For in vivo assay, BALB/c mice with an average weight of 30 g were purchased. Bacteria were inoculated into mice by the tape stripping technique. After abscess formation, mice were treated with propolis extract.

Results

The mean zone of inhibition and standard deviation for each concentration were 17 ± 0.816 at 650 μg/ml, 14.6 ± 0.471 at 500 μg/ml, 12 ± 1.41 at 300 μg/ml, 9.6 ± 0.942 at 200 μg/ml, and 2.3 ± 0.471 at 100 μg/ml of the propolis extract against S. aureus. It was observed that by increasing the concentration of the propolis extract, the antibacterial and antioxidant activities also increased. The extracts showed less antibacterial potential compared to gentamicin. The abscess size was also decreased in mice groups treated with the propolis extract topically and orally in comparison with the untreated mice group.

Conclusions

To the author’s best knowledge, this study is the first attempt to demonstrate that an ethanolic PBP extract has antibacterial potential against S. aureus-induced infections.

Keywords: propolis; S. aureus ; in vitro ; in vivo ; BALB/c

1 Introduction

The Greek words, staphyle meaning “bunch of grapes” and coccus meaning “spherical bacteria,” were combined to form the word staphylococci. The Latin word aureus meaning “gold” was applied to these bacteria because of their yellow to a yellowish-white colonial appearance on an enriched medium [1]. A pathogenic member of the micrococcus family and the genus Staphylococcus, Staphylococcus aureus is a Gram-positive, non-motile, facultative anaerobe, and about 1 µm in size [2]. Due to the formation of carotenoids and hemolysin, it produces golden colonies on a rich medium and hemolysis on blood agar containing 5% sheep and horse blood. However, because cell division occurs at various planes, it appears as bluish-grape-like colonies when stained with Gram stain [2]. Humans’ gastrointestinal tracts, nares, and skin are all colonized by S. aureus [3]. About 20% of the human population has stable colonization, whereas the other 30% has varying levels of colonization [3,4]. S. aureus is a very resilient organism that can endure dry surfaces for an extended amount of time. It is also resistant to desiccation and can withstand high-level concentrations of salt, which serves as a basis for its selection of growth media over other bacteria [5]. It is the causative agent of a wide range of infections in humans and animals with a significant impact on public health [6]. Significant public health implications were brought about by host specialization, the capacity to acquire and lose virulence and resistance genes, and the possibility of zoonotic spread [6,7,8]. Invasive diseases caused by S. aureus include bacteremia, sepsis, pneumonia, osteomyelitis, endocarditis, and skin and soft tissue infections [3]. The development of purulent abscess lesions surrounding a nidus of the pathogen, predominantly as a result of neutrophil infiltration, is the pathological hallmark of S. aureus infection [9]. It causes dermatitis in dogs, septicemia and arthritis in chickens, botryomycosis in horses, mastitis in cows, and botryomycosis in horses [6,10]. Antimicrobial resistance is becoming more common all around the world. Pathogens that cause nosocomial infections have shown an increase in resistance and so have organisms that cause community-acquired diseases. In addition to the well-known pathogens, opportunistic microorganisms have developed resistance. Increased illness, mortality, and medical costs due to antimicrobial resistance highlight the need for novel antimicrobial agents [11].

Propolis is a mixture of beeswax and resins collected by the honeybees (Hymenoptera: Apis mellifera) from plant buds, leaves, and exudates [12]. Bees use propolis to protect their hives against assault by other insects. The word “propolis” is derived from the Greek letters “pro” and “polis,” which together indicate “town” or “city” [13]. In addition to using it as a building material, bees use propolis to keep bacterial and fungal concentrations in the hive at low levels [14]. Propolis serves as a biocide in the hive, active against invasive bacteria, fungi, and even invading larvae [15]. The treatment of infections with propolis has a long history in traditional oriental medicine [15]. As an antiseptic and anti-inflammatory agent for treating wounds and burns, propolis has long been used in traditional Chinese medicine to treat infections as well as in ethnopharmacology in Europe [16]. Propolis has been well recognized as a beneficial ingredient in medicine due to its numerous pharmacological qualities, such as antifungal [17], antiviral [18], antioxidant [19], and antibacterial [20]. Propolis samples have been shown to contain more than 150 different substances, including polyphenols, phenolic aldehydes, sesquiterpene quinines, amino acids, steroids, and inorganic substances. Propolis is an antioxidant-rich natural material that acts as a bodily defense against free radicals [15]. Propolis has different characteristics and a different chemical makeup depending on where it comes from [17], and these variances in makeup are mostly caused by variations in the bearing plants [21].

As a result, the number of resistant strains is quickly increasing worldwide [22]. In particular, given the increase in microorganisms that have evolved resistance to modern medicines, novel therapies for infectious disorders are urgently needed [23]. In Pakistan’s industrial apiaries, propolis is made alongside honey. Although it is scraped off from beehive walls and frames, it is discarded since it is deemed useless. Due to a dearth of studies into its many benefits, propolis is regarded as useless in Pakistan. To the author’s best knowledge, there have been no studies conducted on the antibacterial potential (particularly, S. aureus) of Pakistani bee propolis (PBP) obtained from the current study area. Therefore, the objective of the current study was to assess the in vitro and in vivo antibacterial activity of PBP obtained from beehives in the Kohat region, against S. aureus-induced infections.

2 Materials and methods

2.1 Sample collectiont

A sample of PBP was taken from beehives in the apiary of Kohat University of Science and Technology. The sample was manually collected, cut into small pieces, and kept in the dark until processing (Figure 1).

Figure 1 (a) Beehives at the research site at Kohat University of Science and Technology, Kohat. (b) PBP in small pieces kept in the dark until processing.
Figure 1

(a) Beehives at the research site at Kohat University of Science and Technology, Kohat. (b) PBP in small pieces kept in the dark until processing.

2.2 Extraction of propolis

The dried PBP sample was crumpled in an electric grinder. The ground PBP extract was diluted in an ethanol solvent in a ratio of 1:10 (1 g PBP/10 ml ethanol solvent) and kept in airtight bottles at 25°C for 14 days. The bottles were shaken briefly every 5 h. After 14 days, the solution was filtered via paper using a filter. By employing a rotary vacuum evaporator to evaporate the solvent, the filtrated extract was concentrated to obtain a crude extract. For experiments, the final crude extract was maintained at 4°C (Figure 2).

Figure 2 (a) Filtration of the ethanolic diluted solution of PBP. (b) The evaporation of solvent from the diluted PBP using rotary vacuum evaporation. (c) Crude extract of PBP.
Figure 2

(a) Filtration of the ethanolic diluted solution of PBP. (b) The evaporation of solvent from the diluted PBP using rotary vacuum evaporation. (c) Crude extract of PBP.

2.3 Study design

The in vitro activity of PBP was determined in the Lab of Molecular Parasitology and Virology, Department of Zoology, KUST. A culture of S. aureus was provided by the Department of Microbiology, and the BALB/c mice used in the in vivo study were provided by the Veterinary Research Institute, Peshawar.

2.3.1 Bacterial culture

The nutrient broth was primarily used to create bacterial suspensions. About 0.39 g of the nutrient broth powder was dissolved in 30 ml of distilled water. Then, 10 ml of the nutrient broth solution was added to three test tubes that were each 10 ml in size. Following that, 30 μl of the bacterial suspension from the stock culture was poured into two test tubes, and a third test tube was maintained as a control to be compared with the other test tubes to determine whether or not bacterial growth had taken place (Figure 3).

Figure 3 Bacterial culture of S. aureus used in the study.
Figure 3

Bacterial culture of S. aureus used in the study.

2.3.2 Stock solution and dilution of propolis extracts

The Stock solution was prepared using 10 mg of the crude extract of PBP dissolved in 10 ml of ethanol. From this stock solution, concentrations of 100, 200, 350, 500, and 650 μg/ml were used for in vitro study.

2.3.3 In vitro activity

The agar well diffusion method was followed to determine the antibacterial activity of PBP against S. aureus. About 20 ml of the Mueller–Hinton agar medium was used to make test plates with a diameter of 10 cm. The medium was autoclaved along with Petri plates, loop, cork borer, tips and cotton swab, etc. at 121°C for 20 min to sterilize. The sterilized medium was poured into Petri dishes on cooling and shifted to the laminar flow hood under sterilized conditions. After the medium had solidified, using sterile glass-made pipettes connected to a vacuum pump, 8 mm diameter wells were punched in the agar plates. Sterile swabs were dipped into the bacterial suspension inoculated onto plate surfaces by rubbing it at 90°; again, the cotton swab was dipped in the bacterial culture and rubbed at 180° to make the bacterial culture lawn. Each well was filled with 30 μl of the extract. These plates were incubated for 24 h at 37°C. After the incubation period, the zones of bacterial growth inhibition around the holes were measured and recorded. Each of the antibacterial assays was conducted in triplicate and the mean of results were noted. A gentamicin antibacterial disc was used as a control during this study.

2.3.4 Mice model for in vivo activity

Thirty healthy BALB/c mice with an average weight of 30 g were purchased. All attempts were made to minimize the suffering of the mice during the trial. All mice were kept in vented plastic cages at a managed animal care facility, with a humidity of 50–60% and 12 h light/12 h dark cycles, with ample food and distilled water.

2.3.5 Preparation of propolis ointment for topical application

The ethanol extract of PBP was prepared as an ointment using petroleum jelly (melting point: 60–65°C) at a concentration of 50%. The ointment was kept in a sterile glass container, properly sealed, and preserved at 4°C for application.

2.3.6 Antibacterial agents

The commercial topical antibiotics (Effigenta: Cipro) were purchased from a local drugstore and it was used as a standard antibacterial drug in in vivo study.

2.3.7 Bacteria inoculation

Bacteria were inoculated into mice using the tape-stripping technique (Figure 4). Using a sterilized razor, mice’s backs were shaved; then, small strips of elastic bandage tape were applied and removed from a 2 × 2 cm2 dorsal area, until the skin glistened and reddened without bleeding. Then, 70% ethanol was swabbed on the mouse’s bare back. A sterilized blade was used to shave the backs of the mice. Small strips of the elastic bandage tape were put and removed from a 2 × 2 cm2 dorsal region 10–20 times until the skin glistened and reddened without bleeding (Tatiya et al., [24]).

Figure 4 Tape stripping technique used in the current study for bacterial inoculation in mice.
Figure 4

Tape stripping technique used in the current study for bacterial inoculation in mice.

2.3.8 Treatment of mice

Abscess appeared after 3 days of inoculation. The mice were divided into groups and subgroups and given treatment for up to 14 days after infection. Group-1 had 18 infected mice of which 6 mice were treated with 650 μg/ml/day of the PBP ethanolic extract (orally and topically), 6 were treated with 500 μg/ml/day of the PBP extract both topically and orally, and 6 mice were treated with 350 μg/ml/day. Group-2 containing 3 mice was infected but untreated, Group 3 containing 3 mice was treated with petroleum jelly, and Group-4 containing 3 mice was treated with standard antibiotic drugs. Group-5 containing 3 mice is the control group. Treatments were carried out two times daily for a further 14 days (Figure 5).

Figure 5 Abscess in mice after 3 days of inoculation of S. aureus.
Figure 5

Abscess in mice after 3 days of inoculation of S. aureus.

2.3.9 Measurement of the abscess size

During the treatment, the width and length of abscesses of the different mice groups were measured from day 1 to day 14 with the help of Vernier calipers (Figure 6). The abscess volume [V = 4/3π(L/2)2 × W/2] and area [A = π(L/2) × W/2] were calculated using the abscess length and width measurements (Bunce et al., [25]; Lukomski, et al., [26]).

Figure 6 Abscess measurement carried out in the current study.
Figure 6

Abscess measurement carried out in the current study.

2.3.10 Hematological analysis

Blood was taken from each mouse through the intracardiac channel using 1 ml sterile disposable syringes having 26 mm × 6 mm needles. Ethylenediaminetetraacetic acid (EDTA) tubes were then used to collect the blood. The absolute counts for white blood cells (WBCs), erythrocytes, lymphocytes, hematocrit (HCT), platelets, and hemoglobin (HGB) were collected using an Auto Hematology Analyzer by the conventional technique with certain changes (Hoff [27]).

2.4 Determination of vitamin C

A colorimetric approach was used to estimate the amount of vitamin C [28]. The extract was incubated in a water bath at a temperature of 60oC with the addition of 2.5 ml of oxalic acid (4%), 0.5 ml of sulfuric acid (5%), 2 ml of ammonium molybdate, and 3 ml of distilled water. After cooling, the absorbance of the resultant solution was measured at 515 nm using a spectrometer. A fresh ascorbic acid solution made was used to plot the calibration curve.

2.5 Determination of total phenols

Total phenols were determined by the procedure based on the Folin–Ciocalteu method [29]. In a test tube, 500 ml of sodium carbonate, 250 ml of the Folin–Ciocalteu reagent, and 1 ml of the sample extract were combined. After being homogenized and allowed to react for 30 min at room temperature, the absorbance was measured at 710 nm using a spectrophotometer.

2.6 Determination of antioxidant activity

The antioxidant activity of the propolis extract was determined using the free radical-scavenging compound 1-1-diphenyl-2-picrylhydrazyl (DPPH) [30]. About 3 ml of a 60 mM ethanolic solution of DPPH was mixed with 1 ml of propolis extracts at varied concentrations. After 30 min, absorbance readings were taken at 517 nm at room temperature. The negative control was the absorbance of a blank sample made up of an equal volume of methanol and DPPH solution. The IC50 values were calculated using the % inhibition against the gallic acid (phenol) and ascorbic acid (vitamin C) contents.

2.7 Statistical analysis

Statistical assessment of obtained data was performed in vitro and in vivo using Minitab to examine the results of antibacterial activity of PBP extracts and to determine the variance in several parameters, such as mean and standard deviation.

3 Results

3.1 In vitro assay of the ethanolic extract of PBP against S. aureus

The in vitro activity of the ethanolic extract of PBP is shown in Table 1 and Figure 7. Five different concentrations of the ethanolic extract of PBP (100, 200, 350, 500, and 650 μg/ml) were used in determining the in vitro activity in triplicates. At 650 μg/ml, the extract had the greatest antibacterial activity, followed by 500 and 350 μg/ml, with 100 μg/ml having the least inhibition of the bacterial activity. The inhibition of S. aureus increased with the increase in the concentration of the PBP extract.

Table 1

In vitro assay of the PBP extract against S. aureus

Concentration (μg/ml) Inhibition 1 Inhibition 2 Inhibition 3 Mean value (mm) ± SD
100 3 2 2 2.33 ± 0.471
200 11 9 9 9.6 ± 0.942
350 14 11 11 12 ± 1.41
500 15 15 14 14.6 ± 0.471
65 18 17 16 17 ± 0.816
Control 21 21 19 20 ± 0.942
Figure 7 In vitro activity of the PBP extract against S. aureus.
Figure 7

In vitro activity of the PBP extract against S. aureus.

3.2 In vivo assay of the PBP extract against S. aureus in mice

3.2.1 Mean abscess size in the mice group treated with the ethanolic extract of PBP (350 μg/ml/day) topically and orally

The daywise distribution of the mean abscess size in the mice group treated with 350 μg/ml/day of the PBP extract topically and orally is shown in Table 2. The mean abscess size (topically and orally) was measured for up to 14 days. The wound-healing capacity of 350 μg/ml/kg/day PBP was much lesser than at the other two concentrations (500 and 650 μg/ml/day). When compared with the other two concentrations of PBP, the lowest wound-healing capacity was 350 μg/ml/day of the PBP extract. The topically treated mice group with a concentration of 350 μg/ml/day of PBP reduced the abscess area from 2.17 cm2 ± to 0.33 cm2 ± and reduced the abscess volume from 2.45  cm3 ± to 0.16 cm3. The mice group treated with a concentration of 350 μg/ml/day of the PBP extract orally reduced the abscess area from 2.04 cm2 ± 0.158 to 0.4 cm2 ± 0.035 and the volume was reduced from 2.22 cm3 ± to 0.22 cm3 ± in 14 days of treatment.

Table 2

Mean abscess size in the mice group treated with the ethanolic extract of PBP (350 μg/ml/day) topically and orally

Days Concentration (μg/ml) Topically treated mice group Orally treated mice group
Mean area (cm2) ± SD Mean volume (cm3) ± SD Mean area (cm2) ± SD Mean volume (cm3) ± SD
1 350 2.17 ± 0.166 2.45 ± 0.256 2.04 ± 0.158 2.22 ± 0.299
2 350 2.04 ± 0.117 2.14 ± 0.163 1.94 ± 0.134 2.04 ± 0.225
3 350 1.92 ± 0.157 2.04 ± 0.225 1.76 ± 0.199 1.83 ± 0.246
4 350 1.72 ± 0.113 1.71 ± 0.164 1.63 ± 0.164 1.67 ± 0.212
5 350 1.53 ± 0.160 1.36 ± 0.094 1.28 ± 0.260 1.12 ± 0.384
6 350 1.28 ± 0.942 1.12 ± 0.127 1.34 ± 0.185 1.09 ± 0.473
7 350 1.22 ± 0.077 1.01 ± 0.098 1.17 ± 0.184 1.07 ± 0.218
8 350 1.06 ± 0.116 0.85 ± 0.128 1.04 ± 0.092 0.86 ± 0.148
9 350 0.88 ± 0.107 0.65 ± 0.106 0.86 ± 0.083 0.69 ± 0.081
10 350 0.80 ± 0.100 0.55 ± 0.089 0.75 ± 0.106 0.59 ± 0.038
11 350 062 ± 0.057 0.39 ± 0.049 0.74 ± 0.029 0.49 ± 0.102
12 350 0.53 ± 0.032 0.34 ± 0.062 0.54 ± 0.089 0.35 ± 0.083
13 350 0.43 ± 0.053 0.24 ± 0385 0.49 ± 0.085 0.29 ± 0.071
14 350 0.33 ± 0.030 0.16 ± 0.008 0.4 ± 0.035 0.22 ± 0.016

3.2.2 Mean abscess size in the mice group treated with the ethanolic extract of PBP (500 μg/ml/day) topically and orally

The daywise distribution of the mean abscess size for each group treated with 500 μg/ml/day of the PBP extract is given in Table 3. In the mice group treated with 500 μg/ml/day, there was a decrease in the abscess size but it was less than that at a concentration of 650 μg/ml/day. In these 14 days of treatment, the area decreased from 2.21 cm2 ± 0.061 to 0.2 cm2 ± 0.021, and volume reduced from 2.59 cm3 ± 0.065 to 0.06 cm3 ± 0.004 in the mice treated with 500 μg/day of the PBP extract topically.

The mice group treated orally with the same concentration of PBP reduced the abscess size. However, the wound-healing capacity of the mice treated topically at the same concentration was lower compared to that given orally. Overall, in the 14 days of treatment, the area decreased from 1.95 cm2 ± 0.103 to 0.32 cm2 ± 0.037 and the volume decreases from 2.08 cm3 ± 0.188 to 0.14 cm3 ± 0.026 (Table 3).

Table 3

Mean abscess size in the mice group treated with the ethanolic extract of PBP (500 μg/ml/day) topically and orally

Days Concentration (μg/ml) Topically treated mice group Orally treated mice group
Mean area (cm2) ± SD Mean volume (cm3) ± SD Mean area (cm2) ± SD Mean volume (cm3) ± SD
1 500 2.21 ± 0.061 2.59 ± 0.065 1.95 ± 0.103 2.08 ± 0.188
2 500 2.12 ± 0.192 2.17 ± 0.166 1.8 ± 0.113 1.83 ± 0.164
3 500 1.91 ± 0.042 2.03 ± 0.203 1.68 ± 0.146 1.65 ± 0.227
4 500 1.63 ± 0.004 1.59 ± 0.077 1.53 ± 0.089 1.43 ± 0.124
5 500 1.49 ± 0.565 1.42 ± 0.050 1.32 ± 0.081 1.18 ± 0.112
6 500 1.24 ± 0.047 1.11 ± 0.069 1.15 ± 0.089 0.95 ± 0.108
7 500 1.16 ± 0.133 0.86 ± 0.057 1 ± 0.042 0.77 ± 0.032
8 500 0.90 ± 0.047 0.68 ± 0.030 0.88 ± 0.010 0.65 ± 0.106
9 500 0.74 ± 0.040 0.51 ± 0.024 0.69 ± 0.061 0.46 ± 0.062
10 500 0.58 ± 0.063 0.35 ± 0.050 0.55 ± 0.053 0.35 ± 0.032
11 500 0.45 ± 0.059 0.24 ± 0.038 0.47 ± 0.061 0.25 ± 0.051
12 500 0.34  ± 0.049 0.16 ± 0.029 0.44 ± 0.041 0.23 ± 0.028
13 500 0.26 ± 0.021 0.11 ± 0.024 0.4 ± 0.050 0.19 ± 0.032
14 500 0.2 ± 0.021 0.06 ± 0.004 0.32 ± 0.037 0.14 ± 0.026

3.2.3 Mean abscess size in the mice group treated with the ethanolic extract of PBP (650 μg/ml/kg/day) topically and orally

The daywise distribution of the mean abscess size in the mice group treated with 650 μg/ml/day of the PBP extract topically and orally is shown in Table 4. The mean abscess size (topically, orally) was measured for up to 14 days. The mice group receiving 650 μg/ml/day of PBP topically showed a decrease in the mean abscess size from 12.04 cm2 ± 0.117 to 0.13 cm2 ± 0.018 in area and a decrease in the volume from 2.09 cm3 ± 0.276 to 0.04 cm3 ± 0.008 after 14 days of treatment.

Table 4

Mean abscess size in the mice group treated with the ethanolic extract of PBP (650 μg/ml/day) topically and orally

Days Concentration (μg/ml) Topically treated mice group Orally treated mice group
Mean area (cm2) ± SD Mean volume (cm3) ± SD Mean area (cm2) ± SD Mean volume (cm3) ± SD
1 650 2.04 ± 0.117 2.09 ± 0.276 2.31 ± 0.127 2.73 ± 0.056
2 650 1.94 ± 0.094 1.83 ± 0.174 2.04 ± 0.117 2.09 ± 0.183
3 650 1.76 ± 0.097 1.73 ± 0.183 1.84 ± 0.149 1.80 ± 0.237
4 650 1.53 ± 0.160 1.40 ± 0.225 1.60 ± 0.140 1.47 ± 0.213
5 650 1.26 ± 0.190 1.17 ± 0.268 1.45 ± 0.054 1.18 ± 0.184
6 650 1.06 ± 0.087 0.89 ± 0.183 1.19 ± 0.120 0.96 ± 0.192
7 650 0.91 ± 0.103 0.68 ± 0.151 1.00 ± 0.111 0.72 ± 0.130
8 650 0.66 ± 0.145 0.49 ± 0.098 0.77 ± 0.065 0.49 ± 0.086
9 650 0.56 ± 0.092 0.33 ± 0.078 0.65 ± 0.065 0.38 ± 0.067
10 650 0.47 ± 0.078 0.25 ± 0.044 0.51 ± 0.061 0.27 ± 0.054
11 650 0.34 ± 0.083 0.16 ± 0.049 0.39 ± 0.051 0.18 ± 0.043
12 650 0.30 ± 0.023 0.13 ± 0.014 0.30 ± 0.018 0.12 ± 0.016
13 650 0.20 ± 0.037 0.07 ± 0.016 0.21 ± 0.018 0.15 ± 0.106
14 650 0.13 ± 0.018 0.04 ± 0.008 0.16 ± 0.030 0.12 ± 0.048

The mice group treated with the same concentration of PBP extract orally showed a decrease in the mean abscess size from 2.09 cm3 ± 0.276 to 0.04 cm3 ± 0.008 area while it showed a decrease in the volume from 2.73 cm3 ± 0.056 to 0.12 cm3 ± 0.048. Overall, the highest antibacterial activity of the PBP extract was observed at a concentration of 650 μg/ml.

3.2.4 Mean abscess size in the untreated mice group and the mice group treated with petroleum jelly

The abscess size begins to grow in the mice group in the untreated and treated with petroleum jelly. Petroleum jelly showed no role in the healing of the abscess and the abscess size increases considerably day by day; similarly, the abscess size also increases in the untreated mice group. In these 14 days, the abscess area in the untreated mice group increased from 2.35 cm2 ± 0.245 to 4.07 cm2 ± 0.230 and the volume increased from 2.44 cm3 ± 0.064 to 6.47 cm3 ± 0.584 (Table 5).

Table 5

Mean abscess size in the untreated mice group and in petroleum jelly-treated mice group

Days Untreated mice group Mice group treated with petroleum jelly
Mean area (cm2) ± SD Mean volume (cm3) ± SD Mean area (cm2) ± SD Mean volume (cm3) ± SD
1 2.35 ± 0.245 2.44 ± 0.064 2.12 ± 0.009 2.39 ± 0.056
2 2.40 ± 0.202 2.49 ± 0.118 2.16 ± 0.066 2.43 ± 0.056
3 2.54 ± 0.114 3.03 ± 0.208 2.34 ± 0.618 2.74 ± 0.198
4 2.63 ± 0.174 3.26 ± 0.352 2.44 ± 0.071 2.90 ± 0.069
5 2.88 ± 0.141 3.68 ± 0.263 2.57 ± 0.059 3.18 ± 0.204
6 3.03 ± 0.256 4.01 ± 0.549 2.62 ± 0.061 3.24 ± 0.204
7 3.10 ± 0.091 4.21 ± 0.260 2.79 ± 0.078 3.27 ± 0.344
8 3.41 ± 0.232 4.87 ± 0.475 2.92 ± 0.066 3.80 ± 0.233
9 3.66 ± 0.235 5.413 ± 0.408 2.97 ± 0.009 3.86 ± 0.151
10 3.83 ± 0.758 4.78 ± 0.106 3.18 ± 0.073 4.14 ± 0.089
11 3.93 ± 0.231 5.91 ± 0.560 3.34 ± 0.082 4.41 ± 0.193
12 4.3 ± 0.938 5.2 ± 0.521 3.51 ± 0.211 4.94 ± 0.341
13 4.11 ± 0.292 6.47 ± 0.584 3.61 ± 0.004 5.17 ± 0.179
14 4.07 ± 0.230 6.47 ± 0.584 3.96 ± 0.009 5.92 ± 0.200

3.2.5 Mean abscess size in the mice group treated with the topical antibiotic

The mice group treated with the topical antibiotic showed considerable response to abscess healing. It was observed that as compared to the PBP extract, the wound-healing ratio of the topical antibiotic was quite positive. The mice group treated with the topical antibiotic was properly cured within 14 days. After a thorough observation of the wound till healing, it was finally concluded that the wound area was found maculated. In these 14 days, the abscess area decreases from 2.05 cm2 ± 0.094 to 0.06 cm2 ± 0.024 in the topical antibiotic-treated mice group. Similarly, the volume decreased from 2.29 cm3 ± 0.128 to 0.04 cm3 ± 0.042 (Table 6).

Table 6

Mean abscess size in the mice group treated with the topical antibiotic

Days Mean area (cm2) ± SD Mean volume (cm3) ± SD
1 2.05 ± 0.094 2.29 ± 0.128
2 1.80 ± 0.089 1.89 ± 0.1161
3 1.56 ± 0.106 1.52 ± 0.131
4 1.34 ± 0.101 1.22 ± 0.111
5 1.21 ± 0.159 0.97 ± 0.098
6 0.96 ± 0.087 0.75 ± 0.082
7 0.79 ± 0.075 0.57 ± 0.069
8 0.64 ± 0.073 0.41 ± 0.057
9 0.50 ± 0.061 0.29 ± 0.044
10 0.38 ± 0.054 0.2 ± 0.032
11 0.28 ± 0.049 0.12 ± 0.024
12 0.19 ± 0.038 0.07 ± 0.020
13 0.14 ± 0.004 0.04 ± 0.004
14 0.06 ± 0.024 0.04 ± 0.042

3.3 Hematological analysis

The hematological analysis of mice groups was performed after 14 days of bacterial infection in the PBP extract-treated mice groups and untreated mice group and was compared with the uninfected control group. The blood parameters include WBCs, granulocytes (GRA), red blood cells (RBCs), HGB, HCT, mean corpuscular volume (MCV), mean corpuscular hemoglobin (MCH), the mean corpuscular hemoglobin concentration (MCHC), platelet count (PLT), and the mean platelet volume (MPV), as shown in Tables 7 and 8.

Table 7

Hematological analysis of mice groups treated with PBP extract topically

Parameters Uninfected, control Infected, antibiotics treated (+) Infected, untreated (−ve) Infected, petroleum jelly treated (−ve) Group 1 topically treated with 650 μg/ml PBP extract Group 2 topically treated with 500  μg/ml PBP extract Normal range
WBCs (×109/L) 2.06 ± 0.205 5.23 ± 0.339 11.56 ± 0.826 10.93 ± 0.895 7.9 ± 0.163 8.5 ± 0.804 0.8–6.8
GRA (×109/L) 1.23 ± 0.249 1.6 ± 0.081 8.4 ± 0.430 9.03 ± 0.451 1.9 ± 0.163 3.26 ± 0.329 0.1–1.8
RBCs (×1012/L) 13.1 ± 0.492 12.66 ± 0.124 10.46 ± 0.917 9.73 ± 0.980 12.2 ± 0.216 11.4 ± 0.432 11.0–14.3
HGB (g/dl) 34 ± 1.208 35.13 ± 1.543 28.2 ± 0.648 26.9 ± 0.927 33.56 ± 1.796 31.53 ± 1.552 8.6–38.9
HCT (%) 36.16 ± 1.087 37.26 ± 1.407 32.53 ± 1.146 30.46 ± 0.865 34.33 ± 2.269 31.6 ± 1.423 34.6–44.0
MCV (fl (L)) 52.3 ± 1.247 53.66 ± 0.942 47 ± 1.632 43.66 ± 2.494 49.33 ± 1.247 46 ± 1.632 48.2–58.3
MCH pg (L) 17.2 ± 0.216 17.03 ± 0.249 14.7 ± 0.368 13.8 ± 0.535 16.46 ± 0.618 15.86 ± 0.449 15.8–19.0
MCHC (g/dl) 32.36 ± 0.740 31.06 ± 0.967 26.6 ± 0.571 24.43 ± 0.612 28.76 ± 1.699 26.5 ± 1.796 30.2–35.3
PLT (×109/L(H) 1,436 ± 24.94 1,461 ± 25.95 1,554 ± 31.67 1,596 ± 10.70 1,447 ± 26.24 1,463 ± 28.77 450–1,690
MPV (fl) 4.8 ± 0.244 5.13 ± 0.205 5.68 ± 0.220 5.1 ± 0.163 4.93 ± 0.286 4.56 ± 0.249 3.8–6.0
Table 8

Hematological analysis of mice groups treated with PBP extract orally

Parameters Uninfected, control Infected, antibiotics treated ( +) Infected, untreated (−ve) Infected, petroleum jelly treated (−ve) Group 1 orally treated with 650  μg/ml PBP extract Group 2 orally treated with 500  μg/ml PBP extract Normal range
WBCs (×109/L) 2. 06 ± 0.205 5.23 ± 0.339 11.56 ± 0.826 10.93 ± 0.895 8.8 ± 0.616 7.2 ± 0.535 0.8–6.8
GRA (×109/L) 1.23 ± 0.249 1.6 ± 0.081 8.4 ± 0.430 9.03 ± 0.451 2.36 ± 0.205 4.03 ± 0.498 0.1–1.8
RBCs (×1012/L) 13.1 ± 0.492 12.66 ± 0.124 10.46 ± 0.917 9.73 ± 0.980 10.46 ± 0.612 10.26 ± 0.478 11.0–14.3
HGB (g/dl) 34 ± 1.208 35.13 ± 1.543 28.2 ± 0.648 26.9 ± 0.927 31.26 ± 1.146 28.8 ± 1.143 8.6–38.9
HCT (%) 36.16 ± 1.087 37.26 ± 1.407 32.53 ± 1.146 30.46 ± 0.865 32.53 ± 2.366 28.76 ± 1.844 34.6–44.0
MCV (fl (L)) 52.3 ± 1.247 53.66 ± 0.942 47 ± 1.632 43.66 ± 2.494 46.33 ± 2.494 42.76 ± 1.247 48.2–58.3
MCH pg (L) 17.2 ± 0.216 17.03 ± 0.249 14.7 ± 0.368 13.8 ± 0.535 15.57 ± 0.539 14.5 ± 0.668 15.8–19.0
MCHC (g/dl) 32.36 ± 0.740 31.06 ± 0.967 26.6 ± 0.571 24.43 ± 0.612 26.43 ± 1.844 24 ± 2.043 30.2–35.3
PLT (×109/L(H)) 1,436 ± 24.94 1,461 ± 25.95 1,554 ± 31.67 1,596 ± 10.70 1,458 ± 27.471 1,480 ± 18.80 450–1,690
MPV (fL) 4.8 ± 0.244 5.13 ± 0.205 5.68 ± 0.220 5.1 ± 0.163 4.53 ± 0.329 4.2 ± 0.294 3.8–6.0

3.3.1 Mean count of WBCs and GRA in mice groups

The mean count of WBCs in the untreated mice group was higher than the normal level (11.56 × 109/L ± 0.826) compared to the control group (2.06 × 109/L ± 0.205); similarly, the mice group treated with petroleum jelly showed an increase in the mean count of WBCs (10.93 × 109/L ± 0.895). The mice group treated with the PBP extract topically and orally showed a slight increase in the mean count of WBCs. The mean count of WBCs was 7.9 × 109/L ± 0.163 in the mice group treated with 650 μg/ml topically and 8.5 × 109/L ± 0.804 in the 500 μg/ml topically treated mice group. While the number of WBCs in the orally treated mice groups is 8.8 × 109/L ± 0.616 in the 650 μg/ml mice group and 7.2 × 109/L ± 0.535 in the 500 μg/ml mice group treated orally (Tables 7 and 8).

The mean value of GRA slightly increased in mice groups treated with PBP extract (1.23 × 109/L ± 0.249) in the 650 μg/ml topically treated mice group, and was 3.26 × 109/L ± 0.329 in the mice group treated with 500 μg/ml topically. Similarly, the mean count of GRA in the mice group treated with PBP extract orally was 2.36 × 109/L ± 0.205 in the 650 μg/ml treated mice group and 4.03 × 109/L ± 0.498 in the 500 μg/ml treated mice group. While the increase in the mean count of GRA was observed in negative control mice groups (8.4 × 109/L ± 0.430in the untreated mice group, (9.03 × 109/L ± 0.451) in the mice group treated with petroleum jelly in comparison with a control group of mice (1.23 × 109/L ± 0.249) (Tables 7 and 8).

3.3.2 Mean values of RBCs and HGB in mice groups

The mean values of RBCs were decreased in the untreated and mice group treated with petroleum jelly compared to the control group. The mean count of RBCs in the untreated mice group was 10.46 × 1012 ± 0.917 and 9.73 ± 0.980 × 1012 in the mice group treated with petroleum jelly, while the mean count of RBCs in the mice group treated with PBP extract topically and orally was normal. The mean counts of RBCs in mice groups treated with PBP were 12.2 × 1012 ± 0.216 in the 650 μg/ml topically treated mice group, 11.4 × 1012 ± 0.432 in the 500 μg/ml topically treated mice group, 10.46 × 1012 ± 0.612 in the 650 μg/ml orally treated mice group, and 10.26 × 1012 ± 0.478 in the mice group treated with 500 μg/ml/kg of PBP extract orally. The mean count of RBCs in the mice group treated with topical antibiotic was 12.66 × 1012 ± 0.124 and in the mice group that was uninfected was 13.1 × 1012 ± 0.492 (Tables 7 and 8).

The level of HGB was normal in all mice groups, but this ratio was high in mice groups treated with topical antibiotics and in the mice group treated with 650 μg/ml/kg PBP extract.

3.3.3 Mean percentage of HCT in mice groups

The HCT percentage was decreased in the mice groups in which S. aureus was inoculated compared to the mice group that was uninfected. The percentage of HCT was above the normal level in the mice group treated with topical antibiotic and the percentage was hardly equal to the normal level in the mice group treated with 650 μg/ml/kg of PBP extract (Tables 7 and 8).

3.3.4 MCV and MCHC in mice groups

The level of MCV was also decreased in all groups except in the mice group treated with the topical antibiotic and in the mice group treated with 650 μg/ml/kg of PBP extract. Similarly, it was normal in the mice group treated with 650 and 500 μg/ml/kg of PBP extract (Tables 7 and 8). The level of MCHC was only normal in the mice group that was uninfected and in the mice group that was treated with the topical antibiotic. In the rest of the mice groups, the level of MCHC decreased.

3.4 Yield percent, vitamin C, and total phenols in the ethanol extract of propolis

Estimating total phenols and vitamin C is important since the antioxidant activity is represented by these measurements. It is an important primary component that is responsible for antioxidant activity and is related to the protection of several oxidative stress-related illnesses [31]. Almost all the concentrations indicated a considerable amount of vitamin C that ranged between 23.53 ± 4.15 and 25.92 ± 3.49 and total phenols ranged from 11.75 ± 2.03 to 11.47 ± 1.68. The percent yield of extractable compounds in the ethanol extract of PBP is presented in Table 9.

Table 9

Yield percent, vitamin C, and total phenols in the ethanol extract of PBP

Concentration (μg/ml) Yield (%) Vitamin C (µg/ml) Phenols (µg/ml)
100 10.70 23.53 ± 4.15 11.75 ± 2.03
200 9.82 19.10 ± 3.70 13.25 ± 1.56
350 11.92 17.47 ± 3.21 8.55 ± 0.90
500 9.47 20.85 ± 2.18 8.68 ± 1.26
650 11.72 25.92 ± 3.49 11.47 ± 1.68

3.5 Antioxidant activity

DPPH is often used to assess the antioxidant potential of different sample extracts [32]. The free radical scavenging abilities of the propolis extract concentrations were measured. As shown in Table 10, the free radical scavenging activity was present at all the concentrations. All the concentrations showed free radical scavenging activity. The PBP sample concentrations showed 328.21, 365.40, 347.20, 335.88, and 445.92 µg/ml antioxidant activity. A comparison of the percentage of inhibition in the antioxidant activity of the ethanol extract of PBP sample concentrations was evaluated with gallic acid (phenol) and ascorbic acid (vitamin C) as standards for scavenging DPPH free radicals, and the results are presented in Table 10.

Table 10

IC50 values of the ethanol extract of propolis sample concentrations with ascorbic acid (vitamin C) and gallic acid (phenol)

Propolis sample concentration (μg/ml) DPPH IC50 (µg/ml)
100 445.92
200 335.88
350 347.20
500 365.40
650 328.21
Gallic acid 188.31
Ascorbic acid 276.51

4 Discussion

To the author’s best knowledge, no in vivo studies have been conducted earlier on PBP against any bacteria, particularly S. aureus; however, a single study showed that propolis obtained from other regions showed efficacy against S. aureus [33]. The current in vitro results indicated that the extract of PBP has antibacterial activity against S. aureus. The current study showed an increase in the antibacterial activity with an increase in the extract concentration. The findings of the current study are in agreement with those of Lu et al. [33], who also showed that propolis has antibacterial action against S. aureus and that the bactericidal ability of propolis improves as the extract concentration increases. The findings of an in vivo investigation revealed that topical therapy with an ethanolic extract of propolis was more efficient than orally treating the group. The highest antibacterial activity of the PBP extract in vivo was observed at 650 μg/ml; the mean abscess area of the topically treated group with ethanolic extract of PBP before treatment was 2.04 cm2 ± 0.117 and after 14 days of treatment, it was decreased to 0.13 cm2 ± 0.018. Similarly, the mean abscess volume before treatment was 2.09 cm3 ± 0.276 and after the treatment, it decreased to 0.04 cm3 ± 0.008. The abscess area and volume of the mice before receiving the same ethanolic extract orally were found to be2.31 cm2 ± 0.127 and 2.73 cm3 ± 0.056; after treatment, they were 0.16 cm2 ± 0.030 and 0.12 cm3 ± 0.048. After 14 days of therapy, the center of the treated wounds developed a scar. All PBP-treated groups had fewer scars than the negative control group and those treated with petroleum jelly. The propolis wound-healing properties are most likely owing to its anti-inflammatory and antioxidant properties.

The hematological parameters, including RBCs, WBCs, Hb, platelet, and HCT (uninfected, ethanolic extract topically orally treated mice, topical antibiotic, and petroleum jelly treated mice groups) were analyzed after treatment. The mean counts of RBCs, Hb, and HCT were found to be decreased in the infected untreated mice group and mice groups treated with petroleum jelly groups, compared to uninfected groups; however, a slighter increase was observed in WBCs. The presence of a high WBC count indicates emotional and physical stress, as well as the immune system’s fight against infection [34]. The count of GRA increases in untreated mice groups and mice groups treated with petroleum jelly. GRA are WBCs with tiny granules that help fight viral and bacterial infections. For infections, autoimmune disorders, and blood cell cancer, the number of GRA (granulocytosis) increases, and the organism suffers abnormal breeding, pale skin, heavy sweating when sleeping, weariness, and appetite loss [35]. There are no studies previously conducted on the hematological parameters of infected mice after oral and topical treatment with honey bee propolis against induced S. aureus infection in BALB C mice. The amount of active compounds present in the ethanolic extract of propolis might have contributed toward the scavenging of free radicals.

Based on the findings of this study, it is possible to infer that PBP has promising potential in the fight against S. aureus infection. For the greatest understanding, further research should be focused on identifying the antibacterial bioactive components in PBP and analyzing antibacterial properties at the compound level.

5 Conclusions

The current study concluded that an ethanolic extract of PBP had both in vitro and in vivo antibacterial potential against S. aureus-induced infections in mice. The in vitro study showed that inhibition of S. aureus increased when the concentration of PBP extract was increased. After in vivo treatment, a decrease in the abscess size was observed with an increase in the concentration of ethanolic extracts of PBP in BALB/c mice infected with S. aureus. Moreover, total phenols and vitamin C content showed antioxidant activity at all concentrations. It is recommended further to assess its mechanism of action for use as a natural antimicrobial agent in a variety of applications.

Acknowledgements

The authors wish to thank the Princess Nourah bint Abdulrahman University Researchers Supporting Project (number PNURSP2023R33), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia for the financial support.

  1. Funding information: This study was funded by Princess Nourah bint Abdulrahman University Researchers Supporting Project (number PNURSP2023R33), Princess Nourah bint Abdulrahman University, Riyadh, Saudi Arabia.

  2. Author contributions: S.M. (investigation and writing/part of his Masters of Philosophy in Zoology dissertation); S.H. (conceptualization and supervision); S.I.A. (co-supervision and guidance); A.U. (animal modeling), and A.A. (review and editing, resources).

  3. Conflict of interest: The authors declare no conflict of interest.

  4. Ethical approval: The Research Ethical Approval Committee of Kohat University of Science and Technology (KUST), Kohat, granted approval for the experimental study wide letter Ref No. /KUST/Ethical Committee/1941, dated 25/06/2021.

  5. Data availability statement: The datasets generated during and/or analyzed during the current study are available from Sumbal Haleem on reasonable request.

References

[1] Eshetie S, Tarekegn F, Moges F, Amsalu A, Birhan W, Huruy K. Methicillin resistant Staphylococcus aureus in Ethiopia: a meta-analysis. BMC Infect Dis. 2016;16:1–9.10.1186/s12879-016-2014-0Search in Google Scholar PubMed PubMed Central

[2] Plata K, Rosato AE, Wegrzyn G. Staphylococcus aureus as an infectious agent: overview of biochemistry and molecular genetics of its pathogenicity. Acta Biochim Pol. 2009;56(4):597–612.10.18388/abp.2009_2491Search in Google Scholar

[3] Lowy FD. Staphylococcus aureus infections. N Engl J Med. 1998;339:520–32.10.1056/NEJM199808203390806Search in Google Scholar PubMed

[4] Von Eiff C, Becker K, Machka K, Stammer H, Peters G. Nasal carriage as a source of Staphylococcus aureus bacteremia. N Engl J Med. 2001;344:11–6.10.1056/NEJM200101043440102Search in Google Scholar PubMed

[5] Fozia F, Ahmad N, Buoharee ZA, Ahmad I, Aslam M, Wahab A, et al. Characterization and evaluation of antimicrobial potential of Trigonella incise (Linn) mediated biosynthesized silver nanoparticles. Molecules; 2004;27(14):4618.10.3390/molecules27144618Search in Google Scholar PubMed PubMed Central

[6] Luzzago C, Locatelli C, Franco A, Scaccabarozzi L, Gualdi V, Viganò R, et al. Clonal diversity, virulence-associated genes and antimicrobial resistance profile of Staphylococcus aureus isolates from nasal cavities and soft tissue infections in wild ruminants in Italian Alps. Vet Microbiol. 2014;170:157–61.10.1016/j.vetmic.2014.01.016Search in Google Scholar PubMed

[7] Holden MT, Feil EJ, Lindsay JA, Peacock SJ, Day NP, Enright MC, et al. Complete genomes of two clinical Staphylococcus aureus strains: evidence for the rapid evolution of virulence and drug resistance. Proceedings of the National Academy of Sciences. vol. 101; 2004. p. 9786–91.Search in Google Scholar

[8] Saleha A, Zunita Z. Methicillin resistant Staphylococcus aureus (MRSA): an emerging veterinary and zoonotic pathogen of public health concern and some studies in Malaysia. J Anim Vet Adv. 2010;9:1094–8.10.3923/javaa.2010.1094.1098Search in Google Scholar

[9] Cheng AG, Kim HK, Burts ML, Krausz T, Schneewind O, Missiakas DM. Genetic requirements for Staphylococcus aureus abscess formation and persistence in host tissues. FASEB J. 2009;23:3393–404.10.1096/fj.09-135467Search in Google Scholar PubMed PubMed Central

[10] Zunita Z, Bashir A, Hafizal A. Occurrence of multidrug resistant Staphylococcus aureus in horses in Malaysia. Vet World. 2008;1:165.Search in Google Scholar

[11] Levy SB. Factors impacting on the problem of antibiotic resistance. J Antimicrob Chemother. 2002;49:25–30.10.1093/jac/49.1.25Search in Google Scholar PubMed

[12] Ghisalberti E. Propolis: a review. BEE World. 1979;60:59–84.10.1080/0005772X.1979.11097738Search in Google Scholar

[13] Elnakady YA, Rushdi AI, Franke R, Abutaha N, Ebaid H, Baabbad M, et al. Characteristics, chemical compositions and biological activities of propolis from Al-Bahah, Saudi Arabia. Sci Rep. 2017;7:1–13.10.1038/srep41453Search in Google Scholar PubMed PubMed Central

[14] Popova M, Silici S, Kaftanoglu O, Bankova V. Antibacterial activity of Turkish propolis and its qualitative and quantitative chemical composition. Phytomedicine. 2005;12:221–8.10.1016/j.phymed.2003.09.007Search in Google Scholar PubMed

[15] Marcucci MC. Propolis: chemical composition, biological properties and therapeutic activity. Apidologie. 1995;26:83–99.10.1051/apido:19950202Search in Google Scholar

[16] Cheng PC, Wong G. Honey bee propolis: prospects in medicine. Bee World. 1996;77:8–15.10.1080/0005772X.1996.11099278Search in Google Scholar

[17] Kujumgiev A, Tsvetkova I, Serkedjieva Y, Bankova V, Christov R, Popov S. Antibacterial, antifungal and antiviral activity of propolis of different geographic origin. J Ethnopharmacol. 1999;64:235–40.10.1016/S0378-8741(98)00131-7Search in Google Scholar PubMed

[18] Amoros M, Lurton E, Boustie J, Girre L, Sauvager F, Cormier M. Comparison of the anti-herpes simplex virus activities of propolis and 3-methyl-but-2-enyl caffeate. J Nat Products. 1994;57:644–7.10.1021/np50107a013Search in Google Scholar PubMed

[19] Isla MI, Moreno MN, Sampietro A, Vattuone MA. Antioxidant activity of Argentine propolis extracts. J Ethnopharmacology. 2001;76:165–70.10.1016/S0378-8741(01)00231-8Search in Google Scholar PubMed

[20] Lu LC, Chen YW, Chou CC. Antibacterial and DPPH free radical-scavenging activities of the ethanol extract of propolis collected in Taiwan. J Food Drug Anal. 2003;11:277–82.10.38212/2224-6614.2676Search in Google Scholar

[21] Markham KR, Mitchell KA, Wilkins AL, Daldy JA, Lu Y. HPLC and GC-MS identification of the major organic constituents in New Zeland propolis. Phytochemistry. 1996;42:205–11.10.1016/0031-9422(96)83286-9Search in Google Scholar

[22] Chopra I. The increasing use of silver-based products as antimicrobial agents: a useful development or a cause for concern?. J Antimicrob Chemother. 2007;59:587–90.10.1093/jac/dkm006Search in Google Scholar PubMed

[23] Jeljaszewicz J, Mlynarczyk G, Mlynarczyk A. Antibiotic resistance in Gram-positive cocci. Int J Antimicrob Agents. 2000;16:473–8.10.1016/S0924-8579(00)00289-2Search in Google Scholar PubMed

[24] Tatiya-Aphiradee N, Chatuphonprasert W, Jarukamjorn K. In vivo antibacterial activity of Garcinia mangostana pericarp extract against methicillin-resistant Staphylococcus aureus in a mouse superficial skin infection model. Pharm Biol. 2016;54(11):2606–15.10.3109/13880209.2016.1172321Search in Google Scholar PubMed

[25] Bunce C, Wheeler L, Reed G, Musser J, Barg N. Murine model of cutaneous infection with gram-positive cocci. Infect Immun. 1992;60(7):2636–40.10.1128/iai.60.7.2636-2640.1992Search in Google Scholar PubMed PubMed Central

[26] Lukomski S, Montgomery CA, Rurangirwa J, Geske RS, Barrish JP, Adams GJ, et al. Extracellular cysteine protease produced by Streptococcus pyogenes participates in the pathogenesis of invasive skin infection and dissemination in mice. Infect Immun. 1999;67(4):1779–88.10.1128/.67.4.1779-1788.1999Search in Google Scholar

[27] Hoff J, Rlatg LVT. Methods of blood collection in the mouse. Lab Anim. 2000;29(10):47–53.Search in Google Scholar

[28] Yen YH, Shih CH, Chang CH. Effect of adding ascorbic acid and glucose on the antioxidative properties during storage of dried carrot. Food Chem. 2008;107(1):265–72.10.1016/j.foodchem.2007.08.013Search in Google Scholar

[29] Chang CC, Yang MH, Wen HM, Chern JC. Estimation of total flavonoid content in propolis by two complementary colorimetric methods. J Food Drug Anal. 2002;10:3.10.38212/2224-6614.2748Search in Google Scholar

[30] Goyal AK, Middha SK, Sen A. Evaluation of the DPPH radical scavenging activity, total phenols and antioxidant activities in Indian wild Bambusa vulgaris Vittata” methanolic leaf extract. J Nat Pharm. 2010;1(1):40.10.4103/2229-5119.73586Search in Google Scholar

[31] Padayatty SJ, Katz A, Wang Y, Eck P, Kwon O, Lee JH, et al. Vitamin C as an antioxidant: evaluation of its role in disease prevention. J Am Coll Nutr. 2003;22(1):18–35.10.1080/07315724.2003.10719272Search in Google Scholar PubMed

[32] Hatano T, Edamatsu R, Hiramatsu M, Mori A, Fujita Y, Yasuhara T, et al. Effects of the interaction of tannins with co-existing substances. VI.: effects of tannins and related polyphenols on superoxide anion radical, and on 1, 1-Diphenyl-2-picrylhydrazyl radical. Chem Pharm Bull. 1989;37(8):2016–21.10.1248/cpb.37.2016Search in Google Scholar

[33] Lu LC, Chen YW, Chou CC. Antibacterial activity of propolis against Staphylococcus aureus. Int J Food Microbiol. 2005;102:213–20.10.1016/j.ijfoodmicro.2004.12.017Search in Google Scholar PubMed

[34] Shanker K, Mohan GK, Hussain MA, Jayarambabu N, Pravallika PL. Green biosynthesis, characterization, in vitro antidiabetic activity, and investigational acute toxicity studies of some herbal-mediated silver nanoparticles on animal models. Pharmacogn Mag. 2017;13:188.10.4103/0973-1296.188316Search in Google Scholar

[35] Akah PA, Alemji JA. Studies on the effects of Vernonia amygdalina leaf extract and fractions on biochemical and hematological parameters in diabetic rats. Planta Medica. 2009;75:PG53.10.1055/s-0029-1234707Search in Google Scholar
Received: 2023-03-30
Revised: 2023-04-26
Accepted: 2023-05-07
Published Online: 2023-05-30

© 2023 the author(s), published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  54. In vitro antiproliferative efficacy of Annona muricata seed and fruit extracts on several cancer cell lines
  55. An experimental study for chemical characterization of artificial anterior cruciate ligament with coated chitosan as biomaterial
  56. Prevalence of residual risks of the transfusion-transmitted infections in Riyadh hospitals: A two-year retrospective study
  57. Computational and experimental investigation of antibacterial and antifungal properties of Nicotiana tabacum extracts
  58. Reinforcement of cementitious mortars with hemp fibers and shives
  59. X-ray shielding properties of bismuth-borate glass doped with rare earth ions
  60. Green supported silver nanoparticles over modified reduced graphene oxide: Investigation of its antioxidant and anti-ovarian cancer effects
  61. Orthogonal synthesis of a versatile building block for dual functionalization of targeting vectors
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  66. Antioxidant, sensory, and functional properties of low-alcoholic IPA beer with Pinus sylvestris L. shoots addition fermented using unconventional yeast
  67. Screening and optimization of extracellular pectinase produced by Bacillus thuringiensis SH7
  68. Determination of polyphenols in Chinese jujube using ultra-performance liquid chromatography–mass spectrometry
  69. Synergistic effects of harpin and NaCl in determining soybean sprout quality under non-sterile conditions
  70. Field evaluation of different eco-friendly alternative control methods against Panonychus citri [Acari: Tetranychidae] spider mite and its predators in citrus orchards
  71. Exploring the antimicrobial potential of biologically synthesized zero valent iron nanoparticles
  72. NaCl regulates goldfish growth and survival at three food supply levels under hypoxia
  73. An exploration of the physical, optical, mechanical, and radiation shielding properties of PbO–MgO–ZnO–B2O3 glasses
  74. A novel statistical modeling of air pollution and the COVID-19 pandemic mortality data by Poisson, geometric, and negative binomial regression models with fixed and random effects
  75. Treatment activity of the injectable hydrogels loaded with dexamethasone In(iii) complex on glioma by inhibiting the VEGF signaling pathway
  76. An alternative approach for the excess lifetime cancer risk and prediction of radiological parameters
  77. Panax ginseng leaf aqueous extract mediated green synthesis of AgNPs under ultrasound condition and investigation of its anti-lung adenocarcinoma effects
  78. Study of hydrolysis and production of instant ginger (Zingiber officinale) tea
  79. Novel green synthesis of zinc oxide nanoparticles using Salvia rosmarinus extract for treatment of human lung cancer
  80. Evaluation of second trimester plasma lipoxin A4, VEGFR-1, IL-6, and TNF-α levels in pregnant women with gestational diabetes mellitus
  81. Antidiabetic, antioxidant and cytotoxicity activities of ortho- and para-substituted Schiff bases derived from metformin hydrochloride: Validation by molecular docking and in silico ADME studies
  82. Antioxidant, antidiabetic, antiglaucoma, and anticholinergic effects of Tayfi grape (Vitis vinifera): A phytochemical screening by LC-MS/MS analysis
  83. Identification of genetic polymorphisms in the stearoyl CoA desaturase gene and its association with milk quality traits in Najdi sheep
  84. Cold-acclimation effect on cadmium absorption and biosynthesis of polyphenolics, and free proline and photosynthetic pigments in Spirogyra aequinoctialis
  85. Analysis of secondary metabolites in Xinjiang Morus nigra leaves using different extraction methods with UPLC-Q/TOF-MS/MS technology
  86. Nanoarchitectonics and performance evaluation of a Fe3O4-stabilized Pickering emulsion-type differential pressure plugging agent
  87. Investigating pyrolysis characteristics of Shengdong coal through Py-GC/MS
  88. Extraction, phytochemical characterization, and antifungal activity of Salvia rosmarinus extract
  89. Introducing a novel and natural antibiotic for the treatment of oral pathogens: Abelmoschus esculentus green-formulated silver nanoparticles
  90. Optimization of gallic acid-enriched ultrasonic-assisted extraction from mango peels
  91. Effect of gamma rays irradiation in the structure, optical, and electrical properties of samarium doped bismuth titanate ceramics
  92. Combinatory in silico investigation for potential inhibitors from Curcuma sahuynhensis Škorničk. & N.S. Lý volatile phytoconstituents against influenza A hemagglutinin, SARS-CoV-2 main protease, and Omicron-variant spike protein
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  94. Twofold interpenetrated 3D Cd(ii) complex: Crystal structure and luminescent property
  95. Study on the microstructure and soil quality variation of composite soil with soft rock and sand
  96. Ancient spring waters still emerging and accessible in the Roman Forum area: Chemical–physical and microbiological characterization
  97. Extraction and characterization of type I collagen from scales of Mexican Biajaiba fish
  98. Finding small molecular compounds to decrease trimethylamine oxide levels in atherosclerosis by virtual screening
  99. Prefatory in silico studies and in vitro insecticidal effect of Nigella sativa (L.) essential oil and its active compound (carvacrol) against the Callosobruchus maculatus adults (Fab), a major pest of chickpea
  100. Polymerized methyl imidazole silver bromide (CH3C6H5AgBr)6: Synthesis, crystal structures, and catalytic activity
  101. Using calcined waste fish bones as a green solid catalyst for biodiesel production from date seed oil
  102. Influence of the addition of WO3 on TeO2–Na2O glass systems in view of the feature of mechanical, optical, and photon attenuation
  103. Naringin ameliorates 5-fluorouracil elicited neurotoxicity by curtailing oxidative stress and iNOS/NF-ĸB/caspase-3 pathway
  104. GC-MS profile of extracts of an endophytic fungus Alternaria and evaluation of its anticancer and antibacterial potentialities
  105. Green synthesis, chemical characterization, and antioxidant and anti-colorectal cancer effects of vanadium nanoparticles
  106. Determination of caffeine content in coffee drinks prepared in some coffee shops in the local market in Jeddah City, Saudi Arabia
  107. A new 3D supramolecular Cu(ii) framework: Crystal structure and photocatalytic characteristics
  108. Bordeaux mixture accelerates ripening, delays senescence, and promotes metabolite accumulation in jujube fruit
  109. Important application value of injectable hydrogels loaded with omeprazole Schiff base complex in the treatment of pancreatitis
  110. Color tunable benzothiadiazole-based small molecules for lightening applications
  111. Investigation of structural, dielectric, impedance, and mechanical properties of hydroxyapatite-modified barium titanate composites for biomedical applications
  112. Metal gel particles loaded with epidermal cell growth factor promote skin wound repair mechanism by regulating miRNA
  113. In vitro exploration of Hypsizygus ulmarius (Bull.) mushroom fruiting bodies: Potential antidiabetic and anti-inflammatory agent
  114. Alteration in the molecular structure of the adenine base exposed to gamma irradiation: An ESR study
  115. Comprehensive study of optical, thermal, and gamma-ray shielding properties of Bi2O3–ZnO–PbO–B2O3 glasses
  116. Lewis acids as co-catalysts in Pd-based catalyzed systems of the octene-1 hydroethoxycarbonylation reaction
  117. Synthesis, Hirshfeld surface analysis, thermal, and selective α-glucosidase inhibitory studies of Schiff base transition metal complexes
  118. Protective properties of AgNPs green-synthesized by Abelmoschus esculentus on retinal damage on the virtue of its anti-inflammatory and antioxidant effects in diabetic rat
  119. Effects of green decorated AgNPs on lignin-modified magnetic nanoparticles mediated by Cydonia on cecal ligation and puncture-induced sepsis
  120. Treatment of gastric cancer by green mediated silver nanoparticles using Pistacia atlantica bark aqueous extract
  121. Preparation of newly developed porcelain ceramics containing WO3 nanoparticles for radiation shielding applications
  122. Utilization of computational methods for the identification of new natural inhibitors of human neutrophil elastase in inflammation therapy
  123. Some anticancer agents as effective glutathione S-transferase (GST) inhibitors
  124. Clay-based bricks’ rich illite mineral for gamma-ray shielding applications: An experimental evaluation of the effect of pressure rates on gamma-ray attenuation parameters
  125. Stability kinetics of orevactaene pigments produced by Epicoccum nigrum in solid-state fermentation
  126. Treatment of denture stomatitis using iron nanoparticles green-synthesized by Silybum marianum extract
  127. Characterization and antioxidant potential of white mustard (Brassica hirta) leaf extract and stabilization of sunflower oil
  128. Characteristics of Langmuir monomolecular monolayers formed by the novel oil blends
  129. Strategies for optimizing the single GdSrFeO4 phase synthesis
  130. Oleic acid and linoleic acid nanosomes boost immunity and provoke cell death via the upregulation of beta-defensin-4 at genetic and epigenetic levels
  131. Unraveling the therapeutic potential of Bombax ceiba roots: A comprehensive study of chemical composition, heavy metal content, antibacterial activity, and in silico analysis
  132. Green synthesis of AgNPs using plant extract and investigation of its anti-human colorectal cancer application
  133. The adsorption of naproxen on adsorbents obtained from pepper stalk extract by green synthesis
  134. Treatment of gastric cancer by silver nanoparticles encapsulated by chitosan polymers mediated by Pistacia atlantica extract under ultrasound condition
  135. In vitro protective and anti-inflammatory effects of Capparis spinosa and its flavonoids profile
  136. Wear and corrosion behavior of TiC and WC coatings deposited on high-speed steels by electro-spark deposition
  137. Therapeutic effects of green-formulated gold nanoparticles by Origanum majorana on spinal cord injury in rats
  138. Melanin antibacterial activity of two new strains, SN1 and SN2, of Exophiala phaeomuriformis against five human pathogens
  139. Evaluation of the analgesic and anesthetic properties of silver nanoparticles supported over biodegradable acacia gum-modified magnetic nanoparticles
  140. Review Articles
  141. Role and mechanism of fruit waste polyphenols in diabetes management
  142. A comprehensive review of non-alkaloidal metabolites from the subfamily Amaryllidoideae (Amaryllidaceae)
  143. Discovery of the chemical constituents, structural characteristics, and pharmacological functions of Chinese caterpillar fungus
  144. Eco-friendly green approach of nickel oxide nanoparticles for biomedical applications
  145. Advances in the pharmaceutical research of curcumin for oral administration
  146. Rapid Communication
  147. Determination of the contents of bioactive compounds in St. John’s wort (Hypericum perforatum): Comparison of commercial and wild samples
  148. Retraction
  149. Retraction of “Two mixed-ligand coordination polymers based on 2,5-thiophenedicarboxylic acid and flexible N-donor ligands: The protective effect on periodontitis via reducing the release of IL-1β and TNF-α”
  150. Topical Issue on Phytochemicals, biological and toxicological analysis of aromatic medicinal plants
  151. Anti-plasmodial potential of selected medicinal plants and a compound Atropine isolated from Eucalyptus obliqua
  152. Anthocyanin extract from black rice attenuates chronic inflammation in DSS-induced colitis mouse model by modulating the gut microbiota
  153. Evaluation of antibiofilm and cytotoxicity effect of Rumex vesicarius methanol extract
  154. Chemical compositions of Litsea umbellata and inhibition activities
  155. Green synthesis, characterization of silver nanoparticles using Rhynchosia capitata leaf extract and their biological activities
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  158. A phytoconstituent 6-aminoflavone ameliorates lipopolysaccharide-induced oxidative stress mediated synapse and memory dysfunction via p-Akt/NF-kB pathway in albino mice
  159. Anti-diabetic potentials of Sorbaria tomentosa Lindl. Rehder: Phytochemistry (GC-MS analysis), α-amylase, α-glucosidase inhibitory, in vivo hypoglycemic, and biochemical analysis
  160. Assessment of cytotoxic and apoptotic activities of the Cassia angustifolia aqueous extract against SW480 colon cancer
  161. Biochemical analysis, antioxidant, and antibacterial efficacy of the bee propolis extract (Hymenoptera: Apis mellifera) against Staphylococcus aureus-induced infection in BALB/c mice: In vitro and in vivo study
  162. Assessment of essential elements and heavy metals in Saudi Arabian rice samples underwent various processing methods
  163. Two new compounds from leaves of Capparis dongvanensis (Sy, B. H. Quang & D. V. Hai) and inhibition activities
  164. Hydroxyquinoline sulfanilamide ameliorates STZ-induced hyperglycemia-mediated amyleoid beta burden and memory impairment in adult mice
  165. An automated reading of semi-quantitative hemagglutination results in microplates: Micro-assay for plant lectins
  166. Inductively coupled plasma mass spectrometry assessment of essential and toxic trace elements in traditional spices consumed by the population of the Middle Eastern region in their recipes
  167. Phytochemical analysis and anticancer activity of the Pithecellobium dulce seed extract in colorectal cancer cells
  168. Impact of climatic disturbances on the chemical compositions and metabolites of Salvia officinalis
  169. Physicochemical characterization, antioxidant and antifungal activities of essential oils of Urginea maritima and Allium sativum
  170. Phytochemical analysis and antifungal efficiency of Origanum majorana extracts against some phytopathogenic fungi causing tomato damping-off diseases
  171. Special Issue on 4th IC3PE
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  174. Synergetic effect of adsorption and photocatalysis by zinc ferrite-anchored graphitic carbon nitride nanosheet for the removal of ciprofloxacin under visible light irradiation
  175. Exploring anticancer activity of the Indonesian guava leaf (Psidium guajava L.) fraction on various human cancer cell lines in an in vitro cell-based approach
  176. The comparison of gold extraction methods from the rock using thiourea and thiosulfate
  177. Special Issue on Marine environmental sciences and significance of the multidisciplinary approaches
  178. Sorption of alkylphenols and estrogens on microplastics in marine conditions
  179. Cytotoxic ketosteroids from the Red Sea soft coral Dendronephthya sp.
  180. Antibacterial and biofilm prevention metabolites from Acanthophora spicifera
  181. Characteristics, source, and health risk assessment of aerosol polyaromatic hydrocarbons in the rural and urban regions of western Saudi Arabia
  182. Special Issue on Advanced Nanomaterials for Energy, Environmental and Biological Applications - Part II
  183. Green synthesis, characterization, and evaluation of antibacterial activities of cobalt nanoparticles produced by marine fungal species Periconia prolifica
  184. Combustion-mediated sol–gel preparation of cobalt-doped ZnO nanohybrids for the degradation of acid red and antibacterial performance
  185. Perinatal supplementation with selenium nanoparticles modified with ascorbic acid improves hepatotoxicity in rat gestational diabetes
  186. Evaluation and chemical characterization of bioactive secondary metabolites from endophytic fungi associated with the ethnomedicinal plant Bergenia ciliata
  187. Enhancing photovoltaic efficiency with SQI-Br and SQI-I sensitizers: A comparative analysis
  188. Nanostructured p-PbS/p-CuO sulfide/oxide bilayer heterojunction as a promising photoelectrode for hydrogen gas generation
https://doi.org/10.1515/chem-2022-0340
Keywords for this article
propolis; S. aureus; in vitro; in vivo; BALB/c
Creative Commons
BY 4.0

Articles in the same Issue

  1. Characteristics, source, and health risk assessment of aerosol polyaromatic hydrocarbons in the rural and urban regions of western Saudi Arabia
  2. Regular Articles
  3. A network-based correlation research between element electronegativity and node importance
  4. Pomegranate attenuates kidney injury in cyclosporine-induced nephrotoxicity in rats by suppressing oxidative stress
  5. Ab initio study of fundamental properties of XInO3 (X = K, Rb, Cs) perovskites
  6. Responses of feldspathic sandstone and sand-reconstituted soil C and N to freeze–thaw cycles
  7. Robust fractional control based on high gain observers design (RNFC) for a Spirulina maxima culture interfaced with an advanced oxidation process
  8. Study on arsenic speciation and redistribution mechanism in Lonicera japonica plants via synchrotron techniques
  9. Optimization of machining Nilo 36 superalloy parameters in turning operation
  10. Vacuum impregnation pre-treatment: A novel method for incorporating mono- and divalent cations into potato strips to reduce the acrylamide formation in French fries
  11. Characterization of effective constituents in Acanthopanax senticosus fruit for blood deficiency syndrome based on the chinmedomics strategy
  12. Comparative analysis of the metabolites in Pinellia ternata from two producing regions using ultra-high-performance liquid chromatography–electrospray ionization–tandem mass spectrometry
  13. The assessment of environmental parameter along the desalination plants in the Kingdom of Saudi Arabia
  14. Effects of harpin and carbendazim on antioxidant accumulation in young jujube leaves
  15. The effects of in ovo injected with sodium borate on hatching performance and small intestine morphology in broiler chicks
  16. Optimization of cutting forces and surface roughness via ANOVA and grey relational analysis in machining of In718
  17. Essential oils of Origanum compactum Benth: Chemical characterization, in vitro, in silico, antioxidant, and antibacterial activities
  18. Translocation of tungsten(vi) oxide/gadolinium(iii) fluoride in tellurite glasses towards improvement of gamma-ray attenuation features in high-density glass shields
  19. Mechanical properties, elastic moduli, and gamma ray attenuation competencies of some TeO2–WO3–GdF3 glasses: Tailoring WO3–GdF3 substitution toward optimum behavioral state range
  20. Comparison between the CIDR or sponge with hormone injection to induce estrus synchronization for twining and sex preselection in Naimi sheep
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  22. Psoralea corylifolia (babchi) seeds enhance proliferation of normal human cultured melanocytes: GC–MS profiling and biological investigation
  23. A novel electrochemical micro-titration method for quantitative evaluation of the DPPH free radical scavenging capacity of caffeic acid
  24. Comparative study between supported bimetallic catalysts for nitrate remediation in water
  25. Persicaline, an alkaloid from Salvadora persica, inhibits proliferation and induces apoptosis and cell-cycle arrest in MCF-7 cells
  26. Determination of nicotine content in locally produced smokeless tobacco (Shammah) samples from Jazan region of Saudi Arabia using a convenient HPLC-MS/MS method
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  28. Integrated geophysical techniques applied for petroleum basins structural characterization in the central part of the Western Desert, Egypt
  29. The impact of chemical modifications on gamma-ray attenuation properties of some WO3-reinforced tellurite glasses
  30. Microwave and Cs+-assisted chemo selective reaction protocol for synthesizing 2-styryl quinoline biorelevant molecules
  31. Structural, physical, and radiation absorption properties of a significant nuclear power plant component: A comparison between REX-734 and 316L SS austenitic stainless steels
  32. Effect of Moringa oleifera on serum YKL-40 level: In vivo rat periodontitis model
  33. Investigating the impact of CO2 emissions on the COVID-19 pandemic by generalized linear mixed model approach with inverse Gaussian and gamma distributions
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  36. Performance analyses of detonation engine cogeneration cycles
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  38. Untargeted metabolomics revealing changes in aroma substances in flue-cured tobacco
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  41. Optimization of ultra-high pressure-assisted extraction of total phenols from Eucommia ulmoides leaves by response surface methodology
  42. Harpin enhances antioxidant nutrient accumulation and decreases enzymatic browning in stored soybean sprouts
  43. Physicochemical and biological properties of carvacrol
  44. Radix puerariae in the treatment of diabetic nephropathy: A network pharmacology analysis and experimental validation
  45. Anti-Alzheimer, antioxidants, glucose-6-phosphate dehydrogenase effects of Taverniera glabra mediated ZnO and Fe2O3 nanoparticles in alloxan-induced diabetic rats
  46. Experimental study on photocatalytic CO2 reduction performance of ZnS/CdS-TiO2 nanotube array thin films
  47. Epoxy-reinforced heavy metal oxides for gamma ray shielding purposes
  48. Black mulberry (Morus nigra L.) fruits: As a medicinal plant rich in human health-promoting compounds
  49. Promising antioxidant and antimicrobial effects of essential oils extracted from fruits of Juniperus thurifera: In vitro and in silico investigations
  50. Chloramine-T-induced oxidation of Rizatriptan Benzoate: An integral chemical and spectroscopic study of products, mechanisms and kinetics
  51. Study on antioxidant and antimicrobial potential of chemically profiled essential oils extracted from Juniperus phoenicea (L.) by use of in vitro and in silico approaches
  52. Screening and characterization of fungal taxol-producing endophytic fungi for evaluation of antimicrobial and anticancer activities
  53. Mineral composition, principal polyphenolic components, and evaluation of the anti-inflammatory, analgesic, and antioxidant properties of Cytisus villosus Pourr leaf extracts
  54. In vitro antiproliferative efficacy of Annona muricata seed and fruit extracts on several cancer cell lines
  55. An experimental study for chemical characterization of artificial anterior cruciate ligament with coated chitosan as biomaterial
  56. Prevalence of residual risks of the transfusion-transmitted infections in Riyadh hospitals: A two-year retrospective study
  57. Computational and experimental investigation of antibacterial and antifungal properties of Nicotiana tabacum extracts
  58. Reinforcement of cementitious mortars with hemp fibers and shives
  59. X-ray shielding properties of bismuth-borate glass doped with rare earth ions
  60. Green supported silver nanoparticles over modified reduced graphene oxide: Investigation of its antioxidant and anti-ovarian cancer effects
  61. Orthogonal synthesis of a versatile building block for dual functionalization of targeting vectors
  62. Thymbra spicata leaf extract driven biogenic synthesis of Au/Fe3O4 nanocomposite and its bio-application in the treatment of different types of leukemia
  63. The role of Ag2O incorporation in nuclear radiation shielding behaviors of the Li2O–Pb3O4–SiO2 glass system: A multi-step characterization study
  64. A stimuli-responsive in situ spray hydrogel co-loaded with naringenin and gentamicin for chronic wounds
  65. Assessment of the impact of γ-irradiation on the piperine content and microbial quality of black pepper
  66. Antioxidant, sensory, and functional properties of low-alcoholic IPA beer with Pinus sylvestris L. shoots addition fermented using unconventional yeast
  67. Screening and optimization of extracellular pectinase produced by Bacillus thuringiensis SH7
  68. Determination of polyphenols in Chinese jujube using ultra-performance liquid chromatography–mass spectrometry
  69. Synergistic effects of harpin and NaCl in determining soybean sprout quality under non-sterile conditions
  70. Field evaluation of different eco-friendly alternative control methods against Panonychus citri [Acari: Tetranychidae] spider mite and its predators in citrus orchards
  71. Exploring the antimicrobial potential of biologically synthesized zero valent iron nanoparticles
  72. NaCl regulates goldfish growth and survival at three food supply levels under hypoxia
  73. An exploration of the physical, optical, mechanical, and radiation shielding properties of PbO–MgO–ZnO–B2O3 glasses
  74. A novel statistical modeling of air pollution and the COVID-19 pandemic mortality data by Poisson, geometric, and negative binomial regression models with fixed and random effects
  75. Treatment activity of the injectable hydrogels loaded with dexamethasone In(iii) complex on glioma by inhibiting the VEGF signaling pathway
  76. An alternative approach for the excess lifetime cancer risk and prediction of radiological parameters
  77. Panax ginseng leaf aqueous extract mediated green synthesis of AgNPs under ultrasound condition and investigation of its anti-lung adenocarcinoma effects
  78. Study of hydrolysis and production of instant ginger (Zingiber officinale) tea
  79. Novel green synthesis of zinc oxide nanoparticles using Salvia rosmarinus extract for treatment of human lung cancer
  80. Evaluation of second trimester plasma lipoxin A4, VEGFR-1, IL-6, and TNF-α levels in pregnant women with gestational diabetes mellitus
  81. Antidiabetic, antioxidant and cytotoxicity activities of ortho- and para-substituted Schiff bases derived from metformin hydrochloride: Validation by molecular docking and in silico ADME studies
  82. Antioxidant, antidiabetic, antiglaucoma, and anticholinergic effects of Tayfi grape (Vitis vinifera): A phytochemical screening by LC-MS/MS analysis
  83. Identification of genetic polymorphisms in the stearoyl CoA desaturase gene and its association with milk quality traits in Najdi sheep
  84. Cold-acclimation effect on cadmium absorption and biosynthesis of polyphenolics, and free proline and photosynthetic pigments in Spirogyra aequinoctialis
  85. Analysis of secondary metabolites in Xinjiang Morus nigra leaves using different extraction methods with UPLC-Q/TOF-MS/MS technology
  86. Nanoarchitectonics and performance evaluation of a Fe3O4-stabilized Pickering emulsion-type differential pressure plugging agent
  87. Investigating pyrolysis characteristics of Shengdong coal through Py-GC/MS
  88. Extraction, phytochemical characterization, and antifungal activity of Salvia rosmarinus extract
  89. Introducing a novel and natural antibiotic for the treatment of oral pathogens: Abelmoschus esculentus green-formulated silver nanoparticles
  90. Optimization of gallic acid-enriched ultrasonic-assisted extraction from mango peels
  91. Effect of gamma rays irradiation in the structure, optical, and electrical properties of samarium doped bismuth titanate ceramics
  92. Combinatory in silico investigation for potential inhibitors from Curcuma sahuynhensis Škorničk. & N.S. Lý volatile phytoconstituents against influenza A hemagglutinin, SARS-CoV-2 main protease, and Omicron-variant spike protein
  93. Physical, mechanical, and gamma ray shielding properties of the Bi2O3–BaO–B2O3–ZnO–As2O3–MgO–Na2O glass system
  94. Twofold interpenetrated 3D Cd(ii) complex: Crystal structure and luminescent property
  95. Study on the microstructure and soil quality variation of composite soil with soft rock and sand
  96. Ancient spring waters still emerging and accessible in the Roman Forum area: Chemical–physical and microbiological characterization
  97. Extraction and characterization of type I collagen from scales of Mexican Biajaiba fish
  98. Finding small molecular compounds to decrease trimethylamine oxide levels in atherosclerosis by virtual screening
  99. Prefatory in silico studies and in vitro insecticidal effect of Nigella sativa (L.) essential oil and its active compound (carvacrol) against the Callosobruchus maculatus adults (Fab), a major pest of chickpea
  100. Polymerized methyl imidazole silver bromide (CH3C6H5AgBr)6: Synthesis, crystal structures, and catalytic activity
  101. Using calcined waste fish bones as a green solid catalyst for biodiesel production from date seed oil
  102. Influence of the addition of WO3 on TeO2–Na2O glass systems in view of the feature of mechanical, optical, and photon attenuation
  103. Naringin ameliorates 5-fluorouracil elicited neurotoxicity by curtailing oxidative stress and iNOS/NF-ĸB/caspase-3 pathway
  104. GC-MS profile of extracts of an endophytic fungus Alternaria and evaluation of its anticancer and antibacterial potentialities
  105. Green synthesis, chemical characterization, and antioxidant and anti-colorectal cancer effects of vanadium nanoparticles
  106. Determination of caffeine content in coffee drinks prepared in some coffee shops in the local market in Jeddah City, Saudi Arabia
  107. A new 3D supramolecular Cu(ii) framework: Crystal structure and photocatalytic characteristics
  108. Bordeaux mixture accelerates ripening, delays senescence, and promotes metabolite accumulation in jujube fruit
  109. Important application value of injectable hydrogels loaded with omeprazole Schiff base complex in the treatment of pancreatitis
  110. Color tunable benzothiadiazole-based small molecules for lightening applications
  111. Investigation of structural, dielectric, impedance, and mechanical properties of hydroxyapatite-modified barium titanate composites for biomedical applications
  112. Metal gel particles loaded with epidermal cell growth factor promote skin wound repair mechanism by regulating miRNA
  113. In vitro exploration of Hypsizygus ulmarius (Bull.) mushroom fruiting bodies: Potential antidiabetic and anti-inflammatory agent
  114. Alteration in the molecular structure of the adenine base exposed to gamma irradiation: An ESR study
  115. Comprehensive study of optical, thermal, and gamma-ray shielding properties of Bi2O3–ZnO–PbO–B2O3 glasses
  116. Lewis acids as co-catalysts in Pd-based catalyzed systems of the octene-1 hydroethoxycarbonylation reaction
  117. Synthesis, Hirshfeld surface analysis, thermal, and selective α-glucosidase inhibitory studies of Schiff base transition metal complexes
  118. Protective properties of AgNPs green-synthesized by Abelmoschus esculentus on retinal damage on the virtue of its anti-inflammatory and antioxidant effects in diabetic rat
  119. Effects of green decorated AgNPs on lignin-modified magnetic nanoparticles mediated by Cydonia on cecal ligation and puncture-induced sepsis
  120. Treatment of gastric cancer by green mediated silver nanoparticles using Pistacia atlantica bark aqueous extract
  121. Preparation of newly developed porcelain ceramics containing WO3 nanoparticles for radiation shielding applications
  122. Utilization of computational methods for the identification of new natural inhibitors of human neutrophil elastase in inflammation therapy
  123. Some anticancer agents as effective glutathione S-transferase (GST) inhibitors
  124. Clay-based bricks’ rich illite mineral for gamma-ray shielding applications: An experimental evaluation of the effect of pressure rates on gamma-ray attenuation parameters
  125. Stability kinetics of orevactaene pigments produced by Epicoccum nigrum in solid-state fermentation
  126. Treatment of denture stomatitis using iron nanoparticles green-synthesized by Silybum marianum extract
  127. Characterization and antioxidant potential of white mustard (Brassica hirta) leaf extract and stabilization of sunflower oil
  128. Characteristics of Langmuir monomolecular monolayers formed by the novel oil blends
  129. Strategies for optimizing the single GdSrFeO4 phase synthesis
  130. Oleic acid and linoleic acid nanosomes boost immunity and provoke cell death via the upregulation of beta-defensin-4 at genetic and epigenetic levels
  131. Unraveling the therapeutic potential of Bombax ceiba roots: A comprehensive study of chemical composition, heavy metal content, antibacterial activity, and in silico analysis
  132. Green synthesis of AgNPs using plant extract and investigation of its anti-human colorectal cancer application
  133. The adsorption of naproxen on adsorbents obtained from pepper stalk extract by green synthesis
  134. Treatment of gastric cancer by silver nanoparticles encapsulated by chitosan polymers mediated by Pistacia atlantica extract under ultrasound condition
  135. In vitro protective and anti-inflammatory effects of Capparis spinosa and its flavonoids profile
  136. Wear and corrosion behavior of TiC and WC coatings deposited on high-speed steels by electro-spark deposition
  137. Therapeutic effects of green-formulated gold nanoparticles by Origanum majorana on spinal cord injury in rats
  138. Melanin antibacterial activity of two new strains, SN1 and SN2, of Exophiala phaeomuriformis against five human pathogens
  139. Evaluation of the analgesic and anesthetic properties of silver nanoparticles supported over biodegradable acacia gum-modified magnetic nanoparticles
  140. Review Articles
  141. Role and mechanism of fruit waste polyphenols in diabetes management
  142. A comprehensive review of non-alkaloidal metabolites from the subfamily Amaryllidoideae (Amaryllidaceae)
  143. Discovery of the chemical constituents, structural characteristics, and pharmacological functions of Chinese caterpillar fungus
  144. Eco-friendly green approach of nickel oxide nanoparticles for biomedical applications
  145. Advances in the pharmaceutical research of curcumin for oral administration
  146. Rapid Communication
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  148. Retraction
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  153. Evaluation of antibiofilm and cytotoxicity effect of Rumex vesicarius methanol extract
  154. Chemical compositions of Litsea umbellata and inhibition activities
  155. Green synthesis, characterization of silver nanoparticles using Rhynchosia capitata leaf extract and their biological activities
  156. GC-MS analysis and antibacterial activities of some plants belonging to the genus Euphorbia on selected bacterial isolates
  157. The abrogative effect of propolis on acrylamide-induced toxicity in male albino rats: Histological study
  158. A phytoconstituent 6-aminoflavone ameliorates lipopolysaccharide-induced oxidative stress mediated synapse and memory dysfunction via p-Akt/NF-kB pathway in albino mice
  159. Anti-diabetic potentials of Sorbaria tomentosa Lindl. Rehder: Phytochemistry (GC-MS analysis), α-amylase, α-glucosidase inhibitory, in vivo hypoglycemic, and biochemical analysis
  160. Assessment of cytotoxic and apoptotic activities of the Cassia angustifolia aqueous extract against SW480 colon cancer
  161. Biochemical analysis, antioxidant, and antibacterial efficacy of the bee propolis extract (Hymenoptera: Apis mellifera) against Staphylococcus aureus-induced infection in BALB/c mice: In vitro and in vivo study
  162. Assessment of essential elements and heavy metals in Saudi Arabian rice samples underwent various processing methods
  163. Two new compounds from leaves of Capparis dongvanensis (Sy, B. H. Quang & D. V. Hai) and inhibition activities
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  167. Phytochemical analysis and anticancer activity of the Pithecellobium dulce seed extract in colorectal cancer cells
  168. Impact of climatic disturbances on the chemical compositions and metabolites of Salvia officinalis
  169. Physicochemical characterization, antioxidant and antifungal activities of essential oils of Urginea maritima and Allium sativum
  170. Phytochemical analysis and antifungal efficiency of Origanum majorana extracts against some phytopathogenic fungi causing tomato damping-off diseases
  171. Special Issue on 4th IC3PE
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  175. Exploring anticancer activity of the Indonesian guava leaf (Psidium guajava L.) fraction on various human cancer cell lines in an in vitro cell-based approach
  176. The comparison of gold extraction methods from the rock using thiourea and thiosulfate
  177. Special Issue on Marine environmental sciences and significance of the multidisciplinary approaches
  178. Sorption of alkylphenols and estrogens on microplastics in marine conditions
  179. Cytotoxic ketosteroids from the Red Sea soft coral Dendronephthya sp.
  180. Antibacterial and biofilm prevention metabolites from Acanthophora spicifera
  181. Characteristics, source, and health risk assessment of aerosol polyaromatic hydrocarbons in the rural and urban regions of western Saudi Arabia
  182. Special Issue on Advanced Nanomaterials for Energy, Environmental and Biological Applications - Part II
  183. Green synthesis, characterization, and evaluation of antibacterial activities of cobalt nanoparticles produced by marine fungal species Periconia prolifica
  184. Combustion-mediated sol–gel preparation of cobalt-doped ZnO nanohybrids for the degradation of acid red and antibacterial performance
  185. Perinatal supplementation with selenium nanoparticles modified with ascorbic acid improves hepatotoxicity in rat gestational diabetes
  186. Evaluation and chemical characterization of bioactive secondary metabolites from endophytic fungi associated with the ethnomedicinal plant Bergenia ciliata
  187. Enhancing photovoltaic efficiency with SQI-Br and SQI-I sensitizers: A comparative analysis
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