Home Physical Sciences Biological evaluation of CH3OH and C2H5OH of Berberis vulgaris for in vivo antileishmanial potential against Leishmania tropica in murine models
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Biological evaluation of CH3OH and C2H5OH of Berberis vulgaris for in vivo antileishmanial potential against Leishmania tropica in murine models

  • Qasim Ali , Sumbal Haleem EMAIL logo , Salman Ahmad , Qaisar Jamal , Tariq Ahmad , Afshan Khan , Shehzad Ali , Amal Alotaibi , Jyoti Singh and Adil Khan
Published/Copyright: November 6, 2024
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Open Chemistry
From the journal Open Chemistry Volume 22 Issue 1

Abstract

Leishmaniasis is one of the global health issues and is still being handled with costly and sometimes unsuccessful compounds having serious side effects, highlighting the importance of seeking new potent antileishmanial compounds. Herbal medicines have been considered as the main source of prevention and treatment for a wide variety of diseases as well as other photogenetic diseases over the last few centuries. The current study was designed to investigate the in vitro and in vivo antileishmanial efficacy of ethanolic and methanolic extracts of Berberis vulgaris root collected from Kurez region of District Orakzai, Khyber Pakhtunkhwa, Pakistan. Stationary growth-phase metacyclic promastigotes form of Leishmania tropica was incubated in vitro in methanolic and ethanolic extracts using amphotericin B as a positive control. The antileishmanial activity of B. vulgaris extracts was measured after the incubation period using methoxynitrosulfophenyl-tetrazolium carboxanilide assay. For the in vivo study, BALB/c mice were infected with metacyclic L. tropica promastigotes, and lesions appeared after 28 days of inoculum. The results of study research showed that B. vulgaris extract had a powerful antileishmanial activity on promastigotes of L. tropica at different concentrations (5, 10, 25, 50, and 75 μg/mL). The inhibition concentration 50 values for ethanolic and methanolic extracts of B. vulgaris were determined to be 15.37 and 17.55 μg/mL, respectively. In the in vivo activity, it was observed that B. vulgaris ethanolic extract at the concentration of 1.5 mg/kg decreased the lesion diameter in BALB/c infected mice. The ethanolic extract topically and orally reduced the lesion size 0.51 ± 0.023 and 0.56 ± 0.008 mm, while methanolic extract both topically and orally decrease the lesion diameter of 0.63 ± 0.008 and 0.68 ± 0.009 mm relatively, in comparison with negative control (1.45 ± 0.016 mm). Hematological parameters of mice including blood red blood cells, hematocrit, and hemoglobin in mice groups (infected non-treated) were found to be decreased, while the mice group treated with extract demonstrated nearly similar results to non-infected group. It is concluded from the current study that antileishmanial activity of B. vulgaris from Pakistan against L. tropica in both in vitro and in vivo showed a promising antileishmanial activity. This study might be helpful in the control strategies of cutaneous leishmaniasis caused by L. tropica.

Keywords: Berberis vulgaris ; L. tropica ; Kurez region; BALB/c; AmpB

1 Introduction

Leishmaniasis is a cluster of diseases induced by more than 20 different species of leishmania protozoan parasites that cause various forms of human leishmaniasis, ranging from dermal ulcers to fatal visceral forms. Leishmaniasis is transmitted through the bites of infected female Phlebotomus or Lutzomyia sand flies. In 98 different countries and territories, it is endemic, impacting 12 million individuals and threatening more than 350 million people around the globe. Clinically, leishmaniasis exists in three major forms: cutaneous leishmaniasis (CL), mucocutaneous leishmaniasis, and visceral leishmaniasis [1,2].

In Pakistan, around 21,000–35,000 cases, including both anthroponotic (ACL) and zoonotic forms of CL, are reported annually [3]. ACL, primarily associated with Leishmania tropica, occurs unpredictably and is prevalent in urban areas of Baluchistan, Azad Jammu Kashmir, Punjab, Khyber Pakhtunkhwa (KP), and the former Federally Administered Tribal Areas (FATA) [3,4]. Leishmaniasis is characterized by sporadic outbreaks attributed to L. tropica in KP, the northwestern province of Pakistan [5]. Transmission of CL occurs through blood-sucking sand flies [6], with Pakistan recording around 37 species and sub-species of these insects [7]. Sand flies of the genera Phlebotomus and Lutzomyia transmit Leishmania parasites in the old and new worlds, respectively, and are found in diverse habitats ranging from tropical rainforests to deserts [8].

Currently, drug therapy is the primary prevention method for leishmaniasis due to the absence of an effective vaccine [6,9]. Pentavalent antimony compounds, including meglumine antimony and sodium stibogluconate, despite their toxicity, high costs, and resistance issues, remain the first-line therapy for CL [10]. Ancient civilizations relied on medicinal plants to combat diseases such as cancer and infections. Today, in drug development, animal models play a crucial role in understanding disease mechanisms, assessing treatment safety, and confirming drug effectiveness. However, it is challenging to find an animal model that perfectly mimics human disease. Rodent models, like the mouse model for various Leishmania species, help researchers study CL and understand immune responses, although they do not fully replicate human pathology [11].

Given the challenges associated with existing antileishmanial drugs, researchers are exploring new compounds, both natural and synthetic, for their potential efficacy. One promising natural option is European barberry (Berberis vulgaris), known as “Zereshk” in Persian. European barberry contains bioactive compounds such as berbamine, palmatine, and berberine, traditionally used for various ailments including cardiovascular, gastrointestinal, respiratory, skin, renal, and infectious diseases. Previous literature showed that Berberis species demonstrated multiple biological activities [12,13,14,15]. Studies have shown that European barberry and its derivatives possess antifungal, antibacterial, and antiparasitic properties against certain pathogens. Some research indicates promising in vitro antileishmanial activity of European barberry, prompting further investigation into its in vivo potential. Therefore, this study aims to evaluate the in vivo antileishmanial and lesion control effects of European barberry against both promastigote and amastigote forms of L. tropica.

2 Materials and methods

2.1 Study area

Fresh roots of B. vulgaris were collected from the Kurez region (coordinates: 33°–33′ to 33°–54′ N and 70°–36′ to 71°–22′ E) in District Orakzai, KP, Pakistan (previously a part of the region called FATA). Orakzai District is characterized by its mountainous terrain and valleys, with elevations ranging from 6,000 to 7,000 feet [16] (Figure 1).

Figure 1 Map shows the area of Orakzai from where B. vulgaris root was collected.
Figure 1

Map shows the area of Orakzai from where B. vulgaris root was collected.

2.2 Collection of plant materials

The fresh root of B. vulgaris samples was identified through botanical keys [17]. The root was washed under the tap water to remove debris, and those specimens were numbered and kept in the laboratory of Molecular Parasitology and Virology Department of Zoology, Kohat University of Science and Technology (KUST), and dried at 30–40°C undershade for 10–15 days. The dried roots were size-reduced to coarse powder with the aid of electric grinder [18].

2.3 Preparation of extracts

The plant material was first air-dried and then ground into a fine powder. Approximately 50 grams of the powdered root of B. vulgaris was subjected to extraction using a Soxhlet apparatus with 500 mL of 95% ethanol and methanol as solvents, respectively. The extraction process continued for 6–8 h until the solvent in the Soxhlet apparatus became colorless, indicating complete extraction.

After the extraction, the crude extracts were filtered using a solvent filtration apparatus. The solvent was then removed from the filtrate by evaporating it under reduced pressure using a rotary vacuum evaporator at a temperature not exceeding 40°C [17,18]. This ensured the preservation of heat-sensitive phytochemicals. The percentage yield of the dried extracts is recorded in Table 1, with the ethanolic extract yielding approximately 14.38% and the methanolic extract yielding 10.22%, according to the given formula:

Average yield % = Weight of the extract adter solvent removal Dry weight of plant sample × 100

Table 1

Methanolic extract of B. vulgaris against L. tropica promastigote

Concentrations µg/mL Inhibition 1 (%) Inhibition 2 (%) Inhibition 3 (%) Mean value (%) SD IC50 µg/mL
75 95.0 99.0 99.5 97.83 ± 2.01 17.55
50 89.2 93.6 96.0 92.93 ± 2.81
25 39.2 43.0 44.6 42.26 ± 2.26
10 29.0 28.5 30.8 29.43 ± 0.98
5 16.4 18.0 19.5 17.96 ± 1.26

2.4 Parasitic culture

Preserved isolates of L. tropica KWH23, acquired from the Cell Culture Lab at the Institute of Zoological Sciences (formerly Department of Zoology), Peshawar University, were cultured in M199 growth medium supplemented with 10% heat-inactivated fetal calf serum (HI-FCS), 100 μg/mL penicillin, 100 μg/mL streptomycin, 50 μg/mL kanamycin, and 5 μg/mL hemin. Culturing was conducted in a bio-level two-crop laboratory under appropriate laboratory conditions. The culture was incubated in an anaerobic environment at 24 to 26°C, and growth was recorded daily for 10 days by counting using a Neubauer Hemocytometer (Sigma-Aldrich BR717810-1EA BLAUBRAND). During the logarithmic growth phase, there was a significant increase in promastigote count. It was at this stage that the promastigotes were harvested by centrifugation and used for in vitro assays at 1 × 105 cells/mL [19].

2.5 Stock solutions and dilutions of extracts

Each ethanolic and methanolic extract was diluted into five different concentrations (5, 10, 25, 50, and 75 µg/mL), prepared through serial dilutions in 0.5% dimethyl sulfoxide (DMSO) using the formula C 1 V 1 = C 2 V 2 [20].

2.6 In vitro activity of B. vulgaris against promastigote

For the assessment of the antileishmanial activity of B. vulgaris extracts, an in vitro assay was conducted using 96-well flat-bottom plates. Promastigotes were quantified in culture suspension using an enhanced Neubauer Hemocytometer prior to the application of the extracts. From a viable bulk culture of promastigotes (3 × 106 parasites/mL), 1 × 106 promastigotes per well in 200 µL of fresh Roswell park memorial institute (RPMI)-1640 medium supplemented with 10% fetal bovine serum (FBS) were seeded in each well of a 96-well dish. Approximately 20 mL of promastigote culture was needed for each 96-well plate. The five different concentrations of both ethanolic and methanolic extracts of B. vulgaris were applied. The negative control group was treated with 0.5% DMSO. Each concentration of the extracts was tested in triplicate. The 96-well plate was then incubated for 48 h at 26°C. Following the 48 h incubation period, the number of promastigotes in each well (both treated and control groups) was counted using a microscope and an Improved Neubauer Hemocytometer [17].

2.7 Methoxynitrosulfophenyl-tetrazolium carboxanilide (XTT) assay

Following the incubation period, a solution containing XTT (4 mg/mL) in phosphate buffered saline (PBS) (pH 7.0 at 37°C) with peroxymonosulfate (0.06 mg/mL) was applied (20 µL per well), and the plate was reincubated for an additional 4 h at 26°C. After the 4 h incubation, the percentage inhibition within each well (both treated and control) was assessed using an HT microplate reader, with a test wavelength of 450 nm and a reference filter of 650 nm [19]. The % age inhibition was calculated from these absorbance values using the following formula:

% Inhibition = Control OD − Test OD Control OD × 100 ,

where the OD represents the optical density.

The 50% inhibitory concentrations were calculated using the nonlinear regression in GraphPad prism software.

2.8 Animal model

Male BALB/c mice aged 4 to 6 weeks, with an average weight of approximately 30 g, were procured from the Peshawar Veterinary Research Institute and transported to the Molecular Parasitology and Virology Laboratory at the Department of Zoology, KUST, Kohat. They were treated in accordance with applicable protocols for the ethical use of laboratory animals. Every effort was made to minimize the discomfort of the mice throughout the duration of the research. The mice were housed in ventilated plastic cages under controlled conditions of 23 ± 2°C temperature, 55 to 60% humidity, and a 12 h light–dark cycle (as shown in Figure 2). They were provided with ample food and purified water in the animal care facility managed by the laboratory [21].

Figure 2 Use of Balb/C mice model for in vivo activity under favorable condition.
Figure 2

Use of Balb/C mice model for in vivo activity under favorable condition.

2.9 Mice inoculation

The obtained promastigotes form of L. tropica were collected in sterile tubes until they were needed for infecting the mice. The promastigotes were counted using a hemocytometer under an inverted microscope. Once counted, the promastigotes were centrifuged at 2,000 rpm for 10 min at 4°C. After centrifugation, the supernatants were removed, leaving behind the pellet, which was then diluted in 10 mL of fresh RPMI-1640 medium containing 10% FBS. Subsequently, 10 µL of the promastigotes of L. tropica (2 × 106 cells/mL) was injected subcutaneously into the base of the tail and the footpad of the mice to induce infection [21].

2.10 In vivo activity of B. vulgaris against infected mice

After 28 days of inoculation, the development of lesions was observed. The mice were then divided into groups and subgroups. A total of 21 mice were randomly assigned into 4 groups as follows: Group 1 consisted of 3 untreated infected mice, Group 2 consisted of 3 infected mice treated with PBS, Group 3 consisted of 12 infected mice further subdivided into 2 subgroups: subgroup 1 contained 6 infected mice treated with methanolic extract (3 mice treated orally and 3 topically), subgroup 2 contained 6 infected mice treated with ethanolic extract (3 mice treated orally and 3 topically), and Group 4 consisted of 3 healthy mice (as shown in flow sheet diagram in Figure 3). Treatment with pre-determined doses of B. vulgaris extract began 4 weeks post-infection and continued daily for 8 weeks [19].

Figure 3 Flow sheet diagram of the control and experimental groups and subgroups for the in vitro activity.
Figure 3

Flow sheet diagram of the control and experimental groups and subgroups for the in vitro activity.

2.11 Lesion size measurement

The diameter of the lesion was measured using a Vernier caliper at two diameters (D and d) at right angles to each other both before and after treatment. The lesion size (in millimeters) was calculated using the formula: S = (D + d)/2/2 [19].

2.12 Hematological analysis

A one-use 1 mL syringe and a 26 × 6 mm needle were used to collect 0.8 mL of whole blood from each mouse post-treatment via an intracardiac route. The blood was then transferred into ethylenediamine tetraacetic acid tubes for hematological variable analysis. Absolute measurements for red blood cells (RBCs), hematocrit, hemoglobin, white blood cells (WBCs), and lymphocytes were recorded using an auto Hematology Analyzer following the standard protocols [22].

2.13 Statistical analysis

Statistical analysis of the data obtained from both the in vitro and in vivo assays was conducted using Minitab to analyze the results of the antileishmanial activity of B. vulgaris extracts. This included calculating the mean and standard deviation and determining variations in different parameters. Additionally, for the in vitro assay, the inhibition concentration 50 (IC50) values were calculated through linear regression analysis using GraphPad Prism 5 Software.

3 Results

3.1 Activity of methanolic extract of B. vulgaris against promastigote form of L. tropica

The activity of the methanolic extract of B. vulgaris against the promastigote form of L. tropica was investigated and found to be lower compared to the ethanolic extract. Similar to the ethanolic extract, five concentrations were tested for the methanolic extract to measure its anti-promastigote activity. The inhibition rates were highest at the concentration of 75 µg/mL (97.83 ± 2.01%), followed by 50 µg/mL (92.93 ± 2.81%), with the lowest inhibition observed at 5 µg/mL (17.96 ± 1.26%). Statistical analysis revealed that the inhibition at 50 µg/mL and 75 µg/mL concentrations were significantly similar (Figure 4). The IC50 value, representing the concentration at which 50% inhibition is achieved, was calculated to be 17.55 μg/mL, as shown in Table 1.

Figure 4 Activity of B. vulgaris methanolic extract against promastigote form of L. tropica.
Figure 4

Activity of B. vulgaris methanolic extract against promastigote form of L. tropica.

3.2 Activity of amphotericin B against promastigote

In the in vitro model against L. tropica promastigote, amphotericin B was used as a positive control. Five different concentrations of 1, 2.5, 5, 7.5, and 10 µg/mL were employed to assess its activity against Leishmania sp. The maximum inhibitory potential of the standard amphotericin B was observed at 10 µg/mL, followed by 7.5 µg/mL, with the lowest inhibition seen at 1 µg/mL (as shown in Figure 5). The IC50 value for the control compound was determined to be 2.52 µg/mL.

Figure 5 Amphotericin B-positive control activity against promastigotes.
Figure 5

Amphotericin B-positive control activity against promastigotes.

3.3 Comparison of ethanolic and methanolic extracts in in vitro assay

The comparison between the ethanolic and methanolic extracts revealed that the percentage inhibition rate was higher in the ethanolic extracts compared to that in the methanolic extracts of B. vulgaris in the in vitro activity against the promastigote form of L. tropica (as shown in Figure 6). Another notable finding was that increasing the concentration of the ethanol extract marginally slowed down the inhibition rate, although this difference was not statistically significant when compared to the methanol extract.

Figure 6 Comparison of ethanolic and methanolic extracts against L. tropica promastigote.
Figure 6

Comparison of ethanolic and methanolic extracts against L. tropica promastigote.

3.4 In vivo antileishmanial effect of B. vulgaris

In vivo study evaluated the efficacy of ethanolic and methanolic extract of B. vulgaris root against L. tropica amastigote form in mice model. To examine the lesion size control effects of B. vulgaris in vivo, male BALB/c mice were affected by L. tropica amastigote, and the two extracts were administered 1.5 mg/kg daily topically and orally for 2 months post-infection. As shown the Table 2, the mean lesion diameter of mice group treated with ethanolic extract topically administered was measured to be their highest value (0.51 ± 0.023) and lowest value (0.90 ± 0.040) in comparison with negative control (0.85 ± 0.001 to 1.45 ± 0.016). In another mice group that received the same ethanolic extract orally, the mean lesion diameter was measured and their highest value was 0.56 ± 0.008 and the lowest was 0.89 ± 0.009. The mean lesion size in the mice group treated topically reduced more compared with that in the mice group receiving the same extract orally. The lesion size decreased in the mice group treated topically with methanolic extract, which were found to have the highest value 0.63 ± 0.008 and the lowest value of 0.93 ± 0.023, whereas the orally treated group have the highest value of 0.68 ± 0.009 and the lowest value of 0.94 ± 0.032. In the first week of treatment, the lesion diameter was not decreased in all groups of mice, while the lesion size grew more dramatically as the weeks increased. The highest activity of B. vulgaris extract against L. tropica was observed in the ethanolic extract as compared to that in the methanolic extract in both mice group treated with topically and orally in in vivo mice model (Figures 7 and 8).

Table 2

Antileishmanial activity of B. vulgaris in ethanolic and methanolic solvents against L. tropica promastigote both topically and orally

Weeks Concentrations (mg/kg/day) Extract Mean lesion size (mm) ± SD Extract Mean lesion size (mm) ± SD Negative control
Topically Orally Topically Orally
1 1.5 Ethanolic 0.90 ± 0.040 0.89 ± 0.009 Methanolic 0.93 ± 0.023 0.94 ± 0.032 0.85 ± 0.001
2 1.5 Ethanolic 0.87 ± 0.020 0.88 ± 0.023 Methanolic 0.91 ± 0.023 0.92 ± 0.004 0.88 ± 0.023
3 1.5 Ethanolic 0.84 ± 0.009 0.86 ± 0.014 Methanolic 0.89 ± 0.009 0.91 ± 0.012 0.94 ± 0.023
4 1.5 Ethanolic 0.80 ± 0.009 0.82 ± 0.020 Methanolic 0.86 ± 0.014 0.89 ± 0.009 1.01 ± 0.014
5 1.5 Ethanolic 0.74 ± 0.008 0.76 ± 0.012 Methanolic 0.81 ± 0.023 0.85 ± 0.000 1.11 ± 0.029
6 1.5 Ethanolic 0.68 ± 0.009 0.70 ± 0.009 Methanolic 0.76 ± 0.012 0.80 ± 0.009 1.23 ± 0.032
7 1.5 Ethanolic 0.60 ± 0.016 0.63 ± 0.008 Methanolic 0.70 ± 0.009 0.74 ± 0.008 1.33 ± 0.045
8 1.5 Ethanolic 0.51 ± 0.023 0.56 ± 0.008 Methanolic 0.63 ± 0.008 0.68 ± 0.009 1.45 ± 0.016
Figure 7 In vivo activity of ethanolic extract of B. vulgaris against L. tropica.
Figure 7

In vivo activity of ethanolic extract of B. vulgaris against L. tropica.

Figure 8 In vivo activity of methanolic extract of B. vulgaris against L. tropica.
Figure 8

In vivo activity of methanolic extract of B. vulgaris against L. tropica.

3.5 Hematological analysis

The hematological analysis of mice blood was conducted after 8 weeks of infection, comparing both treated and untreated infected mice with a control group of uninfected mice. The blood parameters included RBCs, hematocrit, hemoglobin, WBCs, and lymphocytes, as shown in Table 3, Figure 9.

Table 3

Hematological analysis of blood parameters of mice groups infected and uninfected

Blood parameters Noninfected Hematological analysis after 8 weeks of infection
Infected without treatment Infected with treatment
RBCs (×1012/mL) 7.66 ± 1.52 6.33 ± 0.28 7.00 ± 1.00
Hematocrit (%) 37.66 ± 1.52 34.66 ± 1.15 36.00 ± 0.57
Hemoglobin (g/dl) 12.66 ± 1.52 10.66 ± 1.52 11.33 ± 0.57
WBC (mm3) 8,321 ± 145 7,866 ± 188 8,210 ± 81.64
Lymph (×103/mm3) 29.12 ± 11.21 32.6 ± 13.32 28.20 ± 11.02
Figure 9 Comparative hematological analysis of mice’s blood post 8 week infection shows (a) RBCs, (b) WBCs, (c) hemoglobin, (d) hematocrit, and (e) lymphocyte.
Figure 9

Comparative hematological analysis of mice’s blood post 8 week infection shows (a) RBCs, (b) WBCs, (c) hemoglobin, (d) hematocrit, and (e) lymphocyte.

In the untreated infected mice group, the mean value of RBCs decreased (6.33 ± 0.28), whereas in the treated infected mice group, it increased (7.00 ± 1.00) compared to the control group of uninfected mice. Similarly, the mean values of hematocrit and hemoglobin decreased in the untreated infected mice group (34.66 ± 1.15 and 10.66 ± 1.52, respectively), but slightly increased in the treated infected mice group (36.00 ± 0.57 and 11.33 ± 0.57, respectively).

Furthermore, the mean value of WBCs decreased in the untreated infected mice group (7,866 ± 188), while it increased in the treated infected mice group (8,210 ± 81.64). Additionally, the mean value of lymphocytes increased in the untreated infected mice group (32.6 ± 13.32), but decreased after treatment, with all these mean values compared to the control group of uninfected mice.

4 Discussion

Leishmaniasis poses a significant public health challenge in tropical and subtropical regions, where it is transmitted through the bite of infected female sand-flies. Endemic in 98 countries and territories, leishmaniasis affects 12 million people and threatens around 350 million individuals worldwide. CL accounts for a majority of cases, affecting 1.5 million people annually, with approximately 90% of cases occurring in countries such as Pakistan, Iraq, Syria, Saudi Arabia, Peru, Iran, and Afghanistan [23]. Despite being a global health concern, leishmaniasis is still treated with costly and sometimes ineffective compounds that carry serious side effects, underscoring the need for new therapeutic options. Pentavalent antimonials, pentamidine, and amphotericin B are among the standard agents used for leishmaniasis treatment [24]. However, these drugs have several limitations, including the need for regular intramuscular or intravenous injections over a period of 20–28 days, potential toxicity, parasite resistance, and high treatment costs [24,25,26]. Due to the adverse effects associated with pentavalent antimonials, there is growing interest in natural remedies. Plant-based components and extracts offer promising alternatives due to their lower side effects, cost-effectiveness, and widespread availability. In this study, we evaluated the in vitro and in vivo antileishmanial effects of ethanolic and methanolic extracts of B. vulgaris against promastigote and amastigote forms of L. tropica.

Our results demonstrated potent antileishmanial activity of B. vulgaris extract against promastigotes of L. tropica at concentrations ranging from 5 to 75 µg/mL, with parasite inhibition ranging from 22.23 to 99.38% and an IC50 value of 15.37 µg/mL. Interestingly, the ethanolic extract showed higher inhibition rates compared to the methanolic extract at the same concentrations, with inhibition rates of 97.83 and 17.96%, respectively, and an IC50 value of 17.55 µg/mL for the methanolic extract. Overall, our findings suggest that ethanolic extract of B. vulgaris exhibits superior antileishmanial activity compared to its methanolic counterpart in in vitro assays against L. tropica promastigotes. Several studies have investigated the antimicrobial effects of B. vulgaris and its bioactive compounds, consistently showing effective activity against various microorganisms. For instance, research conducted by Mahmoudvand et al. [17] demonstrated that the extract of B. vulgaris and berberine effectively inhibited the growth of L. tropica and L. major promastigotes in a dosage-dependent manner, with IC50 values ranging from 2.1 to 26.6 µg/mL. Another study by Ozbilgin et al. [27] observed a percentage inhibition of parasites between 88.0 and 100.0% in the presence of B. vulgaris ethanol extract, with an IC50 value of 444.81 ± 2.12 µg/mL.

Our study aligns with previous research, showing that the chloroform extract of N. sativa and ethanolic extracts of B. vulgaris significantly inhibit the efficiency of L. tropica promastigotes compared to the standard medication, with IC50 values of 7.83 and 4.83 µg/mL, respectively [17]. Furthermore, both extracts dramatically reduce the growth rate of amastigotes compared to the positive control (p < 0.05), suggesting the efficient antileishmanial activity against L. tropica in vitro. Previous studies have also highlighted the anticandidal effects of B. vulgaris extract, particularly from ethanol extracts, attributed to bioactive compounds such as berberine. While the mechanism influencing the antifungal function of berberine is not fully understood [28], our findings support the notion of significant anticandidal impact.

Interestingly, berberine has shown inhibition effects on the proliferation of hepatoma and leukemia cell lines in vitro [29], yet it is not considered toxic at medical dosages. However, some side effects have been reported at high dosages [30]. Nevertheless, B. vulgaris extracts with selectivity indexes ≥ 10 revealed protection to macrophages and clarity to parasites, suggesting safety for cell line consideration despite considerable cytotoxicity at high concentrations [31].

It is understood that there is a future for natural products in trying to seek appropriate and selective agents for the Leishmaniasis therapy. A significant advantage of the systematic diversity of this product screening is the substances that could generate natural products a source of novel antileishmaniasis lead compounds. The findings of our research show that the extract of B. vulgaris has a strong suppression effect on leishmaniasis and after treatment decrease in lesion size with an increased in concentration of ethanolic B. vulgaris extracts in infected BALB/c mice with the L. tropica amastigotes.

There is no one single study that has been reported of B. vulgaris against L. tropica in in vivo model. But some studies of B. vulgaris are present against different species of Leishmania that they supported our study against L. tropica. The results of the researcher study show that 20% root bark extracts of B. vulgaris have a powerful reducing effect on leishmaniasis [32]. Fatah et al. [33] reported a reduced lesion size following treatment with increasing concentrations of ethanolic extracts from the root, stem, and leaf of B. vulgaris in BALB/c mice infected with the promastigote form of L. major. The aqueous extracts of B. vulgaris fruits have been reported that had an effective activity against Echinococcus granulosus at lower concentration (4 mg/mL) and short time of viability [34].

Some other studies of different plant species extracts show their activities against L. tropica. Ozbel and Ozbilgin [35] reported that while the acidified extract of Haplophyllum myrtifolium showed promising results in an in vitro study, it had limited effectiveness in reducing lesion size in mice infected with L. tropica during in vivo testing at a concentration of 50 mg/kg. Our parasite burden and cytokine manufacturing findings support the safe and feasible therapy of leishmaniasis with the new formulation of PM-SLNs (paromomycin sulfate–solid lipid nanoparticles), and the use of SLN as drug delivery framework could even regulate the propagation form of L. tropica parasites in mice that have been infected [36].

In contrast, it is stated that B. vulgaris had shown toxicity against different parasites but it is proven from the study that the reduction in the density of the lesion, the amount of parasites, and the weight gain of BALB/c mice first infected with L. major, at 20, 40, and 80% of ethanolic stem bark extracts, was reported, followed by treatment. The 20% of extract was found to be effective, but 80% of the extract was harmful [37].

5 Conclusion

Therefore, the aforementioned studies suggested that our conclusion of the current study revealed that B. vulgaris ethanolic and methanolic extracts had promising antileishmanial activity in both in vitro and in vivo models and can regulate CL in mice infected with L. tropica. This outcome has also created a scientific proof that herbal plants can be used for the prevention and therapy of CL in traditional medicine. In summary, our findings underscore the significant effectiveness of B. vulgaris ethanol extracts against L. tropica, likely attributed to bioactive compounds such as polyphenols and berberine. However, further research is needed to elucidate the mechanisms of intervention of B. vulgaris and its components against Leishmania sp.

Acknowledgement

The authors wish to thank Princess Nourah bint Abdulrahman University Researchers Supporting Project Number (PNURSP2024R33), Riyadh, Saudi Arabia.

  1. Funding information: This research was financially supported by Princess Nourah bint Abdulrahman University Researchers Supporting Project Number (PNURSP2024R33), Riyadh, Saudi Arabia.

  2. Author contribution: Qasim Ali: conceptualization, data curation, methodology, validation, visualization, formal analysis, reviewing, editing and writing – original draft. Sumbal Haleem: supervision, formal analysis, methodology, conceptualization and writing – review and editing. Salman Ahmad: supervision, software, resources, formal analysis, visualization, writing – review and editing. Qaisar Jamal: resources, software, formal analysis, writing – review and editing. Tariq Ahmad: visualization, writing – review and editing. Afshan Khan: formal analysis, writing – review and editing. Shehzad Ali: formal analysis, writing – review and editing. Amal Alotaibi: funding acquisition, resources, writing – review and editing. Jyoti Singh: visualization, writing – review and editing. Adil Khan: writing – review and editing. All authors have read and agreed to the published version of the manuscript.

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

  4. Ethical approval: The ethical approval (ZO320182013) of this study was obtained from Research Ethical Committee, Kohat University of Science and Technology, Kohat (KUST) Khyber Pakhtunkhwa, Pakistan, for this experimental study.

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

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Received: 2024-06-25
Revised: 2024-08-19
Accepted: 2024-08-31
Published Online: 2024-11-06

© 2024 the author(s), published by De Gruyter

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

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https://doi.org/10.1515/chem-2024-0096
Keywords for this article
Berberis vulgaris; L. tropica; Kurez region; BALB/c; AmpB
Creative Commons
BY 4.0

Articles in the same Issue

  1. Regular Articles
  2. Porous silicon nanostructures: Synthesis, characterization, and their antifungal activity
  3. Biochar from de-oiled Chlorella vulgaris and its adsorption on antibiotics
  4. Phytochemicals profiling, in vitro and in vivo antidiabetic activity, and in silico studies on Ajuga iva (L.) Schreb.: A comprehensive approach
  5. Synthesis, characterization, in silico and in vitro studies of novel glycoconjugates as potential antibacterial, antifungal, and antileishmanial agents
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  10. Phytochemical and physicochemical studies of different apple varieties grown in Morocco
  11. Synthesis of multi-template molecularly imprinted polymers (MT-MIPs) for isolating ethyl para-methoxycinnamate and ethyl cinnamate from Kaempferia galanga L., extract with methacrylic acid as functional monomer
  12. Nutraceutical potential of Mesembryanthemum forsskaolii Hochst. ex Bioss.: Insights into its nutritional composition, phytochemical contents, and antioxidant activity
  13. Evaluation of influence of Butea monosperma floral extract on inflammatory biomarkers
  14. Cannabis sativa L. essential oil: Chemical composition, anti-oxidant, anti-microbial properties, and acute toxicity: In vitro, in vivo, and in silico study
  15. The effect of gamma radiation on 5-hydroxymethylfurfural conversion in water and dimethyl sulfoxide
  16. Hollow mushroom nanomaterials for potentiometric sensing of Pb2+ ions in water via the intercalation of iodide ions into the polypyrrole matrix
  17. Determination of essential oil and chemical composition of St. John’s Wort
  18. Computational design and in vitro assay of lantadene-based novel inhibitors of NS3 protease of dengue virus
  19. Anti-parasitic activity and computational studies on a novel labdane diterpene from the roots of Vachellia nilotica
  20. Microbial dynamics and dehydrogenase activity in tomato (Lycopersicon esculentum Mill.) rhizospheres: Impacts on growth and soil health across different soil types
  21. Correlation between in vitro anti-urease activity and in silico molecular modeling approach of novel imidazopyridine–oxadiazole hybrids derivatives
  22. Spatial mapping of indoor air quality in a light metro system using the geographic information system method
  23. Iron indices and hemogram in renal anemia and the improvement with Tribulus terrestris green-formulated silver nanoparticles applied on rat model
  24. Integrated track of nano-informatics coupling with the enrichment concept in developing a novel nanoparticle targeting ERK protein in Naegleria fowleri
  25. Cytotoxic and phytochemical screening of Solanum lycopersicum–Daucus carota hydro-ethanolic extract and in silico evaluation of its lycopene content as anticancer agent
  26. Protective activities of silver nanoparticles containing Panax japonicus on apoptotic, inflammatory, and oxidative alterations in isoproterenol-induced cardiotoxicity
  27. pH-based colorimetric detection of monofunctional aldehydes in liquid and gas phases
  28. Investigating the effect of resveratrol on apoptosis and regulation of gene expression of Caco-2 cells: Unravelling potential implications for colorectal cancer treatment
  29. Metformin inhibits knee osteoarthritis induced by type 2 diabetes mellitus in rats: S100A8/9 and S100A12 as players and therapeutic targets
  30. Effect of silver nanoparticles formulated by Silybum marianum on menopausal urinary incontinence in ovariectomized rats
  31. Synthesis of new analogs of N-substituted(benzoylamino)-1,2,3,6-tetrahydropyridines
  32. Response of yield and quality of Japonica rice to different gradients of moisture deficit at grain-filling stage in cold regions
  33. Preparation of an inclusion complex of nickel-based β-cyclodextrin: Characterization and accelerating the osteoarthritis articular cartilage repair
  34. Empagliflozin-loaded nanomicelles responsive to reactive oxygen species for renal ischemia/reperfusion injury protection
  35. Preparation and pharmacodynamic evaluation of sodium aescinate solid lipid nanoparticles
  36. Assessment of potentially toxic elements and health risks of agricultural soil in Southwest Riyadh, Saudi Arabia
  37. Theoretical investigation of hydrogen-rich fuel production through ammonia decomposition
  38. Biosynthesis and screening of cobalt nanoparticles using citrus species for antimicrobial activity
  39. Investigating the interplay of genetic variations, MCP-1 polymorphism, and docking with phytochemical inhibitors for combatting dengue virus pathogenicity through in silico analysis
  40. Ultrasound induced biosynthesis of silver nanoparticles embedded into chitosan polymers: Investigation of its anti-cutaneous squamous cell carcinoma effects
  41. Copper oxide nanoparticles-mediated Heliotropium bacciferum leaf extract: Antifungal activity and molecular docking assays against strawberry pathogens
  42. Sprouted wheat flour for improving physical, chemical, rheological, microbial load, and quality properties of fino bread
  43. Comparative toxicity assessment of fisetin-aided artificial intelligence-assisted drug design targeting epibulbar dermoid through phytochemicals
  44. Acute toxicity and anti-inflammatory activity of bis-thiourea derivatives
  45. Anti-diabetic activity-guided isolation of α-amylase and α-glucosidase inhibitory terpenes from Capsella bursa-pastoris Linn.
  46. GC–MS analysis of Lactobacillus plantarum YW11 metabolites and its computational analysis on familial pulmonary fibrosis hub genes
  47. Green formulation of copper nanoparticles by Pistacia khinjuk leaf aqueous extract: Introducing a novel chemotherapeutic drug for the treatment of prostate cancer
  48. Improved photocatalytic properties of WO3 nanoparticles for Malachite green dye degradation under visible light irradiation: An effect of La doping
  49. One-pot synthesis of a network of Mn2O3–MnO2–poly(m-methylaniline) composite nanorods on a polypyrrole film presents a promising and efficient optoelectronic and solar cell device
  50. Groundwater quality and health risk assessment of nitrate and fluoride in Al Qaseem area, Saudi Arabia
  51. A comparative study of the antifungal efficacy and phytochemical composition of date palm leaflet extracts
  52. Processing of alcohol pomelo beverage (Citrus grandis (L.) Osbeck) using saccharomyces yeast: Optimization, physicochemical quality, and sensory characteristics
  53. Specialized compounds of four Cameroonian spices: Isolation, characterization, and in silico evaluation as prospective SARS-CoV-2 inhibitors
  54. Identification of a novel drug target in Porphyromonas gingivalis by a computational genome analysis approach
  55. Physico-chemical properties and durability of a fly-ash-based geopolymer
  56. FMS-like tyrosine kinase 3 inhibitory potentials of some phytochemicals from anti-leukemic plants using computational chemical methodologies
  57. Wild Thymus zygis L. ssp. gracilis and Eucalyptus camaldulensis Dehnh.: Chemical composition, antioxidant and antibacterial activities of essential oils
  58. 3D-QSAR, molecular docking, ADMET, simulation dynamic, and retrosynthesis studies on new styrylquinolines derivatives against breast cancer
  59. Deciphering the influenza neuraminidase inhibitory potential of naturally occurring biflavonoids: An in silico approach
  60. Determination of heavy elements in agricultural regions, Saudi Arabia
  61. Synthesis and characterization of antioxidant-enriched Moringa oil-based edible oleogel
  62. Ameliorative effects of thistle and thyme honeys on cyclophosphamide-induced toxicity in mice
  63. Study of phytochemical compound and antipyretic activity of Chenopodium ambrosioides L. fractions
  64. Investigating the adsorption mechanism of zinc chloride-modified porous carbon for sulfadiazine removal from water
  65. Performance repair of building materials using alumina and silica composite nanomaterials with electrodynamic properties
  66. Effects of nanoparticles on the activity and resistance genes of anaerobic digestion enzymes in livestock and poultry manure containing the antibiotic tetracycline
  67. Effect of copper nanoparticles green-synthesized using Ocimum basilicum against Pseudomonas aeruginosa in mice lung infection model
  68. Cardioprotective effects of nanoparticles green formulated by Spinacia oleracea extract on isoproterenol-induced myocardial infarction in mice by the determination of PPAR-γ/NF-κB pathway
  69. Anti-OTC antibody-conjugated fluorescent magnetic/silica and fluorescent hybrid silica nanoparticles for oxytetracycline detection
  70. Curcumin conjugated zinc nanoparticles for the treatment of myocardial infarction
  71. Identification and in silico screening of natural phloroglucinols as potential PI3Kα inhibitors: A computational approach for drug discovery
  72. Exploring the phytochemical profile and antioxidant evaluation: Molecular docking and ADMET analysis of main compounds from three Solanum species in Saudi Arabia
  73. Unveiling the molecular composition and biological properties of essential oil derived from the leaves of wild Mentha aquatica L.: A comprehensive in vitro and in silico exploration
  74. Analysis of bioactive compounds present in Boerhavia elegans seeds by GC-MS
  75. Homology modeling and molecular docking study of corticotrophin-releasing hormone: An approach to treat stress-related diseases
  76. LncRNA MIR17HG alleviates heart failure via targeting MIR17HG/miR-153-3p/SIRT1 axis in in vitro model
  77. Development and validation of a stability indicating UPLC-DAD method coupled with MS-TQD for ramipril and thymoquinone in bioactive SNEDDS with in silico toxicity analysis of ramipril degradation products
  78. Biosynthesis of Ag/Cu nanocomposite mediated by Curcuma longa: Evaluation of its antibacterial properties against oral pathogens
  79. Development of AMBER-compliant transferable force field parameters for polytetrafluoroethylene
  80. Treatment of gestational diabetes by Acroptilon repens leaf aqueous extract green-formulated iron nanoparticles in rats
  81. Development and characterization of new ecological adsorbents based on cardoon wastes: Application to brilliant green adsorption
  82. A fast, sensitive, greener, and stability-indicating HPLC method for the standardization and quantitative determination of chlorhexidine acetate in commercial products
  83. Assessment of Se, As, Cd, Cr, Hg, and Pb content status in Ankang tea plantations of China
  84. Effect of transition metal chloride (ZnCl2) on low-temperature pyrolysis of high ash bituminous coal
  85. Evaluating polyphenol and ascorbic acid contents, tannin removal ability, and physical properties during hydrolysis and convective hot-air drying of cashew apple powder
  86. Development and characterization of functional low-fat frozen dairy dessert enhanced with dried lemongrass powder
  87. Scrutinizing the effect of additive and synergistic antibiotics against carbapenem-resistant Pseudomonas aeruginosa
  88. Preparation, characterization, and determination of the therapeutic effects of copper nanoparticles green-formulated by Pistacia atlantica in diabetes-induced cardiac dysfunction in rat
  89. Antioxidant and antidiabetic potentials of methoxy-substituted Schiff bases using in vitro, in vivo, and molecular simulation approaches
  90. Anti-melanoma cancer activity and chemical profile of the essential oil of Seseli yunnanense Franch
  91. Molecular docking analysis of subtilisin-like alkaline serine protease (SLASP) and laccase with natural biopolymers
  92. Overcoming methicillin resistance by methicillin-resistant Staphylococcus aureus: Computational evaluation of napthyridine and oxadiazoles compounds for potential dual inhibition of PBP-2a and FemA proteins
  93. Exploring novel antitubercular agents: Innovative design of 2,3-diaryl-quinoxalines targeting DprE1 for effective tuberculosis treatment
  94. Drimia maritima flowers as a source of biologically potent components: Optimization of bioactive compound extractions, isolation, UPLC–ESI–MS/MS, and pharmacological properties
  95. Estimating molecular properties, drug-likeness, cardiotoxic risk, liability profile, and molecular docking study to characterize binding process of key phyto-compounds against serotonin 5-HT2A receptor
  96. Fabrication of β-cyclodextrin-based microgels for enhancing solubility of Terbinafine: An in-vitro and in-vivo toxicological evaluation
  97. Phyto-mediated synthesis of ZnO nanoparticles and their sunlight-driven photocatalytic degradation of cationic and anionic dyes
  98. Monosodium glutamate induces hypothalamic–pituitary–adrenal axis hyperactivation, glucocorticoid receptors down-regulation, and systemic inflammatory response in young male rats: Impact on miR-155 and miR-218
  99. Quality control analyses of selected honey samples from Serbia based on their mineral and flavonoid profiles, and the invertase activity
  100. Eco-friendly synthesis of silver nanoparticles using Phyllanthus niruri leaf extract: Assessment of antimicrobial activity, effectiveness on tropical neglected mosquito vector control, and biocompatibility using a fibroblast cell line model
  101. Green synthesis of silver nanoparticles containing Cichorium intybus to treat the sepsis-induced DNA damage in the liver of Wistar albino rats
  102. Quality changes of durian pulp (Durio ziberhinus Murr.) in cold storage
  103. Study on recrystallization process of nitroguanidine by directly adding cold water to control temperature
  104. Determination of heavy metals and health risk assessment in drinking water in Bukayriyah City, Saudi Arabia
  105. Larvicidal properties of essential oils of three Artemisia species against the chemically insecticide-resistant Nile fever vector Culex pipiens (L.) (Diptera: Culicidae): In vitro and in silico studies
  106. Design, synthesis, characterization, and theoretical calculations, along with in silico and in vitro antimicrobial proprieties of new isoxazole-amide conjugates
  107. The impact of drying and extraction methods on total lipid, fatty acid profile, and cytotoxicity of Tenebrio molitor larvae
  108. A zinc oxide–tin oxide–nerolidol hybrid nanomaterial: Efficacy against esophageal squamous cell carcinoma
  109. Research on technological process for production of muskmelon juice (Cucumis melo L.)
  110. Physicochemical components, antioxidant activity, and predictive models for quality of soursop tea (Annona muricata L.) during heat pump drying
  111. Characterization and application of Fe1−xCoxFe2O4 nanoparticles in Direct Red 79 adsorption
  112. Torilis arvensis ethanolic extract: Phytochemical analysis, antifungal efficacy, and cytotoxicity properties
  113. Magnetite–poly-1H pyrrole dendritic nanocomposite seeded on poly-1H pyrrole: A promising photocathode for green hydrogen generation from sanitation water without using external sacrificing agent
  114. HPLC and GC–MS analyses of phytochemical compounds in Haloxylon salicornicum extract: Antibacterial and antifungal activity assessment of phytopathogens
  115. Efficient and stable to coking catalysts of ethanol steam reforming comprised of Ni + Ru loaded on MgAl2O4 + LnFe0.7Ni0.3O3 (Ln = La, Pr) nanocomposites prepared via cost-effective procedure with Pluronic P123 copolymer
  116. Nitrogen and boron co-doped carbon dots probe for selectively detecting Hg2+ in water samples and the detection mechanism
  117. Heavy metals in road dust from typical old industrial areas of Wuhan: Seasonal distribution and bioaccessibility-based health risk assessment
  118. Phytochemical profiling and bioactivity evaluation of CBD- and THC-enriched Cannabis sativa extracts: In vitro and in silico investigation of antioxidant and anti-inflammatory effects
  119. Investigating dye adsorption: The role of surface-modified montmorillonite nanoclay in kinetics, isotherms, and thermodynamics
  120. Antimicrobial activity, induction of ROS generation in HepG2 liver cancer cells, and chemical composition of Pterospermum heterophyllum
  121. Study on the performance of nanoparticle-modified PVDF membrane in delaying membrane aging
  122. Impact of cholesterol in encapsulated vitamin E acetate within cocoliposomes
  123. Review Articles
  124. Structural aspects of Pt(η3-X1N1X2)(PL) (X1,2 = O, C, or Se) and Pt(η3-N1N2X1)(PL) (X1 = C, S, or Se) derivatives
  125. Biosurfactants in biocorrosion and corrosion mitigation of metals: An overview
  126. Stimulus-responsive MOF–hydrogel composites: Classification, preparation, characterization, and their advancement in medical treatments
  127. Electrochemical dissolution of titanium under alternating current polarization to obtain its dioxide
  128. Special Issue on Recent Trends in Green Chemistry
  129. Phytochemical screening and antioxidant activity of Vitex agnus-castus L.
  130. Phytochemical study, antioxidant activity, and dermoprotective activity of Chenopodium ambrosioides (L.)
  131. Exploitation of mangliculous marine fungi, Amarenographium solium, for the green synthesis of silver nanoparticles and their activity against multiple drug-resistant bacteria
  132. Study of the phytotoxicity of margines on Pistia stratiotes L.
  133. Special Issue on Advanced Nanomaterials for Energy, Environmental and Biological Applications - Part III
  134. Impact of biogenic zinc oxide nanoparticles on growth, development, and antioxidant system of high protein content crop (Lablab purpureus L.) sweet
  135. Green synthesis, characterization, and application of iron and molybdenum nanoparticles and their composites for enhancing the growth of Solanum lycopersicum
  136. Green synthesis of silver nanoparticles from Olea europaea L. extracted polysaccharides, characterization, and its assessment as an antimicrobial agent against multiple pathogenic microbes
  137. Photocatalytic treatment of organic dyes using metal oxides and nanocomposites: A quantitative study
  138. Antifungal, antioxidant, and photocatalytic activities of greenly synthesized iron oxide nanoparticles
  139. Special Issue on Phytochemical and Pharmacological Scrutinization of Medicinal Plants
  140. Hepatoprotective effects of safranal on acetaminophen-induced hepatotoxicity in rats
  141. Chemical composition and biological properties of Thymus capitatus plants from Algerian high plains: A comparative and analytical study
  142. Chemical composition and bioactivities of the methanol root extracts of Saussurea costus
  143. In vivo protective effects of vitamin C against cyto-genotoxicity induced by Dysphania ambrosioides aqueous extract
  144. Insights about the deleterious impact of a carbamate pesticide on some metabolic immune and antioxidant functions and a focus on the protective ability of a Saharan shrub and its anti-edematous property
  145. A comprehensive review uncovering the anticancerous potential of genkwanin (plant-derived compound) in several human carcinomas
  146. A study to investigate the anticancer potential of carvacrol via targeting Notch signaling in breast cancer
  147. Assessment of anti-diabetic properties of Ziziphus oenopolia (L.) wild edible fruit extract: In vitro and in silico investigations through molecular docking analysis
  148. Optimization of polyphenol extraction, phenolic profile by LC-ESI-MS/MS, antioxidant, anti-enzymatic, and cytotoxic activities of Physalis acutifolia
  149. Phytochemical screening, antioxidant properties, and photo-protective activities of Salvia balansae de Noé ex Coss
  150. Antihyperglycemic, antiglycation, anti-hypercholesteremic, and toxicity evaluation with gas chromatography mass spectrometry profiling for Aloe armatissima leaves
  151. Phyto-fabrication and characterization of gold nanoparticles by using Timur (Zanthoxylum armatum DC) and their effect on wound healing
  152. Does Erodium trifolium (Cav.) Guitt exhibit medicinal properties? Response elements from phytochemical profiling, enzyme-inhibiting, and antioxidant and antimicrobial activities
  153. Integrative in silico evaluation of the antiviral potential of terpenoids and its metal complexes derived from Homalomena aromatica based on main protease of SARS-CoV-2
  154. 6-Methoxyflavone improves anxiety, depression, and memory by increasing monoamines in mice brain: HPLC analysis and in silico studies
  155. Simultaneous extraction and quantification of hydrophilic and lipophilic antioxidants in Solanum lycopersicum L. varieties marketed in Saudi Arabia
  156. Biological evaluation of CH3OH and C2H5OH of Berberis vulgaris for in vivo antileishmanial potential against Leishmania tropica in murine models
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