https://doi.org/10.5812/gct-157124

Investigating the Antimicrobial Properties and Pigmentation of Several Medicinal Plants on Antibiotic-Resistant Salmonella typhimurium

authors:

avatar Azadeh Mojiri ORCID 1 , avatar Abbas Bozorgmehr 2 , avatar Afsaneh Mirshekari 3 , avatar Marziye Rezaei 4 , *

Assistant Professor of Statistics, Department of Statistics, Faculty of Sciences, University of Zabol, Zabol, Iran
Faculty of Art and Architecture, University of Sistan and Baluchistan, Zahedan, Iran
Deparment of Gastroenterology and Hepatology, Amir Al Momenin Hospital, School of Medicine, Zabol University of Medical Sciences, Zabol, Iran
Department of Painting, Faculty of Art and Architecture, University of Sistan and Baluchistan, Zahedan, Iran
Gene, Cell and Tissue: Vol.12, issue 1; e157124
published online: December 5, 2024
article type: Research Article
received: October 21, 2024
revised: October 30, 2024
accepted: October 30, 2024

How To Cite Mojiri A, Bozorgmehr A, Mirshekari A, Rezaei M. Investigating the Antimicrobial Properties and Pigmentation of Several Medicinal Plants on Antibiotic-Resistant Salmonella typhimurium. Gene Cell Tissue. 2025;12(1):e157124. https://doi.org/10.5812/gct-157124.

Abstract

Background:

The aim of this study was to investigate the antimicrobial properties and pigmentation effects of several medicinal plants on antibiotic-resistant Salmonella typhimurium.

Methods:

Medicinal plant extracts were prepared using ethanol as a solvent, and the antimicrobial activity was assessed by measuring the diameter of the inhibition zones using the microdilution method. The pigmentation effect of the plant extracts, indicated by pink coloration, was evaluated using an ELISA reader.

Results:

The findings showed that the maximum inhibition zone diameter for Nannorrhops ritchiana ethanolic extract was 8 mm, while the minimum was 1 mm. For Ficus religiosa leaves, the maximum inhibition zone was 15 mm, and the minimum was 2 mm. The inhibition zone for musk ranged from 1 mm (minimum) to 18 mm (maximum). Capparis spinosa L. fruits exhibited an inhibition zone diameter of 15 mm.

Conclusions:

The results indicate that medicinal plants possess significant inhibitory effects against Salmonella typhimurium and can be considered potential treatments for infections caused by this bacterium.

1. Background

Salmonella typhimurium is commonly transmitted to humans through the fecal-oral route. In humans, its primary colonization sites are the ileum, liver, spleen, gallbladder, and blood (1-3). This bacterium is a major cause of bacteremia, septicemia, typhoid fever, and diarrhea (4).

Complications of typhoid fever include leukopenia, thrombocytopenia, and elevated levels of C-reactive protein (CRP) and alanine aminotransferase (ALT) (5, 6). Contaminated water and poor socioeconomic conditions are key factors contributing to the spread of enteric fever (6, 7). In 2019, Pakistan introduced the typhoid conjugate vaccine, approved by the World Health Organization, to combat typhoid fever (8, 9). The vaccine's results were highly effective in reducing infection rates (10).

Until the 1970s, antibiotics such as ampicillin, chloramphenicol, and cotrimoxazole (trimethoprim-sulfamethoxazole) were commonly used to treat S. typhimurium infections. Unfortunately, widespread bacterial drug resistance has necessitated the development of new treatments (9, 11-15).

Nannorrhops ritchiana (Griff) Aitch is a species native to Pakistan, Afghanistan, and Iran. This versatile and resilient shrub thrives under extreme environmental conditions, such as strong winds, extreme temperatures, and water scarcity (16). This plant has been commonly used in different countries (17-31). Historically, the leaves and stems of N. ritchiana were used to make mats, fences, and house roofs (32, 33). The dried leaves, stems, and petioles of the Mezri palm have also been used as household fuel. In southern Europe and subtropical regions of the Americas, N. ritchiana is cultivated as an ornamental plant (34).

Temple figs, belonging to the Ficus genus and the Moraceae family, are perennial, evergreen plants (35). Among the therapeutic properties of temple figs are their antibacterial, antiviral, and antifungal activities, as well as acetylcholinesterase inhibition. Extractive compounds from this plant have applications in treating skin diseases (inflammation, swelling, and wound healing), breast cancer, vaginal diseases, digestive and respiratory disorders, epilepsy, nervous system issues, and regulating the menstrual cycle (36, 37).

Ducrosia anethifolia, native to Iran and other parts of the Middle East, has essential oils (DaEO) containing bioactive compounds such as simene. These oils exhibit antimicrobial activity against various bacteria and fungi (38, 39). Studies suggest that combining essential oils with complementary antimicrobial properties can create stronger preservation methods compared to using individual oils alone (40-43).

The Capparis spinosa plant, from the Capparidaceae family, is native to the Mediterranean basin and is widely found in Iran (44, 45). This plant contains compounds that contribute to disease prevention and play a role in reducing cancer incidence (46).

2. Methods

The plants used in this research were collected from the plains of Sistan and Baluchistan. Forty grams of dry plant powder were crushed and placed in half-liter jars containing 200 mL of 96% ethanol. These jars were placed on a shaker for 24 hours, then filtered, and the extract was stored in a refrigerator at 4°C.

2.1. Isolation of Bacteria

Stool samples were collected from Zabol city and kept at room temperature for up to 6 hours immediately after collection. The samples were then transferred to selective culture media, including Salmonella-Shigella agar and Simon sulfite agar, and incubated at 37°C for 24 hours. Twelve strains of S. typhimurium were subsequently isolated and identified using differential cultures. The diameter of the inhibition zone of the plant extract was determined using the well diffusion method against S. typhimurium.

3. Results

The results of the study showed that the maximum diameter of the inhibition halo for the Doz ethanolic extract was 8 mm, while the minimum diameter was 1 mm. For fig leaves, the maximum and minimum inhibition diameters were 15 mm and 2 mm, respectively. The musk extract exhibited inhibition diameters ranging from a minimum of 1 mm to a maximum of 18 mm. Additionally, the inhibition diameter for snake grass fruits was recorded as 15 mm (Table 1).

Table 1.

The Diameter of the Inhibition Zone of the Ethanol Extract of Medicinal Plants at a Concentration of 100 mg/mL

Strain BacteriaNannorrhops ritchianaFicus religiosaDucrosia anethifoliaCapparis spinose L. Fruit
12212
23631
31321
43231
518915
68572
7615184
82131
9115413
1031052
113542
1261586

4. Discussion

Many studies have demonstrated a direct relationship between the phenolic and flavonoid content of different plant organs and their antioxidant potential.

In one study investigating the antimicrobial and antifungal effects of Nannorrhops ritchiana leaves, the maximum diameter of the inhibitory halo was observed at a concentration of 300 µg/mL (34). Additionally, the ethanolic fraction of the aerial parts of Nannorrhops ritchiana exhibited significant antifungal activity against Candida albicans, Aspergillus niger, and Microsporum canis, along with moderate inhibition (56%) against Staphylococcus aureus (47). Another study showed that this plant demonstrated good antibacterial effects against Proteus mirabilis, Shigella flexneria, Escherichia coli, and Staphylococcus aureus (48).

In the study by Daing et al., the minimum inhibitory concentration (MIC) for Escherichia coli, Staphylococcus aureus, Salmonella enterica, and Enterococcus faecalis strains was found to be 6.67, 4.17, 5, and 80 mg/mL, respectively (49). Similarly, in the study by Tkachenko et al., the halo created by fig leaf extract in 200 and 400 µl plates of bacterial suspension measured 8.83 mm and 13.42 mm, respectively (50).

A study exploring changes in Ducrosia anethifolia ethanolic extract reported the highest levels of total phenols (148 ± 1.7 mg gallic acid equivalent (GAE) per gram of dry weight) and flavonoids (1.5 ± 97 mg quercetin equivalent (QE) per gram dry weight), along with notable antioxidant, antibacterial, and anti-inflammatory activities (51).

In Almuhanna's study, the methanolic extract of Ducrosia anethifolia demonstrated efficacy against biofilms of methicillin-resistant Staphylococcus aureus (MRSA) and Pseudomonas aeruginosa on cut wounds in diabetic rats. The extract was more effective against MRSA than Pseudomonas aeruginosa in both in vitro and in vivo tests (52). GC-MS analysis of the ethyl acetate fraction of the methanolic extract revealed key compounds such as 8-ethoxy psoralen (6.5%), prongnin (6.26%), isoaromadendrene epoxide (7.5%), aromadendrene oxide (0.96%), and acid methyl ester (0.46%) (53).

In Obaro et al.'s study, the anti-inflammatory properties of palm oil (PO) and the synergistic effects of an aqueous extract polyherbal formulation (AEPHF) containing Zingiber officinale, Curcuma longa, and Allium sativum were evaluated. The results indicated a significant reduction in paw diameter in the treatment groups compared to the control group (P < 0.01) (54).

Eslammanesh's research investigated the relationship among phenol and flavonoid content, antioxidant properties, and antimicrobial activity of methanolic extracts from nine medicinal plants. The results showed that the methanol extract of Nerium oleander contained the highest phenolic content (3.36 mg/g), while Calotropis procera had the lowest (0.48 mg/g). Furthermore, C. procera extract exhibited the most effective antioxidant properties (85.54 mg/mL), whereas Malva sylvestris extract demonstrated the lowest role in inhibiting free radicals (21.80 mg/mL) (55).

4.1. Conclusions

The results of the study showed that medicinal plants with good antimicrobial properties can play a good role in the treatment and control of salmonella bacteria.

Acknowledgements

References

  • 1.

    Ray B, Raha A. Typhoid and Enteric Fevers in Intensive Care Unit. Indian J Crit Care Med. 2021;25(Suppl 2):S144-9. [PubMed ID: 34345129]. [PubMed Central ID: PMC8327799]. https://doi.org/10.5005/jp-journals-10071-23842.

  • 2.

    Informatics G, Berger S; G.S. Team. Infectious Diseases of China. Los Angeles, CA, USA: GIDEON Informatics Inc; 2023.

  • 3.

    Crump JA, Sjolund-Karlsson M, Gordon MA, Parry CM. Epidemiology, Clinical Presentation, Laboratory Diagnosis, Antimicrobial Resistance, and Antimicrobial Management of Invasive Salmonella Infections. Clin Microbiol Rev. 2015;28(4):901-37. [PubMed ID: 26180063]. [PubMed Central ID: PMC4503790]. https://doi.org/10.1128/CMR.00002-15.

  • 4.

    Dougan G, Baker S. Salmonella enterica serovar Typhi and the pathogenesis of typhoid fever. Annu Rev Microbiol. 2014;68:317-36. [PubMed ID: 25208300]. https://doi.org/10.1146/annurev-micro-091313-103739.

  • 5.

    Bhutta ZA, Naqvi SH, Razzaq RA, Farooqui BJ. Multidrug-resistant typhoid in children: presentation and clinical features. Rev Infect Dis. 1991;13(5):832-6. [PubMed ID: 1962094]. https://doi.org/10.1093/clinids/13.5.832.

  • 6.

    Yaramis A, Yildirim I, Katar S, Ozbek MN, Yalçin I, Tas MA, et al. Clinical and laboratory presentation of typhoid fever. Int Pediatrics. 2001;16(4):227-31.

  • 7.

    Kariuki S. Typhoid fever in sub-Saharan Africa: challenges of diagnosis and management of infections. J Infect Dev Ctries. 2008;2(6):443-7. [PubMed ID: 19745521]. https://doi.org/10.3855/jidc.159.

  • 8.

    Akram J, Khan AS, Khan HA, Gilani SA, Akram SJ, Ahmad FJ, et al. Extensively Drug-Resistant (XDR) Typhoid: Evolution, Prevention, and Its Management. Biomed Res Int. 2020;2020:6432580. [PubMed ID: 32462008]. [PubMed Central ID: PMC7212280]. https://doi.org/10.1155/2020/6432580.

  • 9.

    Butt MH, Saleem A, Javed SO, Ullah I, Rehman MU, Islam N, et al. Rising XDR-Typhoid Fever Cases in Pakistan: Are We Heading Back to the Pre-antibiotic Era? Front Public Health. 2021;9:794868. [PubMed ID: 35111719]. [PubMed Central ID: PMC8801676]. https://doi.org/10.3389/fpubh.2021.794868.

  • 10.

    Farooqui A, Khan A, Kazmi SU. Investigation of a community outbreak of typhoid fever associated with drinking water. BMC Public Health. 2009;9:476. [PubMed ID: 20021691]. [PubMed Central ID: PMC2804617]. https://doi.org/10.1186/1471-2458-9-476.

  • 11.

    Yang YA, Chong A, Song J. Why Is Eradicating Typhoid Fever So Challenging: Implications for Vaccine and Therapeutic Design. Vaccines (Basel). 2018;6(3). [PubMed ID: 30042307]. [PubMed Central ID: PMC6160957]. https://doi.org/10.3390/vaccines6030045.

  • 12.

    Levine MM, Simon R. The Gathering Storm: Is Untreatable Typhoid Fever on the Way? mBio. 2018;9(2). [PubMed ID: 29559573]. [PubMed Central ID: PMC5874914]. https://doi.org/10.1128/mBio.00482-18.

  • 13.

    Qamar FN, Yousafzai MT, Khalid M, Kazi AM, Lohana H, Karim S, et al. Outbreak investigation of ceftriaxone-resistant Salmonella enterica serotype Typhi and its risk factors among the general population in Hyderabad, Pakistan: a matched case-control study. Lancet Infect Dis. 2018;18(12):1368-76. [PubMed ID: 30507460]. https://doi.org/10.1016/S1473-3099(18)30483-3.

  • 14.

    Yousafzai MT, Qamar FN, Shakoor S, Saleem K, Lohana H, Karim S, et al. Ceftriaxone-resistant Salmonella Typhi Outbreak in Hyderabad City of Sindh, Pakistan: High Time for the Introduction of Typhoid Conjugate Vaccine. Clin Infect Dis. 2019;68(Suppl 1):S16-21. [PubMed ID: 30767003]. [PubMed Central ID: PMC6376099]. https://doi.org/10.1093/cid/ciy877.

  • 15.

    Nizamuddin S, Ching C, Kamal R, Zaman MH, Sultan F. Continued Outbreak of Ceftriaxone-Resistant Salmonella enterica Serotype Typhi across Pakistan and Assessment of Knowledge and Practices among Healthcare Workers. Am J Trop Med Hyg. 2021;104(4):1265-70. [PubMed ID: 33534746]. [PubMed Central ID: PMC8045622]. https://doi.org/10.4269/ajtmh.20-0783.

  • 16.

    Naseem S, Naseem S, Bashir E, Shirin K, Sheikh SA. Biogeochemical evaluation ofNannorrhops ritchiana: A Mg-flora from Khuzdar, Balochistan, Pakistan. Chinese J Geochem. 2005;24(4):327-37. https://doi.org/10.1007/bf02873795.

  • 17.

    Mussarat S, Abdel-Salam NM, Tariq A, Wazir SM, Ullah R, Adnan M. Use of Ethnomedicinal Plants by the People Living around Indus River. Evid Based Complement Alternat Med. 2014;2014:212634. [PubMed ID: 24778701]. [PubMed Central ID: PMC3979063]. https://doi.org/10.1155/2014/212634.

  • 18.

    Hussain W, Badshah L, Ullah M, Ali M, Ali A, Hussain F. Quantitative study of medicinal plants used by the communities residing in Koh-e-Safaid Range, northern Pakistani-Afghan borders. J Ethnobiol Ethnomed. 2018;14(1):30. [PubMed ID: 29695281]. [PubMed Central ID: PMC5922303]. https://doi.org/10.1186/s13002-018-0229-4.

  • 19.

    Ali M, Hussain K, Ullah M, Ali U, Ullah Khan S, Bussmann RW, et al. Nannorrhops ritchieana (Griff.) Aitch. (Arecaceae) – a traditional multipurpose plant species of Pakistan. Ethnobotany Res Applications. 2020;19. https://doi.org/10.32859/era.19.35.1-10.

  • 20.

    Aziz MA, Adnan M, Khan AH, Rehman AU, Jan R, Khan J. Ethno-medicinal survey of important plants practiced by indigenous community at Ladha subdivision, South Waziristan agency, Pakistan. J Ethnobiol Ethnomed. 2016;12(1):53. [PubMed ID: 27846856]. [PubMed Central ID: PMC5111204]. https://doi.org/10.1186/s13002-016-0126-7.

  • 21.

    Khan SU, Khan FU, Khan IU, Muhammad N, Badshah S, Khan A, et al. Biosorption of nickel (II) and copper (II) ions from aqueous solution using novel biomass derived from Nannorrhops ritchiana (Mazri Palm). Desalination Water Treat. 2016;57(9):3964-74. https://doi.org/10.1080/19443994.2014.989268.

  • 22.

    Adnan M, Ullah I, Tariq A, Murad W, Azizullah A, Khan AL, et al. Ethnomedicine use in the war affected region of northwest Pakistan. J Ethnobiol Ethnomed. 2014;10:16. [PubMed ID: 24484608]. [PubMed Central ID: PMC3932995]. https://doi.org/10.1186/1746-4269-10-16.

  • 23.

    Murad W, Ahmad A, Gilani SA, Khan MA. Indigenous knowledge and folk use of medicinal plants by the tribal communities of Hazar Nao Forest, Malakand District, North Pakistan. J Med Plants Res. 2011;5(7):1072-86.

  • 24.

    Marwat SK, Rehman FU, Usman K, Khakwani AZ, Ghulam S, Anwar N, et al. Medico-ethnobotanical studies of edible wild fruit plants species from the flora of north western Pakistan (DI Khan district). J Med Plants Res. 2011;5(16):3679-86.

  • 25.

    Khalid S, Shah SZ. Plants That No Body Wanted: An Assessment of the Conservation Status of Plant in Mohmand Agency FATA, Pakistan. J Biodiv Environment Sci (JBES). 2016;8:195-205.

  • 26.

    Ullah A. Diversity of Life Form And Leaf Size Classes at Sheikh Buddin National Park, Dera Ismail Khan, Khyber Pakhtunkhwa, Pakistan. South Asian J Life Sci. 2015;1(1):6-13. https://doi.org/10.14737/journal.sajls/2015/3.1.6.13.

  • 27.

    Mosti S, Raffaelli M, Tardelli M. A contribution to the flora of Wadi Andur (Dhofar, Southern Oman). Webbia. 2006;61(2):253-60. https://doi.org/10.1080/00837792.2006.10670805.

  • 28.

    Ajaib M, Khan Q, Khan Z. A contribution to the ethnobotanical studies of some plants of Loralai District, Baluchistan. Biologia (Pakistan). 2013;59(2):323-7.

  • 29.

    Panhwar AQ, Abro HIDAYTULLAH. Ethnobotanical studies of Mahal Kohistan (Khirthar national park). Pak J Bot. 2007;39(7):2301-15.

  • 30.

    Naseem S, Bashir E, Ahmed P, Rafique T, Hamza S, Kaleem M. Impact of Seawater Intrusion on the Geochemistry of Groundwater of Gwadar District, Balochistan and Its Appraisal for Drinking Water Quality. Arabian J Sci Engineering. 2017;43(1):281-93. https://doi.org/10.1007/s13369-017-2679-8.

  • 31.

    Thomas R, Tengberg M, Moulhérat C, Marcon V, Besenval R. Analysis of a protohistoric net from Shahi Tump, Baluchistan (Pakistan). Archaeolog Anthropolog Sci. 2011;4(1):15-23. https://doi.org/10.1007/s12520-011-0078-8.

  • 32.

    Haq ZU, Khan SM; Abdullah. The indispensable bond between Mazri Palm (Nannorrhops ritchiana) and the Indian Porcupine (Hystrix indica) leads them towards extinction!. Biodiversity Conservation. 2019;28(12):3387-8. https://doi.org/10.1007/s10531-019-01823-7.

  • 33.

    Goodman SM, Ghafoor A. The ethnobotany of southern Balochistan, Pakistan : with particular reference to medicinal plants. Chicago, IL 60605, United States: Field Museum of Natural History; 1992. https://doi.org/10.5962/bhl.title.2542.

  • 34.

    Mahmood A. Phytochemical Analysis and Comprehensive Evaluation of Antimicrobial Activity of Nannorhops Ritchiana Leaves (Mazari Palm). World J Pharm Pharmaceutical Sci. 2017:173-89. https://doi.org/10.20959/wjpps20176-9336.

  • 35.

    Hesami M, Tohidfar M, Alizadeh M, Daneshvar MH. Effects of sodium nitroprusside on callus browning of Ficus religiosa: an important medicinal plant. J Forestry Res. 2018;31(3):789-96. https://doi.org/10.1007/s11676-018-0860-x.

  • 36.

    Priyanka K, Sahu PL, Singh S. Optimization of processing parameters for the development of Ficus religiosa L. extract loaded solid lipid nanoparticles using central composite design and evaluation of antidiabetic efficacy. J Drug Delivery Sci Technol. 2018;43:94-102. https://doi.org/10.1016/j.jddst.2017.08.006.

  • 37.

    Suriyakalaa U, Ramachandran R, Doulathunnisa JA, Aseervatham SB, Sankarganesh D, Kamalakkannan S, et al. Upregulation of Cyp19a1 and PPAR-gamma in ovarian steroidogenic pathway by Ficus religiosa: A potential cure for polycystic ovary syndrome. J Ethnopharmacol. 2021;267:113540. [PubMed ID: 33152430]. https://doi.org/10.1016/j.jep.2020.113540.

  • 38.

    Mahboubi M, Feizabadi MM. Antimicrobial Activity ofDucrosia anethifoliaEssential Oil and Main Component, Decanal Against Methicillin-Resistant and Methicillin-SusceptibleStaphylococcus aureus. J Essential Oil Bearing Plants. 2009;12(5):574-9. https://doi.org/10.1080/0972060x.2009.10643760.

  • 39.

    Shahabipour S, Firuzi O, Asadollahi M, Faghihmirzaei E, Javidnia K. Essential oil composition and cytotoxic activity ofDucrosia anethifoliaandDucrosia flabellifoliafrom Iran. J Essential Oil Res. 2013;25(2):160-3. https://doi.org/10.1080/10412905.2013.773656.

  • 40.

    Alizadeh behbahani B, Noshad M, Falah F. The combined effect of the combined Fennel and Clove essential oils on Staphylococcus epidermidis, Bacillus cereus, Salmonella typhi and Enterobacter aerogenes using Checkerboard assay (fractional inhibitory concentration index). Food Sci Technol. 2020;17(106):75-83. https://doi.org/10.52547/fsct.17.106.75.

  • 41.

    Bassole IH, Juliani HR. Essential oils in combination and their antimicrobial properties. Molecules. 2012;17(4):3989-4006. [PubMed ID: 22469594]. [PubMed Central ID: PMC6268925]. https://doi.org/10.3390/molecules17043989.

  • 42.

    Targino de Souza Pedrosa G, Pimentel TC, Gavahian M, Lucena de Medeiros L, Pagán R, Magnani M. The combined effect of essential oils and emerging technologies on food safety and quality. Lwt. 2021;147. https://doi.org/10.1016/j.lwt.2021.111593.

  • 43.

    Yangilar F, Yildiz PO. Effects of using combined essential oils on quality parameters of bio-yogurt. J Food Process Preservation. 2018;42(1). https://doi.org/10.1111/jfpp.13332.

  • 44.

    Hall JC, Sytsma KJ, Iltis HH. Phylogeny of Capparaceae and Brassicaceae based on chloroplast sequence data. Am J Bot. 2002;89(11):1826-42. [PubMed ID: 21665611]. https://doi.org/10.3732/ajb.89.11.1826.

  • 45.

    Ramezani-Gask M, Bahrani MJ, Shekafandeh A, Salehi H, Taghvaei M, Al-Ahmadi MJ. A comparison of different propagation methods of common Caper-bush (Capparis spinosa L.) as a new horticultural crop. Int J Plant Dev Biol. 2008;2:106-10.

  • 46.

    Çaliş İ, Kuruüzüm A, Rüedi P. 1H-Indole-3 acetonitrile glycosides from Capparis spinosa fruits. Phytochemistry. 1999;50(7):1205-8. https://doi.org/10.1016/s0031-9422(98)00669-4.

  • 47.

    Zeeshan M. Phytochemical and pharmacological studies of aerial parts of nannorrhops ritchiana [dissertation]. The Islamia University of Bahawalpur Pakistan; 2019.

  • 48.

    Dehghani M, Beyzaei H, Ebrahimnezhad Z. Chemical Composition, Antioxidant Potential, and Antimicrobial Activity of Nannorrhops ritchiana (Griff) Aitch. Arch Advances Biosci. 2023;14(1):9-1.

  • 49.

    Daing I, Pathak AK, Bhat A, Sharma RK, Zargar A. In vitro Antioxidant and Antibacterial Efficacy of Condensed Tannins Containing Tree Leaves Extract of Jammu Province. J Animal Res. 2017;7(1). https://doi.org/10.5958/2277-940x.2017.00023.7.

  • 50.

    Tkachenko H, Buyun L, Terech-Majewska E, Honcharenko V, Prokopiv A, Osadowski Z. Preliminary in vitro screening of the antibacterial activity of leaf extracts from various Ficus species (Moraceae) against Yersinia ruckeri. Fisheries Aquatic Life. 2019;27(1):15-26. https://doi.org/10.2478/aopf-2019-0002.

  • 51.

    Sharifi-Rad M. [Evaluation of phytochemical, antioxidant, antibacterial and anti-inflammatory properties of Moshgak (Ducrosia anethifolia (DC.) Boiss.) at different phenological stages]. Iran J Med Aromatic Plants Res. 2022;37(6):971-88. FA. https://doi.org/10.22092/ijmapr.2021.355808.3056.

  • 52.

    Almuhanna Y. Effect of Ducrosia anethifolia methanol extract against methicillin resistant Staphylococcus aureus and Pseudomonas aeruginosa biofilms on excision wound in diabetic mice. Frontiers Cell Infection Microbiol. 2024;14:1386483.

  • 53.

    Elsharkawy ER, Abdallah EM, Shiboob MH, Alghanem S. Phytochemical, antioxidant and antibacterial potential of Ducrosia anethifolia in northern border region of Saudi Arabia. J Pharm Res Int. 2019;31:1-8.

  • 54.

    Obaro PO, Obaro-Onezeyi OE, Dike AM. Synergistic Anti-Inflammatory Effect of a Polyherbal Formulation and Palm Oil on Induced Inflammatory Models in Albino Wistar Rats. Res Biotechnol Environmental Sci. 2024;3(3):39-45. https://doi.org/10.58803/rbes.v3i3.49.

  • 55.

    Eslammanesh T, Rezaei M, Dahmardeh N, Anoosha A. Investigation of the Antimicrobial Activity of Nine Medicinal Plants on Standard Bacteria. Res Biotechnol Envir Sci. 2024;3(2):29-38. https://doi.org/10.58803/rbes.v3i2.47.