Phenotypic and Molecular Characterization of Antimicrobial Resistance and Virulence Determinants in Pseudomonas aeruginosa Isolated from Burn Patients
DOI:
https://doi.org/10.23851/mjs.v37i2.1864Keywords:
Pseudomonas aeruginosa, Burns, Antibiotics, Virulence genes, ESBLAbstract
Background: The pathogen “Pseudomonas aeruginosa (P. aeruginosa)” is extremely hazardous for people with weak immune systems because it has several virulence factors and can resist antibiotics. Objective: To isolate and molecularly identify P. aeruginosa from burn and wound infections and to evaluate its antimicrobial resistance patterns, ESBL production, and virulence characteristics. Methods: A total of 150 burn and wound samples were collected from patients at Erbil West Emergency Hospital and processed immediately. P. aeruginosa was isolated using selective media and confirmed molecularly by PCR targeting rpoB and oprL genes. Virulence genes (nan1, plcH, exoT, toxA, aprA) were detected by PCR. Antimicrobial susceptibility testing was performed against 14 antibiotics using the disk diffusion method. ESBL production was detected using the Double Disc Synergy Test (DDST). Hemolytic and proteolytic activities were evaluated using blood agar and skim milk agar, respectively, while pigment production was assessed on cetrimide agar. Results: Out of 150 samples, 40 P. aeruginosa isolates were identified. Imipenem showed the highest efficacy, while complete resistance was observed against AMP, CTX, P, AMC, and C. Resistance rates were ATM (32.5%), MEM (42.5%), TOB, AK, and CN (45%), CIP (62.5%), CAZ (67.5%), and TE (80%). ESBL production was detected in 26 isolates (65%). β-hemolysis was observed in 25 isolates (62.5%), and strong proteolytic activity was detected in 35 isolates (87.5%). Typical pigment production was observed on cetrimide agar. Conclusions: The study reveals a high prevalence of MDR and ESBL-producing P. aeruginosa with considerable virulence potential in burns and wounds. Imipenem still holds its position as the most promising therapeutic agent; this emphasizes the need for continuous surveillance and proper antibiotic use.
Downloads
References
N. Ahmed, Z. Ali, M. Riaz, B. Zeshan, J. I. Wattoo, and M. N. Aslam, “Evaluation of antibiotic resistance and virulence genes among clinical isolates of Pseudomonas aeruginosa from cancer patients,” Asian Pacific Journal of Cancer Prevention, vol. 21, no. 5, pp. 1333–1338, 2020.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.31557/APJCP.2020.21.5.1333
R. Gharieb, M. Saad, M. Khedr, A. El Gohary, and H. Ibrahim, “Occurrence, virulence, carbapenem resistance, susceptibility to disinfectants and public health hazard of Pseudomonas aeruginosa isolated from animals, humans and environment in intensive farms,” Journal of Applied Microbiology, vol. 132, no. 1, pp. 256–267, 2021.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1111/jam.15191
N. Sathe, P. Beech, L. Croft, C. Suphioglu, A. Kapat, and E. Athan, “Pseudomonas aeruginosa: Infections and novel approaches to treatment ‘knowing the enemy’ the threat of Pseudomonas aeruginosa and exploring novel approaches to treatment,” Infectious Medicine, vol. 2, no. 3, pp. 178–194, 2023.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1016/j.imj.2023.05.003
M. D. Younus, O. F. Bahjat, and S. A. Rashid, “Antibiotic susceptibility pattern, molecular characterization of virulence genes among Pseudomonas aeruginosa isolated from burn patients,” Cihan University-Erbil Scientific Journal, vol. 5, no. 1, pp. 36–41, 2021.
CrossRef | Google Scholar DOI: https://doi.org/10.24086/cuesj.v5n1y2021.pp36-41
M. D. Younus, Z. F. A. Abdulrahman, O. F. Bahjat, N. L. Ali, S. A. Rashid, and A. S. Alkhouri, “Plasmid profiling, genetic site determination of antibiotic resistance gene of Pseudomonas aeruginosa isolated from burned patients,” in 4th International Conference on Biological & Health Sciences (CIC-BIOHS’2022), Cihan University-Erbil, Jul. 2022, pp. 68–75.
CrossRef | Google Scholar DOI: https://doi.org/10.24086/biohs2022/paper.538
R. F. Polse, H. M. Khalid, and W. M. S. Mero, “Distribution of blaOXA-10, blaPER-1, and blaSHV genes in ESBL-producing Pseudomonas aeruginosa strains isolated from burn patients,” Scientific Reports, vol. 13, no. 1, Art no. 18402, 2023.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1038/s41598-023-45417-4
F. Piri, K. Amini, and M. Mohammadi, “Inhibitory effect of iron oxide nanoparticles on CTX-M gene expression in extended-spectrum βeta-lactamase-producing Pseudomonas aeruginosa isolated from burn patients,” Journal of Advances in Medical and Biomedical Research, vol. 30, no. 140, pp. 289–294, 2022.
CrossRef | Google Scholar DOI: https://doi.org/10.30699/jambs.30.140.289
M. K. Pattanayak, S. Tomar, A. Gaur, and S. Goel, “Phenotypic detection of multidrug-resistance Pseudomonas aeruginosa isolated from various clinical samples,” International Journal of Health Sciences, vol. 6, no. S6, pp. 883–893, 2022.
CrossRef | Google Scholar
T. Wang, X. Du, L. Ji, Y. Han, J. Dang, J. Wen, Y. Wang, Q. Pu, M. Wu, and H. Liang, “Pseudomonas aeruginosa T6SS-mediated molybdate transport contributes to bacterial competition during anaerobiosis,” Cell Reports, vol. 35, no. 2, Art no. 108957, 2021.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1016/j.celrep.2021.108957
M. T. Jasim, A. F. A. Alzubaidi, and S. M. D. Al-Rubaye, “Isolation and identification of Staphylococcus aureus and Pseudomonas aeruginosa bacteria from burns and wounds patients in Diyala governorate,” International Journal of Health Sciences, vol. 6, no. S9, pp. 273–282, 2022.
CrossRef | Google Scholar DOI: https://doi.org/10.53730/ijhs.v6nS9.12222
B. Magalhães, B. Valot, M. M. H. Abdelbary, G. Prod’hom, G. Greub, L. Senn, and D. S. Blanc, “Combining standard molecular typing and whole genome sequencing to investigate Pseudomonas aeruginosa epidemiology in intensive care units,” Frontiers in Public Health, vol. 8, Art no. 3, Jan. 2020.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.3389/fpubh.2020.00003
V. B. Nehmatulla, “Isolation and identification of Candida species and some superficial mycosis associated with diaper dermatitis in Erbil city,” Polytechnic Journal, vol. 11, no. 1, pp. 98–103, 2021.
CrossRef | Google Scholar DOI: https://doi.org/10.25156/ptj.v11n1y2021.pp98-103
M. Kaur and M.-P. Mingeot-Leclercq, “Maintenance of bacterial outer membrane lipid asymmetry: Insight into MlaA,” BMC Microbiology, vol. 24, no. 1, Art no. 186, 2024.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1186/s12866-023-03138-8
M. A. Khattab, M. S. Nour, and N. M. ElSheshtawy, “Genetic identification of Pseudomonas aeruginosa virulence genes among different isolates,” Journal of Microbial & Biochemical Technology, vol. 7, no. 5, pp. 274–277, 2015.
CrossRef | Google Scholar
I. Mitov, T. Strateva, and B. Markova, “Prevalence of virulence genes among Bulgarian nosocomial and cystic fibrosis isolates of Pseudomonas aeruginosa,” Brazilian Journal of Microbiology, vol. 41, no. 3, pp. 588–595, 2010.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1590/S1517-83822010000300008
F. Faraji, M. Mahzounieh, A. Ebrahimi, F. Fallah, O. Teymournejad, and B. Lajevardi, “Molecular detection of virulence genes in Pseudomonas aeruginosa isolated from children with cystic fibrosis and burn wounds in Iran,” Microbial Pathogenesis, vol. 99, pp. 1–4, Oct. 2016.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1016/j.micpath.2016.07.013
B. Noomi, “Detection of virulence factors of Pseudomonas aeruginosa in different animals by using bacteriological and molecular methods,” Iraqi Journal of Veterinary Sciences, vol. 32, no. 2, pp. 205–210, 2019.
CrossRef | Google Scholar DOI: https://doi.org/10.33899/ijvs.2019.153851
I. S. Aljebory, “Genetic detection and identification of some virulence factors genes among Pseudomonas aeruginosa samples in Kirkuk province – Iraq,” International Journal of Pharmaceutical Quality Assurance, vol. 10, no. 3, pp. 147–150, 2019.
CrossRef DOI: https://doi.org/10.25258/ijpqa.10.3.8
A. I. Cotar, M. C. Chifiriuc, O. Banu, and V. Lazar, “Molecular characterization of virulence patterns in Pseudomonas aeruginosa strains isolated from respiratory and wound samples,” Biointerface Research in Applied Chemistry, vol. 3, no. 2, pp. 551–558, 2013.
Google Scholar | Link
G. İnat, B. Sırıken, C. Başkan, İ. Erol, T. Yıldırım, and A. Çiftci, "Quorum sensing systems and related virulence factors in Pseudomonas aeruginosa isolated from chicken meat and ground beef," Scientific Reports, vol. 11, no. 1, Art no. 15639, 2021.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1038/s41598-021-94906-x
S. Phan, C. H. Feng, R. Huang, Z. X. Lee, Y. Moua, O. J. Phung, and J. R. Lenhard, "Relative abundance and detection of Pseudomonas aeruginosa from chronic wound infections globally," Microorganisms, vol. 11, no. 5, Art no. 1210, 2023.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.3390/microorganisms11051210
M. Lichtenberg, T. H. Jakobsen, M. Kühl, M. Kolpen, P. Ø. Jensen, and T. Bjarnsholt, "The structure-function relationship of Pseudomonas aeruginosa in infections and its influence on the microenvironment," FEMS Microbiology Reviews, vol. 46, no. 5, Art no. fuac018, 2022.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1093/femsre/fuac018
N. Mathlouthi, C. Al-Bayssari, A. El Salabi, S. Bakour, S. Ben Gwierif, A. A. Zorgani, Y. Jridi, K. Ben Slama, J.-M. Rolain, and C. Chouchani, "Carbapenemases and extended-spectrum β-lactamases producing Enterobacteriaceae isolated from Tunisian and Libyan hospitals," The Journal of Infection in Developing Countries, vol. 10, no. 7, pp. 718-727, 2016.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.3855/jidc.7426
S. N. Mahaseth, L. Chaurasia, B. Jha, and R. K. Sanjana, "Prevalence and antimicrobial susceptibility pattern of Pseudomonas aeruginosa isolated from various clinical samples in a tertiary care hospital," Janaki Medical College Journal of Medical Science, vol. 8, no. 2, pp. 11-17, 2020.
CrossRef | Google Scholar DOI: https://doi.org/10.3126/jmcjms.v8i2.33972
B. L. Aghaee, M. Khan Mirzaei, M. Y. Alikhani, A. Mojtahedi, and C. F. Maurice, "Improving the inhibitory effect of phages against Pseudomonas aeruginosa isolated from a burn patient using a combination of phages and antibiotics," Viruses, vol. 13, no. 2, Art no. 334, 2021.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.3390/v13020334
B. Hosien, H. Belhaj, and A. Atia, "Characteristics of antibiotic-resistant bacteria in Libya based on different source of infections," Libyan International Medical University Journal, vol. 7, no. 2, pp. 039-044, 2022.
CrossRef | Google Scholar DOI: https://doi.org/10.1055/s-0042-1759621
A. Radhika, J. Lakshmi, K. Ariyanachi, and V. Sakthivadivel, "Detection of metallo beta-lactamase (MBL) producing Pseudomonas aeruginosa in a Tertiary Care Hospital, Ghanpur, Medchal, India," Maedica - A Journal of Clinical Medicine, vol. 17, no. 1, pp. 134-142, 2022.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.26574/maedica.2022.17.1.134
N. S. Budayanti, D. N. Aisyah, N. N. D. Fatmawati, N. M. A. Tarini, Z. Kozlakidis, and W. Adisasmito, "Identification and distribution of pathogens in a major tertiary hospital of Indonesia," Frontiers in Public Health, vol. 7, Art no. 395, Jan. 2020.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.3389/fpubh.2019.00395
M. B. Sannathimmappa, V. Nambiar, R. Aravindakshan, and N. M. Al-Kasaby, "Profile and antibiotic-resistance pattern of bacteria isolated from endotracheal secretions of mechanically ventilated patients at a tertiary care hospital," Journal of Education and Health Promotion, vol. 10, no. 1, Art no. 195, 2021.
CrossRef | Google Scholar DOI: https://doi.org/10.4103/jehp.jehp_1517_20
J. Alamu, L. Kakithakara Vajravelu, B. Venkatesan, and J. Thulukanam, "Correlation of phenotypic and genotypic virulence markers, antimicrobial susceptibility pattern, and outcome of Pseudomonas aeruginosa sepsis infection," Microbial Pathogenesis, vol. 170, Art no. 105716, Sep. 2022.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1016/j.micpath.2022.105716
Z. Asmare, M. A. Reta, Y. Gashaw, E. Getachew, A. Sisay, M. Gashaw, E. Tamrat, A. A. Kidie, W. Abebe, T. Misganaw, et al., "Antimicrobial resistance profile of Pseudomonas aeruginosa clinical isolates from healthcare-associated infections in Ethiopia: A systematic review and meta-analysis," PLOS ONE, vol. 19, no. 8, Art no. e0308946, 2024.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1371/journal.pone.0308946
B. Schwartz, K. Klamer, J. Zimmerman, P. B. Kale-Pradhan, and A. Bhargava, "Multidrug resistant Pseudomonas aeruginosa in clinical settings: A review of resistance mechanisms and treatment strategies," Pathogens, vol. 13, no. 11, Art no. 975, 2024.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.3390/pathogens13110975
A. E. Laudy, P. Róg, K. Smolińska-Król, M. Ćmiel, A. Słoczyńska, J. Patzer, D. Dzierżanowska, R. Wolinowska, B. Starościak, and S. Tyski, "Prevalence of ESBL-producing Pseudomonas aeruginosa isolates in Warsaw, Poland, detected by various phenotypic and genotypic methods," PLOS ONE, vol. 12, no. 6, Art no. e0180121, 2017.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1371/journal.pone.0180121
S. Mushtaq, D. Meunier, A. Vickers, N. Woodford, and D. M. Livermore, "Activity of imipenem/relebactam against Pseudomonas aeruginosa producing ESBLs and carbapenemases," Journal of Antimicrobial Chemotherapy, vol. 76, no. 2, pp. 434-442, 2020.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1093/jac/dkaa456
A. C. Gales, G. Stone, D. F. Sahm, M. G. Wise, and E. Utt, "Incidence of ESBLs and carbapenemases among Enterobacterales and carbapenemases in Pseudomonas aeruginosa isolates collected globally: Results from ATLAS 2017-2019," Journal of Antimicrobial Chemotherapy, vol. 78, no. 7, pp. 1606-1615, 2023.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1093/jac/dkad127
M. S. Rezai, F. Ahangarkani, A. Rafiei, A. Hajalibeig, and M. Bagheri-Nesami, "Extended-Spectrum beta-lactamases producing Pseudomonas aeruginosa isolated from patients with ventilator associated nosocomial infection," Archives of Clinical Infectious Diseases, vol. 13, no. 4, Art no. e13974, 2018.
CrossRef | Google Scholar DOI: https://doi.org/10.5812/archcid.13974
M. F. Kengne, A. T. Mbaveng, O. Karimo, B. S. T. Dadjo, O. D. Tsobeng, W. J. T. Marbou, and V. Kuete, "Frequency of fecal carriage of ESBL resistance genes in multidrug-resistant Pseudomonas aeruginosa isolates from cancer patients at Laquintinie Hospital, Douala, Littoral Region, Cameroon," International Journal of Microbiology, vol. 2024, no. 1, Art no. 7685878, 2024.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1155/2024/7685878
N. Saleh, H. U. Abdu, and I. Yusuf, "Disinfectant activity of Eucalyptus globulus leaves extracts against MRSA and ESBL producing Pseudomonas aeruginosa isolated from hospital environment," Bima Journal of Science and Technology Gombe, vol. 8, no. 2A, pp. 65-73, 2024.
CrossRef | Google Scholar
W. O. Ordu, C. Mbata, and M. T. Pius, "Molecular profiling of antibiotic-resistant Pseudomonas aeruginosa isolated from patients with urinary tract infections in Rivers State University teaching hospital," International Journal of Pathogen Research, vol. 14, no. 1, pp. 27-41, 2025.
CrossRef | Google Scholar DOI: https://doi.org/10.9734/ijpr/2025/v14i1338
A. A. Elnegery, W. K. Mowafy, T. A. Zahra, and N. T. Abou El-Khier, "Study of quorum-sensing LasR and RhlR genes and their dependent virulence factors in Pseudomonas aeruginosa isolates from infected burn wounds," Access Microbiology, vol. 3, no. 3, Art no. 211, 2021.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1099/acmi.0.000211
D. Zhang, J. Palmer, K. H. Teh, M. M. A. Calinisan, and S. Flint, "Milk fat influences proteolytic enzyme activity of dairy pseudomonas species," International Journal of Food Microbiology, vol. 320, Art no. 108543, May 2020.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1016/j.ijfoodmicro.2020.108543
S. Grbavčić, D. Bezbradica, L. Izrael-Živković, N. Avramović, N. Milosavić, I. Karadžić, and Z. Knežević-Jugović, "Production of lipase and protease from an indigenous Pseudomonas aeruginosa strain and their evaluation as detergent additives: compatibility study with detergent ingredients and washing performance," Bioresource Technology, vol. 102, no. 24, pp. 11226-11233, 2011.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1016/j.biortech.2011.09.076
M. R. Marwa, A.-T. Marwa, and E. A. Amal, "Phenotypic and genotypic characterization of Pseudomonas aeruginosa isolates from Egyptian hospitals," African Journal of Microbiology Research, vol. 10, no. 39, pp. 1645-1653, 2016.
CrossRef | Google Scholar DOI: https://doi.org/10.5897/AJMR2016.8254
R. EL-Mahdy and G. El-Kannishy, "Virulence factors of carbapenem-resistant Pseudomonas aeruginosa in hospital-acquired infections in Mansoura, Egypt," Infection and Drug Resistance, vol. 12, pp. 3455-3461, Nov. 2019.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.2147/IDR.S222329
W. F. Mohamed, A. A. Askora, M. M. H. Mahdy, E. A. EL-Hussieny, and H. M. Abu-Shady, "Isolation and characterization of bacteriophages active against Pseudomonas aeruginosa strains isolated from diabetic foot infections," Archives of Razi Institute, vol. 77, no. 6, pp. 2187-2200, 2022.
CrossRef | Google Scholar
D. Sperandio, G. Rossignol, J. Guerillon, N. Connil, N. Orange, M. G. Feuilloley, and A. Merieau, "Cell-associated hemolysis activity in the clinical strain of Pseudomonas fluorescens MFN1032," BMC Microbiology, vol. 10, no. 1, Art no. 124, 2010.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1186/1471-2180-10-124
I. M. Jawher and M. G. Hasan, "Molecular identification of Pseudomonas aeruginosa in meat at Mosul city retails using PCR technique," Iraqi Journal of Veterinary Sciences, vol. 36, no. 4, pp. 1083-1087, 2022.
CrossRef | Google Scholar DOI: https://doi.org/10.33899/ijvs.2022.133086.2173
M. D. Y. Ali and Z. Abdulrahman, "Molecular identification, susceptibility pattern, and detection of some virulence genes in Pseudomonas aeruginosa isolated from burn patients," Plant Archives, vol. 20, no. 1, pp. 2573-2580, 2020.
Google Scholar | Link
R. Lavenir, D. Jocktane, F. Laurent, S. Nazaret, and B. Cournoyer, "Improved reliability of Pseudomonas aeruginosa PCR detection by the use of the species-specific ecfX gene target," Journal of Microbiological Methods, vol. 70, no. 1, pp. 20-29, 2007.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1016/j.mimet.2007.03.008
V. Nikbin, M. M. Aslani, Z. Sharafi, M. Hashemipour, F. Shahcheraghi, and G. Ebrahimipour, "Molecular identification and detection of virulence genes among Pseudomonas aeruginosa isolated from different infectious origins," Iranian Journal of Microbiology, vol. 4, no. 3, pp. 118-123, 2012.
Google Scholar | Link
N. El Husseini, J. A. Carter, and V. T. Lee, "Urinary tract infections and catheter-associated urinary tract infections caused by Pseudomonas aeruginosa," Microbiology and Molecular Biology Reviews, vol. 88, no. 4, Art no. e00066-22, 2024.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1128/mmbr.00066-22
A. K. Jasim and A. A. Hussein, "Detection genotyping virulence factor among Pseudomonas aeruginosa isolated from burns patients," International Journal of Advanced Multidisciplinary Research and Studies, vol. 3, no. 4, pp. 1209-1214, 2023.
Google Scholar | Link
J. R. Mackinder, L. A. Hinkel, K. Schutz, K. Eckstrom, K. Fisher, and M. J. Wargo, "Sphingosine induction of the Pseudomonas aeruginosa hemolytic phospholipase C/sphingomyelinase (PlcH)," Journal of Bacteriology, vol. 206, no. 3, Art no. e00382-23, 2024.
CrossRef | Google Scholar | PubMed
E. A. Edward, M. R. El Shehawy, A. Abouelfetouh, and E. Aboulmagd, "Prevalence of different virulence factors and their association with antimicrobial resistance among Pseudomonas aeruginosa clinical isolates from Egypt," BMC Microbiology, vol. 23, no. 1, Art no. 161, 2023.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1186/s12866-023-02897-8
I. Jurado-Martín, M. Sainz-Mejías, and S. McClean, "Pseudomonas aeruginosa: An audacious pathogen with an adaptable arsenal of virulence factors," International Journal of Molecular Sciences, vol. 22, no. 6, Art no. 3128, 2021.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.3390/ijms22063128
J. N. Carey, S. Lamont, D. J. Wozniak, A. A. Dandekar, and M. R. Parsek, "Quorum sensing regulation of Psl polysaccharide production by Pseudomonas aeruginosa," Journal of Bacteriology, vol. 206, no. 12, Art no. e00312-24, 2024.
CrossRef | Google Scholar | PubMed DOI: https://doi.org/10.1128/jb.00312-24
Downloads
Key Dates
Received
Revised
Accepted
Published
Data Availability Statement
The data that support the findings of this study are available from the corresponding authors upon reasonable request.
Issue
Section
License
Copyright (c) 2026 Maad Abdulla Mansur, Mohammed Hakeem Khalaf

This work is licensed under a Creative Commons Attribution 4.0 International License.
(Starting May 5, 2024) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution (CC-BY) 4.0 License that allows others to share the work with an acknowledgement of the work’s authorship and initial publication in this journal.














