Antibiotic susceptibility and biofilm forming ability of Staphylococcus aureus isolated from Jordanian patients with diabetic foot ulcer
-
Dima Owais
,
Rania M. Al-Groom
,
Tareq Nayef AlRamadneh
,
Laila Alsawalha
,
Mohd Sajjad Ahmad Khan
,
Omar H. Yousef
,
Shereen Z. Burjaq
Abstract
Background and Objectives: Microbial biofilm is characterized by the irreversible attachment of planktonic cells to a surface and is usually associated with high antimicrobial resistance with worsening the wound healing. The objective of the study was to determine the prevalence of Staphylococcus aureus in diabetic foot ulcers (DFUs) of diabetic patients and to investigate antibiotic susceptibility patterns of these isolates. In addition to screen biofilm forming ability of isolated S. aureus.
Materials and Methods: A total of 112 non-healing wound swabs of diabetic foot patients were collected and cultured on different culture media to identify and characterize 98 isolates. The S. aureus isolates were examined for their antibiotic susceptibility to different antimicrobial agents. Furthermore, S. aureus isolates were evaluated for their biofilm production capability using the Tissue Culture Plate Method (TPC). The level of icaA gene expression was determined by RT-PCR.
Results: The results of this study showed that these non-healing wounds yield positive cultures, with an average of 1.67 organisms per sample. The isolates showed highest resistance against oxacillin (95.2%) and lowest resistance against linezolid (3.7%). All isolates were biofilm producers and a significant association with the icaA gene expression level was recorded.
Conclusion: This study showed that S. aureus isolates have a great ability to produce biofilms that are associated with the chronicity of wounds in diabetic patients. Routine screening for biofilm formers in chronic wounds and their antibiotic susceptibility testing will help in early treatment and prevent any other complications.
1. Halim M, Halim A. The effects of inflammation, aging and oxidative stress on the pathogenesis of diabetes mellitus (type 2 diabetes). Diabetes Metab Syndr 2019; 13: 1165-1172.
2. Bowers S, Franco E. Chronic wounds: evaluation and management. Am Fam Physician 2020; 101: 159-166.
3. James GA, Swogger E, Wolcott R, Pulcini Ed, Secor P, Sestrich J, et al. Biofilms in chronic wounds. Wound Repair Regen 2008; 16: 37-44.
4. Fekadu G, Bula K, Bayisa G, Turi E, Tolossa T, Kasaye HK. Challenges and factors associated with poor glycemic control among type 2 diabetes mellitus patients at Nekemte Referral Hospital, Western Ethiopia. J Multidiscip Healthc 2019; 12: 963-974.
5. Moore Z, Avsar P, Wilson P, Mairghani M, O’Connor T, Nugent L, et al. Diabetic foot ulcers: treatment overview and cost considerations. J Wound Care 2021; 30: 786-791.
6. Ena J, Carretero-Gomez J, Arevalo-Lorido JC, Sanchez-Ardila C, Zapatero-Gaviria A, Gomez-Huelgas R. The association between elevated foot skin temperature and the incidence of diabetic foot ulcers: a meta-analysis. Int J Low Extrem Wounds 2021; 20: 111-1118.
7. Porselvi A, Uma Shankar MS, Lakshmi KS, Sankar V. A retrospective qualitative study on current diabetic foot ulcer management and discussion on extended role of clinical pharmacist. Marmara Pharm J 2017; 21: 412-418.
8. Giurato L, Meloni M, Izzo V, Uccioli L. Osteomyelitis in diabetic foot: a comprehensive overview. World J Diabetes 2017; 8: 135-142.
9. Maheswary T, Nurul AA, Fauzi MB. The insights of microbes’ roles in wound healing: A comprehensive review. Pharmaceutics 2021; 13: 981.
10. Rubio JA, Jiménez S, Lázaro-Martínez JL. Mortality in patients with diabetic foot ulcers: causes, risk factors, and their association with evolution and severity of ulcer. J Clin Med 2020; 9: 3009.
11. Polikandrioti M, Vasilopoulos G, Koutelekos I, Panoutsopoulos G, Gerogianni G, Babatsikou F, et al. Quality of life in diabetic foot ulcer: associated factors and the impact of anxiety/depression and adherence to self-care. Int J Low Extrem Wounds 2020; 19: 165-179.
12. Alfonsi V, Gorgoni M, Scarpelli S, Zivi P, Sdoia S, Mari E, et al. Changes in sleep pattern and dream activity across and after the COVID‐19 lockdown in Italy: A longitudinal observational study. J Sleep Res 2022; 31(2): e13500.
13. Matta-Gutierrez G, Garcia-Morales E, Garcia-Alvarez Y, Álvaro-Afonso FJ, Molines-Barroso RJ, Lazaro-Martinez JL. The influence of multidrug-resistant bacteria on clinical outcomes of diabetic foot ulcers: a systematic review. J Clin Med 2021; 10: 1948.
14. Seo KS, Park N, Rutter JK, Park Y, Baker CL, Thornton JA, et al. Role of Glucose-6-phosphate in metabolic adaptation of Staphylococcus aureus in diabetes. Microbiol Spectr 2021; 9(2): e0085721.
15. Shettigar K, Jain S, Bhat DV, Acharya R, Ramachandra L, Satyamoorthy K, et al. Virulence determinants in clinical Staphylococcus aureus from monomicrobial and polymicrobial infections of diabetic foot ulcers. J Med Microbiol 2016; 65: 1392-1404.
16. Jneid J, Lavigne JP, La Scola B, Cassir N. The diabetic foot microbiota: A review. Hum Microb J 2017; 5-6: 1-6.
17. Mendoza RA, Hsieh JC, Galiano RD (2019). The impact of biofilm formation on wound healing. Wound Healing-Current Perspectives. https://doi.org/https://doi.org/10.5772/intechopen.85020
18. Schaumburg F, Ngoa UA, Köck R, Adegnika AA, Kremsner PG, Lell B, et al. Virulence factors and genotypes of Staphylococcus aureus from infection and carriage in Gabon. Clin Microbiol Infect 2011; 17: 1507-1513.
19. Chopra S, Harjai K, Chhibber S. Antibiotic susceptibility of ica-positive and ica-negative MRSA in different phases of biofilm growth. J Antibiot (Tokyo) 2015; 68: 15-22.
20. Goswami S, Sarkar R, Saha P, Maity A, Sarkar T, Das D, et al. Effect of human placental extract in the management of biofilm mediated drug resistance–A focus on wound management. Microb Pathog 2017; 111: 307-315.
21. Wu Y-K, Cheng N-C, Cheng C-M. Biofilms in chronic wounds: pathogenesis and diagnosis. Trends Biotechnol 2019; 37: 505-517.
22. Masadeh MM, Mhaidat NM, Alzoubi KH, Hussein EI, Al-Trad EI. In vitro determination of the antibiotic susceptibility of biofilm-forming Pseudomonas aeruginosa and Staphylococcus aureus: possible role of proteolytic activity and membrane lipopolysaccharide. Infect Drug Resist 2013; 6: 27-32.
23. Ababneh Q, Abu Laila S, Jaradat Z. Prevalence, genetic diversity, antibiotic resistance and biofilm formation of Acinetobacter baumannii isolated from urban environments. J Appl Microbiol 2022; 133: 3617-3633.
24. Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, et al (2009). Bergey’s manual of systematic bacteriology: Volume 3: The Firmicutes. Springer Science & Business Media.
25. Hassan A, Usman J, Kaleem F, Omair M, Khalid A, Iqbal M. Evaluation of different detection methods of biofilm formation in the clinical isolates. Braz J Infect Dis 2011; 15: 305-311.
26. Mohamed WF, Sharaf SA, Aboshady HM, Sharaf M. Phenotypic and genotypic evaluation of biofilm formation among orthopedic patients showing prosthetic joint infection by molecular techniques. Egypt J Exp Biol (Bot) 2020; 16: 105-113.
27. Slany M, Oppelt J, Cincarova L. Formation of Staphylococcus aureus biofilm in the presence of sublethal concentrations of disinfectants studied via a transcriptomic analysis using transcriptome sequencing (RNA-seq). Appl Environ Microbiol 2017; 83(24): e01643-17.
28. Atshan SS, Nor Shamsudin M, Sekawi Z, Lung LT, Hamat RA, Karunanidhi A, et al. Prevalence of adhesion and regulation of biofilm-related genes in different clones of Staphylococcus aureus. J Biomed Biotechnol 2012; 2012: 976972.
29. Lee S, Choi KH, Yoon Y. Effect of NaCl on biofilm formation of the isolate from Staphylococcus aureus outbreak linked to ham. Korean J Food Sci Anim Resour 2014; 34: 257-261.
30. Shakur JA, Abd Aburesha R. Gene expression of agr system in Staphylococcus aureus and it is relation with antibiotic resistance. Hist Med 2023; 9: 1513-1518.
31. Song P, Rudan D, Zhu Y, Fowkes FJI, Rahimi K, Fowkes FGR, et al. Global, regional, and national prevalence and risk factors for peripheral artery disease in 2015: an updated systematic review and analysis. Lancet Glob Health 2019; 7(8): e1020-e1030.
32. Ponirakis G, Elhadd T, Al Ozairi E, Brema I, Chinnaiyan S, Taghadom E, et al. Prevalence and risk factors for diabetic peripheral neuropathy, neuropathic pain and foot ulceration in the Arabian Gulf region. J Diabetes Investig 2022; 13: 1551-1559.
33. Pataky Z, Vischer U. Diabetic foot disease in the elderly. Diabetes Metab 2007; 33 Suppl 1: S56-S65.
34. Kim EJ, Han K-S. Factors related to self-care behaviours among patients with diabetic foot ulcers. J Clin Nurs 2020; 29: 1712-1722.
35. Kautzky-Willer A, Leutner M, Harreiter J. Sex differences in type 2 diabetes. Diabetologia 2023; 66: 986-1002.
36. Ciarambino T, Crispino P, Leto G, Mastrolorenzo E, Para O, Giordano M. Influence of gender in diabetes mellitus and its complication. Int J Mol Sci 2022; 23: 8850.
37. Banu A, Noorul Hassan MM, Rajkumar J, Srinivasa S. Spectrum of bacteria associated with diabetic foot ulcer and biofilm formation: a prospective study. Australas Med J 2015; 8: 280-285.
38. Costa D, Ielapi N, Caprino F, Giannotta N, Sisinni A, Abramo A, et al. Social aspects of diabetic foot: a scoping review. Soc Sci 2022; 11: 149.
39. Jain SK, Barman R. Bacteriological profile of diabetic foot ulcer with special reference to drug-resistant strains in a tertiary care center in North-East India. Indian J Endocrinol Metab 2017; 21: 688-694.
40. Citron DM, Goldstein EJ, Merriam CV, Lipsky BA, Abramson MA. Bacteriology of moderate-to-severe diabetic foot infections and in vitro activity of antimicrobial agents. J Clin Microbiol 2007; 45: 2819-2828.
41. Belbase A, Pant ND, Nepal K, Neupane B, Baidhya R, Baidya R, et al. Antibiotic resistance and biofilm production among the strains of Staphylococcus aureus isolated from pus/wound swab samples in a tertiary care hospital in Nepal. Ann Clin Microbiol Antimicrob 2017; 16: 15.
42. Jouhar L, Jaafar RF, Nasreddine R, Itani O, Haddad F, Rizk N, et al. Microbiological profile and antimicrobial resistance among diabetic foot infections in Lebanon. Int Wound J 2020; 17: 1764-1773.
43. Palomo AT, Pires APM, Matielo MF, de Athayde Soares R, Pecego C, Sacilotto R, et al. Microbiology of diabetic foot infections in a tertiary care hospital in Sao Paulo, Brazil. Antibiotics (Basel) 2022; 11: 1125.
44. Bose JL, Lehman MK, Fey PD, Bayles KW. Contribution of the Staphylococcus aureus atl AM and GL Murein hydrolase activities in cell division, autolysis, and biofilm formation. PLoS One 2012; 7(7): e42244.
45. Murali TS, Kavitha S, Spoorthi J, Bhat DV, Prasad ASB, Upton Z, et al. Characteristics of microbial drug resistance and its correlates in chronic diabetic foot ulcer infections. J Med Microbiol 2014; 63: 1377-1385.
46. Mahler BJ, Schmidt TS, Nowell LH, Qi SL, Van Metre PC, Hladik ML, et al. Biofilms provide new insight into pesticide occurrence in streams and links to aquatic ecological communities. Environ Sci Technol 2020; 54: 5509-5519.
47. Di Domenico EG, Rimoldi SG, Cavallo I, D’Agosto G, Trento E, Cagnoni G, et al. Microbial biofilm correlates with an increased antibiotic tolerance and poor therapeutic outcome in infective endocarditis. BMC Microbiol 2019; 19: 228.
48. Mohammed SW, Radif HM. Detection of icaA gene expression in clinical biofilm-producing Staphylococcus aureus isolates. Iraqi J Sci 2020; 61: 3154-3163.
49. Harapanahalli AK, Chen Y, Li J, Busscher HJ, van der Mei HC. Influence of adhesion force on icaA and cidA gene expression and production of matrix components in Staphylococcus aureus biofilms. Appl Environ Microbiol 2015; 81: 3369-3378.
2. Bowers S, Franco E. Chronic wounds: evaluation and management. Am Fam Physician 2020; 101: 159-166.
3. James GA, Swogger E, Wolcott R, Pulcini Ed, Secor P, Sestrich J, et al. Biofilms in chronic wounds. Wound Repair Regen 2008; 16: 37-44.
4. Fekadu G, Bula K, Bayisa G, Turi E, Tolossa T, Kasaye HK. Challenges and factors associated with poor glycemic control among type 2 diabetes mellitus patients at Nekemte Referral Hospital, Western Ethiopia. J Multidiscip Healthc 2019; 12: 963-974.
5. Moore Z, Avsar P, Wilson P, Mairghani M, O’Connor T, Nugent L, et al. Diabetic foot ulcers: treatment overview and cost considerations. J Wound Care 2021; 30: 786-791.
6. Ena J, Carretero-Gomez J, Arevalo-Lorido JC, Sanchez-Ardila C, Zapatero-Gaviria A, Gomez-Huelgas R. The association between elevated foot skin temperature and the incidence of diabetic foot ulcers: a meta-analysis. Int J Low Extrem Wounds 2021; 20: 111-1118.
7. Porselvi A, Uma Shankar MS, Lakshmi KS, Sankar V. A retrospective qualitative study on current diabetic foot ulcer management and discussion on extended role of clinical pharmacist. Marmara Pharm J 2017; 21: 412-418.
8. Giurato L, Meloni M, Izzo V, Uccioli L. Osteomyelitis in diabetic foot: a comprehensive overview. World J Diabetes 2017; 8: 135-142.
9. Maheswary T, Nurul AA, Fauzi MB. The insights of microbes’ roles in wound healing: A comprehensive review. Pharmaceutics 2021; 13: 981.
10. Rubio JA, Jiménez S, Lázaro-Martínez JL. Mortality in patients with diabetic foot ulcers: causes, risk factors, and their association with evolution and severity of ulcer. J Clin Med 2020; 9: 3009.
11. Polikandrioti M, Vasilopoulos G, Koutelekos I, Panoutsopoulos G, Gerogianni G, Babatsikou F, et al. Quality of life in diabetic foot ulcer: associated factors and the impact of anxiety/depression and adherence to self-care. Int J Low Extrem Wounds 2020; 19: 165-179.
12. Alfonsi V, Gorgoni M, Scarpelli S, Zivi P, Sdoia S, Mari E, et al. Changes in sleep pattern and dream activity across and after the COVID‐19 lockdown in Italy: A longitudinal observational study. J Sleep Res 2022; 31(2): e13500.
13. Matta-Gutierrez G, Garcia-Morales E, Garcia-Alvarez Y, Álvaro-Afonso FJ, Molines-Barroso RJ, Lazaro-Martinez JL. The influence of multidrug-resistant bacteria on clinical outcomes of diabetic foot ulcers: a systematic review. J Clin Med 2021; 10: 1948.
14. Seo KS, Park N, Rutter JK, Park Y, Baker CL, Thornton JA, et al. Role of Glucose-6-phosphate in metabolic adaptation of Staphylococcus aureus in diabetes. Microbiol Spectr 2021; 9(2): e0085721.
15. Shettigar K, Jain S, Bhat DV, Acharya R, Ramachandra L, Satyamoorthy K, et al. Virulence determinants in clinical Staphylococcus aureus from monomicrobial and polymicrobial infections of diabetic foot ulcers. J Med Microbiol 2016; 65: 1392-1404.
16. Jneid J, Lavigne JP, La Scola B, Cassir N. The diabetic foot microbiota: A review. Hum Microb J 2017; 5-6: 1-6.
17. Mendoza RA, Hsieh JC, Galiano RD (2019). The impact of biofilm formation on wound healing. Wound Healing-Current Perspectives. https://doi.org/https://doi.org/10.5772/intechopen.85020
18. Schaumburg F, Ngoa UA, Köck R, Adegnika AA, Kremsner PG, Lell B, et al. Virulence factors and genotypes of Staphylococcus aureus from infection and carriage in Gabon. Clin Microbiol Infect 2011; 17: 1507-1513.
19. Chopra S, Harjai K, Chhibber S. Antibiotic susceptibility of ica-positive and ica-negative MRSA in different phases of biofilm growth. J Antibiot (Tokyo) 2015; 68: 15-22.
20. Goswami S, Sarkar R, Saha P, Maity A, Sarkar T, Das D, et al. Effect of human placental extract in the management of biofilm mediated drug resistance–A focus on wound management. Microb Pathog 2017; 111: 307-315.
21. Wu Y-K, Cheng N-C, Cheng C-M. Biofilms in chronic wounds: pathogenesis and diagnosis. Trends Biotechnol 2019; 37: 505-517.
22. Masadeh MM, Mhaidat NM, Alzoubi KH, Hussein EI, Al-Trad EI. In vitro determination of the antibiotic susceptibility of biofilm-forming Pseudomonas aeruginosa and Staphylococcus aureus: possible role of proteolytic activity and membrane lipopolysaccharide. Infect Drug Resist 2013; 6: 27-32.
23. Ababneh Q, Abu Laila S, Jaradat Z. Prevalence, genetic diversity, antibiotic resistance and biofilm formation of Acinetobacter baumannii isolated from urban environments. J Appl Microbiol 2022; 133: 3617-3633.
24. Vos P, Garrity GM, Jones D, Krieg NR, Ludwig W, Rainey FA, et al (2009). Bergey’s manual of systematic bacteriology: Volume 3: The Firmicutes. Springer Science & Business Media.
25. Hassan A, Usman J, Kaleem F, Omair M, Khalid A, Iqbal M. Evaluation of different detection methods of biofilm formation in the clinical isolates. Braz J Infect Dis 2011; 15: 305-311.
26. Mohamed WF, Sharaf SA, Aboshady HM, Sharaf M. Phenotypic and genotypic evaluation of biofilm formation among orthopedic patients showing prosthetic joint infection by molecular techniques. Egypt J Exp Biol (Bot) 2020; 16: 105-113.
27. Slany M, Oppelt J, Cincarova L. Formation of Staphylococcus aureus biofilm in the presence of sublethal concentrations of disinfectants studied via a transcriptomic analysis using transcriptome sequencing (RNA-seq). Appl Environ Microbiol 2017; 83(24): e01643-17.
28. Atshan SS, Nor Shamsudin M, Sekawi Z, Lung LT, Hamat RA, Karunanidhi A, et al. Prevalence of adhesion and regulation of biofilm-related genes in different clones of Staphylococcus aureus. J Biomed Biotechnol 2012; 2012: 976972.
29. Lee S, Choi KH, Yoon Y. Effect of NaCl on biofilm formation of the isolate from Staphylococcus aureus outbreak linked to ham. Korean J Food Sci Anim Resour 2014; 34: 257-261.
30. Shakur JA, Abd Aburesha R. Gene expression of agr system in Staphylococcus aureus and it is relation with antibiotic resistance. Hist Med 2023; 9: 1513-1518.
31. Song P, Rudan D, Zhu Y, Fowkes FJI, Rahimi K, Fowkes FGR, et al. Global, regional, and national prevalence and risk factors for peripheral artery disease in 2015: an updated systematic review and analysis. Lancet Glob Health 2019; 7(8): e1020-e1030.
32. Ponirakis G, Elhadd T, Al Ozairi E, Brema I, Chinnaiyan S, Taghadom E, et al. Prevalence and risk factors for diabetic peripheral neuropathy, neuropathic pain and foot ulceration in the Arabian Gulf region. J Diabetes Investig 2022; 13: 1551-1559.
33. Pataky Z, Vischer U. Diabetic foot disease in the elderly. Diabetes Metab 2007; 33 Suppl 1: S56-S65.
34. Kim EJ, Han K-S. Factors related to self-care behaviours among patients with diabetic foot ulcers. J Clin Nurs 2020; 29: 1712-1722.
35. Kautzky-Willer A, Leutner M, Harreiter J. Sex differences in type 2 diabetes. Diabetologia 2023; 66: 986-1002.
36. Ciarambino T, Crispino P, Leto G, Mastrolorenzo E, Para O, Giordano M. Influence of gender in diabetes mellitus and its complication. Int J Mol Sci 2022; 23: 8850.
37. Banu A, Noorul Hassan MM, Rajkumar J, Srinivasa S. Spectrum of bacteria associated with diabetic foot ulcer and biofilm formation: a prospective study. Australas Med J 2015; 8: 280-285.
38. Costa D, Ielapi N, Caprino F, Giannotta N, Sisinni A, Abramo A, et al. Social aspects of diabetic foot: a scoping review. Soc Sci 2022; 11: 149.
39. Jain SK, Barman R. Bacteriological profile of diabetic foot ulcer with special reference to drug-resistant strains in a tertiary care center in North-East India. Indian J Endocrinol Metab 2017; 21: 688-694.
40. Citron DM, Goldstein EJ, Merriam CV, Lipsky BA, Abramson MA. Bacteriology of moderate-to-severe diabetic foot infections and in vitro activity of antimicrobial agents. J Clin Microbiol 2007; 45: 2819-2828.
41. Belbase A, Pant ND, Nepal K, Neupane B, Baidhya R, Baidya R, et al. Antibiotic resistance and biofilm production among the strains of Staphylococcus aureus isolated from pus/wound swab samples in a tertiary care hospital in Nepal. Ann Clin Microbiol Antimicrob 2017; 16: 15.
42. Jouhar L, Jaafar RF, Nasreddine R, Itani O, Haddad F, Rizk N, et al. Microbiological profile and antimicrobial resistance among diabetic foot infections in Lebanon. Int Wound J 2020; 17: 1764-1773.
43. Palomo AT, Pires APM, Matielo MF, de Athayde Soares R, Pecego C, Sacilotto R, et al. Microbiology of diabetic foot infections in a tertiary care hospital in Sao Paulo, Brazil. Antibiotics (Basel) 2022; 11: 1125.
44. Bose JL, Lehman MK, Fey PD, Bayles KW. Contribution of the Staphylococcus aureus atl AM and GL Murein hydrolase activities in cell division, autolysis, and biofilm formation. PLoS One 2012; 7(7): e42244.
45. Murali TS, Kavitha S, Spoorthi J, Bhat DV, Prasad ASB, Upton Z, et al. Characteristics of microbial drug resistance and its correlates in chronic diabetic foot ulcer infections. J Med Microbiol 2014; 63: 1377-1385.
46. Mahler BJ, Schmidt TS, Nowell LH, Qi SL, Van Metre PC, Hladik ML, et al. Biofilms provide new insight into pesticide occurrence in streams and links to aquatic ecological communities. Environ Sci Technol 2020; 54: 5509-5519.
47. Di Domenico EG, Rimoldi SG, Cavallo I, D’Agosto G, Trento E, Cagnoni G, et al. Microbial biofilm correlates with an increased antibiotic tolerance and poor therapeutic outcome in infective endocarditis. BMC Microbiol 2019; 19: 228.
48. Mohammed SW, Radif HM. Detection of icaA gene expression in clinical biofilm-producing Staphylococcus aureus isolates. Iraqi J Sci 2020; 61: 3154-3163.
49. Harapanahalli AK, Chen Y, Li J, Busscher HJ, van der Mei HC. Influence of adhesion force on icaA and cidA gene expression and production of matrix components in Staphylococcus aureus biofilms. Appl Environ Microbiol 2015; 81: 3369-3378.
| Files | ||
| Issue | Vol 16 No 4 (2024) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v16i4.16303 | |
| Keywords | ||
| Antimicrobial resistance; Biofilm; Diabetes; Diabetic foot; Staphylococcus aureus | ||
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How to Cite
1.
Owais D, Al-Groom R, AlRamadneh T, Alsawalha L, Ahmad Khan MS, Yousef O, Burjaq S. Antibiotic susceptibility and biofilm forming ability of Staphylococcus aureus isolated from Jordanian patients with diabetic foot ulcer. Iran J Microbiol. 2024;16(4):450-458.
