Resistance profiles of Staphylococcus aureus isolates against frequently used antibiotics at private sector laboratories in Jordan
-
Rania Al-Groom
,
Ghina Al-Saraireh
,
Sultan Ayesh Mohammed Saghir
,
Mohd Sajjad Ahmad Khan
,
Areej M. Almanaseer
,
Laila Alswalha
,
Wesal Alraei
,
Dalia Abu Al-Haijaa
,
Maha Hdaib
,
Anas Da'meh
,
Shereen Z Burjaq
,
Omar Al-Dmour
,
Fuad Alhawarat
Abstract
Background and Objectives: Staphylococcus aureus (S. aureus) is one of the most important pathogens, responsible for a range of infections. This study aimed to assess resistance patterns in S. aureus isolates obtained from certain private-sector laboratories against commonly used antimicrobial agents.
Materials and Methods: The process involved collecting various samples from several private laboratories and then identifying S. aureus isolates using biochemical characterization. The antibiotic susceptibility of these isolates was determined by disc diffusion method . Furthermore, Rt-PCR was employed to identify two genes namely the methicillin/oxacillin resistance genes (mecA), and (SCCmec).
Results: The findings of the current study exhibited that females constituted a larger proportion of the participants (59.1%) compared to males (40.9%), with a mean participant age of 40.82 years. Gram-positive bacteria were more prevalent (71.3%) than Gram-negative bacteria (18.3%), with S. aureus being the most frequent isolate (60.9%). Urine samples represented the highest collected sample type (47.8%). Out of the 115 bacterial isolates, 85.2% exhibited multidrug resistance to antibiotics such as cefazolin, gentamicin, vancomycin, and ceftazidime. Clindamycin was the most effective antibiotic, with a sensitivity rate of 62.9%, followed by teicoplanin and meropenem, each with a sensitivity rate of 52.9%. Methicillin-resistant Staphylococcus aureus (MRSA) strains were susceptabile to vancomycin and teicoplanin. The methicillin/oxacillin resistant isolates showed significant association with mecA and SCCA genes.
Conclusion: This study highlighted the multi-drug resistance in S. aureus isolates, stressing the need for stringent antibiotic stewardship, continuous surveillance, and further research into alternative treatments, including novel antibiotics and combination therapy, to combat resistant strains.
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8. Mehta Y, Hegde A, Pande R, Zirpe KG, Gupta V, Ahdal J, et al. Methicillin-resistant Staphylococcus aureus in Intensive care unit setting of India: A review of clinical Burden, Patterns of Prevalence, Preventive Measures, and future Strategies. Indian J Crit Care Med 2020; 24: 55-62.
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11. Salam MA, Al-Amin MY, Salam MT, Pawar JS, Akhter N, Rabaan AA, et al. Antimicrobial resistance: A Growing serious threat for global public Health. Healthcare (Basel) 2023; 11: 1946.
12. Lessa FC, Sievert DM. Antibiotic resistance: A global problem and the need to do more. Clin Infect Dis 2023; 77(Suppl 1): S1-S3.
13. Chen L, Kumar S, Wu H. A review of current antibiotic resistance and promising antibiotics with novel modes of action to combat antibiotic resistance. Arch Microbiol 2023; 205: 356.
14. Reygaert WC. An overview of the antimicrobial resistance mechanisms of bacteria. AIMS Microbiol 2018; 4: 482-501.
15. Oliveira M, Antunes W, Mota S, Madureira-Carvalho Á, Dinis-Oliveira RJ, Dias da Silva D. An overview of the recent advances in antimicrobial resistance. Microorganisms 2024; 12: 1920.
16. Erkmen O (2021). Laboratory practices in microbiology. Academic Press. https://www.sciencedirect.com/book/9780323910170/laboratory-practices-in-microbiology
17. Kateete DP, Kimani CN, Katabazi FA, Okeng A, Okee MS, Nanteza A, et al. Identification of Staphylococcus aureus: DNase and Mannitol salt agar improve the efficiency of the tube coagulase test. Ann Clin Microbiol Antimicrob 2010; 9: 23.
18. Khatoon H, Anokhe A, Kalia V. Catalase Test: A Biochemical protocol for bacterial identification. AgriCos e-Newslet 2022; 3: 53-55.
19. Pumipuntu N, Kulpeanprasit S, Santajit S, Tunyong W, Kong-Ngoen T, Hinthong W, et al. Screening method for Staphylococcus aureus identification in subclinical bovine mastitis from dairy farms. Vet World 2017; 10: 721-726.
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21. Zhou J, Cai Y, Liu Y, An H, Deng K, Ashraf MA, et al. Breaking down the cell wall: Still an attractive antibacterial strategy. Front Microbiol 2022; 13: 952633.
22. Ghaznavi-Rad E, Nor Shamsudin M, Sekawi Z, van Belkum A, Neela V. A simplified multiplex PCR assay for fast and easy discrimination of globally distributed staphylococcal cassette chromosome mec types in meticillin-resistant Staphylococcus aureus. J Med Microbiol 2010; 59: 1135-1139.
23. Ghasemian A, Najar Peerayeh S, Bakhshi B, Mirzaee M. The Microbial surface Components Recognizing adhesive matrix Molecules (MSCRAMMs) genes among clinical isolates of Staphylococcus aureus from Hospitalized children. Iran J Pathol 2015; 10: 258-264.
24. Rafif Khairullah A, Rehman S, Agus Sudjarwo S, Helmi Effendi M, Chasyer Ramandinianto S, Aega Gololodo M, et al. Detection of mecA gene and methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and risk factors from farms in Probolinggo, Indonesia. F1000Res 2022; 11: 722.
25. Garoy EY, Gebreab YB, Achila OO, Tekeste DG, Kesete R, Ghirmay R, et al. Methicillin-Resistant Staphylococcus aureus (MRSA): Prevalence and Antimicrobial Sensitivity Pattern among Patients-A Multicenter study in Asmara, Eritrea. Can J Infect Dis Med Microbiol 2019; 2019: 8321834.
26. Tălăpan D, Sandu AM, Rafila A. Antimicrobial resistance of Staphylococcus aureus isolated between 2017 and 2022 from infections at a Tertiary care hospital in Romania. Antibiotics (Basel) 2023; 12: 974.
27. Massele A, Rogers AM, Gabriel D, Mayanda A, Magoma S, Cook A, et al. A Narrative review of recent Antibiotic Prescribing practices in Ambulatory care in Tanzania: Findings and Implications. Medicina (Kaunas) 2023; 59: 2195.
28. Nixon J, Hennessy J, Baird RW. Tracking trends in the Top End: clindamycin and erythromycin resistance in group A Streptococcus in the northern Territory, 2012-2023. Commun Dis Intell (2018) 2024; 48: 10.33321/cdi.2024.48.31.
29. Cheung GYC, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence 2021; 12: 547-569.
30. Fahim NAE. Prevalence and antimicrobial susceptibility profile of multidrug-resistant bacteria among intensive care units patients at Ain Shams university hospitals in Egypt-a retrospective study. J Egypt Public Health Assoc 2021; 96: 7.
31. CDC (2019). Antibiotic resistance threats in the United States. US Department of Health and Human Services: Washington, DC, USA.
32. Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. P T 2015; 40: 277-283.
33. Guo Y, Song G, Sun M, Wang J, Wang Y. Prevalence and therapies of antibiotic-resistance in Staphylococcus aureus. Front Cell Infect Microbiol 2020; 10: 107.
34. Idrees MM, Saeed K, Shahid MA, Akhtar M, Qammar K, Hassan J, et al. Prevalence of mecA-and mecC-Associated Methicillin-Resistant Staphylococcus aureus in clinical Specimens, Punjab, Pakistan. Biomedicines 2023; 11: 878.
35. Fitzgerald JR, Sturdevant DE, Mackie SM, Gill SR, Musser JM. Evolutionary genomics of Staphylococcus aureus: insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic. Proc Natl Acad Sci U S A 2001; 98: 8821-8826.
36. Tao S, Chen H, Li N, Wang T, Liang W. The spread of antibiotic resistance genes in Vivo model. Can J Infect Dis Med Microbiol 2022; 2022: 3348695.
37. Al-Nsour EH, Al-Hadithi HT, Al-Groom RM, Abushattal S, Naser AY, Al Nsour AH, et al. Increased incidence of methicillin resistant Staphylococcus aureus and methicillin resistant Staphylococcus epidermidis in the skin and nasal carriage among healthcare workers and inanimate hospital surfaces after the COVID-19 pandemic. Iran J Microbiol 2024; 16: 584-597.
2. Pal M, Kerorsa GB, Marami LM, Kandi V. Epidemiology, Pathogenicity, animal infections, antibiotic resistance, public health significance, and economic impact of Staphylococcus aureus: A comprehensive review. Am J Public Health Res 2020; 8: 14-21.
3. Linz MS, Mattappallil A, Finkel D, Parker D. Clinical impact of Staphylococcus aureus skin and soft tissue infections. Antibiotics (Basel) 2023; 12: 557.
4. Howden BP, Giulieri SG, Wong Fok Lung T, Baines SL, Sharkey LK, Lee JYH, et al. Staphylococcus aureus host interactions and adaptation. Nat Rev Microbiol 2023; 21: 380-395.
5. Igler C, Rolff J, Regoes R. Multi-step vs. single-step resistance evolution under different drugs, pharmacokinetics, and treatment regimens. Elife 2021; 10: e64116.
6. Majumder MAA, Rahman S, Cohall D, Bharatha A, Singh K, Haque M, et al. Antimicrobial Stewardship: fighting antimicrobial resistance and protecting global public health. Infect Drug Resist 2020; 13: 4713-4738.
7. Cheung GYC, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence 2021; 12: 547-569.
8. Mehta Y, Hegde A, Pande R, Zirpe KG, Gupta V, Ahdal J, et al. Methicillin-resistant Staphylococcus aureus in Intensive care unit setting of India: A review of clinical Burden, Patterns of Prevalence, Preventive Measures, and future Strategies. Indian J Crit Care Med 2020; 24: 55-62.
9. Samuel P, Kumar YS, Suthakar BJ, Karawita J, Sunil Kumar D, Vedha V, et al. Methicillin-Resistant Staphylococcus aureus Colonization in Intensive care and burn units: A Narrative review. Cureus 2023; 15(10): e47139.
10. Chamchod F, Palittapongarnpim P. Effects of the proportion of high-risk patients and control strategies on the prevalence of methicillin-resistant Staphylococcus aureus in an intensive care unit. BMC Infect Dis 2019; 19: 1026.
11. Salam MA, Al-Amin MY, Salam MT, Pawar JS, Akhter N, Rabaan AA, et al. Antimicrobial resistance: A Growing serious threat for global public Health. Healthcare (Basel) 2023; 11: 1946.
12. Lessa FC, Sievert DM. Antibiotic resistance: A global problem and the need to do more. Clin Infect Dis 2023; 77(Suppl 1): S1-S3.
13. Chen L, Kumar S, Wu H. A review of current antibiotic resistance and promising antibiotics with novel modes of action to combat antibiotic resistance. Arch Microbiol 2023; 205: 356.
14. Reygaert WC. An overview of the antimicrobial resistance mechanisms of bacteria. AIMS Microbiol 2018; 4: 482-501.
15. Oliveira M, Antunes W, Mota S, Madureira-Carvalho Á, Dinis-Oliveira RJ, Dias da Silva D. An overview of the recent advances in antimicrobial resistance. Microorganisms 2024; 12: 1920.
16. Erkmen O (2021). Laboratory practices in microbiology. Academic Press. https://www.sciencedirect.com/book/9780323910170/laboratory-practices-in-microbiology
17. Kateete DP, Kimani CN, Katabazi FA, Okeng A, Okee MS, Nanteza A, et al. Identification of Staphylococcus aureus: DNase and Mannitol salt agar improve the efficiency of the tube coagulase test. Ann Clin Microbiol Antimicrob 2010; 9: 23.
18. Khatoon H, Anokhe A, Kalia V. Catalase Test: A Biochemical protocol for bacterial identification. AgriCos e-Newslet 2022; 3: 53-55.
19. Pumipuntu N, Kulpeanprasit S, Santajit S, Tunyong W, Kong-Ngoen T, Hinthong W, et al. Screening method for Staphylococcus aureus identification in subclinical bovine mastitis from dairy farms. Vet World 2017; 10: 721-726.
20. Nikolic P, Mudgil P. The cell wall, cell Membrane and Virulence factors of Staphylococcus aureus and their role in antibiotic resistance. Microorganisms 2023; 11: 259.
21. Zhou J, Cai Y, Liu Y, An H, Deng K, Ashraf MA, et al. Breaking down the cell wall: Still an attractive antibacterial strategy. Front Microbiol 2022; 13: 952633.
22. Ghaznavi-Rad E, Nor Shamsudin M, Sekawi Z, van Belkum A, Neela V. A simplified multiplex PCR assay for fast and easy discrimination of globally distributed staphylococcal cassette chromosome mec types in meticillin-resistant Staphylococcus aureus. J Med Microbiol 2010; 59: 1135-1139.
23. Ghasemian A, Najar Peerayeh S, Bakhshi B, Mirzaee M. The Microbial surface Components Recognizing adhesive matrix Molecules (MSCRAMMs) genes among clinical isolates of Staphylococcus aureus from Hospitalized children. Iran J Pathol 2015; 10: 258-264.
24. Rafif Khairullah A, Rehman S, Agus Sudjarwo S, Helmi Effendi M, Chasyer Ramandinianto S, Aega Gololodo M, et al. Detection of mecA gene and methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and risk factors from farms in Probolinggo, Indonesia. F1000Res 2022; 11: 722.
25. Garoy EY, Gebreab YB, Achila OO, Tekeste DG, Kesete R, Ghirmay R, et al. Methicillin-Resistant Staphylococcus aureus (MRSA): Prevalence and Antimicrobial Sensitivity Pattern among Patients-A Multicenter study in Asmara, Eritrea. Can J Infect Dis Med Microbiol 2019; 2019: 8321834.
26. Tălăpan D, Sandu AM, Rafila A. Antimicrobial resistance of Staphylococcus aureus isolated between 2017 and 2022 from infections at a Tertiary care hospital in Romania. Antibiotics (Basel) 2023; 12: 974.
27. Massele A, Rogers AM, Gabriel D, Mayanda A, Magoma S, Cook A, et al. A Narrative review of recent Antibiotic Prescribing practices in Ambulatory care in Tanzania: Findings and Implications. Medicina (Kaunas) 2023; 59: 2195.
28. Nixon J, Hennessy J, Baird RW. Tracking trends in the Top End: clindamycin and erythromycin resistance in group A Streptococcus in the northern Territory, 2012-2023. Commun Dis Intell (2018) 2024; 48: 10.33321/cdi.2024.48.31.
29. Cheung GYC, Bae JS, Otto M. Pathogenicity and virulence of Staphylococcus aureus. Virulence 2021; 12: 547-569.
30. Fahim NAE. Prevalence and antimicrobial susceptibility profile of multidrug-resistant bacteria among intensive care units patients at Ain Shams university hospitals in Egypt-a retrospective study. J Egypt Public Health Assoc 2021; 96: 7.
31. CDC (2019). Antibiotic resistance threats in the United States. US Department of Health and Human Services: Washington, DC, USA.
32. Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. P T 2015; 40: 277-283.
33. Guo Y, Song G, Sun M, Wang J, Wang Y. Prevalence and therapies of antibiotic-resistance in Staphylococcus aureus. Front Cell Infect Microbiol 2020; 10: 107.
34. Idrees MM, Saeed K, Shahid MA, Akhtar M, Qammar K, Hassan J, et al. Prevalence of mecA-and mecC-Associated Methicillin-Resistant Staphylococcus aureus in clinical Specimens, Punjab, Pakistan. Biomedicines 2023; 11: 878.
35. Fitzgerald JR, Sturdevant DE, Mackie SM, Gill SR, Musser JM. Evolutionary genomics of Staphylococcus aureus: insights into the origin of methicillin-resistant strains and the toxic shock syndrome epidemic. Proc Natl Acad Sci U S A 2001; 98: 8821-8826.
36. Tao S, Chen H, Li N, Wang T, Liang W. The spread of antibiotic resistance genes in Vivo model. Can J Infect Dis Med Microbiol 2022; 2022: 3348695.
37. Al-Nsour EH, Al-Hadithi HT, Al-Groom RM, Abushattal S, Naser AY, Al Nsour AH, et al. Increased incidence of methicillin resistant Staphylococcus aureus and methicillin resistant Staphylococcus epidermidis in the skin and nasal carriage among healthcare workers and inanimate hospital surfaces after the COVID-19 pandemic. Iran J Microbiol 2024; 16: 584-597.
| Files | ||
| Issue | Vol 17 No 2 (2025) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v17i2.18382 | |
| Keywords | ||
| Staphylococcus aureus; Multidrug-resistant organisms; Methicillin-resistant Staphylococcus aureus strains; MecA; SCCmec | ||
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This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Al-Groom R, Al-Saraireh G, Saghir SAM, Ahmad Khan MS, Almanaseer A, Alswalha L, Alraei W, Abu Al-Haijaa D, Hdaib M, Da’meh A, Burjaq S, Al-Dmour O, Alhawarat F. Resistance profiles of Staphylococcus aureus isolates against frequently used antibiotics at private sector laboratories in Jordan. Iran J Microbiol. 2025;17(2):229-238.
