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Efficacy of aztreonam/avibactam against Stenotrophomonas maltophilia alone and in combination with tigecycline

Year 2024, Volume: 54 Issue: 3, 395 - 402, 30.12.2024
https://doi.org/10.26650/IstanbulJPharm.2024.1536403

Abstract

Background and Aims: Stenotrophomonas maltophilia is a multidrug-resistant opportunistic pathogen that threatens human and public health because of its widespread intrinsic and acquired antibiotic resistance. These bacteria become resistant to aztreonam by degrading it using the beta-lactamases. The aim of this study was to evaluate the effect of aztreonam/avibactam on aztreonam resistance in clinical strains of S. maltophilia and to assess the synergistic potential of aztreonam in combination with tigecycline.
Methods: Minimum Inhibitory Concentrations (MICs) of aztreonam, aztreonam/avibactam, tigecycline, and doxycycline were determined using broth microdilution in sixty-six S. maltophilia isolates. Additionally, six isolates with the most common MICs of aztreonam/avibactam against the strains, 2 μg/ml and 4 μg/ml were selected from among the sixty-six tested strains, and the effectiveness of the combination of aztreonam/avibactam with tigecycline was determined using both the checkerboard test and the time-dependent killing method.
Results: Aztreonam/avibactam restored aztreonam activity in 96.9% of resistant S. maltophilia isolates. Half of the isolates were susceptible to tigecycline, whereas all were susceptible to doxycycline. The combination of aztreonam/avibactam with tigecycline was found to have an additive effect against all isolates in the checkerboard experiment in which the activity of aztreonam/avibactam in combination with tigecycline was investigated against six isolates. In the time-dependent killing experiment, the combination exerted a synergistic effect against two isolates.
Conclusion: Aztreonam/avibactam appears to be an important alternative for reversing aztreonam resistance in S. maltophilia. Additionally, tetracyclines, such as tigecycline and doxycycline, are highly effective against these bacteria. To confirm these promising findings, further in vitro, in vivo, and clinical studies are required.

Supporting Institution

Gazi University Scientific Research Projects Unit

Project Number

TKB-2023-8817

References

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  • Biagi, M., Lamm, D., Meyer, K., Vialichka, A., Jurkovic, M., Patel S, & Wenzler, E. (2020b). Activity of aztreonam in combination with avibactam, clavulanate, relebactam, and vaborbactam against multidrug-resistant Stenotrophomonas maltophilia. Antimicrobial Agents and Chemotheraphy 64(12), e00297-20. https://doi.org/10. 1128/AAC.00297-20 google scholar
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  • Cai, B., Tillotson, G., Benjumea, D., Callahan, P., & Echols, R. (2020). The burden of bloodstream infections due to Stenotrophomonas maltophilia in the United States: a large, retrospective database study. In Open Forum on Infectious Diseases (Vol. 7, No. 5, p. ofaa141). US: Oxford University Press. google scholar
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  • Gülmez, D., Cakar, A., Şener, B., Hasçelik, G., & Karakaya, J. (2010). Comparison of different antimicrobial susceptibility testing meth-ods for Stenotrophomonas maltophilia and results of synergy test-ing. Journal of Infection and Chemotherapy, 16(5), 322-328. google scholar
  • Hafiz, T. A., Aldawood, E., Albloshi, A., Alghamdi, S. S., Mubaraki, M. A., Alyami, A. S., & Aldriwesh, M. G. (2022). Stenotrophomonas maltophilia epidemiology, resistance charac-teristics, and clinical outcomes: understanding of the recent three years’ trends. Microorganisms, 10(12), 2506. google scholar
  • Karamanlıoğlu, D., & Dizbay, M. (2019). In vitro combination of tige-cycline with other antibiotics in Stenotrophomonas maltophilia isolates. Turkish Journal of Medical Sciences, 49(2), 683-686. google scholar
  • Lin, Q., Zou, H., Chen, X., Wu, M., Ma, D., Yu, H., ... & Huang, S. (2021). Avibactam potentiated the activity of both ceftazidime and aztreonam against S. maltophilia clinical isolates in vitro. BMC Microbiology, 21, 1-6. google scholar
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  • Mojica, M. F., Bonomo, R. A., & Van Duin, D. (2023). Treatment approaches for severe Stenotrophomonas maltophilia infections. Current Opinion in Infectious Diseases, 36(6), 572-584. google scholar
  • Mojica, M. F., Humphries, R., Lipuma, J. J., Mathers, A. J., Rao, G. G., Shelburne, S. A., ... & Bonomo, R. A. (2022). Clinical challenges treating Stenotrophomonas maltophilia infections: an update. JAC-Antimicrobial Resistance, 4(3), dlac040. google scholar
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  • Ranieri, E. M., Denicolo, S., Stolfa, S., Dalfino, L., Bavaro, D. F., Sara-cino, A., ... & Mosca, A. (2023). Looking for Stenotrophomonas maltophilia treatment: in vitro activity of ceftazidime/avibactam alone and in combination with aztreonam. Journal of Chemother-apy, 35(7), 610-613. google scholar
  • Rizvi, M., Ahmed, J., Khan, F., Shukla, I., & Malik, A. (2013). As-sessment of combination therapy by time kill curve analysis and chequerboard assay for treatment of multi-drug resistant Pseu-domonas aeruginosa isolates. Journal of Global Antimicrobial Resistance, 1(2), 103-108. google scholar
  • Roemhild, R., Bollenbach, T., & Andersson, D. I. (2022). The physiol-ogy and genetics of bacterial responses to antibiotic combinations. Nature Reviews Microbiology, 20(8), 478-490. google scholar
  • Rossolini, G. M., Arhin, F. F., & Kantecki, M. (2024). In vitro ac-tivity of aztreonam-avibactam and comparators against Metallo-P-Lactamase-producing Enterobacterales from ATLAS Global Surveillance Program, 2016-2020. Journal of Global Antimicro-bial Resistance, 36, 123-131. google scholar
  • Sader, H. S., Carvalhaes, C. G., Arends, S. R., Castanheira, M., & Mendes, R. E. (2021). Aztreonam/avibactam activity against clin-ical isolates of Enterobacterales collected in Europe, Asia and Latin America in 2019. Journal of Antimicrobial Chemotherapy, 76(3), 659-666. google scholar
  • Sader, H. S., Castanheira, M., Kimbrough, J. H., Kantro, V., & Mendes, R. E. (2023). Aztreonam/avibactam activity against a large collec-tion of carbapenem-resistant Enterobacterales (CRE) collected in hospitals from Europe, Asia and Latin America (2019-21). JAC-Antimicrobial Resistance, 5(2), dlad032. google scholar
  • Sader, H. S., Duncan, L. R., Arends, S. R., Carvalhaes, C. G., & Castan-heira, M. (2020). Antimicrobial activity of aztreonam-avibactam and comparator agents when tested against a large collection of contemporary Stenotrophomonas maltophilia isolates from med-ical centers worldwide. Antimicrobial Agents and Chemotherapy, 64(11), e01433-20. https://doi.org/10.1128/aac.01433-20 google scholar
  • Singh, R., Kim, A., Tanudra, M. A., Harris, J. J., McLaughlin, google scholar
  • R. E., Patey, S., ... & Eakin, A. E. (2015). Pharmacokinet-ics/pharmacodynamics of a p-lactam and p-lactamase inhibitor combination: a novel approach for aztreonam/avibactam. Journal of Antimicrobial Chemotherapy, 70(9), 2618-2626. google scholar
  • Su, B. A., Chen, C. C., Chen, H. J., Lai, H. Y., Tsai, C. H., Lai, C. C., ... & Chao, C. M. (2023). In vitro activities of antimicrobial combi-nations against planktonic and biofilm forms of Stenotrophomonas maltophilia. Frontiers in Microbiology, 14, 1186669. google scholar
  • Tamma, P. D., Aitken, S. L., Bonomo, R. A., Mathers, A. J., van Duin, D., & Clancy, C. J. (2023). Infectious Diseases Society of America 2023 guidance on the treatment of antimicrobial resistant gram-negative infections. Clinical Infectious Diseases, ciad428. google scholar
  • Tyers, M., & Wright, G. D. (2019). Drug combinations: a strategy to extend the life of antibiotics in the 21st century. Nature Reviews Microbiology, 17(3), 141-155 google scholar
  • U.S. Food and Drug Administration. 2023. https://www.fda.gov/drugs/ development-resources/tigecycline-injection-products. Accessed 21 September 2024.Visalli, M. A., Jacobs, M. R., & Appelbaum, P. C. (1998). Activities of three quinolones, alone and in com-bination with extended-spectrum cephalosporins or gentamicin, against Stenotrophomonas maltophilia. Antimicrobial Agents and Chemotherapy, 42(8), 2002-2005. google scholar
  • Wang,C.H.,Yu,C.M.,Hsu,S.T.,&Wu,R.X. (2020). Levofloxacin-resistant Stenotrophomonas maltophilia: risk factors and antibi-otic susceptibility patterns in hospitalized patients. Journal of Hospital Infection, 104(1), 46-52. google scholar
  • White, R. L., Burgess, D. S., Manduru, M., & Bosso, J. A. (1996). Comparison of three different in vitro methods of detecting syn-ergy: time-kill, checkerboard, and E test. Antimicrobial Agents and Chemotherapy, 40(8), 1914-1918. google scholar
  • Zhao, J., Huang, Y., Li, J., Zhang, B., Dong, Z., & Wang, D. (2022). In vitro antibacterial activity and resistance prevention of an-timicrobial combinations for dihydropteroate synthase-carrying Stenotrophomonas maltophilia. Infection and Drug Resistance, 15, 3039-3046. google scholar
  • Zhao, J., Liu, Y., Liu, Y., Wang, D., Ni, W., Wang, R., ... & Zhang, B. (2018). Frequency and genetic determinants of tigecycline re-sistance in clinically isolated Stenotrophomonas maltophilia in Beijing, China. Frontiers in Microbiology, 9, 549. google scholar
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Year 2024, Volume: 54 Issue: 3, 395 - 402, 30.12.2024
https://doi.org/10.26650/IstanbulJPharm.2024.1536403

Abstract

Project Number

TKB-2023-8817

References

  • Alhayani, T., Philpott, C. D., Liao, S., Gentene, A. J., & Mueller, E. W. (2024). Comparison of doxycycline or minocycline to sulfamethoxazole-trimethoprim for treatment of Stenotrophomonas maltophilia pneumonia. Annals of Pharma-cotherapy, 58(1), 21-27. google scholar
  • Andelkovic, M. V., Jankovic, S. M., Kostic, M. J., Zivkovic Zaric, R. S., Opancina, V. D., Zivic, M. Z., ... & Pejcic, A. V. (2019). An-timicrobial treatment of Stenotrophomonas maltophilia invasive infections: systematic review. Journal of Chemotherapy, 31(6), 297-306. google scholar
  • Banar, M., Sattari-Maraji, A., Bayatinejad, G., Ebrahimi, E., Jabal-ameli, L., Beigverdi R, & Jabalameli, F. (2023). Global prevalence and antibiotic resistance in clinical isolates of Stenotrophomonas maltophilia: a systematic review and meta-analysis. Frontiers in Medicine, 10, 1163439. google scholar
  • Biagi, M., Lamm, D., Meyer, K., Vialichka, A., Jurkovic, M., Patel S, & Wenzler, E. (2020b). Activity of aztreonam in combination with avibactam, clavulanate, relebactam, and vaborbactam against multidrug-resistant Stenotrophomonas maltophilia. Antimicrobial Agents and Chemotheraphy 64(12), e00297-20. https://doi.org/10. 1128/AAC.00297-20 google scholar
  • Biagi, M., Tan, X., Wu, T., Jurkovic, M., Vialichka, A., Meyer K. & Wenzler, E. (2020a). Activity of potential alternative treatment agents for Stenotrophomonas maltophilia isolates nonsusceptible to levofloxacin and/or trimethoprim-sulfamethoxazole. Journal of Clinical Microbiology, 58(2), e01603-19. https://doi.org/10.1128/ JCM.01603-19 google scholar
  • Brooke, J. S. (2021). Advances in the microbiology of Stenotrophomonas maltophilia. Clinical Microbiology Reviews, 34(3), e00030-19. https://doi.org/10.1128/CMR.00030- 19 google scholar
  • Cai, B., Tillotson, G., Benjumea, D., Callahan, P., & Echols, R. (2020). The burden of bloodstream infections due to Stenotrophomonas maltophilia in the United States: a large, retrospective database study. In Open Forum on Infectious Diseases (Vol. 7, No. 5, p. ofaa141). US: Oxford University Press. google scholar
  • CLSI (Clinical and Laboratory Standards Institute). (2006). Methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically—seventh edition: M07. Wayne, PA, USA: CLSI google scholar CLSI (Clinical and Laboratory Standards Institute). (2023). Perfor-mance standards for antimicrobial susceptibility testing. 33rd ed. CLSI M100. Wayne, PA, USA: CLSI. google scholar
  • Cornely, O. A., Cisneros, J. M., Torre-Cisneros, J., Rodriguez-Hernandez, M. J., Tallon-Aguilar, L., Calbo, E., ... & Luckey, A. (2020). Pharmacokinetics and safety of aztreonam/avibactam for the treatment of complicated intra-abdominal infections in hos-pitalized adults: results from the REJUVENATE study. Journal of Antimicrobial Chemotherapy, 75(3), 618-627. google scholar
  • Dadashi, M., Hajikhani, B., Nazarinejad, N., Noorisepehr, N., Yazdani, S., Hashemi, A., ... & Fatemeh, S. (2023). Global prevalence and distribution of antibiotic resistance among clinical isolates of Stenotrophomonas maltophilia: a systematic review and meta-analysis. Journal of Global Antimicrobial Resistance 34, 253-267. https://doi.org/10.1016/j.jgar.2023.02.018 google scholar
  • de Almeida Torres, N., Junior, R. M., Lopes, L. F. B., Zeigler, R., & Uip, D. E. (2023). Synergistic combination of aztreonam and ceftazidime/avibactam against resistant Stenotrophomonas mal-tophilia on pancreatitis. The Journal of Infection in Developing Countries, 17(06), 881-885. google scholar
  • Eliopoulos, G. & Moellering Jr., R.C. (1996). Antimicrobial Combi-nations. In: Lorian, V., (Ed.), Antibiotics in Laboratory Medicine (pp. 330-396), Baltimore, USA, The Williams & Wilkins Co. google scholar
  • Emeraud, C., Escaut, L., Boucly, A., Fortineau, N., Bonnin, R. A., Naas, T., & Dortet, L. (2019). Aztreonam plus clavulanate, tazobactam, or avibactam for treatment of infections caused by metallo-^-lactamase-producing Gram-negative bacteria. Antimi-crobial Agents and Chemotherapy, 63(5), e00010-19. google scholar
  • EUCAST (The European Committee on Antimicrobial Susceptibility Testing). (2024a). Breakpoint tables for interpretation of MICs and zone diameters. Version 14.0, 2024. Retrieved from https: //www.eucast.org. google scholar
  • EUCAST (The European Committee on Antimicrobial Suscepti-bility Testing). (2024b). Breakpoints for aztreonam-avibactam May 2024. Retrieved from https://www.eucast.org/clinical_ breakpoints google scholar
  • Gil-Gil, T., Martmez, J. L., & Blanco, P. (2020). Mechanisms of an-timicrobial resistance in Stenotrophomonas maltophilia: a review of current knowledge. Expert Review of Anti-infective Therapy, 18(4), 335-347. google scholar
  • Gülmez, D., Cakar, A., Şener, B., Hasçelik, G., & Karakaya, J. (2010). Comparison of different antimicrobial susceptibility testing meth-ods for Stenotrophomonas maltophilia and results of synergy test-ing. Journal of Infection and Chemotherapy, 16(5), 322-328. google scholar
  • Hafiz, T. A., Aldawood, E., Albloshi, A., Alghamdi, S. S., Mubaraki, M. A., Alyami, A. S., & Aldriwesh, M. G. (2022). Stenotrophomonas maltophilia epidemiology, resistance charac-teristics, and clinical outcomes: understanding of the recent three years’ trends. Microorganisms, 10(12), 2506. google scholar
  • Karamanlıoğlu, D., & Dizbay, M. (2019). In vitro combination of tige-cycline with other antibiotics in Stenotrophomonas maltophilia isolates. Turkish Journal of Medical Sciences, 49(2), 683-686. google scholar
  • Lin, Q., Zou, H., Chen, X., Wu, M., Ma, D., Yu, H., ... & Huang, S. (2021). Avibactam potentiated the activity of both ceftazidime and aztreonam against S. maltophilia clinical isolates in vitro. BMC Microbiology, 21, 1-6. google scholar
  • Liu, J., Xiang, Y., & Zhang, Y. (2024). Stenotrophomonas maltophilia: An urgent threat with increasing antibiotic resistance. Current Microbiology, 81(1), 6. google scholar
  • Mojica, M. F., Bonomo, R. A., & Van Duin, D. (2023). Treatment approaches for severe Stenotrophomonas maltophilia infections. Current Opinion in Infectious Diseases, 36(6), 572-584. google scholar
  • Mojica, M. F., Humphries, R., Lipuma, J. J., Mathers, A. J., Rao, G. G., Shelburne, S. A., ... & Bonomo, R. A. (2022). Clinical challenges treating Stenotrophomonas maltophilia infections: an update. JAC-Antimicrobial Resistance, 4(3), dlac040. google scholar
  • Mojica, M. F., Papp-Wallace, K. M., Taracila, M. A., Barnes, M. D., Rutter, J. D., Jacobs, M. R., ... & Bonomo, R. A. (2017). Avibactam restores the susceptibility of clinical isolates of Stenotrophomonas maltophilia to aztreonam. Antimicrobial Agents and Chemother-apy, 61(10), e00777-17. https://doi.org/10.1128/aac.00777-17 google scholar
  • Odds, F.C. (2003). Synergy, antagonism, and what the chequerboard puts between them. Journal of Antimicrobial Chemotherapy, 52, 1. https://dx.doi.org/10.1093/jac/dkg301 google scholar
  • Ranieri, E. M., Denicolo, S., Stolfa, S., Dalfino, L., Bavaro, D. F., Sara-cino, A., ... & Mosca, A. (2023). Looking for Stenotrophomonas maltophilia treatment: in vitro activity of ceftazidime/avibactam alone and in combination with aztreonam. Journal of Chemother-apy, 35(7), 610-613. google scholar
  • Rizvi, M., Ahmed, J., Khan, F., Shukla, I., & Malik, A. (2013). As-sessment of combination therapy by time kill curve analysis and chequerboard assay for treatment of multi-drug resistant Pseu-domonas aeruginosa isolates. Journal of Global Antimicrobial Resistance, 1(2), 103-108. google scholar
  • Roemhild, R., Bollenbach, T., & Andersson, D. I. (2022). The physiol-ogy and genetics of bacterial responses to antibiotic combinations. Nature Reviews Microbiology, 20(8), 478-490. google scholar
  • Rossolini, G. M., Arhin, F. F., & Kantecki, M. (2024). In vitro ac-tivity of aztreonam-avibactam and comparators against Metallo-P-Lactamase-producing Enterobacterales from ATLAS Global Surveillance Program, 2016-2020. Journal of Global Antimicro-bial Resistance, 36, 123-131. google scholar
  • Sader, H. S., Carvalhaes, C. G., Arends, S. R., Castanheira, M., & Mendes, R. E. (2021). Aztreonam/avibactam activity against clin-ical isolates of Enterobacterales collected in Europe, Asia and Latin America in 2019. Journal of Antimicrobial Chemotherapy, 76(3), 659-666. google scholar
  • Sader, H. S., Castanheira, M., Kimbrough, J. H., Kantro, V., & Mendes, R. E. (2023). Aztreonam/avibactam activity against a large collec-tion of carbapenem-resistant Enterobacterales (CRE) collected in hospitals from Europe, Asia and Latin America (2019-21). JAC-Antimicrobial Resistance, 5(2), dlad032. google scholar
  • Sader, H. S., Duncan, L. R., Arends, S. R., Carvalhaes, C. G., & Castan-heira, M. (2020). Antimicrobial activity of aztreonam-avibactam and comparator agents when tested against a large collection of contemporary Stenotrophomonas maltophilia isolates from med-ical centers worldwide. Antimicrobial Agents and Chemotherapy, 64(11), e01433-20. https://doi.org/10.1128/aac.01433-20 google scholar
  • Singh, R., Kim, A., Tanudra, M. A., Harris, J. J., McLaughlin, google scholar
  • R. E., Patey, S., ... & Eakin, A. E. (2015). Pharmacokinet-ics/pharmacodynamics of a p-lactam and p-lactamase inhibitor combination: a novel approach for aztreonam/avibactam. Journal of Antimicrobial Chemotherapy, 70(9), 2618-2626. google scholar
  • Su, B. A., Chen, C. C., Chen, H. J., Lai, H. Y., Tsai, C. H., Lai, C. C., ... & Chao, C. M. (2023). In vitro activities of antimicrobial combi-nations against planktonic and biofilm forms of Stenotrophomonas maltophilia. Frontiers in Microbiology, 14, 1186669. google scholar
  • Tamma, P. D., Aitken, S. L., Bonomo, R. A., Mathers, A. J., van Duin, D., & Clancy, C. J. (2023). Infectious Diseases Society of America 2023 guidance on the treatment of antimicrobial resistant gram-negative infections. Clinical Infectious Diseases, ciad428. google scholar
  • Tyers, M., & Wright, G. D. (2019). Drug combinations: a strategy to extend the life of antibiotics in the 21st century. Nature Reviews Microbiology, 17(3), 141-155 google scholar
  • U.S. Food and Drug Administration. 2023. https://www.fda.gov/drugs/ development-resources/tigecycline-injection-products. Accessed 21 September 2024.Visalli, M. A., Jacobs, M. R., & Appelbaum, P. C. (1998). Activities of three quinolones, alone and in com-bination with extended-spectrum cephalosporins or gentamicin, against Stenotrophomonas maltophilia. Antimicrobial Agents and Chemotherapy, 42(8), 2002-2005. google scholar
  • Wang,C.H.,Yu,C.M.,Hsu,S.T.,&Wu,R.X. (2020). Levofloxacin-resistant Stenotrophomonas maltophilia: risk factors and antibi-otic susceptibility patterns in hospitalized patients. Journal of Hospital Infection, 104(1), 46-52. google scholar
  • White, R. L., Burgess, D. S., Manduru, M., & Bosso, J. A. (1996). Comparison of three different in vitro methods of detecting syn-ergy: time-kill, checkerboard, and E test. Antimicrobial Agents and Chemotherapy, 40(8), 1914-1918. google scholar
  • Zhao, J., Huang, Y., Li, J., Zhang, B., Dong, Z., & Wang, D. (2022). In vitro antibacterial activity and resistance prevention of an-timicrobial combinations for dihydropteroate synthase-carrying Stenotrophomonas maltophilia. Infection and Drug Resistance, 15, 3039-3046. google scholar
  • Zhao, J., Liu, Y., Liu, Y., Wang, D., Ni, W., Wang, R., ... & Zhang, B. (2018). Frequency and genetic determinants of tigecycline re-sistance in clinically isolated Stenotrophomonas maltophilia in Beijing, China. Frontiers in Microbiology, 9, 549. google scholar
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There are 43 citations in total.

Details

Primary Language English
Subjects Pharmacology and Pharmaceutical Sciences (Other)
Journal Section Original Article
Authors

Özlem Oyardı 0000-0001-9992-7225

Gülbeyaz Altunboğa 0000-0001-7562-7842

Fatıma Nur Olcay 0000-0001-8442-8538

Zayre Erturan 0000-0002-6427-3046

Project Number TKB-2023-8817
Publication Date December 30, 2024
Submission Date August 20, 2024
Acceptance Date September 23, 2024
Published in Issue Year 2024 Volume: 54 Issue: 3

Cite

APA Oyardı, Ö., Altunboğa, G., Olcay, F. N., Erturan, Z. (2024). Efficacy of aztreonam/avibactam against Stenotrophomonas maltophilia alone and in combination with tigecycline. İstanbul Journal of Pharmacy, 54(3), 395-402. https://doi.org/10.26650/IstanbulJPharm.2024.1536403
AMA Oyardı Ö, Altunboğa G, Olcay FN, Erturan Z. Efficacy of aztreonam/avibactam against Stenotrophomonas maltophilia alone and in combination with tigecycline. iujp. December 2024;54(3):395-402. doi:10.26650/IstanbulJPharm.2024.1536403
Chicago Oyardı, Özlem, Gülbeyaz Altunboğa, Fatıma Nur Olcay, and Zayre Erturan. “Efficacy of aztreonam/Avibactam Against Stenotrophomonas Maltophilia Alone and in Combination With Tigecycline”. İstanbul Journal of Pharmacy 54, no. 3 (December 2024): 395-402. https://doi.org/10.26650/IstanbulJPharm.2024.1536403.
EndNote Oyardı Ö, Altunboğa G, Olcay FN, Erturan Z (December 1, 2024) Efficacy of aztreonam/avibactam against Stenotrophomonas maltophilia alone and in combination with tigecycline. İstanbul Journal of Pharmacy 54 3 395–402.
IEEE Ö. Oyardı, G. Altunboğa, F. N. Olcay, and Z. Erturan, “Efficacy of aztreonam/avibactam against Stenotrophomonas maltophilia alone and in combination with tigecycline”, iujp, vol. 54, no. 3, pp. 395–402, 2024, doi: 10.26650/IstanbulJPharm.2024.1536403.
ISNAD Oyardı, Özlem et al. “Efficacy of aztreonam/Avibactam Against Stenotrophomonas Maltophilia Alone and in Combination With Tigecycline”. İstanbul Journal of Pharmacy 54/3 (December 2024), 395-402. https://doi.org/10.26650/IstanbulJPharm.2024.1536403.
JAMA Oyardı Ö, Altunboğa G, Olcay FN, Erturan Z. Efficacy of aztreonam/avibactam against Stenotrophomonas maltophilia alone and in combination with tigecycline. iujp. 2024;54:395–402.
MLA Oyardı, Özlem et al. “Efficacy of aztreonam/Avibactam Against Stenotrophomonas Maltophilia Alone and in Combination With Tigecycline”. İstanbul Journal of Pharmacy, vol. 54, no. 3, 2024, pp. 395-02, doi:10.26650/IstanbulJPharm.2024.1536403.
Vancouver Oyardı Ö, Altunboğa G, Olcay FN, Erturan Z. Efficacy of aztreonam/avibactam against Stenotrophomonas maltophilia alone and in combination with tigecycline. iujp. 2024;54(3):395-402.