Use of aminoglycosides as a therapeutic strategy to fight infections caused by Enterobacteriaceae that produce extended-spectrum β-lactamases

Authors

DOI:

https://doi.org/10.33448/rsd-v11i2.25680

Keywords:

Bacterial infections; Extended spectrum β-lactamases; Enterobacteria; Antibiotics.

Abstract

The treatment of infections caused by enterobacteria that produce extended-spectrum β-lactamases enzymes (ESBLs) is increasingly challenging, so that the indiscriminate and exacerbated use of antibiotics has promoted bacterial resistance and dissemination of these pathogens, making the treatment of these bacteria a public health challenge. Taking into account that aminoglycosides are the antibiotics indicated for the clinical treatment of infections caused by enterobacteria, the objective of this review was to describe the use and effectiveness of aminoglycosides as a therapeutic strategy to combat infections caused by enterobacteria that produce ESBLs. A bibliographic review was carried out through searches in PubMed, Scientific Electronic Library On-line (SCIELO) and Google Scholar databases, selecting articles published between 2011 and 2020, in English, with the following descriptors: Gram-negative bacteria, Resistance and Infections. The results showed that plazomycin is effective against strains of Citrobacter spp., Klebsiella spp. and Enterobacter spp. producing ESBLs, while gentamicin, tobramycin and apramycin are effective against E. coli, Burkholderia spp., Serratia spp., Citrobacter spp., Enterobacter spp. and Klebsiella spp. ESBL producers. Regarding the combination therapy, it can be observed that the combination between two aminoglycosides or between aminoglycosides and other antibiotics promoted a synergistic effect when compared with the monotherapy against E. coli, Enterobacter spp., Enterobacter cloacae and mainly Klebsiella pneumonia producing ESBLs. Therefore, aminoglycosides have shown great potential against this group of bacteria, which represent a great challenge for the medical profession.

References

Abdelraouf, K., Kim, A., Krause, K. M., & Nicolau, D. P. (2018). In vivo efficacy of plazomicin alone or in combination with meropenem or tigecycline against Enterobacteriaceae isolates exhibiting various resistance mechanisms in an immunocompetent murine septicemia model. Antimicrobial Agents and Chemotherapy, 62(8), e01074-18.

Almugadam, B. S., Elbala, A. S., Elkheir, A. S. E., Mazid, M. A., & Osman, S. A. (2018a). Carbapenem resistance Enterobacteriaceae among wound. Clinical Microbiology: Open Access, 7(1), 01-03,

Almugadam, B. S., Ali, N. O., Ahmed, A. B., Ahmed, E. B., & Wang, L. (2018b). Prevalence and antibiotics susceptibility patterns of carbapenem resistant Enterobacteriaceae. Journal of Bacteriology & Mycology: Open Access, 6(3), 187-190.

Avent, M. L., Rogers, B. A., Cheng, A. C., & Paterson, D. L. (2011). Current use of aminoglycosides: indications, pharmacokinetics and monitoring for toxicity. Internal Medicine Journal, 41(6), 441-449.

Barbier, F., Bailly, S., Schwebel, C., Papazian, L., Azoulay, É., Kallel, H., Siami, S., Argaud, l., Marcotte,G., Misset, B., Reignier, J., Darmon, M., Zahar, J., Toledano, D.G., Montmollin, E., Souweine, B., Mourvillier, B., & Timsit, J. F, (2018). Infection-related ventilator-associated complications in ICU patients colonised with extended-spectrum β-lactamase-producing Enterobacteriaceae. Intensive Care Medicine, 44(5), 616-626.

Böttger, E. C., & Crich, D. (2019). Aminoglycosides: time for the resurrection of a neglected class of antibacterials? ACS Infectious Diseases, 6(2), 168-172.

Bruni, G. N., & Kralj, J. M. (2020). Membrane voltage dysregulation driven by metabolic dysfunction underlies bactericidal activity of aminoglycosides. Elife, 9, e58706.

Bush, K. (2018). Past and present perspectives on β-lactamases. Antimicrobial Agents and Chemotherapy, 62(10), e01076-18.

Bush, K. (2013). Proliferation and significance of clinically relevant β‐lactamases. Annals of the New York Academy of Sciences, 1277(1), 84-90.

Bush, K., & Bradford, P. A. (2019). Interplay between β-lactamases and new β-lactamase inhibitors. Nature Reviews Microbiology, 17(5), 295-306.

Bush, K., & Fisher, J. F. (2011). Epidemiological expansion, structural studies, and clinical challenges of new β-lactamases from gram-negative bacteria. Annual Review of Microbiology, 65, 455-478.

Castanheira, M., Deshpande, L. M., Woosley, L. N., Serio, A. W., Krause, K. M., & Flamm, R. K. (2018a). Activity of plazomicin compared with other aminoglycosides against isolates from European and adjacent countries, including Enterobacteriaceae molecularly characterized for aminoglycoside-modifying enzymes and other resistance mechanisms. Journal of Antimicrobial Chemotherapy, 73(12), 3346-3354.

Castanheira, M., Davis, A. P., Mendes, R. E., Serio, A. W., Krause, K. M., & Flamm, R. K. (2018b). In vitro activity of plazomicin against Gram-negative and Gram-positive isolates collected from US hospitals and comparative activities of aminoglycosides against carbapenem-resistant Enterobacteriaceae and isolates carrying carbapenemase genes. Antimicrobial Agents and Chemotherapy, 62(8), e00313-18.

Cebrero-Cangueiro, T., Álvarez-Marín, R., Labrador-Herrera, G., Smani, Y., Cordero-Matía, E., Pachón, J., & Pachón-Ibáñez, M. E. (2018). In vitro activity of pentamidine alone and in combination with aminoglycosides, tigecycline, rifampicin, and doripenem against clinical strains of carbapenemase-producing and/or colistin-resistant Enterobacteriaceae. Frontiers in Cellular and Infection Microbiology, 8(363).

Cheng, M. P., Lee, R. S., Cheng, A. P., De L’Étoile-Morel, S., Demir, K., Yansouni, C. P., Harris, P.; Mcdonald, E. G & Lee, T. C. (2019). Beta-lactam/beta-lactamase inhibitor therapy for potential AmpC-producing organisms: a systematic review and meta-analysis. In Open Forum Infectious Diseases (Vol. 6, No. 7, p. ofz248). US: Oxford University Press.

Clark, J. A., & Burgess, D. S. (2020). Plazomicin: a new aminoglycoside in the fight against antimicrobial resistance. Therapeutic Advances in Infectious Disease, 7, 2049936120952604.

Derin, O., Fonseca, L., Sanchez-Salas, R., & Roberts, M. J. (2020). Infectious complications of prostate biopsy: winning battles but not war. World Journal of Urology, 38(11).

Detsis, M., Karanika, S., & Mylonakis, E. (2017). ICU acquisition rate, risk factors, and clinical significance of digestive tract colonization with extended-Spectrum Beta-lactamase–producing Enterobacteriaceae: a systematic review and meta-analysis. Critical Care Medicine, 45(4), 705-714.

Dhillon, R. H. P., & Clark, J. (2012). ESBLs: a clear and present danger? Critical Care Research and Practice, 2012.

Galani, I., Souli, M., Daikos, G. L., Chrysouli, Z., Poulakou, G., Psichogiou, M., Panagea, T.; Argyropoulou, A.; Stefanou, L.; Plakias, G.; Giamarellou, H. & Petrikkos, G. (2012). Activity of plazomicin (ACHN-490) against MDR clinical isolates of Klebsiella pneumoniae, Escherichia coli, and Enterobacter spp. from Athens, Greece. Journal of Chemotherapy, 24(4), 191-194.

Ghafourian, S., Sadeghifard, N., Soheili, S., & Sekawi, Z. (2015). Extended spectrum beta-lactamases: definition, classification and epidemiology. Current Issues in Molecular Biology, 17(1), 11-22.

Gutiérrez-Gutiérrez, B., & Rodríguez-Baño, J. (2019). Current options for the treatment of infections due to extended-spectrum beta-lactamase-producing Enterobacteriaceae in different groups of patients. Clinical Microbiology and Infection, 25(8), 932-942.

Haenni, M., Châtre, P., & Madec, J. Y. (2014). Emergence of Escherichia coli producing extended-spectrum AmpC β-lactamases (ESAC) in animals. Frontiers in Microbiology, 5, 53.

Haidar, G., Alkroud, A., Cheng, S., Churilla, T. M., Churilla, B. M., Shields, R. K., Doi, Y., Clancy, C. J., & Nguyen, M. H. (2016). Association between the presence of aminoglycoside-modifying enzymes and in vitro activity of gentamicin, tobramycin, amikacin, and plazomicin against Klebsiella pneumoniae carbapenemase-and extended-spectrum-β-lactamase-producing Enterobacter species. Antimicrobial Agents and Chemotherapy, 60(9), 5208-5214.

Jackson, J., Chen, C., & Buising, K. (2013). Aminoglycosides: how should we use them in the 21st century?. Current Opinion in Infectious Diseases, 26(6), 516-525.

Jassem, A. N., Zlosnik, J. E., Henry, D. A., Hancock, R. E., Ernst, R. K., & Speert, D. P. (2011). In vitro susceptibility of Burkholderia vietnamiensis to aminoglycosides. Antimicrobial Agents and Chemotherapy, 55(5), 2256-2264.

Juhas, M., Widlake, E., Teo, J., Huseby, D. L., Tyrrell, J. M., Polikanov, Y. S., Ercan, O.; Petersson, A.; Cao, S.; Aboklaish, A. F.; Rominskia, A.; Crich, D.; Bottger, E. C.; Walsh, T. R.; Hughes, D. & Hobbie, S. N. (2019). In vitro activity of apramycin against multidrug-, carbapenem-and aminoglycoside-resistant Enterobacteriaceae and Acinetobacter baumannii. Journal of Antimicrobial Chemotherapy, 74(4), 944-952.

Mataraci Kara, E., Yilmaz, M., İstanbullu Tosun, A., & Özbek Çelik, B. (2020). Evaluation of the synergy of ceftazidime/avibactam in combination with colistin, doripenem, levofloxacin, tigecycline, and tobramycin against OXA-48 producing Enterobacterales. Journal of Chemotherapy, 32(4), 171-178.

Karaiskos, I., Galani, I., Souli, M., & Giamarellou, H. (2019). Novel β-lactam-β-lactamase inhibitor combinations: expectations for the treatment of carbapenem-resistant Gram-negative pathogens. Expert Opinion on Drug Metabolism & Toxicology, 15(2), 133-149.

Kateregga, J. N., Kantume, R., Atuhaire, C., Lubowa, M. N., & Ndukui, J. G. (2015). Phenotypic expression and prevalence of ESBL-producing Enterobacteriaceae in samples collected from patients in various wards of Mulago Hospital, Uganda. BMC Pharmacology and Toxicology, 16(1), 1-6.

Kizilca, O., Siraneci, R., Yilmaz, A., Hatipoglu, N., Ozturk, E., Kiyak, A., & Ozkok, D. (2012). Risk factors for community‐acquired urinary tract infection caused by ESBL‐producing bacteria in children. Pediatrics International, 54(6), 858-862.

Krause, K. M., Serio, A. W., Kane, T. R., & Connolly, L. E. (2016). Aminoglycosides: an overview. Cold Spring Harbor Perspectives in Medicine, 6(6), a027029.

Lebeaux, D., Chauhan, A., Létoffé, S., Fischer, F., de Reuse, H., Beloin, C., & Ghigo, J. M. (2014). pH-mediated potentiation of aminoglycosides kills bacterial persisters and eradicates in vivo biofilms. The Journal of Infectious Diseases, 210(9), 1357-1366.

Lonchel, C. M., Meex, C., Gangoué-Piéboji, J., Boreux, R., Assoumou, M. C. O., Melin, P., & De Mol, P. (2012). Proportion of extended-spectrum ß-lactamase-producing Enterobacteriaceae in community setting in Ngaoundere, Cameroon. BMC Infectious Diseases, 12(1), 1-7.

Mikhail, S., Singh, N. B., Kebriaei, R., Rice, S. A., Stamper, K. C., Castanheira, M., & Rybak, M. J. (2019). Evaluation of the synergy of ceftazidime-avibactam in combination with meropenem, amikacin, aztreonam, colistin, or fosfomycin against well-characterized multidrug-resistant Klebsiella pneumoniae and Pseudomonas aeruginosa. Antimicrobial Agents and Chemotherapy, 63(8), e00779-19.

Nagai, J., & Takano, M. (2014). Entry of aminoglycosides into renal tubular epithelial cells via endocytosis-dependent and endocytosis-independent pathways. Biochemical Pharmacology, 90(4), 331-337.

Nikolić, E., Brandmajer, T., Bokan, V., Ulyashova, M., & Rubtsova, M. (2018). Prevalence of Escherichia coli resistant to beta-lactam antibiotics among patients with chronic obstructive pulmonary disease and urinary tract infection. The Tohoku Journal of Experimental Medicine, 244(4), 271-277.

Ni, W., Wei, C., Zhou, C., Zhao, J., Liang, B., Cui, J., Wang, R & Liu, Y. (2016). Tigecycline-amikacin combination effectively suppresses the selection of resistance in clinical isolates of KPC-producing Klebsiella pneumoniae. Frontiers in Microbiology, 7, 1304.

Omrani, A. S., & Almaghrabi, R. S. (2017). Complications of hematopoietic stem cell transplantation: bacterial infections. Hematology/Oncology and Stem Cell Therapy, 10(4), 228-232.

Ozbek, B., Mataracı-Kara, E., Er, S., Ozdamar, M., & Yilmaz, M. (2015). In vitro activities of colistin, tigecycline and tobramycin, alone or in combination, against carbapenem-resistant Enterobacteriaceae strains. Journal of Global Antimicrobial Resistance, 3(4), 278-282.

Pagkalis, S., Mantadakis, E., Mavros, M. N., Ammari, C., & Falagas, M. E. (2011). Pharmacological considerations for the proper clinical use of aminoglycosides. Drugs, 71(17), 2277-2294.

Park, J. J., Seo, Y. B., & Lee, J. (2017). Antimicrobial susceptibilities of Enterobacteriaceae in community-acquired urinary tract infections during a 5-year period: a single hospital study in Korea. Infection & Chemotherapy, 49(3), 184-193.

Philippon, A. (2013). Les bêta-lactamases à spectre élargi ou étendu (BLSE). Immuno-Analyse & Biologie Spécialisée, 28(5-6), 287-296.

Rodríguez-Avial, I., Pena, I., Picazo, J. J., Rodríguez-Avial, C., & Culebras, E. (2015). In vitro activity of the next-generation aminoglycoside plazomicin alone and in combination with colistin, meropenem, fosfomycin or tigecycline against carbapenemase-producing Enterobacteriaceae strains. International Journal of Antimicrobial Agents, 46(6), 616-621.

Saravanan, M., Ramachandran, B., & Barabadi, H. (2018). The prevalence and drug resistance pattern of extended spectrum β–lactamases (ESBLs) producing Enterobacteriaceae in Africa. Microbial Pathogenesis, 114, 180-192.

Saravolatz, L. D., & Stein, G. E. (2020). Plazomicin: a new aminoglycoside. Clinical Infectious Diseases, 70(4), 704-709.

Shaikh, S., Fatima, J., Shakil, S., Rizvi, S. M. D., & Kamal, M. A. (2015). Antibiotic resistance and extended spectrum beta-lactamases: Types, epidemiology and treatment. Saudi Journal of Biological Sciences, 22(1), 90-101.

Shields, R. K., Clancy, C. J., Press, E. G., & Nguyen, M. H. (2016). Aminoglycosides for treatment of bacteremia due to carbapenem-resistant Klebsiella pneumoniae. Antimicrobial agents and chemotherapy, 60(5), 3187-3192.

Tang, H. J., Lai, C. C., Chen, C. C., Zhang, C. C., Weng, T. C., Chiu, Y. H., Toh, H. S.; Chiang, S. R.; Yu, W. L.; Ko, W. C & Chuang, Y. C. (2019). Colistin-sparing regimens against Klebsiella pneumoniae carbapenemase-producing K. pneumoniae isolates: combination of tigecycline or doxycycline and gentamicin or amikacin. Journal of Microbiology, Immunology and Infection, 52(2), 273-281.

Thwaites, M., Hall, D., Stoneburner, A., Shinabarger, D., Serio, A. W., Krause, K. M., Marra, A. & Pillar, C. (2018). Activity of plazomicin in combination with other antibiotics against multidrug-resistant Enterobacteriaceae. Diagnostic Microbiology and Infectious Disease, 92(4), 338-345.

Tooke, C. L., Hinchliffe, P., Bragginton, E. C., Colenso, C. K., Hirvonen, V. H., Takebayashi, Y., & Spencer, J. (2019). β-Lactamases and β-Lactamase Inhibitors in the 21st Century. Journal of Molecular Biology, 431(18), 3472-3500.

Walkty, A., Karlowsky, J. A., Baxter, M. R., Adam, H. J., & Zhanel, G. G. (2019). In vitro activity of plazomicin against gram-negative and gram-positive bacterial pathogens isolated from patients in Canadian hospitals from 2013 to 2017 as part of the CANWARD surveillance study. Antimicrobial Agents and Chemotherapy, 63(1), e02068-18.

Yadav, K. K., Adhikari, N., Khadka, R., Pant, A. D., & Shah, B. (2015). Multidrug resistant Enterobacteriaceae and extended spectrum β-lactamase producing Escherichia coli: a cross-sectional study in National Kidney Center, Nepal. Antimicrobial Resistance and Infection Control, 4(1), 1-7.

Yu, W., Zhou, K., Guo, L., Ji, J., Niu, T., Xiao, T., Shen, P & Xiao, Y. (2017). In vitro pharmacokinetics/pharmacodynamics evaluation of fosfomycin combined with amikacin or colistin against KPC2-producing Klebsiella pneumoniae. Frontiers in Cellular and Infection Microbiology, 7, 246.

Published

06/02/2022

How to Cite

SILVA, J. E. B. da; SOUZA, J. B. de; MACÊDO, D. C. dos S.; BARROS, M. C. de S. A.; CAMPOS, L. A. de A.; COSTA JÚNIOR, S. D. da .; FERRAZ CARVALHO, R. de S. .; CAVALCANTI, I. M. F. Use of aminoglycosides as a therapeutic strategy to fight infections caused by Enterobacteriaceae that produce extended-spectrum β-lactamases. Research, Society and Development, [S. l.], v. 11, n. 2, p. e57711225680, 2022. DOI: 10.33448/rsd-v11i2.25680. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/25680. Acesso em: 23 nov. 2024.

Issue

Section

Review Article