Advantages of using liposome-encapsulated antibiotics to fight infections caused by enterobacteria

Authors

DOI:

https://doi.org/10.33448/rsd-v10i6.15439

Keywords:

Gram-negative bactéria; Bacterial resistance; Antimicrobials; Nanotechnology.

Abstract

Introduction: The treatment of diseases caused by enterobacteria is an increasing challenge. This problem results from the inefficiency of antibiotics to fight pathogens or to stimulate phagocytosis of cells of the reticuloendothelial system, mainly against bacteria that install and multiply inside phagocytic cells. Some antibiotics are ineffective at entering cells or have their capacity reduced by the plasma membrane. Thus, the scientific community joins efforts seeking new therapeutic alternatives that overcome these limitations. Liposomes are lipid nanocarriers capable of encapsulating antibiotics, aiming at increasing the specificity of delivery, the concentration of compounds delivered to the site, maintaining the plasma concentration of drugs and protecting the active molecules. Thus, the objective of this review was to describe the main liposomal properties, emphasizing the advantages of using these lipid vesicles to administer antibiotics against infections caused by enterobacteria. Methodology: This is a bibliographic review through searches in national and international electronic databases, selecting articles from 2007 to 2020 using the descriptors: Gram-negative bacteria, bacterial resistance, antimicrobials and nanotechnology. Results: Cationic and furtive liposomes consisting mainly of cholesterol, PEG, phosphatidylcholine and carboxymethyl chitosan encapsulating drugs such as amoxicillin, ciprofloxacin, cloxacillin, vancomycin, azithromycin, amoxicillin, cefepime, gentamicin and cefotaxime have shown antibacterial activity. Liposomes encapsulating drugs such as chloramphenicol, azithromycin, gentamicin and polymyxin B showed greater antibiofilm efficiency compared to enterobacteria when compared to non-encapsulated drugs. Conclusion: The results showed that liposomes have significant therapeutic potential for the treatment of infections caused by enterobacteria.

Author Biographies

Júlio Eduardo Barbosa da Silva, Faculdade São Miguel

Graduando em Biomedicina no Centro Universitário São Miguel. Atualmente é integrante do grupo de pesquisa Microbiologia clínica e Novas Abordagens Terapêuticas (MicroNAT).

Jaqueline Barbosa de Souza, Universidade Federal de Pernambuco

Graduada em Ciências Farmacêuticas pelo Centro Universitário São Miguel. Mestranda pelo Programa de Pós-Graduação em Inovação Terapêutica (PPGIT) da Universidade Federal de Pernambuco (UFPE). Atualmente é integrante do grupo de pesquisa Microbiologia clínica e Novas Abordagens Terapêuticas (MicroNAT).

Daniel Charles dos Santos Macêdo, Universidade Federal de Pernambuco

Graduado em Ciências Farmacêuticas pela Universidade Federal de Pernambuco (UFPE). Mestre pelo Programa de Pós-Graduação em Ciências Farmacêuticas da Universidade Federal de Pernambuco (PPGCF/UFPE). Doutorado pelo PPGCF/UFPE. Atualmente é integrante do grupo de pesquisa Nanotecnologia, Biotecnologia e Cultura de Células (NANOBIOCEL) e do grupo Laboratório de Nanotecnologia Farmacêutica (LNFarm) da UFPE.

Luís André de Almeida Campos, Universidade Federal de Pernambuco

Graduado em Ciências Biológicas pelo Centro Acadêmico de Vitória da Universidade Federal de Pernambuco (CAV/UFPE). Mestre pelo Programa de Pós-graduação em Biologia Aplicada a Saúde da Universidade Federal de Pernambuco (PPGBAS/UFPE). Doutorando pelo Programa de Pós-Graduação em Ciências Biológicas da Universidade Federal de Pernambuco (PPGCB/UFPE). Atualmente, é integra os grupos de pesquisa Microbiologia clínica e Novas Abordagens Terapêuticas (MicroNAT) e do grupo Laboratório de Nanotecnologia Farmacêutica (LNFarm) da UFPE. 

Isabella Macário Ferro Cavalcanti, Universidade Federal de Pernambuco

Graduada em Biomedicina pela Universidade Federal de Pernambuco (UFPE). Especialista em Microbiologia Clínica pela Universidade de Pernambuco (UPE). Mestre pelo Programa de Pós-graduação em Inovação Terapêutica da UFPE (PPGIT/UFPE). Doutora pelo Programa de Pós-graduação em Ciências Biológicas da UFPE (PPGCB/UFPE). Professora Associada I das disciplinas de Microbiologia, Imunologia e Exames Laboratoriais no Centro Acadêmico de Vitória (CAV/UFPE). Membro permanente do Programa de Pós-Graduação de Mestrado Profissional em Ensino de Biologia em Rede Nacional (PROFBIO), conceito 4 da CAPES. Chefe e Pesquisadora do Setor de Microbiologia Clínica do Laboratório de Imunopatologia Keizo Asami da Universidade Federal de Pernambuco (LIKA/UFPE). Membro da Sociedade Brasileira de Microbiologia. Membro do Comitê Científico e Consultivo de Apoio às Ações de Combate ao COVID-19 - CAV/UFPE. Líder do grupo de pesquisa Microbiologia clínica e Novas Abordagens Terapêuticas (MicroNAT).

References

Abed, N. & Couvreur, P. (2014). Nanocarriers for antibiotics: a promising solution to treat intracellular bacterial infections. International Journal of Antimicrobial Agents, 43 (6), 485-496.

Aghapour, Z., Gholizadeh, P., Ganbarov, K., Bialvaei, A. Z., Mahmood, S. S., Tanomand, A., Yousef M.; Asgharzadeh M.; Yousef B. & Kafil, H. S. (2019). Molecular mechanisms related to colistin resistance in Enterobacteriaceae. Infection and Drug Resistance, 12, 965.

Aghdam, M. A., Bagheri, R., Mosafer, J., Baradaran, B., Hashemzaei, M., Baghbanzadeh, A., Guardia M. & Mokhtarzadeh, A. (2019). Recent advances on thermosensitive and pH-sensitive liposomes employed in controlled release. Journal of Controlled Release, 315, 1-22.

Akbarzadeh, A., Rezaei-Sadabady, R., Davaran, S., Joo, S. W., Zarghami, N., Hanifehpour, Y., Samiei M.; Kouhi M. & Nejati-Koshki, K. (2013). Liposome: classification, preparation, and applications. Nanoscale Research Letters, 8 (1), 1-9.

Alhariri, M., Majrashi, M. A., Bahkali, A. H., Almajed, F. S., Azghani, A. O., Khiyami, M. A., Alyamani E. J.; Aljohani S. M. & Halwani, M. A. (2017). Efficacy of neutral and negatively charged liposome-loaded gentamicin on planktonic bacteria and biofilm communities. International Journal of Nanomedicine, 12, 6949.

Aljihani, S. A., Alehaideb, Z., Alarfaj, R. E., Alghoribi, M. F., Akiel, M. A., Alenazi, T. H., Al-Fahad J. A., Al Tamimi, S. M., Albakr, T. M., Alshehri, A., Alyahya, S. M., Yassin, A. E. B. & Halwani, M. A. (2020). Enhancing azithromycin antibacterial activity by encapsulation in liposomes/liposomal-N-acetylcysteine formulations against resistant clinical strains of Escherichia coli. Saudi Journal of Biological Sciences, 27 (11), 3065-3071.

Alotaibi, F. (2019). Carbapenem-resistant Enterobacteriaceae: an update narrative review from Saudi Arabia. Journal of Infection and Public Health, 12 (4), 465-471.

Aryasomayajula, B., Salzano, G. & Torchilin, V. P. (2017). Multifunctional liposomes. Methods in Molecular Biology, 1530, 41-61.

Asfour, H. Z. (2017). Cefotaxime combined ellagic acid in a liposomal form for more stable and antimicrobial effective formula. American Journal of Microbiological Research, 5 (5), 113-117.

Babushkina, I. V., Bondarenko, A. S., Ulyanov, V. Y. & Mamonova, I. A. (2020). Biofilm formation by gram-negative bacteria during implant-associated infection. Bulletin of Experimental Biology and Medicine, 169 (3), 365-368.

Batista, C. M., Carvalho, C. M. B. D. & Magalhães, N. S. S. (2007). Lipossomas e suas aplicações terapêuticas: Estado da arte. Revista Brasileira de Ciências Farmacêuticas, 43 (2), 167-179.

Bennett, J. E.; Dolin, R. & Blaser, M. J. (2014). Mandell, douglas, and bennett's principles and practice of infectious diseases: 2-volume set (Vol. 2). Elsevier Health Sciences.

Briones, E., Colino, C. I. & Lanao, J. M. (2008). Delivery systems to increase the selectivity of antibiotics in phagocytic cells. Journal of Controlled Release, 125 (3), 210-227.

Cai, L., Wang, H., Liang, L., Wang, G., Xu, X. & Wang, H. (2018). Response of formed‐biofilm of Enterobacter cloacae, Klebsiella oxytoca, and Citrobacter freundii to chlorite‐based disinfectants. Journal of Food Science, 83 (5), 1326-1332.

Carole, G. M. B. V., Kouadio, G. N., Baguy, O. M., Djénéba, O. G., Ayayi, A., Bertin, T. K., Anatole T. A., Innocent K. K., Kpoda D. S., Eric T., Ali K., Fernique K., Alphonse K., Mireille D. & Bmr, G. (2018). Antimicrobial resistance profile and molecular characterization of extended-spectrum beta-lactamase genes in enterobacteria isolated from human, animal and environment. Journal of Advances in Microbiology, 10 (1), 1-9.

Cé, R., Pacheco, B. Z., Ciocheta, T. M., Barbosa, F. S., de CS Alves, A., Dallemole, D. R. & Pohlmann, A. R. (2021). Antibacterial activity against Gram-positive bacteria using fusidic acid-loaded lipid-core nanocapsules. Reactive and Functional Polymers, 162 (1), 104876.

Cohen, J.; Powderly, W. & Opal, S. (2016). Infectious diseases. Elsevier.

Daraee, H., Etemadi, A., Kouhi, M., Alimirzalu, S. & Akbarzadeh, A. (2016). Application of liposomes in medicine and drug delivery. Artificial Cells, Nanomedicine, and Biotechnology, 44 (1), 381-391.

Davin-Regli, A., Lavigne, J. P. & Pagès, J. M. (2019). Enterobacter spp.: update on taxonomy, clinical aspects, and emerging antimicrobial resistance. Clinical Microbiology Reviews, 32 (4).

Dias-Souza, M. V., Soares, D. L. & Dos Santos, V. L. (2017). Comparative study of free and liposome-entrapped chloramphenicol against biofilms of potentially pathogenic bacteria isolated from cooling towers. Saudi Pharmaceutical Journal, 25 (7), 999-1004.

Dou, Y., Hynynen, K. & Allen, C. (2017). To heat or not to heat: Challenges with clinical translation of thermosensitive liposomes. Journal of Controlled Release, 249, 63-73.

El-Hammadi, M. M. & Arias, J. L. (2019). An update on liposomes in drug delivery: a patent review (2014-2018). Expert Opinion on Therapeutic Patents, 29 (11), 891-907.

Estrela, C. (2018). Metodologia científica: ciência, ensino, pesquisa. São Paulo, Brasil: Artes Médicas.

Filipczak, N., Pan, J., Yalamarty, S. S. K. & Torchilin, V. P. (2020). Recent advancements in liposome technology. Advanced Drug Delivery Reviews, 156, 04-22.

Fu, Y. Y., Zhang, L., Yang, Y., Liu, C. W., He, Y. N., Li, P. & Yu, X. (2019). Synergistic antibacterial effect of ultrasound microbubbles combined with chitosan-modified polymyxin B-loaded liposomes on biofilm-producing Acinetobacter baumannii. International Journal of Nanomedicine, 14, 1805-1815.

Ghatage, T., Jadhav, S. & Kore, V. (2017). A Review on Stealth Liposomes: Novel Drug Delivery System. International Journal of Scientific Engineering and Technology Research, 6 (14), 2744-2750.

Hamblin, K. A., Armstrong, S. J., Barnes, K. B., Davies, C., Wong, J. P., Blanchard, J. D., Harding S. V., Simpson A. J. H. & Atkins, H. S. (2014). Liposome encapsulation of ciprofloxacin improves protection against highly virulent Francisella tularensis strain Schu S4. Antimicrobial Agents and Chemotherapy, 58 (6), 3053-3059.

Has, C. & Sunthar, P. (2020). A comprehensive review on recent preparation techniques of liposomes. Journal of Liposome Research, 30 (4), 336-365.

Haussler, S. & Fuqua, C. (2013). Biofilms 2012: new discoveries and significant wrinkles in a dynamic field. Journal of Bacteriology, 195 (13), 2947-2958.

Huh, A. J. & Kwon, Y. J. (2011). “Nanoantibiotics”: a new paradigm for treating infectious diseases using nanomaterials in the antibiotics resistant era. Journal of Controlled Release, 156 (2), 128-145.

Ichim, D. L., Duceac, L. D., Marcu, C., Iordache, A. C., Ciomaga, I. M., Luca, A. C., Goroftef E. R. B.; Mitrea G.; Damir D. & Stafie, L. (2019). Synthesis and characterization of colistin loaded nanoparticles used to combat multi-drug resistant microorganisms. Revista de Chimie 70 (10).

Jainamboo, M., Gopukumar, S. & Praseetha, P. (2017). Improving the clinical efficacy of drugs by liposomes against resistant bacteria (Mdr Bacteria) – An in vitro study. International Journal of Pharma and Bio Sciences, 8 (3), 42-57.

Kang, E., Crouse, A., Chevallier, L., Pontier, S. M., Alzahrani, A., Silué, N., Valois F. X. C.; Montagutelli X.; Gruenheid, S. & Malo, D. (2018). Enterobacteria and host resistance to infection. Mammalian Genome, 29 (7), 558-576.

Kumar, A., Alam, A., Rani, M., Ehtesham, N. Z. & Hasnain, S. E. (2017). Biofilms: Survival and defense strategy for pathogens. International Journal of Medical Microbiology, 307 (8), 481-489.

Lewis, K. (2010). Persister cells. Annual Review of Microbiology, 64, 357-372.

Linninge, C., Roth, B., Erlanson-Albertsson, C., Molin, G., Toth, E. & Ohlsson, B. (2018). Abundance of Enterobacteriaceae in the colon mucosa in diverticular disease. World Journal of Gastrointestinal Pathophysiology, 9 (1), 18.

Li, X. X., Shi, S., Rong, L., Feng, M. Q. & Zhong, L. (2018). The impact of liposomal linolenic acid on gastrointestinal microbiota in mice. International Journal of Nanomedicine, 13, 1399-1409.

Loh, B., Gondil, V. S., Manohar, P., Khan, F. M., Yang, H. & Leptihn, S. (2021). Encapsulation and delivery of therapeutic phages. Applied and Environmental Microbiology, 87 (5).

Moghimipour, E. & Handali, S. (2013). Liposomes as drug delivery systems: properties and applications. Research Journal of Pharmaceutical, Biological and Chemical Sciences, 4 (1), 169-185.

Monteiro, N., Martins, M., Martins, A., Fonseca, N. A., Moreira, J. N., Reis, R. L. & Neves, N. M. (2015). Antibacterial activity of chitosan nanofiber meshes with liposomes immobilized releasing gentamicin. Acta Biomaterialia, 18, 196-205.

Montso, K. P., Dlamini, S. B., Kumar, A. & Ateba, C. N. (2019). Antimicrobial resistance factors of extended-spectrum beta-lactamases producing Escherichia coli and Klebsiella pneumoniae isolated from Cattle Farms and Raw Beef in North-West Province, South Africa. BioMed Research International, 2019.

Moyá, M. L., López-López, M., Lebrón, J. A., Ostos, F. J., Pérez, D., Camacho, V., Beck I., Bohórquez V. M., Camean M., Madinabeitia N. & López-Cornejo, P. (2019). Preparation and characterization of new liposomes. Bactericidal activity of cefepime encapsulated into cationic liposomes. Pharmaceutics, 11 (2), 69.

Narayana, P. S. V. V. S. & Srihari, P. S. V. V. (2019). Biofilm resistant surfaces and coatings on implants: A review. Materials Today: Proceedings, 18, 4847-4853.

Nicolosi, D., Cupri, S., Genovese, C., Tempera, G., Mattina, R., & Pignatello, R. (2015). Nanotechnology approaches for antibacterial drug delivery: preparation and microbiological evaluation of fusogenic liposomes carrying fusidic acid. International Journal of Antimicrobial Agents, 45 (6), 622-626.

OPAS-OMS (2017). OMS publica lista de bactérias para as quais se necessitam novos antibióticos urgentemente. https://www.paho.org/bra/index.php?option=com_content&view=article&id=5357:oms-publica-lista-de-bacterias-para-as-quais-se-necessitam-novos-antibioticos-urgentemente&Itemid=812.

Pati, N. B., Doijad, S. P., Schultze, T., Mannala, G. K., Yao, Y., Jaiswal, S., Ryan D.; Suar M.; Gwozdzinski K., Bunk B., Mraheil M. A., Hegemann J. D., Sproer C., Goesmann A., Falgenhauer L., Hain T., Imirzalioglu C., Mshana S. E., Overmann J. & Chakraborty, T. (2018). Enterobacter bugandensis: a novel enterobacterial species associated with severe clinical infection. Scientific Reports, 8 (1), 1-11.

Porcheron G., Garénaux A., Proulx J., Sabri M. & Dozois C. M. (2013). Iro, copper, zin, and manganese transport and regulation in pathogenic Enterobacteria: correlations between strains, site of infection and the relative importance of the differente metal transport systems for virulence. Frontiers in Cellular and Infection Microbiology, Vol. 3.

Ramos-Vivas, J., Chapartegui-González, I., Fernández-Martínez, M., González-Rico, C., Fortún, J., Escudero, R., Marco F., Linares L., Montejo M., Aranzamendi M., Muñoz P., Valerio M., Aguado J. M., Resino E., Ahufnger I. G., Veja A. P., Martínez-Martínez L. & Fariñas, M. C. (2019). Biofilm formation by multidrug resistant Enterobacteriaceae strains isolated from solid organ transplant recipients. Scientific Reports, 9 (1), 1-10.

Rukavina, Z. & Vanić, Ž. (2016). Current trends in development of liposomes for targeting bacterial biofilms. Pharmaceutics, 8 (2), 18.

Ruppé, E., Andremont, A. & Armand-Lefèvre, L. (2018). Digestive tract colonization by multidrug-resistant Enterobacteriaceae in travellers: an update. Travel Medicine and Infectious Disease, 21, 28-35.

Santos, A. L., Dos Santos, A. P., Ito, C. R. M., Queiroz, P. H. P. D., de Almeida, J. A., de Carvalho Júnior, M. A. B., Oliveira C. Z., Avelino M. A. G., Wastowski I. J., Gomes G. P. L. A.; Souza A. C. S., Vasconcelos L. S. N. O. L., Santos M. O., Silva C. A. & Carneiro, L. C. (2020). Profile of Enterobacteria resistant to beta-lactams. Antibiotics, 9 (7), 410.

Trucillo, P., Ferrari, P. F., Campardelli, R., Reverchon, E. & Perego, P. (2020). A supercritical assisted process for the production of amoxicillin-loaded liposomes for antimicrobial applications. The Journal of Supercritical Fluids, 163, 104842.

Vanić, Ž., Rukavina, Z., Manner, S., Fallarero, A., Uzelac, L., Kralj, M., Klaric D. A., Bogdanov A., Raffai T., Virok D. P., Fillipovic-Grcic J. & Škalko-Basnet, N. (2019). Azithromycin-liposomes as a novel approach for localized therapy of cervicovaginal bacterial infections. International Journal of Nanomedicine, 14, 5957.

Vassallo, A., Silletti, M. F., Faraone, I. & Milella, L. (2020). Nanoparticulate antibiotic systems as antibacterial agents and antibiotic delivery platforms to fight infections. Journal of Nanomaterials, 2020.

Zhang, Y. (2014). Persisters, persistent infections and the Yin–Yang model. Emerging Microbes & Infections, 3 (1), 1-10.

Downloads

Published

26/05/2021

How to Cite

SILVA, J. E. B. da .; SOUZA, J. B. de .; MACÊDO, D. C. dos S. .; CAMPOS, L. A. de A. .; CAVALCANTI, I. M. F. Advantages of using liposome-encapsulated antibiotics to fight infections caused by enterobacteria. Research, Society and Development, [S. l.], v. 10, n. 6, p. e15010615439, 2021. DOI: 10.33448/rsd-v10i6.15439. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/15439. Acesso em: 4 nov. 2024.

Issue

Vol. 10 No. 6

Section

Review Article

License

Copyright (c) 2021 Júlio Eduardo Barbosa da Silva; Jaqueline Barbosa de Souza; Daniel Charles dos Santos Macêdo; Luís André de Almeida Campos; Isabella Macário Ferro Cavalcanti

Creative Commons License

This work is licensed under a Creative Commons Attribution 4.0 International License.

Authors who publish with this journal agree to the following terms:

1) Authors retain copyright and grant the journal right of first publication with the work simultaneously licensed under a Creative Commons Attribution License that allows others to share the work with an acknowledgement of the work's authorship and initial publication in this journal.

2) Authors are able to enter into separate, additional contractual arrangements for the non-exclusive distribution of the journal's published version of the work (e.g., post it to an institutional repository or publish it in a book), with an acknowledgement of its initial publication in this journal.

3) Authors are permitted and encouraged to post their work online (e.g., in institutional repositories or on their website) prior to and during the submission process, as it can lead to productive exchanges, as well as earlier and greater citation of published work.