New therapeutic approaches for S.aureus infections treatment
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Authors
Abstract
Staphylococcus aureus (S. aureus) is an opportunistic pathogen that causes a range of diseases, from mild skin and soft tissue infections and food poisoning to serious conditions such as pneumonia, endocarditis, sepsis, and hospital-acquired infections. Due to the aggressive nature of the disease, limitations of existing treatments, and the spread of antibiotic-resistant strains, the development of alternative strategies to combat bacterial infections has progressed faster than the development of new antibiotics.
In this review, we analyze the epidemiological situation of morbidity and mortality associated with S. aureus infection, as well as antimicrobial resistance of this organism on a global scale. We reviewed the pathogenesis and virulent factors of S. aureus, their mechanisms of antibiotic resistance, and the importance of diagnosing staphylococcal infections to ensure timely intervention.
This review also discusses the latest approaches to combating antibiotic resistance in Staphylococcus aureus, including preventive and therapeutic antimicrobial strategies. Such methods as the use of bacteriophages in treatment, antimicrobial peptides, probiotic microorganisms and their metabolites, and the use of inhibitors to suppress bacterial communication are considered.
Keywords
Staphylococcus aureus, pathogenesis, diagnostics,, antibiotic, resistance, therapy
Article Details
References
Vanamala K., Tatiparti K., Bhise K.i et al. Novel approaches for the treatment of methicillin-resistant Staphylococcus aureus: Using nanoparticles to overcome multidrug resistance // Drug Discovery Today. – 2021. - Vol.26. - P. 31-43.doi:10.1016/j.drudis.2020.10.011.
Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis // The Lancet 2022. – Vol. 399. – P. 629–55. doi:10.1016/S0140-6736(21)02724-0
Palma E., Tilocca B., Roncada P. Antimicrobial Resistance in Veterinary Medicine: An Overview // International Journal of Molecular Sciences. – 2020. – Vol. 21(6):1914. doi: 10.3390/ijms21061914
Thomsen J., Abdulrazzaq N.M., The UAE AMR Surveillance Consortium, Menezes G.A., Ayoub Moubareck C., Everett D.B., Senok A. Methicillin resistant Staphylococcus aureus in the United Arab Emirates: a 12-year retrospective analysis of evolving trends // Frontiers in Public Health. – 2023. – Vol. 11:1244351. doi: 10.3389/fpubh.2023.1244351
Cassini A., Högberg L.D., Plachouras D et al. Attributable deaths and disability-adjusted life-years caused by infections with antibiotic-resistant bacteria in the EU and the European Economic Area in 2015: a population-level modelling analysis // Lancet Infect Dis. – 2019. – Vol.19. – Р.56-66. doi:10.1016/S1473-3099(18)30605-4
Fongang H., Mbaveng A.T., Kuete V. Global burden of bacterial infections and drug resistance // Advances in Botanical Research. – 2023. – Vol. 106. – P. 1-20. doi:10.1016/bs.abr.2022.08.001
Central Asian and European surveillance of antimicrobial resistance: annual report 2020. // World Health Organization. Regional Office for Europe. – 2020. URL
Bassetti M., Poulakou G., Ruppe E. Antimicrobial resistance in the next 30 years, humankind, bugs and drugs: a visionary approach // Intensive Care Medicine. – 2017. – Vol. 43. – P. 1464-1475. doi: 10.1007/s00134-017-4878-x.
Oliveira W. F., Silva P. M. S., Silva R. C. S. et. al. Staphylococcus aureus and Staphylococcus epidermidis infections on implants // Journal of Hospital Infection. – 2018. – Vol. 98 (2). – P. 111–117. doi:10.1016/j.jhin.2017.11.008.
Nikolic P., Mudgil P. The Cell Wall, Cell Membrane and Virulence Factors of Staphylococcus aureus and Their Role in Antibiotic Resistance // Microorganisms. - 2023. - Vol. 11, № 2. - P. 259. Crossref
Krishna S. Miller LS. Host-pathogen interactions between the skin and Staphylococcus aureus // Curr Opin Microbiol. – 2012. – Vol. 15. – P. 28–35.
Kane T.L., Carothers K.E., Lee S.W. Virulence Factor Targeting of the Bacterial Pathogen Staphylococcus aureus for Vaccine and Therapeutics // Curr. Drug Targets. - 2018. - Vol. 19, № 2. - P. 111–127. Crossref
Collins J. et al. Offsetting virulence and antibiotic resistance costs by MRSA // ISME J. - 2010. - Vol. 4, № 4. - P. 577–584. doi: 10.1038/ismej.2009.151.
Lindsay J.A., Moore C.E., Day N.P. et. al Microarrays reveal that each of the ten dominant lineages of Staphylococcus aureus has a unique combination of surface-associated and regulatory genes // Journal of bacteriology. – 2006. – Vol. 188(2). – P. 669–676. doi:10.1128/JB.188.2.669-676.2006.
Divyakolu S., Chikkala R., Ratnakar K.S., Sritharan V. Hemolysins of Staphylococcus aureus - An Update on Their Biology, Role in Pathogenesis and as Targets for Anti-Virulence Therapy // Advances in Infectious Diseases. – 2019. – Vol.9. – P. 80-104. doi:10.4236/aid.2019.92007
Pereira-Franchi E.P.L., Barreira M.R.N., da Costa N.d.S.L.M. et al Molecular epidemiology of methicillin-resistant Staphylococcus aureus in the Brazilian primary health care system // Tropical Medicine and International Health. – 2019. – Vol. 24. – P. 339-347. doi:10.1111/tmi.13192
Zaman M., Andreasen M. Cross-talk between individual phenol-soluble modulins in Staphylococcus aureus biofilm enables rapid and efficient amyloid formation // eLife. – 2020. – Vol. 9:e59776. – P. 1-17. doi.org/10.7554/eLife.59776
Uhlemann A-C., Dordel J., Knox JR. Molecular tracing of the emergence, diversification, and transmission of S. aureus sequence type 8 in a New York community // Proc Natl Acad Sci USA. – 2014. – Vol. 111. – P. 6738–6743. doi:10.1073/pnas.1401006111
Gehrke A.-K.E., Giai C., Gómez M.I. Staphylococcus aureus Adaptation to the Skin in Health and Persistent/Recurrent Infections // Antibiotics. - 2023. - Vol. 12, № 10. - P. 1520. doi:10.3390/antibiotics12101520
Bischofberger M., Iacovache I., Gisou van der Goot F. Pathogenic pore-forming proteins: function and host response // Cell Host Microbe. – 2012. – Vol. 12. – P. 266–275. doi: 10.1016/j.chom.2012.08.005. PMID: 22980324.
Dumont A. L. et al. Characterization of a new cytotoxin that contributes to Staphylococcus aureus pathogenesis // Mol. Microbiol. – 2011. – Vol. 79. – P. 814–825. doi: 10.1111/j.1365-2958.2010.07490.x.
Tristan A. et al. Virulence determinants in community and hospital meticillin-resistant Staphylococcus aureus // J. Hosp. Infect. - 2007. - Vol. 65. - P. 105–109. doi:10.1016/S0195-6701(07)60025-5
Jin T. et al. Staphylococcal Protein A, Panton-Valentine Leukocidin and Coagulase Aggravate the Bone Loss and Bone Destruction in Osteomyelitis // Cell. Physiol. Biochem. - 2013. - Vol. 32, № 2. - P. 322–333. doi:10.1159/000354440
Pinchuk I.V., Beswick E.J., Reyes V.E. Staphylococcal Enterotoxins // Toxins. – 2010. – Vol. 2. – P. 2177-2197. doi.org/10.3390/toxins2082177
Guo Y. et al. Prevalence and Therapies of Antibiotic-Resistance in Staphylococcus aureus // Front. Cell. Infect. Microbiol. - 2020. - Vol. 10. - P. 107. doi:10.3389/fcimb.2020.00107.
Rammelkamp CH., Maxon T. Resistance of Staphylococcus aureus to the action of penicillin // Exp Biol M. – 1942. – Vol. 51. – P. 386–389. doi:10.3181/00379727-51-13986.
Peacock S.J., Paterson G.K. Mechanisms of Methicillin Resistance in Staphylococcus aureus // Annu. Rev. Biochem. - 2015. - Vol. 84, № 1. - P. 577–601. doi:10.1146/annurev-biochem-060614-034516.
Lee A., de Lencastre H., Garau J. et al. Methicillin-resistant Staphylococcus aureus // Nat Rev Dis Primers. – 2018. – Vol. 4. – P. 1-23. doi.org/10.1038/nrdp.2018.33
Hartman B.J., Tomasz A. Low-affinity penicillin-binding protein associated with beta-lactam resistance in Staphylococcus aureus // J Bacteriol. – 1984. – Vol. 158(2). – P. 513-516. doi: 10.1128/jb.158.2.513-516.1984.
Janardhanan J., Bouley R., Martínez-Caballero S. et al. The Quinazolinone Allosteric Inhibitor of PBP 2a Synergizes with Piperacillin and Tazobactam against Methicillin-Resistant Staphylococcus aureus // Antimicrob Agents Chemother. – 2019. – Vol.63. – P. 1-12. doi:10.1128/aac.02637-18
Deurenberg, R.H. et al. The molecular evolution of methicillin-resistant Staphylococcus aureus // Clinical Microbiology and Infection. – 2007. – Vol. 13. – P. 222 – 235. doi: 10.1111/j.1469-0691.2006.01573.x
Katayama Y., Ito T., Hiramatsu K. A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus // Antimicrob Agents Ch. – 2000. – Vol. 44. – P. 1549–1555. doi: 10.1128/AAC.44.6.1549-1555.2000.
Harris S.R., Feil E.J., Holden M.T.G. Evolution of MRSA during hospital transmission and intercontinental spread // Science. – 2010. – Vol. 327. – P. 469–474. doi:10.1126/science.1182395.
Atshan S.S., Hamat R.A., Aljaberi M.A. Phage Therapy as an Alternative Treatment Modality for Resistant Staphylococcus aureus Infections // Antibiotics (Basel). – 2023. – Vol.12. – № 286. – P. 1-23. doi: 10.3390/antibiotics12020286
Warraich A.A. et al. Evaluation of anti-biofilm activity of acidic amino acids and synergy with ciprofloxacin on Staphylococcus aureus biofilms // Sci. Rep. – 2020. – Vol. 10, № 1. – P. 9021. doi:10.1038/s41598-020-66082-x
Dickey J., Perrot V. Adjunct phage treatment enhances the effectiveness of low antibiotic concentration against Staphylococcus aureus biofilms in vitro // PLOS ONE. – 2019. – Vol. 14, № 1. – P. e0209390. doi:10.1371/journal.pone.0209390
Danis-Wlodarczyk K.M., Wozniak D.J., Abedon S.T. Treating Bacterial Infections with Bacteriophage-Based Enzybiotics: In Vitro, In Vivo and Clinical Application // Antibiotics. – 2021. – Vol. 10. – P. 1-36. doi: 10.3390/antibiotics10121497
Clegg J. et al. Staphylococcus aureus Vaccine Research and Development: The Past, Present and Future, Including Novel Therapeutic Strategies // Front. Immunol. – 2021. –Vol. 12. –P. 705360. doi: 10.3389/fimmu.2021.705360
Ooi M., Drilling A., Morales S. et al. Safety and tolerability of bacteriophage therapy for chronic rhinosinusitis due to Staphylococcus aureus // JAMA Otolaryngology–Head. Neck Surg. – 2019. – Vol.145. – P.723–729. doi:10.1001/jamaoto.2019.1191
Liu K., Wang C., Zhou X., Guo X., Yang Y., Liu W., Zhao R., Song H Bacteriophage therapy for drug-resistant Staphylococcus aureus infections // Front. Cell. Infect. Microbiol. – 2024. – Vol.14. – P. 1-17. doi: 10.3389/fcimb.2024.1336821
Plumet L., Ahmad-Mansour N., Dunyach-Remy C., Kissa K., Sotto A., Lavigne J.P., Costechareyre D., Molle V. Bacteriophage Therapy for Staphylococcus Aureus Infections: A Review of Animal Models, Treatments, and Clinical Trials // Front Cell Infect Microbiol. – 2022. – Vol.12. – P. 1-16. doi: 10.3389/fcimb.2022.907314.
Piewngam P., Otto M. Probiotics to prevent Staphylococcus aureus disease? // Gut Microbes. – 2019. –Vol. 11. – P. 94–101. doi: 10.1080/19490976.2019.1591137
Yang R. et al. Membrane-Targeting Neolignan-Antimicrobial Peptide Mimic Conjugates to Combat Methicillin-Resistant Staphylococcus aureus (MRSA) Infections // J. Med. Chem. - 2022. - Vol. 65, № 24. - P. 16879–16892. doi:10.1021/acs.jmedchem.2c01674
Kranjec C., Ovchinnikov K.V., Grønseth T. et al. A bacteriocin-based antimicrobial formulation to effectively disrupt the cell viability of methicillin-resistant Staphylococcus aureus (MRSA) biofilms // npj Biofilms Microbiomes. – 2020. – Vol. 6. – P. 1-13. doi:10.1038/s41522-020-00166-4
Newstead L.L., Varjonen K., Nuttall T., Paterson G.K. Staphylococcal-Produced Bacteriocins and Antimicrobial Peptides: Their Potential as Alternative Treatments for Staphylococcus aureus Infections // Antibiotics. - 2020. – Vol. 9. – P. 1-19. doi:10.3390/antibiotics9020040
DiGiandomenico A., Sellman BR. Antibacterial monoclonal antibodies: the next generation? // Curr Opin Microbiol. – 2015. – Vol. 27. – P. 78–85. doi:10.1016/j.mib.2015.07.014.
Hua L. Assessment of an anti-alpha-toxin monoclonal antibody for prevention and treatment of Staphylococcus aureus-induced pneumonia // Antimicrob Agents Chemother. – 2014. – Vol. 58. – P.1108–1117. doi:10.1128/AAC.02190-13
Yu X-Q., Robbie GJ., Wu Y. et al. Safety, tolerability, and pharmacokinetics of MEDI4893, an investigational, extended-half-life, anti- Staphylococcus aureus alpha-toxin human monoclonal antibody, in healthy adults // Antimicrob Agents Chemother. – 2017. – Vol. 61. doi:10.1128/AAC.01020-16.
Chung L., Raffatellu M. Probiotic fengycins dis(Agr)ee with Staphylococcus aureus colonization // Cell Res. 2019. - Vol. 29, № 2. - P. 93–94. doi: 10.1038/s41422-018-0126-3
Piewngam P. et al. Staphylococcus aureus colonisation and strategies for decolonisation // The Lancet Microbe. – 2024. – Vol.5. – P.606-618. doi:10.1016/S2666-5247(24)00040-5
Eggers S., Barker A.K., Valentine S., Hess T., Duster M., Safdar N.. Effect of Lactobacillus rhamnosus HN001 on carriage of Staphylococcus aureus: results of the impact of probiotics for reducing infections in veterans (IMPROVE) study // BMC Infect Dis. 2018. – Vol.18. - № 129. – P. 1-8.doi: 10.1186/s12879-018-3028-6.
Piewngam P., Khongthong S., Roekngam N., Theapparat Y., Sunpaweravong S., Faroongsarng D., Otto M. Probiotic for pathogen-specific Staphylococcus aureus decolonisation in Thailand: a phase 2, double-blind, randomised, placebo-controlled trial // Lancet Microbe. – 2023. – Vol.4. – P.75-83. doi: 10.1016/S2666-5247(22)00322-6.