1887

Abstract

The complexity of the antimicrobial resistance (AMR) crisis and its global impact on healthcare invokes an urgent need to understand the underlying forces and to conceive and implement innovative solutions. Beyond focusing on a traditional pathogen-centric approach to antibiotic discovery yielding diminishing returns, future therapeutic interventions can expand to focus more comprehensively on host-pathogen interactions. In this manner, increasing the resiliency of our innate immune system or attenuating the virulence mechanisms of the pathogens can be explored to improve therapeutic outcomes. Key pathogen survival strategies such as tolerance, persistence, aggregation, and biofilm formation can be considered and interrupted to sensitize pathogens for more efficient immune clearance. Understanding the evolution and emergence of so-called ‘super clones’ that drive AMR spread with rapid clonotyping assays may guide more precise antibiotic regimens. Innovative alternatives to classical antibiotics such as bacteriophage therapy, novel engineered peptide antibiotics, ionophores, nanomedicines, and repurposing drugs from other domains of medicine to boost innate immunity are beginning to be successfully implemented to combat AMR. Policy changes supporting shorter durations of antibiotic treatment, greater antibiotic stewardship, and increased surveillance measures can enhance patient safety and enable implementation of the next generation of targeted prevention and control programmes at a global level.

Funding
This study was supported by the:
  • Amrita Vishwa Vidyapeetham University (Award AM018-2019)
    • Principle Award Recipient: GeethaKumar
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/content/journal/jmm/10.1099/jmm.0.001646
2023-01-09
2024-06-14
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References

  1. de Kraker MEA, Stewardson AJ, Harbarth S. Will 10 million people die a year due to antimicrobial resistance by 2050?. PLoS Med 2016; 13:e1002184 [View Article]
    [Google Scholar]
  2. Mendelson M, Matsoso MP. The World Health Organization Global Action Plan for antimicrobial resistance. S Afr Med J 2015; 105:325 [View Article]
    [Google Scholar]
  3. Ranjalkar J, Chandy SJ. India’s National Action Plan for antimicrobial resistance - an overview of the context, status, and way ahead. J Family Med Prim Care 2019; 8:1828–1834 [View Article]
    [Google Scholar]
  4. World Health Organisation Antimicrobial resistance; 2021 https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance
  5. Munguia J, Nizet V. Pharmacological targeting of the host-pathogen interaction: alternatives to classical antibiotics to combat drug-resistant superbugs. Trends Pharmacol Sci 2017; 38:473–488 [View Article]
    [Google Scholar]
  6. Gradmann C. Magic bullets and moving targets: antibiotic resistance and experimental chemotherapy, 1900-1940. Dynamis 2011; 31:305–321 [View Article]
    [Google Scholar]
  7. Bigger J. TREATMENT OF STAPHYLOCOCCAL INFECTIONS WITH PENICILLIN BY INTERMITTENT STERILISATION. The Lancet 1944; 244:497–500 [View Article]
    [Google Scholar]
  8. Huemer M, Mairpady Shambat S, Bergada-Pijuan J, Söderholm S, Boumasmoud M et al. Molecular reprogramming and phenotype switching in Staphylococcus aureus lead to high antibiotic persistence and affect therapy success. Proc Natl Acad Sci 2021; 118:e2014920118 [View Article]
    [Google Scholar]
  9. Bumann D. Heterogeneous host-pathogen encounters: act locally, think globally. Cell Host Microbe 2015; 17:13–19 [View Article]
    [Google Scholar]
  10. Cunrath O, Bumann D. Host resistance factor SLC11A1 restricts Salmonella growth through magnesium deprivation. Science 2019; 366:995–999 [View Article]
    [Google Scholar]
  11. Karygianni L, Ren Z, Koo H, Thurnheer T. Biofilm matrixome: extracellular components in structured microbial communities. Trends Microbiol 2020; 28:668–681 [View Article]
    [Google Scholar]
  12. Li X, Sun L, Zhang P, Wang Y. Novel approaches to combat medical device-associated biofilms. Coatings 2021; 11:294 [View Article]
    [Google Scholar]
  13. Xiong Y, Chen J, Sun X, Xu G, Li P et al. The antibacterial and antibiofilm activity of telithromycin against Enterococcus spp. isolated from patients in China. Front Microbiol 2020; 11:616797 [View Article]
    [Google Scholar]
  14. Afonina I, Ong J, Chua J, Lu T, Kline KA. Multiplex CRISPRi system enables the study of stage-specific biofilm genetic requirements in Enterococcus faecalis. mBio 2020; 11:e01101-20 [View Article]
    [Google Scholar]
  15. Haripriyan J, Omanakuttan A, Menon ND, Vanuopadath M, Nair SS et al. Clove Bud Oil modulates pathogenicity phenotypes of the opportunistic human pathogen Pseudomonas aeruginosa. Sci Rep 2018; 8:3437 [View Article]
    [Google Scholar]
  16. Qin S, Xiao W, Zhou C, Pu Q, Deng X et al. Pseudomonas aeruginosa: pathogenesis, virulence factors, antibiotic resistance, interaction with host, technology advances and emerging therapeutics. Signal Transduct Target Ther 2022; 7:199 [View Article]
    [Google Scholar]
  17. Jorth P, Staudinger BJ, Wu X, Hisert KB, Hayden H et al. Regional isolation drives bacterial diversification within cystic fibrosis lungs. Cell Host Microbe 2015; 18:307–319 [View Article]
    [Google Scholar]
  18. Prince AS. Biofilms, antimicrobial resistance, and airway infection. N Engl J Med 2002; 347:1110–1111 [View Article]
    [Google Scholar]
  19. Thomassen MJ, Demko CA, Boxerbaum B, Stern RC, Kuchenbrod PJ. Multiple of isolates of Pseudomonas aeruginosa with differing antimicrobial susceptibility patterns from patients with cystic fibrosis. J Infect Dis 1979; 140:873–880 [View Article]
    [Google Scholar]
  20. Smith EE, Buckley DG, Wu Z, Saenphimmachak C, Hoffman LR et al. Genetic adaptation by Pseudomonas aeruginosa to the airways of cystic fibrosis patients. Proc Natl Acad Sci 2006; 103:8487–8492 [View Article]
    [Google Scholar]
  21. Turner KH, Everett J, Trivedi U, Rumbaugh KP, Whiteley M. Requirements for Pseudomonas aeruginosa acute burn and chronic surgical wound infection. PLoS Genet 2014; 10:e1004518 [View Article]
    [Google Scholar]
  22. Bragonzi A, Paroni M, Nonis A, Cramer N, Montanari S et al. Pseudomonas aeruginosa microevolution during cystic fibrosis lung infection establishes clones with adapted virulence. Am J Respir Crit Care Med 2009; 180:138–145 [View Article]
    [Google Scholar]
  23. Winstanley C, O’Brien S, Brockhurst MA. Pseudomonas aeruginosa evolutionary adaptation and diversification in cystic fibrosis chronic lung infections. Trends Microbiol 2016; 24:327–337 [View Article]
    [Google Scholar]
  24. Secor PR, Michaels LA, Ratjen A, Jennings LK, Singh PK. Entropically driven aggregation of bacteria by host polymers promotes antibiotic tolerance in Pseudomonas aeruginosa. Proc Natl Acad Sci 2018; 115:10780–10785 [View Article]
    [Google Scholar]
  25. Morgan SJ, Lippman SI, Bautista GE, Harrison JJ, Harding CL et al. Bacterial fitness in chronic wounds appears to be mediated by the capacity for high-density growth, not virulence or biofilm functions. PLoS Pathog 2019; 15:e1007511 [View Article]
    [Google Scholar]
  26. Tong S, Amand C, Kieffer A, Kyaw MH. Trends in healthcare utilization and costs associated with pneumonia in the United States during 2008-2014. BMC Health Serv Res 2018; 18:715 [View Article]
    [Google Scholar]
  27. Surve MV, Banerjee A. Cell-to-cell phenotypic heterogeneity in pneumococcal pathogenesis. Future Microbiol 2019; 14:647–651 [View Article]
    [Google Scholar]
  28. Surve MV, Bhutda S, Datey A, Anil A, Rawat S et al. Heterogeneity in pneumolysin expression governs the fate of Streptococcus pneumoniae during blood-brain barrier trafficking. PLoS Pathog 2018; 14:e1007168 [View Article]
    [Google Scholar]
  29. Reygaert WC. Department of biomedical sciences, oakland university william beaumont school of medicine, rochester, MI, USA. AIMS Microbiol 2018
    [Google Scholar]
  30. Bag S, Ghosh TS, Banerjee S, Mehta O, Verma J et al. Molecular insights into antimicrobial resistance traits of commensal human gut microbiota. Microb Ecol 2019; 77:546–557 [View Article]
    [Google Scholar]
  31. Pant A, Bag S, Saha B, Verma J, Kumar P et al. Molecular insights into the genome dynamics and interactions between core and acquired genomes of Vibrio cholerae. Proc Natl Acad Sci 2020; 117:23762–23773 [View Article]
    [Google Scholar]
  32. Van Camp P-J, Haslam DB, Porollo A. Prediction of antimicrobial resistance in Gram-negative bacteria from whole-genome sequencing data. Front Microbiol 2020; 11:1013 [View Article]
    [Google Scholar]
  33. Waddington C, Carey ME, Boinett CJ, Higginson E, Veeraraghavan B et al. Exploiting genomics to mitigate the public health impact of antimicrobial resistance. Genome Med 2022; 14:15 [View Article]
    [Google Scholar]
  34. Johnson JR, Tchesnokova V, Johnston B, Clabots C, Roberts PL et al. Abrupt emergence of a single dominant multidrug-resistant strain of Escherichia coli. J Infect Dis 2013; 207:919–928 [View Article]
    [Google Scholar]
  35. Tchesnokova V, Avagyan H, Rechkina E, Chan D, Muradova M et al. Bacterial clonal diagnostics as a tool for evidence-based empiric antibiotic selection. PLoS ONE 2017; 12:e0174132 [View Article]
    [Google Scholar]
  36. Beppler C, Tekin E, White C, Mao Z, Miller JH et al. When more is less: emergent suppressive interactions in three-drug combinations. BMC Microbiol 2017; 17:107 [View Article]
    [Google Scholar]
  37. Lozano-Huntelman NA, Singh N, Valencia A, Mira P, Sakayan M et al. Evolution of antibiotic cross-resistance and collateral sensitivity in Staphylococcus epidermidis using the mutant prevention concentration and the mutant selection window. Evol Appl 2020; 13:808–823 [View Article]
    [Google Scholar]
  38. Tekin E, White C, Kang TM, Singh N, Cruz-Loya M et al. Prevalence and patterns of higher-order drug interactions in Escherichia coli. NPJ Syst Biol Appl 2018; 4:31 [View Article]
    [Google Scholar]
  39. Tekin E, Yeh PJ, Savage VM. General form for interaction measures and framework for deriving higher-order emergent effects. Front Ecol Evol 2018; 6:166 [View Article]
    [Google Scholar]
  40. Menon ND, Kumar MS, Satheesh Babu TG, Bose S, Vijayakumar G et al. A novel N4-like bacteriophage isolated from a wastewater source in South India with activity against several multidrug-resistant clinical Pseudomonas aeruginosa isolates. mSphere 2021; 6:e01215-20 [View Article]
    [Google Scholar]
  41. Labrie SJ, Samson JE, Moineau S. Bacteriophage resistance mechanisms. Nat Rev Microbiol 2010; 8:317–327 [View Article]
    [Google Scholar]
  42. Kortright KE, Chan BK, Koff JL, Turner PE. Phage therapy: a renewed approach to combat antibiotic-resistant bacteria. Cell Host Microbe 2019; 25:219–232 [View Article]
    [Google Scholar]
  43. Onsea J, Wagemans J, Pirnay JP, Di Luca M, Gonzalez-Moreno M et al. Bacteriophage therapy as a treatment strategy for orthopaedic-device-related infections: where do we stand?. Eur Cell Mater 2020; 39:193–210 [View Article]
    [Google Scholar]
  44. Abedon ST, Thomas-Abedon C. Phage therapy pharmacology. Curr Pharm Biotechnol 2010; 11:28–47 [View Article]
    [Google Scholar]
  45. Dufour N, Delattre R, Ricard J-D, Debarbieux L. The lysis of pathogenic Escherichia coli by bacteriophages releases less endotoxin than by β-Lactams. Clin Infect Dis 2017; 64:1582–1588 [View Article]
    [Google Scholar]
  46. Loc-Carrillo C, Abedon ST. Pros and cons of phage therapy. Bacteriophage 2011; 1:111–114 [View Article]
    [Google Scholar]
  47. Van Belleghem JD, Merabishvili M, Vergauwen B, Lavigne R, Vaneechoutte M. A comparative study of different strategies for removal of endotoxins from bacteriophage preparations. J Microbiol Methods 2017; 132:153–159 [View Article]
    [Google Scholar]
  48. Curtright AJ, Abedon ST. Phage therapy: emergent property pharmacology. JBABM 2011; s6:002 [View Article]
    [Google Scholar]
  49. Payne RJH, Jansen VAA. Pharmacokinetic principles of bacteriophage therapy. Clin Pharmacokinet 2003; 42:315–325 [View Article]
    [Google Scholar]
  50. Dąbrowska K, Abedon ST. Pharmacologically aware phage therapy: pharmacodynamic and pharmacokinetic obstacles to phage antibacterial action in animal and human bodies. Microbiol Mol Biol Rev 2019; 83:e00012-19 [View Article]
    [Google Scholar]
  51. Maciejewska B, Olszak T, Drulis-Kawa Z. Applications of bacteriophages versus phage enzymes to combat and cure bacterial infections: an ambitious and also a realistic application?. Appl Microbiol Biotechnol 2018; 102:2563–2581 [View Article]
    [Google Scholar]
  52. Gu Liu C, Green SI, Min L, Clark JR, Salazar KC et al. Phage-antibiotic synergy is driven by a unique combination of antibacterial mechanism of action and stoichiometry. mBio 2020; 11:e01462-20 [View Article]
    [Google Scholar]
  53. Chung PY, Khanum R. Antimicrobial peptides as potential anti-biofilm agents against multidrug-resistant bacteria. J Microbiol Immunol Infect 2017; 50:405–410 [View Article]
    [Google Scholar]
  54. Mwangi J, Hao X, Lai R, Zhang Z-Y. Antimicrobial peptides: new hope in the war against multidrug resistance. Zool Res 2019; 40:488–505 [View Article]
    [Google Scholar]
  55. Hancock REW, Diamond G. The role of cationic antimicrobial peptides in innate host defences. Trends Microbiol 2000; 8:402–410 [View Article]
    [Google Scholar]
  56. Territo MC, Ganz T, Selsted ME, Lehrer R. Monocyte-chemotactic activity of defensins from human neutrophils. J Clin Invest 1989; 84:2017–2020 [View Article]
    [Google Scholar]
  57. Yang D, Biragyn A, Kwak LW, Oppenheim JJ. Mammalian defensins in immunity: more than just microbicidal. Trends Immunol 2002; 23:291–296 [View Article]
    [Google Scholar]
  58. Heilborn JD, Nilsson MF, Kratz G, Weber G, Sørensen O et al. The cathelicidin anti-microbial peptide LL-37 is involved in re-epithelialization of human skin wounds and is lacking in chronic ulcer epithelium. J Invest Dermatol 2003; 120:379–389 [View Article]
    [Google Scholar]
  59. Huang T-C, Lee J-F, Chen J-Y. Pardaxin, an antimicrobial peptide, triggers caspase-dependent and ROS-mediated apoptosis in HT-1080 cells. Mar Drugs 2011; 9:1995–2009 [View Article]
    [Google Scholar]
  60. Papo N, Shahar M, Eisenbach L, Shai Y. A novel lytic peptide composed of DL-amino acids selectively kills cancer cells in culture and in mice. J Biol Chem 2003; 278:21018–21023 [View Article]
    [Google Scholar]
  61. Lehmann J, Retz M, Sidhu SS, Suttmann H, Sell M et al. Antitumor activity of the antimicrobial peptide magainin II against bladder cancer cell lines. Eur Urol 2006; 50:141–147 [View Article]
    [Google Scholar]
  62. Cruciani RA, Barker JL, Zasloff M, Chen HC, Colamonici O. Antibiotic magainins exert cytolytic activity against transformed cell lines through channel formation. Proc Natl Acad Sci 1991; 88:3792–3796 [View Article]
    [Google Scholar]
  63. Etayash H, Qian Y, Pletzer D, Zhang Q, Xie J et al. Host defense peptide-mimicking amphiphilic β-peptide polymer (Bu:DM) exhibiting anti-biofilm, immunomodulatory, and in Vivo anti-infective activity. J Med Chem 2020; 63:12921–12928 [View Article]
    [Google Scholar]
  64. Krenev IA, Umnyakova ES, Eliseev IE, Dubrovskii YA, Gorbunov NP et al. Antimicrobial peptide arenicin-1 derivative Ar-1-(C/A) as complement system modulator. Mar Drugs 2020; 18:631 [View Article]
    [Google Scholar]
  65. Lin L, Nonejuie P, Munguia J, Hollands A, Olson J et al. Azithromycin synergizes with cationic antimicrobial peptides to exert bactericidal and therapeutic activity against highly multidrug-resistant Gram-negative bacterial pathogens. EBioMedicine 2015; 2:690–698 [View Article]
    [Google Scholar]
  66. Belanger CR, Lee AH-Y, Pletzer D, Dhillon BK, Falsafi R et al. Identification of novel targets of azithromycin activity against Pseudomonas aeruginosa grown in physiologically relevant media. Proc Natl Acad Sci 2020; 117:33519–33529 [View Article]
    [Google Scholar]
  67. Mohapatra SS, Dwibedy SK, Padhy I. Polymyxins, the last-resort antibiotics: mode of action, resistance emergence, and potential solutions. J Biosci 2021; 46:85 [View Article]
    [Google Scholar]
  68. Blaskovich MAT, Pitt ME, Elliott AG, Cooper MA. Can octapeptin antibiotics combat extensively drug-resistant (XDR) bacteria?. Expert Rev Anti Infect Ther 2018; 16:485–499 [View Article]
    [Google Scholar]
  69. Velkov T, Roberts KD, Li J. Rediscovering the octapeptins. Nat Prod Rep 2017; 34:295–309 [View Article]
    [Google Scholar]
  70. Becker B, Butler MS, Hansford KA, Gallardo-Godoy A, Elliott AG et al. Synthesis of octapeptin C4 and biological profiling against NDM-1 and polymyxin-resistant bacteria. Bioorg Med Chem Lett 2017; 27:2407–2409 [View Article]
    [Google Scholar]
  71. Pitt ME, Cao MD, Butler MS, Ramu S, Ganesamoorthy D et al. Octapeptin C4 and polymyxin resistance occur via distinct pathways in an epidemic XDR Klebsiella pneumoniae ST258 isolate. J Antimicrob Chemother 2019; 74:582–593 [View Article]
    [Google Scholar]
  72. Blaskovich MAT, Hansford KA, Gong Y, Butler MS, Muldoon C et al. Protein-inspired antibiotics active against vancomycin- and daptomycin-resistant bacteria. Nat Commun 2018; 9:22 [View Article]
    [Google Scholar]
  73. Cho H-K, Karau MJ, Greenwood-Quaintance KE, Hansford KA, Cooper MA et al. In Vitro activity of vancapticin MCC5145 against methicillin-resistant Staphylococcus aureus from periprosthetic joint infection. Antimicrob Agents Chemother 2021; 65:e02443-20 [View Article]
    [Google Scholar]
  74. Adlard PA, Cherny RA, Finkelstein DI, Gautier E, Robb E et al. Rapid restoration of cognition in Alzheimer’s transgenic mice with 8-hydroxy quinoline analogs is associated with decreased interstitial Abeta. Neuron 2008; 59:43–55 [View Article]
    [Google Scholar]
  75. Harbison-Price N, Ferguson SA, Heikal A, Taiaroa G, Hards K et al. Multiple bactericidal mechanisms of the zinc Ionophore PBT2. mSphere 2020; 5:e00157-20 [View Article]
    [Google Scholar]
  76. Brinkmann V, Reichard U, Goosmann C, Fauler B, Uhlemann Y et al. Neutrophil extracellular traps kill bacteria. Science 2004; 303:1532–1535 [View Article]
    [Google Scholar]
  77. Chow OA, von Köckritz-Blickwede M, Bright AT, Hensler ME, Zinkernagel AS et al. Statins enhance formation of phagocyte extracellular traps. Cell Host Microbe 2010; 8:445–454 [View Article]
    [Google Scholar]
  78. Corriden R, Hollands A, Olson J, Derieux J, Lopez J et al. Tamoxifen augments the innate immune function of neutrophils through modulation of intracellular ceramide. Nat Commun 2015; 6:8369 [View Article]
    [Google Scholar]
  79. Hollands A, Corriden R, Gysler G, Dahesh S, Olson J et al. Natural product anacardic acid from cashew nut shells stimulates neutrophil extracellular trap production and bactericidal activity. J Biol Chem 2016; 291:13964–13973 [View Article]
    [Google Scholar]
  80. Sun J, Uchiyama S, Olson J, Morodomi Y, Cornax I et al. Repurposed drugs block toxin-driven platelet clearance by the hepatic Ashwell-Morell receptor to clear Staphylococcus aureus bacteremia. Sci Transl Med 2021; 13:eabd6737 [View Article]
    [Google Scholar]
  81. Sushnitha M, Evangelopoulos M, Tasciotti E, Taraballi F. Cell membrane-based biomimetic nanoparticles and the immune system: immunomodulatory interactions to therapeutic applications. Front Bioeng Biotechnol 2020; 8:627 [View Article]
    [Google Scholar]
  82. Lee N-H, You S, Taghizadeh A, Taghizadeh M, Kim HS. Cell membrane-cloaked nanotherapeutics for targeted drug delivery. Int J Mol Sci 2022; 23:2223 [View Article]
    [Google Scholar]
  83. Escajadillo T, Olson J, Luk BT, Zhang L, Nizet V. A red blood cell membrane-camouflaged nanoparticle counteracts streptolysin O-mediated virulence phenotypes of invasive group A Streptococcus. Front Pharmacol 2017; 8:477 [View Article]
    [Google Scholar]
  84. Kim J-K, Uchiyama S, Gong H, Stream A, Zhang L et al. Engineered biomimetic platelet membrane-coated nanoparticles block Staphylococcus aureus cytotoxicity and protect against lethal systemic infection. Engineering 2021; 7:1149–1156 [View Article]
    [Google Scholar]
  85. Thamphiwatana S, Angsantikul P, Escajadillo T, Zhang Q, Olson J et al. Macrophage-like nanoparticles concurrently absorbing endotoxins and proinflammatory cytokines for sepsis management. Proc Natl Acad Sci 2017; 114:11488–11493 [View Article]
    [Google Scholar]
  86. Broz P, Dixit VM. Inflammasomes: mechanism of assembly, regulation and signalling. Nat Rev Immunol 2016; 16:407–420 [View Article]
    [Google Scholar]
  87. Guo H, Callaway JB, Ting J-Y. Inflammasomes: mechanism of action, role in disease, and therapeutics. Nat Med 2015; 21:677–687 [View Article]
    [Google Scholar]
  88. Cohen TS, Boland ML, Boland BB, Takahashi V, Tovchigrechko A. S. aureus evades macrophage killing through NLRP3-dependent effects on mitochondrial trafficking. Cell Rep 2018; 22:2431–2441 [View Article]
    [Google Scholar]
  89. Bonesso MF, Yeh AJ, Villaruz AE, Joo H-S, McCausland J. Key role of α-toxin in fatal pneumonia caused by Staphylococcus aureus sequence type 398. Am J Respir Crit Care Med 2016; 193:217–220 [View Article]
    [Google Scholar]
  90. Lin L, Xu L, Lv W, Han L, Xiang Y. An NLRP3 inflammasome-triggered cytokine storm contributes to Streptococcal toxic shock-like syndrome (STSLS). PLoS Pathog 2019; 15:e1007795 [View Article]
    [Google Scholar]
  91. Corcoran SE, Halai R, Cooper MA, Page C. Pharmacological inhibition of the Nod-like receptor family pyrin domain containing 3 inflammasome with MCC950. Pharmacol Rev 2021; 73:968–1000 [View Article]
    [Google Scholar]
  92. Spellberg B. The new antibiotic mantra—“Shorter Is Better.”. JAMA Intern Med 2016; 176:1254 [View Article]
    [Google Scholar]
  93. Rubinstein E. Short antibiotic treatment courses or how short is short?. Int J Antimicrob Agents 2007; 30 Suppl 1:S76–9 [View Article]
    [Google Scholar]
  94. Vaughn VM, Flanders SA, Snyder A, Conlon A, Rogers MAM et al. Excess antibiotic treatment duration and adverse events in patients hospitalized with pneumonia: a multihospital cohort study. Ann Intern Med 2019; 171:153–163 [View Article]
    [Google Scholar]
  95. Doron S, Davidson LE. Antimicrobial stewardship. Mayo Clin Proc 2011; 86:1113–1123 [View Article]
    [Google Scholar]
  96. Dyar OJ, Huttner B, Schouten J, Pulcini C. ESGAP (ESCMID Study Group for Antimicrobial stewardshiP) What is antimicrobial stewardship?. Clin Microbiol Infect 2017; 23:793–798 [View Article]
    [Google Scholar]
  97. Mendelson M, Morris AM, Thursky K, Pulcini C. How to start an antimicrobial stewardship programme in a hospital. Clin Microbiol Infect 2020; 26:447–453 [View Article]
    [Google Scholar]
  98. World Health Organization Monitoring and evaluation of the global action plan on antimicrobial resistance: framework and recommended indicators; 2019 https://apps.who.int/iris/bitstream/handle/10665/325006/9789241515665-eng.pdf
  99. World Health Organization Antimicrobial Resistance Division, Surveillance, Prevention and Control. Global antimicrobial resistance surveillance system (GLASS) report: Report: Early Implementation 2020; 2020May
  100. World Health Organization Collaborating Centre for Antimicrobial Resistance Epidemiology and Surveillance, National Institute for Public Health and the Environment, WHO Regional Office for Europe, and European Society of Clinical Microbiology and Infectious Diseases Central Asian and Eastern European Surveillance of Antimicrobial Resistance. Annual report; 2018
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