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Introduction Risk Factors for Antimicrobial Resistance in P A continuous publication, open access, peer-reviewed journal ACCESS ONLINE REVIEW How to manage Pseudomonas aeruginosa infections Matteo Bassetti MD, PhD1, Antonio Vena MD1, Antony Croxatto PhD2, Elda Righi MD, PhD1, Benoit Guery MD, PhD3 1Infectious Diseases Clinic, Department of Medicine, University of Udine and Azienda Sanitaria Universitaria Integrata, Udine, Italy; 2Institute of Microbiology, University of Lausanne, Lausanne, Switzerland; 3Infectious Diseases Service, Department of Medicine, University Hospital and University of Lausanne, Lausanne, Switzerland Abstract involving almost all classes of antibiotics. Clinical approaches Infections with Pseudomonas aeruginosa have become a real to patients with bacteremia, ventilator-associated pneumonia, concern in hospital-acquired infections, especially in critically ill urinary tract infections and skin soft tissue infections are and immunocompromised patients. The major problem leading discussed. Antibiotic combinations are reviewed as well to high mortality lies in the appearance of drug-resistant as an analysis of pharmacokinetic and pharmacodynamic strains. Therefore, a vast number of approaches to develop parameters to optimize P. aeruginosa treatment. Limitations of novel anti-infectives is currently pursued. Diverse strategies current therapies, the potential for alternative drugs and new range from killing (new antibiotics) to disarming (antivirulence) therapeutic options are also discussed. the pathogen. In this review, selected aspects of P. aeruginosa Keywords: bloodstream infection, ceftazidime-avibactam, antimicrobial resistance and infection management will be ceftolozane-tazobactam, multidrug resistance, new antibiotics, addressed. Many studies have been performed to evaluate the Pseudomonas aeruginosa, ventilator associated pneumonia. risk factors for resistance and the potential consequences on mortality and attributable mortality. The review also looks at Citation the mechanisms associated with resistance – P. aeruginosa is Bassetti M, Vena A, Croxatto A, Righi E, Guery B. How to manage a pathogen presenting a large genome, and it can develop a Pseudomonas aeruginosa infections. Drugs in Context 2018; 7: large number of factors associated with antibiotic resistance 212527. DOI: 10.7573/dic.212527 Introduction for resistance and the potential consequences on mortality and attributable mortality. We will then explore the mechanisms One of the most important challenges for physicians is the associated to resistance. P. aeruginosa is a pathogen presenting adequate treatment of infections due to Gram-negative a large genome that can develop a large number of factors pathogens because of the increasing antimicrobial resistance in associated with antibiotic resistance involving almost all the healthcare setting [1]. classes of antibiotics. We will then specifically focus on clinical Among infections caused by Gram-negative rods, Pseudomonas approaches to patients with bacteremia, ventilator-associated aeruginosa has a leading role [2], especially in critically ill and pneumonia, urinary tract infections, and skin and soft-tissue immunocompromised patients. Antimicrobial resistance has infections. Specific syndromes such as ecthyma gangrenosum led to a serious restriction in treatment options for P. aeruginosa will be discussed. In the second part of our work, we will look at infections, which has become a critical and deadly issue causing pharmacokinetic and pharmacodynamic parameters that may a total of 51,000 healthcare infections in the USA per year [3–6]. be exploited to optimize P. aeruginosa treatment. Limitations of Despite this problem, physicians mainly rely on retrospective current therapy, potential alternative drugs and new therapeutic non-randomized controlled studies to derive conclusions about options will also be discussed. the optimal therapeutic management of these infections. Risk factors for antimicrobial In this review, we aim to address selected aspects of P. aeruginosa antimicrobial resistance and infection management. In the resistance in P. aeruginosa first part of this review, we will focus on resistance risks factors. Multi-drug resistance (MDR) has increased dramatically in recent Many studies have been performed to evaluate the risk factors years and is now recognized as a major threat worldwide [7]. Bassetti M, Vena A, Croxatto A, Righi E, Guery B. Drugs in Context 2018; 7: 212527. DOI: 10.7573/dic.212527 1 of 18 ISSN: 1740-4398 REVIEW – How to manage Pseudomonas aeruginosa infections drugsincontext.com Risk factors for the development of MDR strains have been and meta-analysis of the association between resistance evaluated in several studies. A case–control study performed and mortality was performed in neutropenic patients [17]. in Brazil compared 142 patients infected with metallo-β- A total of 30 studies were included; infections related to lactamases (MBLs) strains to 26 patients infected with non MBLs carbapenems-resistant Pseudomonas spp. were reported in strains [8]. The multivariate analysis showed that ICU stay and 18 (60%) studies. Globally, mortality ranged from 33 to 71% in urinary tract infection were the important factors for MBLs patients with carbapenems-resistant Pseudomonas infections. infections. MBLs strains were also associated with a faster onset The results showed an increased mortality in carbapenems- of infection and a faster progression to death. resistant compared to carbapenems-susceptible infections (OR 4.89). This increase in mortality has been described in a A retrospective study conducted over two years, starting in previous meta-analysis [18]. Besides mortality, resistance is 2010, in Brazil evaluated 54 ICU patients with P. aeruginosa also associated with increased cost, using the data from 571 infections [9]. MDR P. aeruginosa was observed in 37% of the admissions with bacteremia, MDR P. aeruginosa bacteremia had cases (20 of 54 patients), 20% of the isolates were positive the highest mean incremental cost (€ 44,709) [19]. for the blaSPM-1-like gene. Interestingly, MDR occurred in patients hospitalized for an average of 87.1 days. A case– Globally, these results show that development of resistance control surveillance study performed in China showed that the has several risk factors linked to the severity of the infection prevalence of MDR P. aeruginosa was 54% among patients with (Apache II, underlying diseases, intubation, catheter) and that P. aeruginosa infection. Independent risk factors were tracheal resistance itself is associated with increased mortality. intubation (odds ratio [OR] 2.21) and use of carbapenems (OR 3.36). MDR strains were associated with a longer hospitalization and a higher mortality (49 versus 20%) [10]. A retrospective Mechanisms of antibiotic resistance study on 63 episodes of carbapenems-resistant P. aeruginosa Bacteria exhibit multiple resistance mechanisms to antibiotics (CRPA) showed that the Acute Physiology and Chronic Health including decreased permeability, expression of efflux systems, Evaluation II (APACHE II) score at the time of CRPA bacteremia production of antibiotic inactivating enzymes and target and the capacity of CRPA to form biofilm were independent modifications.P. aeruginosa exhibits most of these known predictive factors for mortality in patients with CRPA resistance mechanisms through both intrinsic chromosomally bacteremia [11]. Another study also found the APACHE II score encoded or genetically imported resistance determinants as an independent factor for colonization [12]. affecting the major classes of antibiotics such as β-lactams, In a separate population of immunocompromised patients, aminoglycosides, quinolones and polymyxins (Table 1). Eight in a matched case–control study, 31 cases colonized with categories of antibiotics are mainly used to treat P. aeruginosa extensively drug-resistant P. aeruginosa were compared with infections including aminoglycosides (gentamicin, tobramycin, 93 controls. Four factors were associated with colonization: amikacin, netilmicin), carbapenems (imipenem, meropenem), presence of a central venous catheter, presence of a urinary cephalosporins (ceftazidime, cefepime), fluoroquinolones catheter, CRP>10 mg/L, and ciprofloxacin administration (ciprofloxacin, levofloxacin), penicillin with β-lactamase inhibitors [13]. Another study, this time in a retrospective international (BLI) (ticarcillin and piperacillin in combination with clavulanic cohort of P. aeruginosa nosocomial pneumonia, tried to acid or tazobactam), monobactams (aztreonam), fosfomycin and determine the risk factors for MDR and attributable mortality polymyxins (colistin, polymyxin B). The strains of P. aeruginosa are [14]. From 740 patients, 226 were infected with MDR strains. categorized as follows: (1) MDR when resistance is observed in ≥1 Independent factors predictors of MDR were decreasing age, agent in ≥3 categories; (2) extensively drug-resistant (XDR) when diabetes mellitus, and ICU admission. MDR was independently a resistance is observed in ≥ agent in all but ≤ categories; and associated with in-hospital mortality (44.7 versus 31.7% (3) pandrug-resistant (PDR) when the strain is non-susceptible for non-MDR, p=0.001). A prospective observational study to all antimicrobial agents [2]. The emergence of MDR, XDR compared imipenem-resistant (IR) P. aeruginosa (PA) with or and PDR strains occurs in a timely fashion by the modification without MBL-mediated resistance [15]. The researchers found of regulatory mechanisms controlling the
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