Skip to main content
Top
Published in: Antimicrobial Resistance & Infection Control 1/2018

Open Access 01-12-2018 | Research

Risk factors for hospitalized patients with resistant or multidrug-resistant Pseudomonas aeruginosa infections: a systematic review and meta-analysis

Authors: Gowri Raman, Esther E. Avendano, Jeffrey Chan, Sanjay Merchant, Laura Puzniak

Published in: Antimicrobial Resistance & Infection Control | Issue 1/2018

Login to get access

Abstract

Background

Identifying risk factors predicting acquisition of resistant Pseudomonas aeruginosa will aid surveillance and diagnostic initiatives and can be crucial in early and appropriate antibiotic therapy. We conducted a systematic review examining risk factors of acquisition of resistant P. aeruginosa among hospitalized patients.

Methods

MEDLINE®, EMBASE®, and Cochrane Central were searched between 2000 and 2016 for studies examining independent risk factors associated with acquisition of resistant P. aeruginosa, among hospitalized patients. Random effects model meta-analysis was conducted when at least three or more studies were sufficiently similar.

Results

Of the 54 eligible articles, 28 publications (31studies) examined multi-drug resistant (MDR) or extensively drug resistant (XDR) P. aeruginosa and 26 publications (29 studies) examined resistant P. aeruginosa. The acquisition of MDR P. aeruginosa, as compared with non-MDR P. aeruginosa, was significantly associated with intensive care unit (ICU) admission (3 studies: summary adjusted odds ratio [OR] 2.2) or use of quinolones (4 studies: summary adjusted OR 3.59). Acquisition of MDR or XDR compared with susceptible P. aeruginosa was significantly associated with prior hospital stay (4 studies: summary adjusted OR 1.90), use of quinolones (3 studies: summary adjusted OR 4.34), or use of carbapenems (3 studies: summary adjusted OR 13.68). The acquisition of MDR P. aeruginosa compared with non-P. aeruginosa was significantly associated with prior use of cephalosporins (3 studies: summary adjusted OR 3.96), quinolones (4 studies: summary adjusted OR 2.96), carbapenems (6 studies: summary adjusted OR 2.61), and prior hospital stay (4 studies: summary adjusted OR 1.74). The acquisition of carbapenem-resistant P. aeruginosa compared with susceptible P. aeruginosa, was statistically significantly associated with prior use of piperacillin-tazobactam (3 studies: summary adjusted OR 2.64), vancomycin (3 studies: summary adjusted OR 1.76), and carbapenems (7 studies: summary adjusted OR 4.36).

Conclusions

Prior use of antibiotics and prior hospital or ICU stay was the most significant risk factors for acquisition of resistant P. aeruginosa. These findings provide guidance in identifying patients that may be at an elevated risk for a resistant infection and emphasize the importance of antimicrobial stewardship and infection control in hospitals.
Appendix
Available only for authorised users
Literature
1.
go back to reference Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis. 2009;48(1):1):1–12. Boucher HW, Talbot GH, Bradley JS, Edwards JE, Gilbert D, Rice LB, et al. Bad bugs, no drugs: no ESKAPE! An update from the Infectious Diseases Society of America. Clin Infect Dis. 2009;48(1):1):1–12.
2.
3.
go back to reference Vincent JL, Rello J, Marshall J, Silva E, Anzueto A, Martin CD, et al. International study of the prevalence and outcomes of infection in intensive care units. JAMA. 2009;302(21):2323–9.PubMed Vincent JL, Rello J, Marshall J, Silva E, Anzueto A, Martin CD, et al. International study of the prevalence and outcomes of infection in intensive care units. JAMA. 2009;302(21):2323–9.PubMed
4.
go back to reference Driscoll JA, Brody SL, Kollef MH. The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs. 2007;67(3):351–68.PubMed Driscoll JA, Brody SL, Kollef MH. The epidemiology, pathogenesis and treatment of Pseudomonas aeruginosa infections. Drugs. 2007;67(3):351–68.PubMed
5.
go back to reference Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics. http://www.who.int/medicines/publications/global-priority-list-antibiotic-resistant-bacteria/en/ 2017 February 27 [cited 2017 Dec 5]; Global Priority List of Antibiotic-Resistant Bacteria to Guide Research, Discovery, and Development of New Antibiotics. http://​www.​who.​int/​medicines/​publications/​global-priority-list-antibiotic-resistant-bacteria/​en/​ 2017 February 27 [cited 2017 Dec 5];
6.
go back to reference Obritsch MD, Fish DN, MacLaren R, Jung R. National surveillance of antimicrobial resistance in Pseudomonas aeruginosa isolates obtained from intensive care unit patients from 1993 to 2002. Antimicrob Agents Chemother. 2004;48(12):4606–10.PubMedPubMedCentral Obritsch MD, Fish DN, MacLaren R, Jung R. National surveillance of antimicrobial resistance in Pseudomonas aeruginosa isolates obtained from intensive care unit patients from 1993 to 2002. Antimicrob Agents Chemother. 2004;48(12):4606–10.PubMedPubMedCentral
7.
go back to reference Nathwani D, Raman G, Sulham K, Gavaghan M, Menon V. Clinical and economic consequences of hospital-acquired resistant and multidrug-resistant Pseudomonas aeruginosa infections: a systematic review and meta-analysis. Antimicrob Resist Infect Control. 2014;3(1):32.PubMedPubMedCentral Nathwani D, Raman G, Sulham K, Gavaghan M, Menon V. Clinical and economic consequences of hospital-acquired resistant and multidrug-resistant Pseudomonas aeruginosa infections: a systematic review and meta-analysis. Antimicrob Resist Infect Control. 2014;3(1):32.PubMedPubMedCentral
8.
go back to reference Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81.PubMed Magiorakos AP, Srinivasan A, Carey RB, Carmeli Y, Falagas ME, Giske CG, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect. 2012;18(3):268–81.PubMed
9.
go back to reference Raman G, Avendano E, Berger S, Menon V. Appropriate initial antibiotic therapy in hospitalized patients with gram-negative infections: systematic review and meta-analysis. BMC Infect Dis. 2015;15:395.PubMedPubMedCentral Raman G, Avendano E, Berger S, Menon V. Appropriate initial antibiotic therapy in hospitalized patients with gram-negative infections: systematic review and meta-analysis. BMC Infect Dis. 2015;15:395.PubMedPubMedCentral
10.
go back to reference DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.PubMed DerSimonian R, Laird N. Meta-analysis in clinical trials. Control Clin Trials. 1986;7(3):177–88.PubMed
11.
12.
go back to reference Aloush V, Navon-Venezia S, Seigman-Igra Y, Cabili S, Carmeli Y. Multidrug-resistant Pseudomonas aeruginosa: risk factors and clinical impact. Antimicrob Agents Chemother. 2006;50(1):43–8.PubMedPubMedCentral Aloush V, Navon-Venezia S, Seigman-Igra Y, Cabili S, Carmeli Y. Multidrug-resistant Pseudomonas aeruginosa: risk factors and clinical impact. Antimicrob Agents Chemother. 2006;50(1):43–8.PubMedPubMedCentral
13.
go back to reference Bodro M, Sabe N, Tubau F, Llado L, Baliellas C, Gonzalez-Costello J, et al. Extensively drug-resistant Pseudomonas aeruginosa bacteremia in solid organ transplant recipients. Transplantation. 2015;99(3):616–22.PubMed Bodro M, Sabe N, Tubau F, Llado L, Baliellas C, Gonzalez-Costello J, et al. Extensively drug-resistant Pseudomonas aeruginosa bacteremia in solid organ transplant recipients. Transplantation. 2015;99(3):616–22.PubMed
14.
go back to reference Cao B, Wang H, Sun H, Zhu Y, Chen M. Risk factors and clinical outcomes of nosocomial multi-drug resistant Pseudomonas aeruginosa infections. J Hosp Infect. 2004;57(2):112–8.PubMed Cao B, Wang H, Sun H, Zhu Y, Chen M. Risk factors and clinical outcomes of nosocomial multi-drug resistant Pseudomonas aeruginosa infections. J Hosp Infect. 2004;57(2):112–8.PubMed
15.
go back to reference Cilloniz C, Gabarrus A, Ferrer M, Puig dB, Rinaudo M, Mensa J, et al. Community-acquired pneumonia due to multidrug- and non-multidrug-resistant Pseudomonas aeruginosa. Chest. 2016;150(2):415–25.PubMed Cilloniz C, Gabarrus A, Ferrer M, Puig dB, Rinaudo M, Mensa J, et al. Community-acquired pneumonia due to multidrug- and non-multidrug-resistant Pseudomonas aeruginosa. Chest. 2016;150(2):415–25.PubMed
16.
go back to reference Cobos-Trigueros N, Sole M, Castro P, Torres JL, Hernandez C, Rinaudo M, et al. Acquisition of Pseudomonas aeruginosa and its resistance phenotypes in critically ill medical patients: role of colonization pressure and antibiotic exposure. Crit Care. 2015;19:218.PubMedPubMedCentral Cobos-Trigueros N, Sole M, Castro P, Torres JL, Hernandez C, Rinaudo M, et al. Acquisition of Pseudomonas aeruginosa and its resistance phenotypes in critically ill medical patients: role of colonization pressure and antibiotic exposure. Crit Care. 2015;19:218.PubMedPubMedCentral
17.
go back to reference D'Agata EM, Cataldo MA, Cauda R, Tacconelli E. The importance of addressing multidrug resistance and not assuming single-drug resistance in case-control studies. Infect Control Hosp Epidemiol. 2006;27(7):670–4.PubMed D'Agata EM, Cataldo MA, Cauda R, Tacconelli E. The importance of addressing multidrug resistance and not assuming single-drug resistance in case-control studies. Infect Control Hosp Epidemiol. 2006;27(7):670–4.PubMed
18.
go back to reference Dalfino L, Mosca A, Brienza N, Spada M, Coppolecchia S, Miragliotta G, et al. Nosocomial infections in critically ill patients: When should multidrug-resistant Pseudomonas aeruginosa be suspected? Clin Microbiol Infect. 2011;17:S294–5. Conference: 21st ECCMID/27th ICC Milan Italy Conference Start: 20110507 Conference End: 20110510 Conference Publication: (var pagings) Dalfino L, Mosca A, Brienza N, Spada M, Coppolecchia S, Miragliotta G, et al. Nosocomial infections in critically ill patients: When should multidrug-resistant Pseudomonas aeruginosa be suspected? Clin Microbiol Infect. 2011;17:S294–5. Conference: 21st ECCMID/27th ICC Milan Italy Conference Start: 20110507 Conference End: 20110510 Conference Publication: (var pagings)
19.
go back to reference Dantas RC, Ferreira ML, Gontijo-Filho PP, Ribas RM. Pseudomonas aeruginosa bacteraemia: independent risk factors for mortality and impact of resistance on outcome. J Med Microbiol. 2014;63(Pt:12):12–87. Dantas RC, Ferreira ML, Gontijo-Filho PP, Ribas RM. Pseudomonas aeruginosa bacteraemia: independent risk factors for mortality and impact of resistance on outcome. J Med Microbiol. 2014;63(Pt:12):12–87.
20.
go back to reference Defez C, Fabbro-Peray P, Bouziges N, Gouby A, Mahamat A, Daures JP, et al. Risk factors for multidrug-resistant Pseudomonas aeruginosa nosocomial infection. J Hosp Infect. 2004;57(3):209–16.PubMed Defez C, Fabbro-Peray P, Bouziges N, Gouby A, Mahamat A, Daures JP, et al. Risk factors for multidrug-resistant Pseudomonas aeruginosa nosocomial infection. J Hosp Infect. 2004;57(3):209–16.PubMed
21.
go back to reference Gomez-Zorrilla S, Camoez M, Tubau F, Periche E, Canizares R, Dominguez MA, et al. Antibiotic pressure is a major risk factor for rectal colonization by multidrug-resistant Pseudomonas aeruginosa in critically ill patients. Antimicrob Agents Chemother. 2014;58(10):5863–70.PubMedPubMedCentral Gomez-Zorrilla S, Camoez M, Tubau F, Periche E, Canizares R, Dominguez MA, et al. Antibiotic pressure is a major risk factor for rectal colonization by multidrug-resistant Pseudomonas aeruginosa in critically ill patients. Antimicrob Agents Chemother. 2014;58(10):5863–70.PubMedPubMedCentral
22.
go back to reference Johnson LE, D'Agata EM, Paterson DL, Clarke L, Qureshi ZA, Potoski BA, et al. Pseudomonas aeruginosa bacteremia over a 10-year period: multidrug resistance and outcomes in transplant recipients. Transpl Infect Dis. 2009;11(3):227–34.PubMed Johnson LE, D'Agata EM, Paterson DL, Clarke L, Qureshi ZA, Potoski BA, et al. Pseudomonas aeruginosa bacteremia over a 10-year period: multidrug resistance and outcomes in transplant recipients. Transpl Infect Dis. 2009;11(3):227–34.PubMed
23.
go back to reference Joo EJ, Kang CI, Ha YE, Kang SJ, Park SY, Chung DR, et al. Risk factors for mortality in patients with Pseudomonas aeruginosa bacteremia: clinical impact of antimicrobial resistance on outcome. Microb Drug Resist. 2011;17(2):305–12.PubMed Joo EJ, Kang CI, Ha YE, Kang SJ, Park SY, Chung DR, et al. Risk factors for mortality in patients with Pseudomonas aeruginosa bacteremia: clinical impact of antimicrobial resistance on outcome. Microb Drug Resist. 2011;17(2):305–12.PubMed
24.
go back to reference Liew YX, Tan TT, Lee W, Ng JL, Chia DQ, Wong GC, et al. Risk factors for extreme-drug resistant Pseudomonas aeruginosa infections in patients with hematologic malignancies. Am J Infect Control. 2013;41(2):140–4.PubMed Liew YX, Tan TT, Lee W, Ng JL, Chia DQ, Wong GC, et al. Risk factors for extreme-drug resistant Pseudomonas aeruginosa infections in patients with hematologic malignancies. Am J Infect Control. 2013;41(2):140–4.PubMed
25.
go back to reference Lodise TP, Miller CD, Graves J, Furuno JP, McGregor JC, Lomaestro B, et al. Clinical prediction tool to identify patients with Pseudomonas aeruginosa respiratory tract infections at greatest risk for multidrug resistance. Antimicrob Agents Chemother. 2007;51(2):417–22.PubMed Lodise TP, Miller CD, Graves J, Furuno JP, McGregor JC, Lomaestro B, et al. Clinical prediction tool to identify patients with Pseudomonas aeruginosa respiratory tract infections at greatest risk for multidrug resistance. Antimicrob Agents Chemother. 2007;51(2):417–22.PubMed
26.
go back to reference Micek ST, Wunderink RG, Kollef MH, Chen C, Rello J, Chastre J, et al. An international multicenter retrospective study of Pseudomonas aeruginosa nosocomial pneumonia: impact of multidrug resistance. Critical Care (London, England). 2015;19:219.PubMed Micek ST, Wunderink RG, Kollef MH, Chen C, Rello J, Chastre J, et al. An international multicenter retrospective study of Pseudomonas aeruginosa nosocomial pneumonia: impact of multidrug resistance. Critical Care (London, England). 2015;19:219.PubMed
27.
go back to reference Montero M, Sala M, Riu M, Belvis F, Salvado M, Grau S, et al. Risk factors for multidrug-resistant Pseudomonas aeruginosa acquisition. Impact of antibiotic use in a double case-control study. Eur J Clin Microbiol Infect Dis. 2010;29(3):335–9.PubMed Montero M, Sala M, Riu M, Belvis F, Salvado M, Grau S, et al. Risk factors for multidrug-resistant Pseudomonas aeruginosa acquisition. Impact of antibiotic use in a double case-control study. Eur J Clin Microbiol Infect Dis. 2010;29(3):335–9.PubMed
28.
go back to reference Nakamura A, Miyake K, Misawa S, Kuno Y, Horii T, Kondo S, et al. Meropenem as predictive risk factor for isolation of multidrug-resistant Pseudomonas aeruginosa. J Hosp Infect. 2013;83(2):153–5.PubMed Nakamura A, Miyake K, Misawa S, Kuno Y, Horii T, Kondo S, et al. Meropenem as predictive risk factor for isolation of multidrug-resistant Pseudomonas aeruginosa. J Hosp Infect. 2013;83(2):153–5.PubMed
29.
go back to reference Nseir S, Blazejewski C, Lubret R, Wallet F, Courcol R, Durocher A. Risk of acquiring multidrug-resistant gram-negative bacilli from prior room occupants in the intensive care unit. Clin Microbiol Infect. 2011;17(8):1201–8.PubMed Nseir S, Blazejewski C, Lubret R, Wallet F, Courcol R, Durocher A. Risk of acquiring multidrug-resistant gram-negative bacilli from prior room occupants in the intensive care unit. Clin Microbiol Infect. 2011;17(8):1201–8.PubMed
30.
go back to reference Ohmagari N, Hanna H, Graviss L, Hackett B, Perego C, Gonzalez V, et al. Risk factors for infections with multidrug-resistant Pseudomonas aeruginosa in patients with cancer. Cancer. 2005;104(1):205–12.PubMed Ohmagari N, Hanna H, Graviss L, Hackett B, Perego C, Gonzalez V, et al. Risk factors for infections with multidrug-resistant Pseudomonas aeruginosa in patients with cancer. Cancer. 2005;104(1):205–12.PubMed
31.
go back to reference Paramythiotou E, Lucet JC, Timsit JF, Vanjak D, Paugam-Burtz C, Trouillet JL, et al. Acquisition of multidrug-resistant Pseudomonas aeruginosa in patients in intensive care units: role of antibiotics with antipseudomonal activity. Clin Infect Dis. 2004;38(5):670–7.PubMed Paramythiotou E, Lucet JC, Timsit JF, Vanjak D, Paugam-Burtz C, Trouillet JL, et al. Acquisition of multidrug-resistant Pseudomonas aeruginosa in patients in intensive care units: role of antibiotics with antipseudomonal activity. Clin Infect Dis. 2004;38(5):670–7.PubMed
32.
go back to reference Park YS, Lee H, Chin BS, Han SH, Hong SG, Hong SK, et al. Acquisition of extensive drug-resistant Pseudomonas aeruginosa among hospitalized patients: risk factors and resistance mechanisms to carbapenems. J Hosp Infect. 2011;79(1):54–8.PubMed Park YS, Lee H, Chin BS, Han SH, Hong SG, Hong SK, et al. Acquisition of extensive drug-resistant Pseudomonas aeruginosa among hospitalized patients: risk factors and resistance mechanisms to carbapenems. J Hosp Infect. 2011;79(1):54–8.PubMed
33.
go back to reference Pena C, Gomez-Zorrilla S, Suarez C, Dominguez MA, Tubau F, Arch O, et al. Extensively drug-resistant Pseudomonas aeruginosa: risk of bloodstream infection in hospitalized patients. Eur J Clin Microbiol Infect Dis. 2012;31(10):2791–7.PubMed Pena C, Gomez-Zorrilla S, Suarez C, Dominguez MA, Tubau F, Arch O, et al. Extensively drug-resistant Pseudomonas aeruginosa: risk of bloodstream infection in hospitalized patients. Eur J Clin Microbiol Infect Dis. 2012;31(10):2791–7.PubMed
34.
go back to reference Samonis G, Vardakas KZ, Kofteridis DP, Dimopoulou D, Andrianaki AM, Chatzinikolaou I, et al. Characteristics, risk factors and outcomes of adult cancer patients with extensively drug-resistant Pseudomonas aeruginosa infections. Infection. 2014;42(4):721–8.PubMed Samonis G, Vardakas KZ, Kofteridis DP, Dimopoulou D, Andrianaki AM, Chatzinikolaou I, et al. Characteristics, risk factors and outcomes of adult cancer patients with extensively drug-resistant Pseudomonas aeruginosa infections. Infection. 2014;42(4):721–8.PubMed
35.
go back to reference Tumbarello M, Repetto E, Trecarichi EM, Bernardini C, De PG, Parisini A, et al. Multidrug-resistant Pseudomonas aeruginosa bloodstream infections: risk factors and mortality. Epidemiol Infect. 2011;139(11):1740–9.PubMed Tumbarello M, Repetto E, Trecarichi EM, Bernardini C, De PG, Parisini A, et al. Multidrug-resistant Pseudomonas aeruginosa bloodstream infections: risk factors and mortality. Epidemiol Infect. 2011;139(11):1740–9.PubMed
36.
go back to reference Tuncer EG, Sonmezer MC, Tulek N, Erdinc SF, Bulut C, Berkem R, et al. Evaluation of risk factors for nosocomial multidrugresistant Pseudomonas aeruginosa infections. Clin Microbiol Infect. 2012;18:517. Conference: 22nd European Congress of Clinical Microbiology and Infectious Diseases London United Kingdom Conference Start: 20120331 Conference End: 20120403 Conference Publication: (var pagings). Tuncer EG, Sonmezer MC, Tulek N, Erdinc SF, Bulut C, Berkem R, et al. Evaluation of risk factors for nosocomial multidrugresistant Pseudomonas aeruginosa infections. Clin Microbiol Infect. 2012;18:517. Conference: 22nd European Congress of Clinical Microbiology and Infectious Diseases London United Kingdom Conference Start: 20120331 Conference End: 20120403 Conference Publication: (var pagings).
37.
go back to reference Ustun C, Hosoglu S, Geyik MF. Risk factors for multi-drug-resistant Pseudomonas aeruginosa infections in a University Hospital - a case control study. Konuralp Tip Dergisi. 2016;8(2):2016. Ustun C, Hosoglu S, Geyik MF. Risk factors for multi-drug-resistant Pseudomonas aeruginosa infections in a University Hospital - a case control study. Konuralp Tip Dergisi. 2016;8(2):2016.
38.
go back to reference Willmann M, Klimek AM, Vogel W, Liese J, Marschal M, Autenrieth IB, et al. Clinical and treatment-related risk factors for nosocomial colonisation with extensively drug-resistant Pseudomonas aeruginosa in a haematological patient population: a matched case control study. BMC Infect Dis. 2014;14:650.PubMedPubMedCentral Willmann M, Klimek AM, Vogel W, Liese J, Marschal M, Autenrieth IB, et al. Clinical and treatment-related risk factors for nosocomial colonisation with extensively drug-resistant Pseudomonas aeruginosa in a haematological patient population: a matched case control study. BMC Infect Dis. 2014;14:650.PubMedPubMedCentral
39.
go back to reference Pena C, Suarez C, Tubau F, Dominguez A, Sora M, Pujol M, et al. Carbapenem-resistant Pseudomonas aeruginosa: factors influencing multidrug-resistant acquisition in non-critically ill patients. Eur J Clin Microbiol Infect Dis. 2009;28(5):519–22.PubMed Pena C, Suarez C, Tubau F, Dominguez A, Sora M, Pujol M, et al. Carbapenem-resistant Pseudomonas aeruginosa: factors influencing multidrug-resistant acquisition in non-critically ill patients. Eur J Clin Microbiol Infect Dis. 2009;28(5):519–22.PubMed
40.
go back to reference Tuon FF, Gortz LW, Rocha JL. Risk factors for pan-resistant Pseudomonas aeruginosa bacteremia and the adequacy of antibiotic therapy. Braz J Infect Dis. 2012;16(4):351–6.PubMed Tuon FF, Gortz LW, Rocha JL. Risk factors for pan-resistant Pseudomonas aeruginosa bacteremia and the adequacy of antibiotic therapy. Braz J Infect Dis. 2012;16(4):351–6.PubMed
41.
go back to reference Akhabue E, Synnestvedt M, Weiner MG, Bilker WB, Lautenbach E. Cefepime-Resistant Pseudomonas aeruginosa. Emerg Infect Dis. 2011;17(6):1037–43. Akhabue E, Synnestvedt M, Weiner MG, Bilker WB, Lautenbach E. Cefepime-Resistant Pseudomonas aeruginosa. Emerg Infect Dis. 2011;17(6):1037–43. 
42.
go back to reference DalBen MF, Basso M, Garcia CP, Costa SF, Toscano CM, Jarvis WR, et al. Colonization pressure as a risk factor for colonization by multiresistant Acinetobacter spp and carbapenem-resistant Pseudomonas aeruginosa in an intensive care unit.[Erratum appears in Clinics (Sao Paulo). 2013 Dec;68(12):1559]. Clinics (Sao Paulo, Brazil). 2013;68(8):1128–33.PubMed DalBen MF, Basso M, Garcia CP, Costa SF, Toscano CM, Jarvis WR, et al. Colonization pressure as a risk factor for colonization by multiresistant Acinetobacter spp and carbapenem-resistant Pseudomonas aeruginosa in an intensive care unit.[Erratum appears in Clinics (Sao Paulo). 2013 Dec;68(12):1559]. Clinics (Sao Paulo, Brazil). 2013;68(8):1128–33.PubMed
43.
go back to reference Djordjevic Z, Folic M, Ruzic ZD, Ilic G, Jankovic S. Risk factors for carbapenem-resistant Pseudomonas aeruginosa infection in a tertiary care hospital in Serbia. J Infect Dev Ctries. 2013;7(9):686–90.PubMed Djordjevic Z, Folic M, Ruzic ZD, Ilic G, Jankovic S. Risk factors for carbapenem-resistant Pseudomonas aeruginosa infection in a tertiary care hospital in Serbia. J Infect Dev Ctries. 2013;7(9):686–90.PubMed
44.
go back to reference Eagye KJ, Kuti JL, Nicolau DP. Risk factors and outcomes associated with isolation of meropenem high-level-resistant Pseudomonas aeruginosa. Infect Control Hosp Epidemiol. 2009;30(8):746–52.PubMed Eagye KJ, Kuti JL, Nicolau DP. Risk factors and outcomes associated with isolation of meropenem high-level-resistant Pseudomonas aeruginosa. Infect Control Hosp Epidemiol. 2009;30(8):746–52.PubMed
45.
go back to reference Fortaleza CM, Freire MP, Filho DC, de Carvalho RM. Risk factors for recovery of imipenem- or ceftazidime-resistant pseudomonas aeruginosa among patients admitted to a teaching hospital in Brazil. Infect Control Hosp Epidemiol. 2006;27(9):901–6.PubMed Fortaleza CM, Freire MP, Filho DC, de Carvalho RM. Risk factors for recovery of imipenem- or ceftazidime-resistant pseudomonas aeruginosa among patients admitted to a teaching hospital in Brazil. Infect Control Hosp Epidemiol. 2006;27(9):901–6.PubMed
46.
go back to reference Furtado GH, Bergamasco MD, Menezes FG, Marques D, Silva A, Perdiz LB, et al. Imipenem-resistant Pseudomonas aeruginosa infection at a medical-surgical intensive care unit: risk factors and mortality. J Crit Care. 2009;24(4):625–14. Furtado GH, Bergamasco MD, Menezes FG, Marques D, Silva A, Perdiz LB, et al. Imipenem-resistant Pseudomonas aeruginosa infection at a medical-surgical intensive care unit: risk factors and mortality. J Crit Care. 2009;24(4):625–14.
47.
go back to reference Furtado GH, Gales AC, Perdiz LB, Santos AE, Wey SB, Medeiros EA. Risk factors for hospital-acquired pneumonia caused by imipenem-resistant Pseudomonas aeruginosa in an intensive care unit. Anaesth Intensive Care. 2010;38(6):994–1001.PubMed Furtado GH, Gales AC, Perdiz LB, Santos AE, Wey SB, Medeiros EA. Risk factors for hospital-acquired pneumonia caused by imipenem-resistant Pseudomonas aeruginosa in an intensive care unit. Anaesth Intensive Care. 2010;38(6):994–1001.PubMed
48.
go back to reference Gasink LB, Fishman NO, Weiner MG, Nachamkin I, Bilker WB, Lautenbach E. Fluoroquinolone-resistant Pseudomonas aeruginosa: assessment of risk factors and clinical impact. Am J Med. 2006;119(6):526–5. Gasink LB, Fishman NO, Weiner MG, Nachamkin I, Bilker WB, Lautenbach E. Fluoroquinolone-resistant Pseudomonas aeruginosa: assessment of risk factors and clinical impact. Am J Med. 2006;119(6):526–5.
49.
go back to reference Harris AD, Perencevich E, Roghmann MC, Morris G, Kaye KS, Johnson JA. Risk factors for piperacillin-tazobactam-resistant Pseudomonas aeruginosa among hospitalized patients. Antimicrob Agents Chemother. 2002;46(3):854–8.PubMedPubMedCentral Harris AD, Perencevich E, Roghmann MC, Morris G, Kaye KS, Johnson JA. Risk factors for piperacillin-tazobactam-resistant Pseudomonas aeruginosa among hospitalized patients. Antimicrob Agents Chemother. 2002;46(3):854–8.PubMedPubMedCentral
50.
go back to reference Harris AD, Smith D, Johnson JA, Bradham DD, Roghmann MC. Risk factors for imipenem-resistant Pseudomonas aeruginosa among hospitalized patients. Clin Infect Dis. 2002;34(3):340–5.PubMed Harris AD, Smith D, Johnson JA, Bradham DD, Roghmann MC. Risk factors for imipenem-resistant Pseudomonas aeruginosa among hospitalized patients. Clin Infect Dis. 2002;34(3):340–5.PubMed
51.
go back to reference Harris AD, Johnson JK, Thom KA, Morgan DJ, McGregor JC, Ajao AO, et al. Risk factors for development of intestinal colonization with imipenem-resistant Pseudomonas aeruginosa in the intensive care unit setting. Infect Control Hosp Epidemiol. 2011;32(7):719–22.PubMedPubMedCentral Harris AD, Johnson JK, Thom KA, Morgan DJ, McGregor JC, Ajao AO, et al. Risk factors for development of intestinal colonization with imipenem-resistant Pseudomonas aeruginosa in the intensive care unit setting. Infect Control Hosp Epidemiol. 2011;32(7):719–22.PubMedPubMedCentral
52.
go back to reference Hsu DI, Okamoto MP, Murthy R, Wong-Beringer A. Fluoroquinolone-resistant Pseudomonas aeruginosa: risk factors for acquisition and impact on outcomes. J Antimicrob Chemother. 2005;55(4):535–41.PubMed Hsu DI, Okamoto MP, Murthy R, Wong-Beringer A. Fluoroquinolone-resistant Pseudomonas aeruginosa: risk factors for acquisition and impact on outcomes. J Antimicrob Chemother. 2005;55(4):535–41.PubMed
53.
go back to reference Khayr W, Rheault W, Waiters L, Walters A. Epidemiology of ciprofloxacin-resistant Pseudomonas aeruginosa in a veterans affairs hospital. Am J Ther. 2000;7(5):309–12.PubMed Khayr W, Rheault W, Waiters L, Walters A. Epidemiology of ciprofloxacin-resistant Pseudomonas aeruginosa in a veterans affairs hospital. Am J Ther. 2000;7(5):309–12.PubMed
54.
go back to reference Kohlenberg A, Weitzel-Kage D, van der Linden P, Sohr D, Vogeler S, Kola A, et al. Outbreak of carbapenem-resistant Pseudomonas aeruginosa infection in a surgical intensive care unit. J Hosp Infect. 2010;74(4):350–7.PubMed Kohlenberg A, Weitzel-Kage D, van der Linden P, Sohr D, Vogeler S, Kola A, et al. Outbreak of carbapenem-resistant Pseudomonas aeruginosa infection in a surgical intensive care unit. J Hosp Infect. 2010;74(4):350–7.PubMed
55.
go back to reference Lautenbach E, Synnestvedt M, Weiner MG, Bilker WB, Vo L, Schein J, et al. Imipenem resistance in Pseudomonas aeruginosa: emergence, epidemiology, and impact on clinical and economic outcomes. Infect Control Hosp Epidemiol. 2010;31(1):47–53.PubMed Lautenbach E, Synnestvedt M, Weiner MG, Bilker WB, Vo L, Schein J, et al. Imipenem resistance in Pseudomonas aeruginosa: emergence, epidemiology, and impact on clinical and economic outcomes. Infect Control Hosp Epidemiol. 2010;31(1):47–53.PubMed
56.
go back to reference Lee CH, Su TY, Ye JJ, Hsu PC, Kuo AJ, Chia JH, et al. Risk factors and clinical significance of bacteremia caused by Pseudomonas aeruginosa resistant only to carbapenems. J Microbiol Immunol Infect. 2017;50(5):677–83. Lee CH, Su TY, Ye JJ, Hsu PC, Kuo AJ, Chia JH, et al. Risk factors and clinical significance of bacteremia caused by Pseudomonas aeruginosa resistant only to carbapenems. J Microbiol Immunol Infect. 2017;50(5):677–83.
57.
go back to reference Lin KY, Lauderdale TL, Wang JT, Chang SC. Carbapenem-resistant Pseudomonas aeruginosa in Taiwan: prevalence, risk factors, and impact on outcome of infections. J Microbiol Immunol Infect. 2016;49(1):52–9.PubMed Lin KY, Lauderdale TL, Wang JT, Chang SC. Carbapenem-resistant Pseudomonas aeruginosa in Taiwan: prevalence, risk factors, and impact on outcome of infections. J Microbiol Immunol Infect. 2016;49(1):52–9.PubMed
58.
go back to reference Luyt CE, Aubry A, Lu Q, Micaelo M, Brechot N, Brossier F, et al. Imipenem, meropenem, or doripenem to treat patients with Pseudomonas aeruginosa ventilator-associated pneumonia. Antimicrob Agents Chemother. 2014;58(3):1372–80.PubMedPubMedCentral Luyt CE, Aubry A, Lu Q, Micaelo M, Brechot N, Brossier F, et al. Imipenem, meropenem, or doripenem to treat patients with Pseudomonas aeruginosa ventilator-associated pneumonia. Antimicrob Agents Chemother. 2014;58(3):1372–80.PubMedPubMedCentral
59.
go back to reference Onguru P, Erbay A, Bodur H, Baran G, Akinci E, Balaban N, et al. Imipenem-resistant Pseudomonas aeruginosa: risk factors for nosocomial infections. J Korean Med Sci. 2008;23(6):982–7.PubMedPubMedCentral Onguru P, Erbay A, Bodur H, Baran G, Akinci E, Balaban N, et al. Imipenem-resistant Pseudomonas aeruginosa: risk factors for nosocomial infections. J Korean Med Sci. 2008;23(6):982–7.PubMedPubMedCentral
60.
go back to reference Pena C, Guzman A, Suarez C, Dominguez MA, Tubau F, Pujol M, et al. Effects of carbapenem exposure on the risk for digestive tract carriage of intensive care unit-endemic carbapenem-resistant Pseudomonas aeruginosa strains in critically ill patients. Antimicrob Agents Chemother. 2007;51(6):1967–71.PubMedPubMedCentral Pena C, Guzman A, Suarez C, Dominguez MA, Tubau F, Pujol M, et al. Effects of carbapenem exposure on the risk for digestive tract carriage of intensive care unit-endemic carbapenem-resistant Pseudomonas aeruginosa strains in critically ill patients. Antimicrob Agents Chemother. 2007;51(6):1967–71.PubMedPubMedCentral
61.
go back to reference Pereira GH, Levin AS, Oliveira HB, Moretti ML. Controlling the clonal spread of Pseudomonas aeruginosa infection. Infect Control Hosp Epidemiol. 2008;29(6):549–52.PubMed Pereira GH, Levin AS, Oliveira HB, Moretti ML. Controlling the clonal spread of Pseudomonas aeruginosa infection. Infect Control Hosp Epidemiol. 2008;29(6):549–52.PubMed
62.
go back to reference Tam VH, Chang KT, LaRocco MT, Schilling AN, McCauley SK, Poole K, et al. Prevalence, mechanisms, and risk factors of carbapenem resistance in bloodstream isolates of Pseudomonas aeruginosa. Diagn Microbiol Infect Dis. 2007;58(3):309–14.PubMed Tam VH, Chang KT, LaRocco MT, Schilling AN, McCauley SK, Poole K, et al. Prevalence, mechanisms, and risk factors of carbapenem resistance in bloodstream isolates of Pseudomonas aeruginosa. Diagn Microbiol Infect Dis. 2007;58(3):309–14.PubMed
63.
go back to reference Trouillet JL, Vuagnat A, Combes A, Kassis N, Chastre J, Gibert C. Pseudomonas aeruginosa ventilator-associated pneumonia: comparison of episodes due to piperacillin-resistant versus piperacillin-susceptible organisms. Clin Infect Dis. 2002;34(8):1047–54.PubMed Trouillet JL, Vuagnat A, Combes A, Kassis N, Chastre J, Gibert C. Pseudomonas aeruginosa ventilator-associated pneumonia: comparison of episodes due to piperacillin-resistant versus piperacillin-susceptible organisms. Clin Infect Dis. 2002;34(8):1047–54.PubMed
64.
go back to reference Zavascki AP, Cruz RP, Goldani LZ. Risk factors for imipenem-resistant Pseudomonas aeruginosa: a comparative analysis of two case-control studies in hospitalized patients. J Hosp Infect. 2005;59(2):96–101.PubMed Zavascki AP, Cruz RP, Goldani LZ. Risk factors for imipenem-resistant Pseudomonas aeruginosa: a comparative analysis of two case-control studies in hospitalized patients. J Hosp Infect. 2005;59(2):96–101.PubMed
65.
go back to reference Zhang JF, Chen BL, Xin XY, Zhao HB, Wang HY, Song H, et al. Carbapenem resistance mechanism and risk factors of Pseudomonas aeruginosa clinical isolates from a University Hospital in Xi'an, China. Microb Drug Resist. 2009;15(1):41–5.PubMed Zhang JF, Chen BL, Xin XY, Zhao HB, Wang HY, Song H, et al. Carbapenem resistance mechanism and risk factors of Pseudomonas aeruginosa clinical isolates from a University Hospital in Xi'an, China. Microb Drug Resist. 2009;15(1):41–5.PubMed
66.
go back to reference Nicasio AM, Kuti JL, Nicolau DP. The current state of multidrug-resistant gram-negative bacilli in North America. Pharmacotherapy. 2008;28(2):235–49.PubMed Nicasio AM, Kuti JL, Nicolau DP. The current state of multidrug-resistant gram-negative bacilli in North America. Pharmacotherapy. 2008;28(2):235–49.PubMed
67.
go back to reference Buhl M, Peter S, Willmann M. Prevalence and risk factors associated with colonization and infection of extensively drug-resistant Pseudomonas aeruginosa: a systematic review. Expert Rev Anti-Infect Ther. 2015;13(9):1159–70.PubMed Buhl M, Peter S, Willmann M. Prevalence and risk factors associated with colonization and infection of extensively drug-resistant Pseudomonas aeruginosa: a systematic review. Expert Rev Anti-Infect Ther. 2015;13(9):1159–70.PubMed
68.
go back to reference Egger M, Davey SG, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34.PubMedPubMedCentral Egger M, Davey SG, Schneider M, Minder C. Bias in meta-analysis detected by a simple, graphical test. BMJ. 1997;315(7109):629–34.PubMedPubMedCentral
Metadata
Title
Risk factors for hospitalized patients with resistant or multidrug-resistant Pseudomonas aeruginosa infections: a systematic review and meta-analysis
Authors
Gowri Raman
Esther E. Avendano
Jeffrey Chan
Sanjay Merchant
Laura Puzniak
Publication date
01-12-2018
Publisher
BioMed Central
Published in
Antimicrobial Resistance & Infection Control / Issue 1/2018
Electronic ISSN: 2047-2994
DOI
https://doi.org/10.1186/s13756-018-0370-9

Other articles of this Issue 1/2018

Antimicrobial Resistance & Infection Control 1/2018 Go to the issue