Predictors of mortality from extended-spectrum beta-lactamase-producing Enterobacteriaceae bacteremia

Figures & data

Figure 1. Flow diagram of selection process for included studies.

Table 1. Characteristics of studies included in the systematic literature review and meta-analysis.

Author (year)	Country	Design	Period	Population	Death (%)	Mortality day
Kang et al. [17]	Korea	Retrospective cohort study	1998–2002	133 patients with ESBL-producing E. coli or K. pneumoniae bacteremia	34 (25.6)	30
Tumbarello et al. [22]	Italy	Retrospective cohort study	1999–2005	129 patients with ESBL-producing E. coli bacteremia	38 (29.5)	21
Rodríguez-Baño et al. [23]	Spain	Prospective study	2004–2006	96 patients with ESBL-producing E. coli bacteremia	24 (25.0)	14
Wang et al. [24]	Taiwan	Retrospective cohort study	2002–2007	113 patients with ESBL-producing E. coli or K. pneumoniae bacteremia	27 (23.9)	14
Chung et al. [25]	Taiwan	Observational study	2005–2010	124 patients with ESBL-producing E. coli bacteremia	30 (24.2)	28
Lee et al. [26]	Taiwan	Retrospective study	2002–2007	251 patients with ESBL-producing E. coli or K. pneumoniae bacteremia	33 (13.1)	sepsis-related
Ku et al. [21]	Korea	Retrospective cohort study	2006–2010	191 patients with ESBL-producing E. coli or K. pneumoniae bacteremia	47 (24.6)	28
Tamma et al. [27]	USA	Retrospective cohort study	2007-2014	213 patients with ESBL-PE bacteremia	26 (12.2)	14
Ofer-Friedman et al. [28]	Israel and USA	Retrospective cohort study	2008–2012	79 patients with ESBL-PE bacteremia	39 (49.4)	90
Lee et al. [29]	Taiwan	Retrospective case-control study	2007–2012	389 patients with ESBL-producing E. coli or K. pneumoniae bacteremia	71 (18.3)	30
Cheng et al. [20]	Taiwan	Retrospective study	2002–2010	111 patients with bacteremic pneumonia caused by ESBL-producing E. coli or K. pneumoniae	45 (40.5)	30
Ng et al. [30]	Singapore	Retrospective cohort study	2011–2013	151 patients with ESBL-producing E. coli or K. pneumoniae bacteremia	46 (30.5	30
Palacios-Baena et al. [18]	Multinational	Retrospective cohort study	2004–2013	622 patients with ESBL-PE bacteremia	115 (18.5)	30
Yu et al. [31]	Taiwan	Retrospective study	2009–2010	48 patients with ESBL-producing K. pneumoniae bacteremia	27 (56.3)	in hospital
Lo et al. [32]	Taiwan	Retrospective cohort study	2008–2010	299 patients with ESBL-producing E. coli or K. pneumoniae bacteremia	66 (22.1)	30
Chapelet et al. [33]	France	Retrospective cohort study	2008–2015	140 patients with ESBL-producing E. coli bacteremia	22 (15.7)	30
Ko et al. [13]	Korea	Retrospective cohort study	2010–2014	232 patients with ESBL-PE bacteremia	23 (9.9)	30
Xiao et al. [19]	China	Retrospective study	2013-2016	283 patients with ESBL-producing E. coli bacteremia	42 (14.8)	28
Zohar et al. [9]	Israel	Retrospective cohort study	2014-2017	193 patients with ESBL-PE bacteremia	32 (16.6)	30
Mitsuboshi et al. [34]	Japan	Retrospective cohort study	2012-2016	179 patients with ESBL-PE bacteremia	24 (13.4)	30
Benetazzo et al. [10]	France	Retrospective cohort study	2011-2018	307 patients with ESBL-PE bacteremia	125 (40.7)	30
Park et al. [11]	Korea	Retrospective cohort study	2013-2020	324 patients with ESBL-PE bacteremia	40 (12.3)	30

Notes: E. coli: Escherichia coli, ESBL-PE: extended-spectrum β-lactamase-producing Enterobacteriaceae, K. pneumoniae: Klebsiella pneumoniae. Multinational: Spain, Germany, Italy, Greece, Israel, Turkey, South Africa, Canada, USA, Argentina, and Taiwan, USA: United States of America.

Table 2. Results of studies performing multivariable analyses regarding mortality in patients with ESBL-PE bacteremia.

Author (year)	N	Methods	Predictor	RR	95% CI	P-value
Kang et al. [17]	133	Logistic regression	Administration of broad-spectrum	9.18	1.55–54.51	0.015
			cephalosporin as definitive antimicrobial
			therapy (/No)
			Neutropenia (/No)	9.03	1.24–65.97	0.030
			Peritonitis (/No)	10.25	1.26–83.25	0.029
			Presentation with septic shock (/No)	45.25	6.55–312.84	<0.001
			Increasing APACHE II score (per 1)	1.44	1.11–1.87	0.006
Tumbarello et al. [22]	129	Logistic regression	Inadequate initial antimicrobial treatment (/No)	6.22	2.33–16.61	<0.001
			Unknown source (/No)	4.28	1.71–10.69	0.001
			Presentation with septic shock (/No)	5.88	1.26–27.45	0.02
Rodríguez-Baño et al. [23]	96	Conditional	Pitt score >1 (/0-1)	3.9	1.2–12.9	0.02
		logistic regression	High-risk source^a (/No)	5.5	1.4–21.9	0.01
			Severe sepsis or shock (/No)	4.6	1.4–15.2	0.01
			Resistance score >3 (/0-3)	6.5	1.4–30.0	0.01
Wang et al. [24]	113	Logistic regression	Severe sepsis (/No)	24.29	5.62–104.98	<0.001
			Pneumonia (/No)	5.20	1.29–20.95	0.021
			Respiratory failure (/No)	3.45	0.40–29.89	0.261
			Shock (/No)	2.81	0.43–18.42	0.280
			Pitt bacteremia score ≥4 (/< 4)	2.63	0.47–14.64	0.269
			Appropriate empirical therapy (/No)	0.345	0.06–2.03	0.239
			Appropriate definitive therapy (/No)	0.089	0.01–0.58	0.011
Chung et al. [25]	124	Logistic regression	Cancer (/No)	2.81	1.03–7.66	-
			Community-onset (/No)	0.29	0.11–0.77	-
			Shock (/No)	6.75	2.52–18.0	-
Lee et al. [26]	251	Conditional	Age (per 1-yr)	1.01	0.98–1.04	0.42
		logistic regression	Male (/female)	1.13	0.45–2.86	0.80
			Severe sepsis (/No)	15.9	5.84–43.34	<0.001
			Hospital-onset bacteremia (/No)	4.65	1.42–15.24	0.01
			Rapidly fatal underlying disease (/No)	2.07	0.7–6.17	0.20
			Pneumonia (/No)	1.56	0.63–3.88	0.34
			Appropriate antimicrobial therapy (/No)	0.44	0.14–2.36	0.57
			Ertapenem-nonsusceptible isolates^b (/No)	5.12	2.04–12.88	0.001
Ku et al. [21]	191	Logistic regression	Age (per 1-yr)	1.066	0.976–1.165	0.157
			Hospital-acquired (/community-acquired)	0.292	0.067–1.281	0.103
			Hemodialysis (/No)	1.205	0.257–5.658	0.813
			Neutropenia at bacteremia (/No)	3.592	0.955–13.505	0.058
			Use of steroids at bacteremia (/No)	1.188	0.384–3.673	0.765
			Prior antimicrobial therapy within 30 days	9.084	1.570–52.572	0.014
			before bacteremia (/No)
			Urinary tract (/No)	0.076	0.010–0.547	0.011
			Pulmonary (/No)	0.948	0.328–2.743	0.922
			SOFA score (per 1)	1.847	1.493–2.286	<0.001
Tamma et al. [27]	213	Adjusted	Piperacillin-tazobactam (/carbapenem)	1.92	1.07–3.45	0.03
		cox regression	Age (per 10-yr increase)	1.18	0.99–1.41	0.07
			Pitt bacteremia score (per 1)	1.49	1.28–1.72	<0.001
			ICU level care, day 1 (per 1)	4.25	1.86–9.71	<0.001
Ofer-Friedman et al. [28]	79	Logistic regression	Piperacillin-tazobactam case (/carbapenem)	7.9	1.2–53	0.03
			Time at risk^c (per 1 d)	1.1	1.008–1.13	0.03
			Fatal McCabe score (per 1)	26	6–115	<0.001
Lee et al. [29]	389	Logistic regression	Pitt bacteremia score ≥4 (/< 4)	3.2	1.5–6.6	<0.01
			Pneumonia (/No)	4.9	2.5–9.9	<0.01
			Urosepsis (/No)	0.3	0.1–0.8	0.02
			Definitive flomoxef therapy (/carbapenem)	1.4	0.5–4.2	0.52
			Definitive flomoxef therapy for isolates with	5.7	1.9–16.8	<0.01
			flomoxef MICs of 2-8 mg/L (/No)
Cheng et al. [20]	111	Conditional	Solid tumour (/No)	2.09	0.53–8.29	0.30
		logistic regression	Rapidly fatal underlying disease (/No)	5.75	1.54- 21.48	0.009
			Critical illness (Pittsburg bacteremia score of ≥4) (/< 4)	4.28	1.35–13.57	0.013
			Severe sepsis (/No)	4.84	1.55–15.14	0.007
			Appropriate empirical antimicrobial therapy	0.19	0.77–0.55	0.002
			(/No)
Ng et al. [30]	151	Logistic regression	Pitt bacteremia score (per 1)	1.20	0.98–1.48	0.08
			Charlson's comorbidity index (per 1)	0.94	0.81–1.09	0.40
			Respiratory source (/No)	2.81	0.87–9.05	0.08
			Hepatobiliary source (/No)	0.18	0.02–1.48	0.11
			Unknown source (/No)	1.51	0.33–6.92	0.60
			Empiric piperacillin-tazobactam (/carbapenem)	0.99	0.45–2.17	0.99
Palacios-Baena et al. [18]	622	Logistic regression	Age >50 years (/≤50)	2.63	1.18–5.85	0.01
			Klebsiella spp. (/No)	2.08	1.21–3.58	0.008
			Source other than UTI (/No)	3.60	2.02–6.44	<0.001
			McCabe (UF and RF) (/No)	3.91	2.24–6.80	<0.001
			Pitt score >3 (/≤3)	3.04	1.69–5.47	<0.001
			Severe sepsis/septic shock (/No)	4.80	2.72–8.46	<0.001
			Inappropriate early targeted therapy (/No)	2.47	1.58–4.63	0.002
Yu et al. [31]	48	Cox proportional	Nosocomial (/No)	2.29	0.41–12.80	-
		hazards regression	Urinary tract infection (/primary infection)	0.92	0.15–5.64	-
			Stay in intensive care unit (/No)	0.99	0.22–4.45	-
			No removal of CVC (/no CVC line)	0.83	0.21–3.21	-
			Initial appropriate antibiotic therapy (/No)	0.88	0.28–2.77	-
			Charlson score (per 1)	1.43	1.04–1.99	<0.05
			APACHE II score ≥15 (/< 15)	2.55	0.82–7.88	-
Lo et al. [32]	299	Conditioning	Hospital-onset bacteremia (/No)	2.57	1.22–5.45	0.01
		logistic regression	Pneumonia (/No)	1.27	0.65–2.48	0.49
			Urosepsis (/No)	0.47	0.18–1.18	0.12
			Rapidly fatal underlying disease (/No)	5.73	2.51–13.08	<0.001
			Pitt bacteremia score ≥4 points (/< 4)	7.09	3.71–13.56	<0.001
			Fluoroquinolone definitive therapy	0.18	0.03–0.92	0.04
			(/carbapenem)
Chapelet et al. [33]	140	Logistic regression	Age (per 1)	1.01	0.96–1.07	0.784
			Female (/male)	0.85	0.18–4.09	0.836
			Charlson score comorbidities index ≥2 (/< 2)	5.00	0.28–88.36	0.273
			History of hepatic disease (/No)	0.47	0.05–4.79	0.522
			Dementia (/No)	54.51	1.20–2472.22	0.040
			Walking status (able to walk) (/No)	0.03	0.01–0.59	0.021
			Immunosuppressive treatment, including	1.58	0.12–21.55	0.733
			corticosteroid (/No)
			Previous antimicrobial therapy within 30 days	3.34	0.64–17.50	0.153
			before bacteremia (/No)
			Time to blood culture positivity ≤ 480 min	3.20	0.48–21.13	0.228
			(/>480 min)
			SOFA score (per 1)	1.69	1.26–2.27	<0.001
			Neutropenia (/No)	12.94	1.01–166.00	0.049
			Appropriate empirical antibiotic-treatment	0.42	0.08–2.21	0.305
			(/No)
			Urinary tract infection (/No)	0.07	0.01–0.84	0.036
			Pulmonary tract infection (/No)	1.17	0.06–24.61	0.921
Ko et al. [13]	232	Cox proportional	Empirical non-carbapenem use (/carbapenem)	0.83	0.24–2.82	0.76
		hazard regression	Age (per 1)	1.02	0.99–1.06	0.14
			K. pneumoniae infection (/E. coli infection)	2.73	0.83–9.00	0.10
			Antibiotic administration interval^d (per 1 h)	1.02	0.98–1.05	0.32
			Catheter-related BSI (/primary bacteremia)	2.38	0.34–16.77	0.38
			Urinary tract (/primary bacteremia)	0.07	0.01–0.51	0.01
			Intra-abdominal (/primary bacteremia)	1.30	0.41–4.13	0.66
			Others^e (/primary bacteremia)	0.61	0.09–4.17	0.61
			Transfer to ICU within 48 h (/No)	4.99	1.85–13.46	<0.01
			APACHE II (per 1)	1.03	0.96–1.09	0.45
			Charlson’s WIC (per 1)	0.99	0.84–1.17	0.93
Xiao et al. [19]	283	Binary logistic	Lung infection (/No)	2.012	0.912–4.437	0.083
		regression	Urinary catheterization (/No)	1.879	0.891–3.963	0.097
			Prior antibiotics use^f (/No)	1.872	0.886–3.954	0.100
			Total albumin (median, IQR)	0.941	0.887–0.999	0.045
			APACHEII score (per 1)	1.103	1.033–1.177	0.003
Zohar et al. [9]	193	Logistic regression	Age (per 1)	1.04	0.99–1.09	0.093
			Charlson comorbidity index (per 1)	1.21	1.01–1.46	0.040
			Other than E. coli (/E. coli)	1.78	1.06–3.01	0.031
			severe sepsis or septic shock (/No)	3.85	1.69–8.77	0.001
Mitsuboshi et al. [34]	179	Logistic regression	Age ≥ 85 years (/< 85 years)	1.59	0.36–7.02	0.54
			qSOFA scores ≥2 (/< 2)	1.27	0.27–5.97	0.76
			Biliary tract infection (/urinary tract infection)	8.90	0.88–89.90	0.06
			Other sites of infection (/urinary tract infection)	27.50	2.90–260.00	<0.01
Benetazzo et al. [10]	307	Cox proportional	Aminoglycoside (/No)	1.05	0.54–2.06	0.89
		hazard regression	Male sex (/female)	0.50	0.25–1.01	0.05
			55≦age<62 (/<55)	1.64	0.67–4.03	0.28
			62≦age<70 (/<55)	1.49	0.60–3.65	0.39
			Age ≥ 70 (/< 55)	2.67	1.09–6.54	0.03
			Medical admission (/No)	0.72	0.28–1.88	0.51
			Cardiac insufficiency (/No)	2.16	0.78–5.98	0.14
			Transplantation (/No)	5.20	1.4–19.35	0.01
			Hospital acquired infection (/No)	8.67	1.74–43.08	0.01
			5≦SOFA<7 (/<5)	0.54	0.21–1.42	0.76
			7≦SOFA<11 (/<5)	0.52	0.23–1.18	0.12
			SOFA ≥ 11 (/< 5)	1.69	0.66–4.34	0.28
			Duration of vasopressors
			between 24 and 48 h (/< 24 h)	3.02	1.24–7.31	0.01
			>48 h (/< 24 h)	3.61	1.62–8.02	0.002
			Active combination therapy (/No)	0.55	0.28–1.08	0.08
			ARDS (/No)	2.42	1.14–5.16	0.02
			Acute renal failure	2.49	1.14–5.47	0.02
Park et al. [11]	324	Cox proportional	Male sex (/female)	0.91	0.43–1.91	0.80
		hazard regression	E. coli (/No)	0.38	0.17–0.83	0.015
			Nosocomial acquisition (/No)	2.68	1.32–5.42	0.006
			Liver cirrhosis (/No)	1.76	0.58–5.37	0.32
			ESRD (/No)	1.87	0.28–12.57	0.52
			Solid tumour, localized (/No)	1.96	0.93–4.11	0.077
			Metastatic solid tumour (/No)	3.96	1.28–12.24	0.017
			Chemotherapy within 6 months (/No)	1.27	0.47–3.44	0.64
			Charlson’s comorbidity index (per 1)	1.03	0.85–1.25	0.75
			Biliary (/urinary tract)	1.42	0.45–4.43	0.55
			Other (/urinary tract)	1.73	0.74–4.05	0.21
			Pitt bacteremia score (per 1)	1.29	1.06–1.56	0.012
			Severe sepsis or septic shock (/No)	3.14	1.30–7.59	0.011
			Ertapenem (/other carbapenem)	0.60	0.29–1.22	0.16

Notes: APACHE: acute physiology and chronic health evaluation, ARDS: acute respiratory distress syndrome, BSI: bloodstream infection, CI: confidence interval, CVC: central venous catheter, E. coli: Escherichia coli, ESRD: end-stage renal disease, ICU: intensive care unit, K. pneumoniae: Klebsiella pneumoniae, Method: methods of multivariate analysis, MIC: minimum inhibitory concentration, N: sample size, qSOFA: quick SOFA, RF: rapidly fatal, RR: risk ratio, SD: standard deviation, SOFA: sequential organ failure assessment, UF: ultimately fatal, UTI: urinary tract infection, WIC: weighted index of comorbidities.

^a intra-abdominal infection, respiratory tract infection, and unknown source.

^b Ertapenem nonsusceptible was an ertapenem MIC of>0.25 g/ml, according to the breakpoint criteria of CLSI (document M100-S21).

^c Number of days from admission to ESBL culture.

^d Time interval from the diagnosis of bacteremia to administration of appropriate antibiotics.

^e Others included respiratory tract, skin and soft tissue, and central nervous system infections.

^f During the 30 days preceding BSI onset.

Figure 3. Forest plot showing the odds ratio of the mortality for carbapenems versus non-carbapenems in patients with extended-spectrum beta-lactamase-producing Enterobacteriaceae bacteremia.

Table 3. Summary of mortality in ESBL-PE bacteremia patients according to antibiotic comparisons.

Author (year)	Antibiotic comparison	no. of patients, n/N (%)
Kang et al. [17]	carbapenems vs ciprofloxacin (definitive)	8/62 (12.9) vs 3/29 (10.3)
Tamma et al. [27]	carbapenems vs PTZ (empirical)	9/110 (8.2) vs 17/103 (16.5)
Ofer-Friedman et al. [28]	carbapenems vs PTZ (empirical or definitive)	31/69 (44.9) vs 8/10 (80.0)
Lee et al. [29]	carbapenems vs flomoxef (definitive)	33/257 (12.8) vs 38/132 (28.8)
Ng et al. [30]	carbapenems vs PTZ (empirical)	17/57 (29.8) vs 29/94 (30.9)
Lo et al. [32]	carbapenems vs fluoroquinolone (definitive)	64/275 (23.3) vs 2/24 (8.3)
Ko et al. [13]	carbapenems vs non-carbapenems (empirical)	20/175 (11.4) vs 3/48 (6.3)
Xiao et al. [19]	carbapenems vs BLBLI combination (empirical)	15/117 (12.8) vs 17/95 (17.9)

Notes: BLBLI: beta-lactam-beta-lactamase inhibitor, n: sample number, N: sample size, no: numero sign, PTZ: piperacillin-tazobactam, vs: versus.

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Data availability statement

All data generated or analyzed during this study are included in this published article.