Design of the study and setting
The medical records of patients who experienced S. maltophilia pneumonia from January 2012 to January 2017 were collected from 25 ICUs of the French Society of Anaesthesia & Intensive Care Medicine (SFAR) and AZUREA networks [8]. Participating centers and case-mixes are listed in Additional file 1.
The collected data involved both ICU and hospital stays. Follow-up was stopped either after hospital discharge or death, whichever occurred first.
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Participants
Eligibility criteria
All patients aged over 18 years who were admitted to the participating ICUs and presenting with a documented diagnosis of S. maltophilia pneumonia during their ICU stay were eligible.
Source and method of selection
The patient’s files were extracted through French hospital discharge database containing individual records of all hospital stays using International Classification of Disease (ICD-10) for the terms “Stenotrophomonas maltophilia” and “pneumonia.” In addition, ICU medical charts were cross-checked with microbiology laboratory-specific information systems to ensure exhaustivity.
Each medical record was analyzed by local investigators to determine if clinical, biological, and/or radiological signs of S. maltophilia HAP were present, thus excluding respiratory tract colonizations (defined as a positive respiratory sample without clinical, biological, and/or radiological signs of S. maltophilia pneumonia). In case of uncertainty, consensus was obtained between local infectious disease specialists and study coordinators (PG, AB) to clarify S. maltophilia HAP cases.
Definitions
Pneumonia was defined as follows: (i) new or progressive lung infiltrate, (ii) temperature > 38 °C or < 36.5 °C, leukocyte count > 12,000 μl−1 or < 4000 μl−1, purulent endotracheal aspirate or sputum, (iii) positive respiratory sample (see below), and (iv) decline in oxygenation [9, 10]. HAP was defined as a pneumonia not incubating at the time of hospital admission and occurring 48 h or more after admission. Ventilator-associated pneumonia (VAP) was defined as a pneumonia occurring 48 h or more after tracheal intubation [9].
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The clinical cure of S. maltophilia pneumonia was defined by the absence of pneumonia criteria 48 h after antimicrobial therapy cessation. Treatment failure was defined as a failure of first-line treatment or death attributable to S. maltophilia pneumonia. Recurrence was defined as the onset of new pneumonia criteria associated with a positive respiratory sample with S. maltophilia after the initial pneumonia was considered successfully cured.
Empirical antimicrobial therapy was defined as the first agents prescribed for the initial treatment of HAP (effective or not on S. maltophilia) finally diagnosed as being caused by S. maltophilia. Empirical antimicrobial therapy was considered as effective if the S. maltophilia strain cultured from the respiratory sample was susceptible to at least one of the antimicrobial agents. Combination therapy was defined as the administration of at least two antimicrobial agents a priori (before S. maltophilia HAP has been confirmed, usually within 48 h) or a posteriori (after S. maltophilia HAP has been confirmed) effective on the S. maltophilia strain for more than 24 h.
Data collection
Usual demographic variables were collected, including previous hospital stays and previous exposure to antimicrobial therapies (agents and durations). Simplified Acute Physiology Score II (SAPSII) and the Sequential Organ Failure Assessment (SOFA) score were assessed.
On the day of S. maltophilia HAP diagnosis, the SOFA score was collected, as well as the number and type of invasive devices inserted. The severity of hypoxemia was graded according to the Berlin acute respiratory distress syndrome (ARDS) criteria [11]. Requirements for high-flow nasal oxygen therapy, non-invasive or invasive mechanical ventilation, or extracorporeal membrane oxygenation (ECMO) were reported. Empirical antimicrobial therapy and secondary adaptations were recorded, as were durations.
Diagnosis of positive bacterial culture
In case of S. maltophilia isolation, the culture was considered to be positive (either mono- or polymicrobial infection) with the following cutoff: (1) for minimally contaminated lower respiratory tract sample with quantitative culture, the threshold was 104 colony-forming units (CFU)/ml for bronchoalveolar lavage (BAL) and the cutoff was 103 CFU/ml for protected specimen brush (PSB) or protected (plugged) telescoping catheter (PTC); (2) nonprotected sample (endotracheal aspirate, ETA) with quantitative culture (105 CFU/ml); or (3) sputum bacteriology with quantitative culture (107 CFU/ml) [12].
Antimicrobial susceptibility testing (AST)
S. maltophilia identification characteristics (date of isolation and type of respiratory tract sampling) and antimicrobial susceptibility testing were independently performed by each microbiology laboratory. AST was performed on isolates using disk diffusion or automated testing methods according to guidelines and breakpoints established by the European Committee on Antimicrobial Susceptibility Testing (EUCAST) [13].
Data management
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Data were collected and managed using Research Electronic Data Capture (REDCap) software [14]. The database was approved by the institutional review board of the SFAR (IRB00010254-2015-010), which waived the need for signed informed consent of the participants, in accordance with the French legislation on noninterventional studies [15]. The study was declared on clinicaltrials.gov (NCT03506191). This manuscript was written in accordance with the STROBE statement for the reporting of observational studies in epidemiology.
Statistical analysis
The results are expressed as the number of patients (%) for categorical variables and mean (± standard deviation) or median [IQR] for continuous variables.
Prognostic factors associated with time to in-hospital death were studied using the Cox proportional hazard model. Time to in-hospital death was calculated from the diagnostic date of S. maltophilia to death. The follow-up was censored at discharge from the ICU and/or the hospital. Baseline prognostic factors were age, SAPS II, mechanical ventilation at diagnosis, VAP, duration of mechanical ventilation before the diagnosis, SOFA score at diagnosis, bacteremia, mono/polymicrobial pneumonia, use of empirical antimicrobial therapy, and use of empirical antimicrobial therapy effective against S. maltophilia. Other antimicrobial therapy-related variables were not defined as baseline and were thus entered in the model as time-dependent variables, including time elapsed between sample and effective antimicrobial therapy, use of effective combination antimicrobial therapy, and duration of effective antimicrobial therapy against S. maltophilia (monotherapy or combination therapy).
Baseline and time-dependent variables associated (p < 0.05) with outcome in the univariate analysis and that were present at the diagnosis were considered for the multivariate model, and the final model was selected using backward stepwise regression (p < 0.05). Hazard ratios (HR) were calculated accordingly with their 95% confidence intervals (CI).
We compared the time to in-hospital death between patients who received or not an empirical antimicrobial therapy effective against S. maltophilia using propensity score framework. The variables used for propensity score estimations were age, sex, SOFA score at diagnosis, SAPS II, and the ICU length of stay before pneumonia diagnosis. The two groups of patients were matched using a 1:1 nearest neighbor matching algorithm with replacement, using a caliper of 0.2 of the standard deviation of the propensity score on the logit scale [16]. Covariate balance between the two groups was assessed after matching, and we considered an absolute standardized difference (ASD) less than 0.1 as evidence of balance [17]. Then, time to in-hospital death was compared between matched groups using a Cox proportional hazard model. The 95% confidence intervals of the estimated hazard ratio (empirical antimicrobial therapy yes vs no) were estimated using robust standard error [18].
Significance was defined as p values < 0.05. Statistical tests were two-sided. Statistical analyses were performed using R 3.5.0 (R Foundation for Statistical Computing, http://www.R-project.org/, Vienna, Austria).
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