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Original Research: Critical Care |

A Prospective Evaluation of Ventilator-Associated Conditions and Infection-Related Ventilator-Associated ConditionsVentilator-Associated Conditions FREE TO VIEW

Anthony F. Boyer, MD; Noah Schoenberg, MD; Hilary Babcock, MD, MPH; Kathleen M. McMullen, MPH; Scott T. Micek, PharmD; Marin H. Kollef, MD, FCCP
Author and Funding Information

From the Division of Pulmonary and Critical Care Medicine (Drs Boyer, Schoenberg, and Kollef) and the Division of Infectious Diseases (Dr Babcock), Washington University School of Medicine; the Hospital Epidemiology and Infection Prevention Department (Ms McMullen), Barnes-Jewish Hospital; and St. Louis College of Pharmacy (Dr Micek), St. Louis, MO.

CORRESPONDENCE TO: Marin H. Kollef, MD, FCCP, Division of Pulmonary and Critical Care Medicine, Washington University School of Medicine, 660 S Euclid Ave, Campus Box 8052, St. Louis, MO 63110; e-mail: mkollef@dom.wustl.edu


FOR EDITORIAL COMMENT SEE PAGE 5

FUNDING/SUPPORT: The authors have reported to CHEST that no funding was received for this study.

Reproduction of this article is prohibited without written permission from the American College of Chest Physicians. See online for more details.


Chest. 2015;147(1):68-81. doi:10.1378/chest.14-0544
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BACKGROUND:  The Centers for Disease Control and Prevention has shifted policy away from using ventilator-associated pneumonia (VAP) and toward using ventilator-associated conditions (VACs) as a marker of ICU quality. To date, limited prospective data regarding the incidence of VAC among medical and surgical ICU patients, the ability of VAC criteria to capture patients with VAP, and the potential clinical preventability of VACs are available.

METHODS:  This study was a prospective 12-month cohort study (January 2013 to December 2013).

RESULTS:  We prospectively surveyed 1,209 patients ventilated for ≥ 2 calendar days. Sixty-seven VACs were identified (5.5%), of which 34 (50.7%) were classified as an infection-related VAC (IVAC) with corresponding rates of 7.0 and 3.6 per 1,000 ventilator days, respectively. The mortality rate of patients having a VAC was significantly greater than that of patients without a VAC (65.7% vs 14.4%, P < .001). The most common causes of VACs included IVACs (50.7%), ARDS (16.4%), pulmonary edema (14.9%), and atelectasis (9.0%). Among IVACs, 44.1% were probable VAP and 17.6% were possible VAP. Twenty-five VACs (37.3%) were adjudicated to represent potentially preventable events. Eighty-six episodes of VAP occurred in 84 patients (10.0 of 1,000 ventilator days) during the study period. The sensitivity of the VAC criteria for the detection of VAP was 25.9% (95% CI, 16.7%-34.5%).

CONCLUSIONS:  Although relatively uncommon, VACs are associated with greater mortality and morbidity when they occur. Most VACs represent nonpreventable events, and the VAC criteria capture a minority of VAP episodes.

Figures in this Article

Clinical criteria are known to be nonspecific for the diagnosis of ventilator-associated pneumonia (VAP).110 The Centers for Disease Control and Prevention (CDC)/National Healthcare Safety Network (NHSN) has established a surveillance definition for probable nosocomial pneumonia, including VAP.11 Unfortunately, these diagnostic criteria were not validated clinically.12 We previously compared the observed rates of VAP using the CDC/NHSN surveillance method with the CHEST criteria and found that the agreement between the two sets of criteria was poor.13 Others have also noted that US surveillance rates of VAP are decreasing compared with rates in Europe and Asia, whereas clinical diagnoses of VAP in the United States remain prevalent.14,15

Given that VAP surveillance is time consuming and potentially less accurate than clinical/microbiologic criteria and that the use of quantitative lower respiratory tract cultures for the establishment of VAP is not universal, the CDC/NHSN has recently supported efforts aimed at shifting ICU surveillance away from VAP. The CDC/NHSN has focused instead on the occurrence of ventilator-associated “conditions” (VACs) that may circumvent the subjectivity and inaccuracy of the VAP definition, facilitate electronic assessment, and make interfacility comparisons more meaningful.16 This policy shift toward using VACs as a more objective marker of ICU quality has occurred without robust prospective clinical validation for this purpose and served as the impetus for this study. The goals of this study were to prospectively determine the incidence of VACs among patients in medical and surgical ICUs, to assess the potential preventability of VACs, and to assess the ability of the VAC criteria to identify VAP.

Study Population and Data Collection

The study was conducted in the surgical (36 beds) and medical (29 beds) ICUs of Barnes-Jewish Hospital, a 1,250-bed teaching hospital in St. Louis, Missouri. During a 12-month period (January 2013 to January 2014), ICU patient rosters were screened daily. Patients who were mechanically ventilated for ≥ 2 calendar days were monitored daily for the development of either a VAC or an infection-related VAC (IVAC). The Washington University Human Research Protection Office approved the protocol (HRPO number 201209071). The following baseline characteristics were recorded at the time of VAC determination: age, sex, race, cause of respiratory failure, comorbid conditions, APACHE (Acute Physiology and Chronic Health Evaluation) II score17 at ICU admission, and cause of the VAC. Patients with a VAC were followed until hospital discharge or death. Additionally, a determination was made as to whether the VAC represented a potentially preventable event.

Definitions for VAC and IVAC

The definitions used for VAC and IVAC were taken from the recently published update from the CDC.16 To meet the VAC definition, a patient who was mechanically ventilated must have had at least 2 calendar days of stable or decreasing daily minimum positive end-expiratory pressure (PEEP) or Fio2 followed by at least 2 days of increased daily minimum PEEP or Fio2, in which the increase in the daily minimum PEEP is ≥ 3 cm H2O or the increase in the daily minimum Fio2 is ≥ 0.20 (or 20 percentage points in oxygen concentration). We modified the CDC VAC definition with clinical judgment based on ventilator mode, and in some cases mortality, in the 2-day window of VAC eligibility. We included potentially salvageable patients achieving the requirement of an increased daily minimum PEEP or Fio2, but expiring before the 2-calendar day requirement was met. We excluded patients who met the strict interpretation of the CDC VAC criteria but whose deterioration was clinically judged to be consistent with expected impending mortality from their underlying illness. Moreover, although only the Fio2 component of the CDC definition can be applied to patients receiving airway pressure release ventilation (APRV), we included those with a sustained increase in mean airway pressure of ≥ 3 cm H2O. IVACs represent the subset of VACs that are potentially infection related, as evidenced by an abnormal WBC count (≥ 12,000 cells/mm3 or ≤ 4,000 cells/mm3) or temperature (> 38°C or < 36°C) and a new antimicrobial start. IVACs were defined so as to be likely to capture patients with pulmonary and extrapulmonary infections of sufficient severity to trigger respiratory deterioration. The definitions used for possible and probable VAP were taken from the CDC update.16

VAP Definition

The CHEST definition for VAP includes a new or progressive consolidation on chest radiographs plus at least two of the following clinical criteria: fever > 38°C, leukocytosis or leukopenia, and purulent secretions.13 The presence or absence of a new or progressive radiographic infiltrate was based on the interpretation of the chest radiograph by board-certified radiologists who were blinded to the study. The diagnosis of VAP was considered to be microbiologically confirmed if either BAL or protected specimen brush cultures had significant growth using a semiquantitative culture technique (≥ 104 and ≥ 103 colony-forming units/mL, respectively).

Adjudication

For each case, two physician investigators (A. F. B., M. H. K., or N. S.) independently classified each VAC and IVAC as to its preventability. Rater disagreements were resolved by consensus. A preventable VAC was defined as an event resulting in injury to the patient caused by a nonintercepted medical error, either through an act of omission or commission, rather than the underlying illness.18 A nonpreventable VAC was defined as an unavoidable injury caused by the patient’s underlying disease process, associated with appropriate medical care. For example, a pneumothorax associated with central line placement in a patient with severe ARDS was considered preventable, whereas worsening oxygenation in a patient with intraabdominal sepsis despite adequate source control and appropriate antibiotic treatment was considered nonpreventable. Potentially preventable events screened for daily included inappropriate antibiotic therapy (ie, an antibiotic regimen not active against the causative pathogen based on in vitro testing); procedure-related adverse events (eg, pneumothorax, hemorrhage); aspiration of enteral feedings; ventilation with potentially injurious tidal volumes (> 6 mL/kg predicted body weight); pulmonary edema from excess IV fluid; effects of excess sedation (eg, atelectasis, aspiration, hypotension); and catheter-associated blood stream infection, wound infection, urinary catheter-associated infection, or probable VAP per CDC criteria.

Statistical Analysis

All comparisons were unpaired, and all tests of significance were two tailed. Continuous variables were compared using the Student t test for normally distributed variables and the Mann-Whitney U test for nonnormally distributed variables. The χ2 or Fisher exact tests were used to compare categorical variables. For all analyses, a two-tailed P value < .05 was considered statistically significant. Statistical analyses were performed using SPSS, version 11.0 for Windows (IBM).

Over 1 year, 1,209 patients met the inclusion criteria (Fig 1). Of these, 67 VACs were identified (5.5%), of which 34 (50.7%) were classified as an IVAC, with corresponding rates of 7.0 and 3.6 per 1,000 ventilator days, respectively. The baseline characteristics of the patients with VACs and IVACs are shown in Table 1. In addition to IVACs, other common causes of VACs included ARDS (16.4%), pulmonary edema (14.9%), and atelectasis (9.0%). Probable VAP was the most common cause of an IVAC (44.1%), followed by possible VAP (17.6%), and six IVACs without clinical or microbiologic confirmation (17.6%). Extrapulmonary infection or inflammation accounted for three IVACs (pancreatitis = 2, Clostridium difficile infection = 1). Three patients met the criteria for an IVAC; they were ultimately thought to have lung inflammation secondary to ARDS with negative cultures as the cause of fever and/or leukocytosis. The median day of mechanical ventilation during which a VAC occurred was 6.2 (SD, 4.3 days) (Fig 2). The mortality rate of patients having a VAC was significantly greater than that of patients without a VAC (65.7% vs 14.4%, P < .001). Similarly, the duration of mechanical ventilation was significantly longer for patients with a VAC than for patients without a VAC (14.7 ± 8.9 days vs 7.5 ± 6.3 days, P < .001).

Figure Jump LinkFigure 1 –  Analysis of patients with VACs and IVACs. Three VACs had more than one cause. *Other causes included untreated pneumonia, acute lung allograft rejection, malignant airway compression, and metastatic Hodgkin’s lymphoma; #three cases met the technical criteria for an IVAC, but the reason for worsening oxygenation was thought to be ARDS; @patients meeting IVAC criteria without a clear source of infection were identified despite having clinical, radiographic, and microbiologic evaluations performed. C. difficile = Clostridium difficile; CD = calendar day; IVAC = infection-related ventilator-associated condition; TACO = transfusion-associated circulatory overload; TRALI = transfusion-related acute lung injury; VAC = ventilator-associated condition; VAP = ventilator-associated pneumonia.Grahic Jump Location
Table Graphic Jump Location
TABLE 1 ]  Baseline Characteristics

Data are presented as No. (%) unless indicated otherwise. ALI = acute lung injury; APACHE = Acute Physiology and Chronic Health Evaluation; ILD = interstitial lung disease.

a 

Other causes include lymphangitic carcinomatosis, acute lung allograft rejection, metastatic Hodgkin’s lymphoma, hemothorax after thoracentesis, malignant airway compression, and anaphylaxis.

Figure Jump LinkFigure 2 –  Occurrence of VAC and IVAC relative to the start of mechanical ventilation. See Figure 1 legend for expansion of abbreviations.Grahic Jump Location

Twenty-five VACs (37.3%) were adjudicated to represent potentially preventable events. Table 2 lists the VACs and IVACs according to their preventability. The 15 cases of probable VAP were considered preventable and occurred despite investigator-documented adherence to the hospital’s VAP prevention bundle. The 10 additional potentially preventable events resulted from inappropriate antimicrobial coverage (2), insufficient PEEP (2), excessive administration of IV fluids (2), significant aspiration related to endotracheal intubation (2), esophageal perforation from nasogastric tube placement (1), and resuscitation for postoperative femoral artery bleeding (1). Among patients adjudicated to have a nonpreventable VAC, the most common causes were progressive ARDS (11), pulmonary edema in the setting of septic shock (8), and atelectasis despite appropriate ventilator settings (4).

Table Graphic Jump Location
TABLE 2 ]  Clinical Characteristics of Ventilator-Associated Events

AIP = acute interstitial pneumonia; ETA = endotracheal aspirate; IPF = idiopathic pulmonary fibrosis; IVAC = infection-related ventilator-associated complication; MAP = mean airway pressure; MDR = multidrug resistant; MSSA = methicillin sensitive Staphylococcus aureus; NA = not applicable; PEEP = positive end-expiratory pressure; TACO = transfusion-associated circulatory overload; TRALI = transfusion-related acute ling injury; VAC = ventilator-associated condition; VAP = ventilator-associated pneumonia.

a 

Patients meeting IVAC criteria without a clear source of infection identified despite having clinical, radiographic, and microbiologic evaluations performed.

We modified the CDC VAC definition with clinical judgment based on ventilator mode, and in some cases mortality, in the 2-day window of VAC eligibility. We included five potentially salvageable individuals who met the minimum PEEP or Fio2 thresholds but expired before meeting the 2-calendar day requirement and four individuals who had significant increases in mean airway pressure (≥ 3 cm H2O) while on APRV. Excluding these nine individuals resulted in corresponding rates of VAC and IVAC of 4.3 and 2.2 per 1,000 ventilator days, respectively. We also excluded 11 patients who met the surveillance criteria because of impending and expected mortality from their underlying condition and who died very early on calendar day 2. Including these 11 patients would have made our overall VAC rate 6.5% and mortality among VAC patients 70.5%.

Eighty-six episodes of microbiologically confirmed VAP occurred in 84 patients (10.0 of 1,000 ventilator days) during the study period. The sensitivity of VAC for detection of VAP was 25.9% (95% CI, 16.7%-34.5%).

We demonstrated that VACs and IVACs occurred in 5.5% and 2.8% of all medical and surgical patients requiring mechanical ventilation for 2 or more calendar days. Of all the VACs included, 37.3% were adjudicated to represent potentially preventable events, with the remaining VACs representing nonpreventable disease progression. The most common cause of a VAC was possible or probable VAP, and the most common preventable cause of a VAC was probable VAP. The VAC criteria identified a minority of patients with microbiologically confirmed VAP.

To the best of our knowledge, this study represents the first prospective surveillance study to evaluate the occurrence of VACs and IVACs and the clinical conditions captured, and to assess their potential preventability. Our results are consistent with those of retrospective studies demonstrating that the presence of VACs and IVACs is associated with greater hospital mortality. Muscedere et al19 recently evaluated 1,320 patients ventilated for > 48 h over four defined time periods. VACs developed in 10.5%, and IVACs developed in 4.9%. Patients who developed a VAC or an IVAC had significantly more ventilator days, hospital days, and antibiotic days, and greater hospital mortality. They also showed that increased concordance with VAP prevention guidelines during the defined time periods was associated with decreased VAP and VAC rates but no change in IVAC rates. An Australian study performed in a single hospital found the prevalence of VAC to be 28%, with hospital mortality being 20.3% in patients with VAC and 28.2% in those without VAC.20 Similarly, a retrospective US study of three hospitals found the VAC rate to be 23%, with an associated hospital mortality of 38%.21 A recent prospective electronic surveillance for VAC observed that detection of VAP was poor and that small differences in electronic implementation could considerably affect the incidence and mortality rates associated with VACs.22

Our results differ from these previous studies in that our results demonstrate a lower rate of VAC and greater hospital mortality. One explanation for this discrepancy is that we used the most recent CDC recommendation for defining VAC, as opposed to the retrospective studies, which used smaller changes in PEEP and Fio2.20,21 Additionally, our prospective evaluation allowed us to more accurately determine the presence of VAC according to the calendar day requirement. Interestingly, our VAC rate would have been even lower had we excluded the five patients who died prior to reaching the 2-calendar day requirement for PEEP or Fio2 deterioration and the four patients ventilated with APRV, but higher if we included patients whose ventilator changes were caused by their impending death (all 11 considered not preventable).

Our findings demonstrate that most VACs are nonpreventable events. However, the high mortality associated with VAC suggests that any and all opportunities to prevent these events when possible should be undertaken. Ahmed et al23 conducted a retrospective 10-year study to determine the association between specific hospital exposures and the rate of ARDS development among at-risk patients. These investigators evaluated patients who developed ARDS and, thus, presumably would have gone on to be classified as having a VAC. Several potentially preventable hospital exposures were markedly more common among patients developing ARDS, including inadequate antimicrobial therapy, medical and surgical adverse events, hospital-acquired aspiration, ventilation with potentially injurious tidal volumes, and greater volumes of blood product transfusion and fluid administration. Our investigation also suggests that many events can contribute to the development of worsening respiratory failure. These represent events of both omission and commission, rather than simply deterioration of the underlying illness, and thus may be potentially preventable. Like VAP, it is likely that some type of prevention bundle24,25 or prevention protocol26,27 will have to be developed and tested to see if VAC rates can be reduced with concomitant improvement in patient outcomes.

Several limitations of our study should be noted. First, our findings may not be generalizable. This would be especially true for ICUs caring for patients with less disease acuity. Moreover, our data reflect the practices within the ICUs of Barnes-Jewish Hospital and may not apply to hospitals using different ICU staffing models. Second, we used clinical and microbiologic criteria to define the occurrence of VAP, which may have resulted in an underestimation of the number of cases of VAP, because we did not include patients diagnosed with endotracheal cultures. Third, possible VAP was classified as a potentially preventable infection despite the use of a VAP prevention bundle.24 Although we assessed compliance with this bundle, it is possible that a more comprehensive bundle could have reduced the occurrence of VAP.25 Moreover, not all cases of VAP are preventable, as demonstrated by various investigations.24,25 Had we not classified probable VAP as a preventable event, our rate of potentially preventable VACs would have been only 14.9%.

Another limitation of our study is that we included nine cases of VAC that did not strictly meet the CDC/NHSN criteria. These nine cases were assessed to represent obvious respiratory deterioration despite either dying prior to the 2-calendar day requirement or being managed with APRV. Additionally, we excluded 11 patients who met the strict interpretation of the CDC VAC criteria but whose deterioration was clinically judged to be consistent with expected impending mortality from their underlying illness. Inclusion of these patients would have increased the overall rate of VACs observed. Finally, we did not define risk factors for VAC. Future studies should aim at identifying such risk factors to target interventions for their prevention. Our data suggest that the heterogeneity of VAC will limit any single intervention program, unless it targets the most common causes of VAC. This may also explain why the improved adherence to the VAP prevention program in the Canadian experience did not reduce rates of IVACs over time.19

In conclusion, although relatively uncommon, VAC is associated with greater mortality and morbidity when it occurs. Most VACs represent nonpreventable events and identify a minority of VAP episodes. Our data suggest that more study of the VAC criteria is needed before they can be routinely implemented as a comparative tool to assess the medical care provided in the ICU setting.

Author contributions: M. H. K. is the guarantor of the content of the manuscript, including the data and analysis. A. F. B., H. B., S. T. M., and M. H. K. contributed to the study concept and design; N. S., H. B., K. M. M., and S. T. M. contributed to the acquisition of the data; A. F. B., H. B., S. T. M., and M. H. K. contributed to the analysis and interpretation of the data; A. F. B., N. S., H. B, K. M. M., S. T. M., and M. H. K. contributed to the drafting and revision of the manuscript and approval of the final version to be published.

Financial/nonfinancial disclosures: The authors have reported to CHEST the following conflicts of interest: Dr Kollef’s effort was supported by the Barnes-Jewish Hospital Foundation. Drs Boyer, Schoenberg, Babcock, and Micek and Ms McMullen have reported that no potential conflicts of interest exist with any companies/organizations whose products or services may be discussed in this article.

APRV

airway pressure release ventilation

CDC

Centers for Disease Control and Prevention

IVAC

infection-related ventilator-associated condition

NHSN

National Healthcare Safety Network

PEEP

positive end-expiratory pressure

VAC

ventilator-associated condition

VAP

ventilator-associated pneumonia

Andrews CP, Coalson JJ, Smith JD, Johanson WG Jr. Diagnosis of nosocomial bacterial pneumonia in acute, diffuse lung injury. Chest. 1981;80(3):254-258. [CrossRef] [PubMed]
 
Kirtland SH, Corley DE, Winterbauer RH, et al. The diagnosis of ventilator-associated pneumonia: a comparison of histologic, microbiologic, and clinical criteria. Chest. 1997;112(2):445-457. [CrossRef] [PubMed]
 
Papazian L, Thomas P, Garbe L, et al. Bronchoscopic or blind sampling techniques for the diagnosis of ventilator-associated pneumonia. Am J Respir Crit Care Med. 1995;152(6 pt 1):1982-1991. [CrossRef] [PubMed]
 
Wunderink RG, Woldenberg LS, Zeiss J, Day CM, Ciemins J, Lacher DA. The radiologic diagnosis of autopsy-proven ventilator-associated pneumonia. Chest. 1992;101(2):458-463. [CrossRef] [PubMed]
 
Fàbregas N, Ewig S, Torres A, et al. Clinical diagnosis of ventilator associated pneumonia revisited: comparative validation using immediate post-mortem lung biopsies. Thorax. 1999;54(10):867-873. [CrossRef] [PubMed]
 
Koenig SM, Truwit JD. Ventilator-associated pneumonia: diagnosis, treatment, and prevention. Clin Microbiol Rev. 2006;19(4):637-657. [CrossRef] [PubMed]
 
Marquette CH, Copin MC, Wallet F, et al. Diagnostic tests for pneumonia in ventilated patients: prospective evaluation of diagnostic accuracy using histology as a diagnostic gold standard. Am J Respir Crit Care Med. 1995;151(6):1878-1888. [CrossRef] [PubMed]
 
Tejerina E, Esteban A, Fernández-Segoviano P, et al. Accuracy of clinical definitions of ventilator-associated pneumonia: comparison with autopsy findings. J Crit Care. 2010;25(1):62-68. [CrossRef] [PubMed]
 
Torres A, el-Ebiary M, Padró L, et al. Validation of different techniques for the diagnosis of ventilator-associated pneumonia. Comparison with immediate postmortem pulmonary biopsy. Am J Respir Crit Care Med. 1994;149(2 pt 1):324-331. [CrossRef] [PubMed]
 
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Ahmed AH, Litell JM, Malinchoc M, et al. The role of potentially preventable hospital exposures in the development of acute respiratory distress syndrome: a population-based study. Crit Care Med. 2014;42(1):31-39. [CrossRef] [PubMed]
 
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Figures

Figure Jump LinkFigure 1 –  Analysis of patients with VACs and IVACs. Three VACs had more than one cause. *Other causes included untreated pneumonia, acute lung allograft rejection, malignant airway compression, and metastatic Hodgkin’s lymphoma; #three cases met the technical criteria for an IVAC, but the reason for worsening oxygenation was thought to be ARDS; @patients meeting IVAC criteria without a clear source of infection were identified despite having clinical, radiographic, and microbiologic evaluations performed. C. difficile = Clostridium difficile; CD = calendar day; IVAC = infection-related ventilator-associated condition; TACO = transfusion-associated circulatory overload; TRALI = transfusion-related acute lung injury; VAC = ventilator-associated condition; VAP = ventilator-associated pneumonia.Grahic Jump Location
Figure Jump LinkFigure 2 –  Occurrence of VAC and IVAC relative to the start of mechanical ventilation. See Figure 1 legend for expansion of abbreviations.Grahic Jump Location

Tables

Table Graphic Jump Location
TABLE 1 ]  Baseline Characteristics

Data are presented as No. (%) unless indicated otherwise. ALI = acute lung injury; APACHE = Acute Physiology and Chronic Health Evaluation; ILD = interstitial lung disease.

a 

Other causes include lymphangitic carcinomatosis, acute lung allograft rejection, metastatic Hodgkin’s lymphoma, hemothorax after thoracentesis, malignant airway compression, and anaphylaxis.

Table Graphic Jump Location
TABLE 2 ]  Clinical Characteristics of Ventilator-Associated Events

AIP = acute interstitial pneumonia; ETA = endotracheal aspirate; IPF = idiopathic pulmonary fibrosis; IVAC = infection-related ventilator-associated complication; MAP = mean airway pressure; MDR = multidrug resistant; MSSA = methicillin sensitive Staphylococcus aureus; NA = not applicable; PEEP = positive end-expiratory pressure; TACO = transfusion-associated circulatory overload; TRALI = transfusion-related acute ling injury; VAC = ventilator-associated condition; VAP = ventilator-associated pneumonia.

a 

Patients meeting IVAC criteria without a clear source of infection identified despite having clinical, radiographic, and microbiologic evaluations performed.

References

Andrews CP, Coalson JJ, Smith JD, Johanson WG Jr. Diagnosis of nosocomial bacterial pneumonia in acute, diffuse lung injury. Chest. 1981;80(3):254-258. [CrossRef] [PubMed]
 
Kirtland SH, Corley DE, Winterbauer RH, et al. The diagnosis of ventilator-associated pneumonia: a comparison of histologic, microbiologic, and clinical criteria. Chest. 1997;112(2):445-457. [CrossRef] [PubMed]
 
Papazian L, Thomas P, Garbe L, et al. Bronchoscopic or blind sampling techniques for the diagnosis of ventilator-associated pneumonia. Am J Respir Crit Care Med. 1995;152(6 pt 1):1982-1991. [CrossRef] [PubMed]
 
Wunderink RG, Woldenberg LS, Zeiss J, Day CM, Ciemins J, Lacher DA. The radiologic diagnosis of autopsy-proven ventilator-associated pneumonia. Chest. 1992;101(2):458-463. [CrossRef] [PubMed]
 
Fàbregas N, Ewig S, Torres A, et al. Clinical diagnosis of ventilator associated pneumonia revisited: comparative validation using immediate post-mortem lung biopsies. Thorax. 1999;54(10):867-873. [CrossRef] [PubMed]
 
Koenig SM, Truwit JD. Ventilator-associated pneumonia: diagnosis, treatment, and prevention. Clin Microbiol Rev. 2006;19(4):637-657. [CrossRef] [PubMed]
 
Marquette CH, Copin MC, Wallet F, et al. Diagnostic tests for pneumonia in ventilated patients: prospective evaluation of diagnostic accuracy using histology as a diagnostic gold standard. Am J Respir Crit Care Med. 1995;151(6):1878-1888. [CrossRef] [PubMed]
 
Tejerina E, Esteban A, Fernández-Segoviano P, et al. Accuracy of clinical definitions of ventilator-associated pneumonia: comparison with autopsy findings. J Crit Care. 2010;25(1):62-68. [CrossRef] [PubMed]
 
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