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Direct E-Test (AB Biodisk) of Respiratory Samples Improves Antimicrobial Use in Ventilator-Associated Pneumonia

  1. Emilio Bouza1,
  2. María V. Torres1,
  3. Celina Radice1,
  4. Emilia Cercenado1,
  5. Roberto de Diego2,
  6. Carlos Carrillo-Sánchez-1, and
  7. Patricia Muñoz1
  1. 1Departments of Clinical Microbiology and Infectious Diseases, Madrid, Spain
  2. 2Anesthesia, Hospital General Universitario Gregorio Marañón, Universidad Complutense, Madrid, Spain
  1. Reprints or correspondence: Dr. Emilio Bouza, Servicio de Microbiología Clínica y Enfermedades Infecciosas, Hospital General Universitario Gregorio Marañón, Dr. Esquerdo 46, 28007, Madrid, Spain (ebouza{at}microb.net).

  1. Presented in part: 45th Interscience Conference on Antimicrobial Agents and Chemotherapy, Washington, D.C., December 2005 (abstract D-51).

 
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Abstract

Background. Ventilator-associated pneumonia is the most frequently observed nosocomial infection in intensive care units, and it is associated with high morbidity and mortality. Early microbiological diagnosis and the initial administration of appropriate antimicrobial therapy are associated with decreased mortality and potentially reduced costs. Our study evaluates the clinical and financial impact of performing rapid antimicrobial susceptibility tests directly on samples obtained from the lower respiratory tract.

Methods. A prospective, randomized study was performed over a 2-year period. Patients who had a lower respiratory tract infection that was acquired during mechanical ventilation and for whom samples obtained from the respiratory tract were sent for culture were randomized to 1 of 2 groups. Samples were cultured for the control group, and results were reported using standard procedures. Samples were also cultured for the test subject group using standard procedures, but in addition, a rapid antibiogram was immediately performed by placing E-test antibiotic strips (AB Biodisk) directly on respiratory tract samples. Patients in the E-test group received a preliminary laboratory report when it became available. The 2 patient groups were compared according to the following variables: type and severity of underlying conditions, total days of antimicrobial use, number of defined daily doses, cost of acquisition of the antimicrobial agent per episode, days of fever, days receiving mechanical ventilation, days in the intensive care unit, incidence of Clostridium difficile-associated diarrhea, and mortality.

Results. Reporting a rapid E-test was associated with fewer days of fever, fewer days of antibiotic administration until resolution of the episode of ventilator-associated pneumonia, decreased antibiotic consumption, less C. difficile-associated diarrhea, lower costs of antimicrobial agents, and fewer days receiving mechanical ventilation.

Conclusions. A rapid E-test of respiratory tract samples improves antimicrobial use in cases of ventilator-associated pneumonia.

Ventilator-associated pneumonia (VAP) is the most common intensive care unit (ICU)-acquired infection, and it has a mortality rate that ranges from 20% to 50% [1–3]. Early microbiological diagnosis and the administration of appropriate initial antibiotic therapy have proven to be associated with decreased rates of mortality [4–10].

Results of conventional microbiological reports based on full bacterial identification and standard antimicrobial susceptibility tests rarely reach physicians who are attending to patients with VAP within 48–72 h of lower respiratory tract (LRT) sampling. The E-test (AB Biodisk) is a well-known antimicrobial susceptibility test that uses antimicrobial agent-inoculated strips and is inoculum size-independent. The test strips can be used on isolated bacteria or applied directly to clinical samples [11, 12].

Our study evaluates the clinical and economic impact of performing a rapid E-test with 6 key antimicrobial agents by applying the test strips directly to LRT samples and reporting the results. We also examine antimicrobial use and the outcome of patients with VAP in a large teaching institution.

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Materials And Methods

The ethics committee of Hospital General Universitario Gregorio Marañón (Madrid, Spain) approved the study protocol. Our institution is a general reference hospital with a catchment population of 714,000 inhabitants and 1750 beds. It has 3 different ICUs—a medical ICU, a resuscitation service, and a cardiac surgery ICU—with a total of 42 beds. A prospective, randomized study was performed among adults who were admitted to 1 of these ICUs during the period December 2003–December 2005.

Study population.Patients who had a suspected LRT infection that was acquired during mechanical ventilation were preselected for the study if ⩾1 microorganism was observed by a Gram stain of a sample of the first tracheal aspirate that was obtained (i.e., the LRT sample collected when VAP was first suspected). The result of the LRT sample stain was immediately reported by telephone to the attending physicians. Patients were randomized at a ratio of 1 : 2 using the computer program C4 Study Design Pack: Group of Programs for Experiments Development, version 1.1 (GlaxoSmithKline) to receive either a conventional microbiological examination with reporting (control group), or to receive an additional rapid antimicrobial susceptibility E-test (E-test group). All samples obtained from patients with suspected LRT infections (control group and E-test group) were also cultured, and results were reported according to standard procedures. 1 is a schematic representation of our study.

Figure 1
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Figure 1

Schematic representation of our study. The first sample of the episode is a lower respiratory tract (LRT) secretion sample that was collected when ventilator-associated pneumonia (VAP) was first suspected. Follow-up samples are the consecutive samples collected after the LRT secretion sample was collected when VAP was first suspected.

Samples for microbiological diagnosis were obtained by endotracheal aspiration using a 14F sterile probe to a depth of 2 cm from the distal end of the endotracheal tube. The secretions that were obtained were collected in a sterile container (Argyle Lukens Specimen Container; Sherwood Medical) and were transported in sterile packaging to the microbiology laboratory. Standard microbiological procedures included quantitative culturing of a calibrated loop of 0.0025 mL of aspirate in blood agar, chocolate agar, and McConkey agar, and, when required, Legionella agar (blood charcoal yeast extract) [13, 14]. Identification of the microorganisms and antimicrobial susceptibility testing were performed using an automatic system (MicroScan; Dade Behring). Breakpoints were determined in accordance with the Clinical and Laboratory Standards Institute guidelines [15]. Definitive results were reported to the ICU when bacterial identification and antimicrobial susceptibility test results became available.

E-test.The rapid test consisted of an antibiogram that was performed by directly applying E-test strips to 150-mm Mueller-Hinton agar plates that were seeded with LRT secretion samples. The antibiotic strips tested contained oxacillin, piperacillin-tazobactam, cefepime, imipenem, ciprofloxacin, and amikacin. Plates were incubated at 35°–37°C for analysis the following day with transmitted light. The results were evaluated as drug-resistant or drug-susceptible in accordance with the Clinical and Laboratory Standards Institute guidelines [15]. This information was then immediately provided as a preliminary report for the patient's chart, usually within 24 h, without further intervention.

VAP definition.VAP was defined as having a Centers for Disease Control and Prevention [16] and/or a Clinical Pulmonary Infection Score ⩾6 [17] when ⩾1 significant microorganism was isolated by quantitative culturing (>10,000 colony-forming units (cfus) per mL).

Variables recorded included.Age, sex, unit of admission, classification of the severity of the underlying condition according to McCabe/Jackson criteria [18], Charlson comorbidity score [19], prior surgery before the episode of VAP during the present admission, number of antibiotics administered to patients before VAP, previous VAP during the present admission, APACHE II score on admission to the ICU [20], bone score for severity of sepsis [21], microbiological isolates, existence of a concomitant infection, Clostridium difficile-associated diarrhea, mortality of the episode, mortality in the ICU and mortality on discharge, days of antibiotherapy per episode, days of adequate therapy (i.e., duration that the antimicrobial covered microorganism sensitivities), defined daily doses (DDDs) received during the episode, DDDs of adequate therapy (DDDs of an antimicrobial that covered microorganism sensitivities), cost (in €) of the acquisition of antibiotics administered during the episode, days of fever (duration of time that underarm temperature was >38.5°C), days receiving mechanical ventilation, and duration of stay in the ICU.

Statistical analysis.Relationships between baseline variables were evaluated for the randomized groups. Qualitative variables appear with their frequency distribution. Quantitative variables are summarized as mean ± SD or as median (interquartile range). Relationships between variables were evaluated using the χ2 test for categorical variables, and the Student's t test for normally distributed continuous variables. The level of significance was set at P < .05 for all tests. The statistical analysis was performed using SPSS software, version 12.0 (SPSS).

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Results

During the study period (December 2003–December 2005), 4829 patients were admitted to the adult ICUs at our institution. We collected a total of 2779 LRT samples from 1220 patients. Microorganisms were observed by Gram staining in 387 samples sent to the laboratory that were obtained from patients who had suspected LRT infection. The resulting data from gram staining were transmitted to ICU staff via telephone within a median of 111 min ± 73 min (range, 8 min–6 h).

Of the 387 episodes of suspected LRT infection, 250 patients fulfilled the diagnostic criteria of VAP. We excluded the following from the study: 55 episodes of ventilator-associated tracheobronchitis, 39 episodes of severe pneumonia not caused by mechanical ventilation, and 43 cases of mere colonization. Of the 250 patients with bacteriologically confirmed VAP, 167 were enrolled in the E-test group and 83 were enrolled in the control group. These cases constituted the basis of our report.

table 1 summarizes the characteristics of the patients with VAP in the E-test group and in the control group. Univariate analysis did not reveal any differences in the underlying characteristics of the patients in either group. The population included 182 men and 68 women with a mean age of 58.9 ± 17 years. Underlying disease was moderately fatal or rapidly fatal in 37.6% of the patients, and the mean Charlson comorbidity score was 3.43 ± 2.5. Previous surgery was the reason for admission to the ICU for 148 patients (59.2%). The mean APACHE II score on admission to the ICU was 11.6 ± 4.3, and 138 (55.2%) of the cases of VAP were accompanied by a concomitant infection. Regarding the severity of sepsis in patients with VAP, 62 (24.8%) experienced septic shock or multiple organ failure. Previous episodes of VAP had occurred in 18% of the patients, and the mean consumption of antibiotics before diagnosis was 1.8 ± 2 per episode. Globally, 69.6% of cases of VAP were monomicrobial and 30.4% were polymicrobial. The most frequently isolated microorganisms are summarized in table 2. Staphylococcus aureus and Pseudomonas aeruginosa were the most frequent causal agents (42% and 28.4%, respectively).

Table 1
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Table 1

Clinical and demographic characteristics of patients with ventilator-associated pneumonia (VAP).

Table 2
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Table 2

Microorganisms isolated from 250 patients suspected of having ventilator-associated pneumonia (VAP).

All microorganisms and their antimicrobial susceptibilities were ultimately identified using standard methods, and definitive reports were issued a mean of 4.2 days after samples were obtained. The preliminary E-test information regarding antimicrobial susceptibility was included in the patient's chart within a mean of 1.4 ± 0.75 days (range, 1–4 days). Susceptibility results obtained using direct sampling were available within 24 h of receipt of the sample in 75.4% of cases of VAP.

Antimicrobial susceptibility, as determined by E-test, was tested and compared with the results of standard testing methods in 201 microorganisms and 704 antibiotics. In 679 antibiotics (96.44%), there was a good correlation between both methods. Fourteen major errors (1.98%; defined as isolates that were determined to be susceptible by E-test and resistant by the standard method) occurred, and 11 minor errors (1.56%; defined as isolates that were determined to be resistant by E-test and susceptible by the standard method) occurred. These errors involved P. aeruginosa (11 major errors and 10 minor errors), S. aureus (2 major errors), and Acinetobacter baumannii (1 major error and 1 minor error). With regard to major errors, preliminary information provided by the rapid E-test led to an inadequate therapeutic decision in only 5 patients. No attributable mortality could be assigned to VAP.

Initial empirical therapy followed the guidelines for the management of adults with VAP by the American Thoracic Society for all patients [22]. The clinical, therapeutic, and outcome parameters of patients with VAP (E-test group vs. control group) are presented in table 3. Patients from the E-test group had fewer days of fever per episode (4.61 vs. 7.84 days), required fewer days of antibiotic administration to resolve the VAP episode (15.72 vs. 18.92 days), consumed fewer antibiotics (i.e., received fewer DDDs; 31.43 vs. 42.72 doses) and experienced less C. difficile-associated diarrhea (1.8% vs. 9.6%). Furthermore, the early availability of microbiological information led to an improvement in the adequacy of antibiotic therapy. Overall, the E-test group and the control group differed in the percentage of days of adequate therapy (95% vs. 76%) and in the percentage of adequate DDD's prescribed (91% vs. 68%). The cost of the antimicrobial agents prescribed per episode in the E-test group and control group were, respectively, €666 and €984. This does not include administration costs. All parameters had a P value of <.05.

Table 3
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Table 3

Outcome of 250 episodes of ventilator-associated pneumonia (VAP).

Finally, we observed a decrease in time receiving mechanical ventilation from the diagnosis of VAP in the E-test group versus the control group (8 days vs. 12 days; P < .05). Trends towards a shorter total ICU stay (23 days vs. 27 days), fewer overall days receiving mechanical ventilation (17 days vs. 19 days), and a shorter stay in the ICU after diagnosis of VAP (13 days vs. 17 days) were observed, but did not reach statistical significance.

We were unable to show statistically significant differences in the rate of mortality of the episode (32% vs. 29%; P = .7), the rate of mortality in the ICU (46% vs. 40%; P = .3), and the rate of mortality at discharge from the hospital (55% vs. 52%; P = .7).

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Discussion

Preliminary information regarding antimicrobial susceptibility can be provided by the microbiology laboratory for patients with VAP. An early report based on the results obtained by directly applying 6 E-test strips to plated LRT secretion samples is associated with better antibiotic use, less antimicrobial misuse, and a decrease in antimicrobial-related adverse events.

VAP is one of the most common infections acquired by patients in the ICU. It is associated with high morbidity and mortality and considerable economic loss. [3–25]. Early optimal antimicrobial therapy is an essential part of the successful management of VAP, because inadequate initial therapy is consistently associated with increased mortality [26–29].

Standard bacterial isolation, followed by identification and antimicrobial testing, usually takes no fewer than 2–3 days in the microbiology laboratory. This can often lead to inadequate empirical therapy, misuse of antibiotics, or both. Antimicrobial misuse has been associated with higher rates of mortality in the ICU [4–33]. The E-test employs a strip impregnated with an increasing concentration of an antibiotic that is usually placed on purified bacterial cultures, thereby allowing for the MIC of different antimicrobial agents to be determined. The fact that the E-test does not depend on inoculum size makes it ideal for the direct application of these strips to clinical secretion samples in which no standard inoculum size is used [34–36]. Determining a direct antibiogram directly from a sample, without waiting for bacterial isolation, may provide preliminary information that has a very good correlation with standard procedures. This procedure has been performed with culture samples of blood, urine, and CSF when information is urgently required [37, 38]. A preliminary report from our group also revealed a very good correlation between the results obtained from the antimicrobial susceptibility test performed with 6 selected antibiotics directly applied to LRT secretion samples and the results obtained with isolated bacteria and using conventional methods [11].

However, this test presents some limitations. Interpretation of the results in polymicrobial cases is more difficult and requires a certain degree of expertise. The selection of the 6 antimicrobial agents in our study took into account the most frequently observed microorganisms that cause VAP in our institution (i.e., methicillin-resistant S. aureus, P. aeruginosa and enteric bacteria) and the most commonly used antimicrobial agents in our ICUs. We based our selection of patients on Gram stain results, because in our experience, the value of Gram staining for screening of significant quantitative LRT culture in the samples collected when VAP is first suspected is 90% [39].

With our study, we attempted to assess the clinical impact of sending the E-test results to our ICU clinicians with no further intervention. Patients who were managed according to the results of a preliminary antimicrobial susceptibility E-test experienced fewer days of fever per episode, received fewer days of antibiotic administration to resolve the VAP episode, had decreased antibiotic consumption (fewer DDD's), less C. difficile-associated diarrhea, and lower costs of antimicrobial agents, and spent fewer days receiving mechanical ventilation after receiving the diagnosis of VAP. We were able to demonstrate a considerable decrease in antimicrobial misuse, as well as important cost savings. The estimated cost for the test is ∼ €25, including personnel costs. Because we saved €318 on antibiotics per episode, we believe that the test is clearly economically viable. Performance of the E-test is very simple and is within the reach of any microbiology laboratory. Rapid, although possibly imprecise, information from the microbiology laboratory may be of greater value than delayed and more precise information.

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Acknowledgments

We thank the staff of the microbiology laboratory, for their contribution to the study; Cristina Fernandez, for the statistical design; and Thomas O'Boyle, for his revision of English version of the manuscript.

Financial support.Red Española de Investigación en Patología Infecciosas (REIPI) and Fondo de Investigación Sanitaria (FIS). The Spanish Ministry of Health (BEFI BF03/00237, to M.V.T.).

Potential conflict of interest.All authors: no conflicts.

  • Received June 28, 2006.
  • Accepted October 19, 2006.
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  1. Clin Infect Dis. (2007) 44 (3): 382-387. doi: 10.1086/510587
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