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Microbiological Testing and Outcome of Patients With Severe Community-Acquired Pneumonia^*

^* From the Critical Care Department (Drs. Rello, Bodi, and Diaz), Joan XXIII University Hospital, Tarragona; and Microbiology (Dr. Mariscal), Medicine (Dr. Navarro), Pulmonary (Dr. Gallego) and Critical (Dr. Valles) Departments, Hospital de Sabadell, Sabadell, Barcelona, Spain.

Correspondence to: Jordi Rello, MD, PhD, Critical Care Department, Joan XXIII University Hospital, Carrer Dr, Mallafre Guasch 4, 43007 Tarragona, Spain; e-mail: jrc{at}hjxxiii.scs.es

	Abstract

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Study objectives: The study documents the impact of microbiological investigations on therapeutic decisions and outcome in patients with severe community-acquired pneumonia (SCAP).

Design: Retrospective analysis of prospectively collected data.

Setting: ICUs in two teaching Spanish hospitals.

Patients: Two hundred four consecutive patients admitted to intensive care with SCAP.

Interventions: None.

Measurements and results: One hundred six patients required intubation, while 98 other patients did not (81 of these patients were managed with noninvasive mechanical ventilation). The microbiologic diagnosis was established in 57.3% of patients. The most common pathogens were Streptococcus pneumoniae, Legionella pneumophila, and Haemophilus influenzae. Pseudomonas (6.6.% vs 1.0%, p < 0.05) and Legionella (15.1% vs 7.1%, p < 0.05) were more frequently documented in intubated patients. Overall mortality was 23.5% (44.3% in intubated patients), with S pneumoniae (n = 7), Pseudomonas aeruginosa (n = 7), and L pneumophila (n = 5) being the most common lethal pathogens. Bacteriological investigation led to changes in antibiotic prescription in 41.6% of patients, including 11 patients (5%) in whom initial treatment was ineffective against the microbial isolates. The most frequent reason for changes was simplification of therapy in 65 episodes (31.8%).

Conclusions: We conclude that microbiological testing is fully justified in patients with SCAP, because identifying the causative agent and adjusting treatment both impact on patient outcome. Our findings suggest that intubated patients should be empirically treated for Pseudomonas and Legionella while awaiting bacteriology results.

Key Words: etiology • noninvasive ventilation • outcome • respiratory failure • severe community-acquired pneumonia

	Introduction

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Pneumonia, the leading cause of death from infection, has historically been classified into clinical and epidemiologic subgroups such as hospital-acquired pneumonia and community-acquired pneumonia (CAP).¹ This practice was called into question by Sapira and Cochran,² who suggested in a meta-analysis that adequate empirical syndromic treatment based solely on this classification was not possible. The American Thoracic Society reclassified the patients with CAP into four subgroups: outpatients with no comorbidities, outpatients with cardiopulmonary disease or other modifying factors, inpatients not admitted to the ICU, and ICU-admitted patients.³

The Infectious Disease Society of America guidelines agree with the American Thoracic Society recommendations, stating that patients with severe CAP (SCAP) form an etiologically differentiated subgroup that requires a specific therapeutic approach.⁴ However, the recommendations of both Societies on the role of the microbiology laboratory in the diagnosis of lower respiratory tract infections are controversial. The Infectious Disease Society of America guidelines suggest approaches including analysis of sputum by culture and Gram stain, culture of normally sterile specimens such as blood and pleural fluid, and serologic tests. However, no studies demonstrating the value of routine performance of these procedures have been published. Indeed, these procedures consume time and resources in the laboratory, and at least four different studies^{5 6 7 8} reported that routine microbiologic investigation of all adults admitted to the hospital with CAP has a minimal impact on care and is probably unnecessary.⁹

Respiratory failure develops and mechanical ventilation is required in 58 to 87% of patients with SCAP requiring admission to an ICU.^{3 4 10} Several studies have associated the need for conventional ventilatory support with high mortality, ranging from 22 to 54%.¹¹ The term noninvasive mechanical ventilation (NIV) describes the delivery of assisted mechanical ventilation without an artificial endotracheal tube. Several studies^{12 13 14 15} have reported a favorable response to the application of positive pressure via a facial or nasal mask to a variety of populations with respiratory failure. Benhamou et al¹⁵ found no difference in response (60% success) in patients with or without pneumonia. In a series of 27 patients with COPD and SCAP managed with NIV, Meduri et al¹⁶ reported improved gas exchange in 74% and avoidance of intubation in 59%. More recently, Confalonieri et al¹⁷ reported a significant reduction in the rate of endotracheal intubation and duration of ICU stay in patients administered NIV for SCAP.

The primary objective of this study is to describe the use of microbiological investigations in practice in patients admitted to the ICU for SCAP and to evaluate the impact on care of the results obtained. A secondary objective is to evaluate whether patients who underwent intubation had different etiologies compared with nonintubated patients, in an era of NIV.

	Materials and Methods

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Three investigators (J.R., M.B., J.V.) prospectively recorded in a previously designed database selected variables from all patients admitted consecutively for CAP to the ICU of the two participating hospitals in Spain, during the period from January 1, 1993, to January 1, 2000. Patients with a severe, chronic illness or disability in whom pneumonia was an expected terminal event (ie, patients with a lethal condition for which intensive care would be futile) were not considered for admission to the ICU. Patients were admitted to the ICU either because they were potential candidates for mechanical ventilation or because they were judged to be in an unstable condition requiring intensive medical or nursing care. Clinical evidence suggestive of varicella-zoster pneumonia or pneumonia caused by respiratory viruses were cause for exclusion. Also excluded were transplant recipients and patients with neutropenia associated with chemotherapy or hematologic malignancy. Empiric treatment was started immediately after hospital admission.

CAP was defined as an acute lower respiratory tract infection characterized by the following: (1) an acute pulmonary infiltrate evident on the chest radiographs and compatible with pneumonia, (2) confirmatory clinical examination, and (3) acquisition of the infection outside the confines of a hospital, chronic care facility, or nursing home. All patients were followed up during their ICU stay.

The following information was recorded using standardized methods: sex; age; smoking and alcohol habits; prior illnesses; underlying clinical characteristics; impairment of alertness; antibiotic regimen initially prescribed; chest radiographic features at ICU admission; and various laboratory values. Chest radiography and arterial blood gas determinations were performed on ICU admission and repeated daily. Mechanical ventilation requirements, complications during ICU admission, length of ICU stay, radiographic evolution of pneumonia, and patient outcome were also recorded.

Definitions
A patient was considered a smoker if he or she had smoked more than one pack per day within the last 10 years. Alcoholism was defined as consumption of > 80 g of alcoholic beverages per day within the same period. Immunosuppression was considered to be primary immunodeficiency or immunodeficiency secondary to radiation treatment, use of cytotoxic drugs or steroids, or AIDS. HIV testing was performed, after informed consent, in patients with an absolute lymphocyte count < 1,000/µL.

Urine output of < 20 mL/h or total urine output of < 80 mL in 4 h was considered to be due to renal failure, after other causes had been ruled out. Shock was defined as a systolic BP of < 90 mm Hg or the need for vasopressors for > 4 h, after standardized fluid replacement. Preexisting COPD was diagnosed with the same criteria as reported elsewhere.¹⁸ A decreased level of consciousness was defined by a Glasgow coma scale score < 11. Appropriate therapy was defined as the use of at least one antibiotic to which all isolates were susceptible in vitro (or were expected to be susceptible for Pneumocystis carinii or Legionella pneumophila)

Indications for Mechanical Ventilation
Medical management was similar for all patients. Oxygen administration was adjusted to achieve a level of arterial oxygen saturation by oximetry of > 90%. At ICU admission, an attempt was made to adjust both mask and respiratory settings to correct gas exchange impairment using NIV, before considering intubation. The initial ventilatory settings were continuous positive airway pressure of 0 cm H₂O and pressure support ventilation of 5 to 10 cm H₂O. The mask was held on the patient’s face until the patient was in full synchrony with the ventilator. Pressure support ventilation was then increased to obtain an exhaled tidal volume > 6 mL/kg, a respiratory rate < 30 breaths/min, the disappearance of accessory muscle activity, and patient comfort. The level of continuous positive airway pressure was then set at 2 cm H₂O and adjusted up to 8 cm H₂O to improve oxygenation if needed. Ventilatory settings were adjusted on the basis of continuous oximetry, and measurement of respiratory rate and arterial blood gases. We used four types of mechanical ventilators: Puritan Bennett 7200 (Puritan Bennett; Overland Park, KS), Servo 900C (Siemens Elema; Uppsala, Sweden), EVITA 2 (Drager; Lübeck, Germany) and EVITA 4 (Drager). However, a unique utilization standard was followed by all practitioners. Finally, all patients underwent continuous ECG and arterial oxygen saturation monitoring.

Patients who required intubation because of respiratory failure were classified into group 1. Other patients were classified into group 2. Criteria for intubation¹² included the following: one major criterion, or the persistence of two minor criteria after at least 1 h of treatment. Major criteria included the following: respiratory arrest, respiratory pause with loss of consciousness, severe hemodynamic instability (heart rate < 50 beats/min with loss of alertness, and/or systolic BP < 70 mm Hg), and psychomotor agitation making nursing care impossible and necessitating sedation. Minor criteria were a respiratory > 35 breaths/min and above the value of admission, PaO₂/fraction of inspired oxygen < 150, an increase in PaCO₂ > 20% from prior arterial blood gas measurement, and change in mental status attributable to respiratory impairment.

Microbiological Investigations
For all patients, blood samples for cultures and serologic studies were routinely collected at hospital admission. Blood samples for follow-up serologic studies were collected from most patients. Paired serum samples were tested for evidence of complement fixation antibody to influenza A and B viruses, parainfluenza virus, adenovirus, respiratory syncytial virus, Chlamydia species, Coxiella burnetii, and Mycoplasma pneumoniae. The indirect fluorescent antibody technique was used to test for L pneumophila serogroups. A urine enzyme-linked immunosorbent assay or immunochromatographic test (Binax NOW Legionella Urinary Antigen Test; Binax; Portland, ME) was used to identify L pneumophila serogroup 1 in patients with negative culture results. Protected-brush specimen and quantitative cultures were performed for patients who required mechanical ventilation, and BAL was obtained if immunocompromise was present. The fiberoptic bronchoscopic techniques used and laboratory processing of samples have been described in previous studies.¹⁹ A pleural effusion culture was performed in patients in which pleural effusion was documented. Bacterial identification and susceptibility testing were performed by standard methods.

An organism was considered to be the definitive etiologic agent⁵ only if it could be isolated from blood, pleural fluid, a protected specimen brush (cut-off point > 1,000 cfu/mL), or BAL (cut-off point > 10,000 cfu/mL). However, isolation of P carinii or culture of L pneumophila or Mycobacterium tuberculosis from any of the samples obtained was considered the basis of a definitive diagnosis. Other microorganism isolated from sputum were considered "probable" pathogens.⁵ Serologic tests revealing a fourfold increase in antibody levels were also considered to establish a definitive diagnosis. The urinary antigen test for Legionella was interpreted by the presence of visually detectable pink-to-purple colored lines in 15 min. Organisms were considered to be probable pathogens if they were grown in cultures of a tracheal aspirate obtained within 1 h of intubation.

Statistical Analysis
Descriptive analysis was performed. Means were compared using the Mann-Whitney test. Proportions were compared using the ² test with Yates correction or Fisher exact test when necessary. Confidence intervals (CIs) for proportions were obtained assuming binomial distribution. All p values and CIs are two-sided. All interval estimates are 95% CIs.

	Results

TOP Abstract Introduction Materials and Methods Results Discussion References

 
Two hundred ten consecutive adult patients (166 male and 44 female patients) admitted to the ICU for SCAP and acute respiratory failure were included in the study. Six patients had varicella-zoster pneumonia and were excluded from the study. One hundred six patients required endotracheal intubation, and 81 patients received noninvasive ventilation. Mean age was 61.1 ± 17.9 years (54% were > 65 years old). Median age was 60 years. The baseline characteristics of the two groups of patients were similar and are shown in detail in Table 1 . Only one patient had prior aspiration. Patients with COPD were distributed equally in both groups (47 intubated patients in group 1 and 38 nonintubated patients in group 2). HIV infection was present in 17 patients, and was unknown in 11 of them at ICU admission.

	Discussion

TOP Abstract Introduction Materials and Methods Results Discussion References

 
This is the first study to assess the direct impact of diagnostic testing on clinical outcomes in adult patients with CAP requiring admission to an ICU. Several previous reports^{6 7 8 9 20} have evaluated the impact of diagnostic testing in a population hospitalized in medical wards; they state that knowledge of the pathogen may not affect clinical outcome, concluding that routine microbiological investigation of all adults admitted to the hospital is unhelpful and is probably unnecessary. A recent report⁹ suggested that the yield of blood cultures was higher in patients with severe pneumonia. The result of microbiologic investigations in the clinical setting of critically ill patients led to a change in therapy in approximately 40% of cases (and in 75% of patients in whom the etiology was identified). Identification of the organism after the initial incorrect choice of empirical therapy and subsequent correction of treatment to cover the offending pathogen was followed by clinical resolution in 7 of 11 patients. In addition, performing microbiologic studies led to simplification of treatment in one third of patients, contributing to reducing antibiotic expense, potential side effects, and preventing antibiotic abuse. This observation was true for both intubated and nonintubated patients.

Our study provides evidences that cases of SCAP had a different prevalence of etiologies when intubated patients were compared with nonintubated patients. This observation may have implications on the initial prescription of antibiotics to intubated patients. Indeed, nearly half of the intubated patients died, a figure higher than that reported in most previous series of SCAP. This may be due to the systematic implementation of NIV in patients with acute respiratory failure. Pneumococcus was the most frequent cause of pneumonia in all groups. Interestingly, L pneumophila was significantly more frequent in group 1 and was lethal in 21.7% of cases. This confirms prior opinions^{21 22} that urinary testing for Legionella and empiric coverage should be applied to all adults with respiratory failure with no other likely etiology (ie, negative Gram stain), independently of the risk factors. More importantly, comparing the mortality rates of pathogens, P aeruginosa was fourth in the ranking of lethal pathogens between intubated patients (group 1). It was not predicted by the presence of comorbidities. This finding suggests that empiric therapy for intubated patients should be active against this pathogen because a delay in therapy is associated with increased mortality.²³ Seven of eight patients (specific mortality rate of 87.5%) with Pseudomonas pneumonia died, a finding that suggests the need for antipseudomonas agents in the empiric therapy of intubated patients with SCAP and unknown etiologies. No significant differences between the groups were observed when other pathogens were compared. In addition, this study confirms an earlier observation reported by our research team,²⁴ suggesting that M tuberculosis and P carinii should be considered promptly in patients with unknown etiologies. Although infrequent in the immunocompetent host, some HIV-positive patients were still unaware of the underlying infection at ICU hospitalization. Finally, in contrast to prior observations,¹⁰ elderly patients (age > 75 years) presented higher mortality. In addition, the length of stay for survivors was twice that of nonintubated patients.

Several limitations should be taken in account before generalizing our findings. First, the prevalence of certain etiologies (eg, L pneumophila) may be different in other geographic regions,²⁵ or may have changed over 7 years in the presence of outbreaks. Second, therapeutic options may be different in other countries with different rates of sensitivity, antimicrobials available (eg, we have IV clarithromycin, but not IV azithromycin), or differences in prescribing patterns (fluoroquinolones were prescribed to < 10% of patients). Third, the study lasted 7 years, and the approach to diagnosis was improved over the years of the study (eg, antigen detection tests were not available throughout the study period). This may have influenced the identification of etiology and thus may undervalue therapeutic simplification. Another weakness is the variable diagnostic approach for intubated patients: there is an obvious selection bias in that invasive diagnostic testing was primarily performed in patients who had endotracheal intubation. This means that the yield of microorganisms found on invasive testing would potentially be different. Because prevalence is always dependent on standardized systematic and comprehensive screening for any given problem, our estimates of microbiologic prevalence may be potentially inaccurate. Finally, the admission time to the ICU could be quite variable between patients, and this variability may have influence on the success of NIV.

In contrast, this study has several strengths: a large number of consecutive cases were enrolled at two hospitals, the epidemiologic approach, the complete follow-up, and the linking between microbiology and clinical outcome. Several modalities were used to pursue microbiological diagnoses. Finally, this is the first study to evaluate the impact of diagnostic testing on the outcome of SCAP.

In summary, our findings suggest that the severity of disease affects the diagnostic yield and the pathogens involved, in contrast to most previous reports in the setting of hospitalized patients with pneumonia outside the ICU. Our observations support the rationale of performing microbiological studies to establish an etiologic diagnosis in all patients requiring admission to the ICU. Finally, the group of patients who underwent intubation was exposed to a significant risk of infection by relatively infrequent but highly lethal pathogens, such as L pneumophila or P aeruginosa. Thus, these findings suggest that both pathogens should be covered (in addition to the pneumococcus, of course) in the empiric therapy of all intubated patients while awaiting bacteriology results.

	Acknowledgements

 
We thank Dr. Bernat Sanchez for technical assistance and Dr. Jordi Roig for critical review of the manuscript.

	Footnotes

 
Abbreviations: CAP = community-acquired pneumonia; CI = confidence interval; NIV = noninvasive ventilation; SCAP = severe community-acquired pneumonia

Supported in part by a grant from Comissió Interdepartmental de Recerca i Innovació Technològica (2001/128) and Distinció per la Promoció de la Recerca Universitaria.

Received for publication October 23, 2001. Accepted for publication May 21, 2002.

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This Article Abstract Full Text (PDF) Free Submit a response Alert me when this article is cited Alert me when eLetters are posted Alert me if a correction is posted Citation Map Services Email this article to a friend Similar articles in this journal Similar articles in ISI Web of Science Similar articles in PubMed Alert me to new issues of the journal Add to My Personal Article Archive Download to citation manager Citing Articles Citing Articles via HighWire Citing Articles via ISI Web of Science (33) Citing Articles via Google Scholar Google Scholar Articles by Rello, J. Articles by Valles, J. Search for Related Content PubMed PubMed Citation Articles by Rello, J. Articles by Valles, J.