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* From the Emergency (Drs. Pereira Gomes, Soriano, and Velasco), Bronchoscopy (Drs. Pedreira and Negri), and Pathology (Drs. Araújo and Antonângelo) Departments, Hospital das Clínicas da Faculdade de Medicina, University of São Paulo Medical School, São Paulo, Brazil.
Correspondence to: João Carlos Pereira Gomes, MD, Emergency Department, Hospital das Clínicas da Faculdade de Medicina, University of São Paulo, Av. Dr. Enéas de Carvalho Aguiar, 255–5° and s. 5023, 05403–010 São Paulo (SP), Brazil; e-mail: jcpgomes{at}uol.com.br
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Abstract |
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Study objective: To evaluate in ICU patients the impact of BAL in the etiologic diagnosis, treatment, and outcome of pneumonia with treatment failure.
Design: Prospective clinical study.
Setting: Nonsurgical, medical ICU of a university hospital in Brazil.
Patients and participants: Sixty-two episodes of pneumonia treated for at least 72 h without clinical improvement in 53 patients hospitalized for diverse clinical emergencies. Mean duration of hospitalization was 14.2 days. Mean duration of previous antibiotic therapy was 11.4 days.
Interventions: Bronchoscopy and BAL were performed in each episode. BAL fluid was cultivated for aerobic and anaerobic bacteria; the cutoff considered positive was 104 cfu/mL; 103 cfu/mL was also analyzed if under treatment. Pneumocystis carinii, fungi, Legionella spp, and Mycobacterium spp were also researched.
Measurements and results: Fifty-eight of 62 BAL were performed under antibiotics. The results showed positivity in 45 of 62 (72.6%); 42 of the 45 positive episodes (93.3%) had > 104 cfu/mL. The three cases with between 103 and 104 cfu/mL were considered positive and were treated according to BAL cultures. The main agents were Acinetobacter baumannii (37.1%), Pseudomonas aeruginosa (17.7%), and methicillin-resistant Staphylococcus aureus (MRSA; 16.1%); 46.7% of the episodes (21 of 45) were polymicrobial. BAL results directed a change of therapy in 34 episodes (54.8%). Overall mortality was 43.5%. There was no difference in mortality among positives, negatives, and patients who changed therapy guided by BAL culture.
Conclusions: (1) BAL fluid examination was positive in 45 of 62 episodes (72.6%), with 58 of 62 BAL performed under antibiotics. This suggests that BAL may be a sensitive diagnostic method for treatment failures of clinically diagnosed pneumonias, even if performed under antibiotics; (2) the main pathogens in our study were A baumannii, P aeruginosa, and MRSA, and approximately 45% of infections were polymicrobial; (3) BAL culture results directed a change of therapy in 75.6% of positive episodes (34 of 45) and in 54.8% of all episodes of treatment failure (34 of 62); and (4) there was no difference in mortality among positives, negatives, and patients who changed therapy guided by BAL culture.
Key Words: BAL • diagnosis • etiology • ICU • management • pneumonia • treatment failure
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Introduction |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsReferences |
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United States, pneumonia is the sixth-ranking causa mortis, and its treatment generates an estimated annual cost of $23 billion.8 More than 50% of antibiotics in ICUs are prescribed for presumed pulmonary infections.9 10
Etiologic diagnosis of pneumonia remains a challenge. Even in services of excellence, a considerable proportion (40 to 60%) of community-acquired (CAP), nosocomial, and ventilator-associated pneumonias (VAP) persist without defined causes.3 4 5 6 7 The advent of bronchoscopy and quantitative invasive methods such as BAL and protected specimen brush (PSB) have improved sensitivity and specificity in the diagnostic investigation of diffuse pneumonia in immunosuppressed patients, VAP, severe CAP, and pneumonia of difficult resolution.11
Treatment failure, ie, absence of improvement or clinical deterioration during antibiotic therapy, presents a dilemma to physicians.1 12 Thus, our study objective was to evaluate in ICU patients the impact of BAL in the etiologic diagnosis, treatment, and outcome of pneumonia with treatment failure. The setting was a 10-bed nonsurgical, medical ICU of a university hospital in Brazil.
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Materials and Methods |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsReferences |
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72 h
without clinical improvement. They were admitted for different clinical
emergencies to the ICU of the Emergency Department at Hospital das
Clínicas, São Paulo University Medical School, Brazil,
between June 1996 and January 1999. All patients had been hospitalized
for > 72 h at the time BAL was performed. Antimicrobial therapy
decisions and BAL requests were made by the ICU on-duty physicians.
This study was approved by the Hospital’s Ethics Committee for
Research Analysis.
Inclusion Criteria
Clinical diagnosis of pneumonia (new radiographic
infiltrate and two of the three following criteria: fever [temperature
38.0°C] or hypothermia [temperature < 35.0°C[rqb],
purulent bronchial secretion, and WBCs
> 10,000/mm3 or
< 3,000/mm3).
Treatment failure (clinical deterioration or absence of clinical improvement after 72 h of treatment, entailing worsening or persistent fever or hypothermia, purulent secretion, leukocytosis or leukopenia, and worsening of pulmonary infiltrates or of respiratory function measured by gasometric variables such as PO2/fraction of inspired oxygen).
Exclusion Criteria
Contraindications to bronchoscopy include the following: (1)
PO2 < 75 mm Hg even with an
inspired oxygen fraction of 100%; (2) acute cardiac arrhythmia; and
(3) bronchospasm.
Procedure and Specimen Collection
Patients were usually sedated with IV midazolam before
bronchoscopic procedure. The fraction of inspired oxygen was increased
to 100%, and positive end-expiratory pressure was limited to 8 cm
H2O. The bronchoscope used was the Pentax
FB15X (Pentax Instruments, Tokyo, Japan). BAL was performed by
wedging the bronchoscope in the subsegmental bronchus of the most
compromised lobe seen in chest radiography or, in cases of diffuse
radiologic presentation, in the posterior bronchus of the lower lobe.
As little topical lidocaine as possible was used so as not to interfere
with bacterial growth (never > 20 mg per bronchus). Aspiration of
secretions by the bronchoscope was avoided. Three aliquots were
separately instilled and retrieved. A first aliquot of 20 mL of
distilled water was instilled, gently aspirated with a syringe, and
sampled for Legionella culture and direct immunofluorescence. Two 60-mL
aliquots of sterile saline solution were then separately instilled and
aspirated, pooled, and sent for microbiologic analysis.
Microbiology of BAL Fluid
Retrieved BAL fluid was processed for the following: (1) aerobic
and anaerobic bacteria quantitative culture using sheep blood agar,
MacConkey’s agar, and chocolate agar; (2) microscopic examination by
Gram’s and Ziehl-Neelsen stains and by potassium hydroxide (mycologic
examination); (3) direct examination for Pneumocystis
carinii by toluidine blue stain; (4) direct immunofluorescence for
Legionella pneumophila; (5) cytologic study; (6) fungi
culture (Sabouraud agar and Mycosel agar); (7) mycobacterial culture
(Lowenstein-Jensen agar and Bactec 460); and (8) Legionella spp culture
(buffered charcoal-yeast extract medium). Bacterial
identification and susceptibility tests (Kirby Bauer disk-diffusion
method) were performed by standard methods.
Etiologic Diagnosis
The following were considered etiologic agents of pneumonia: (1)
bacteria with > 104 cfu/mL in BAL quantitative
culture (according to clinical judgment, > 103
cfu/mL was considered positive); and (2) demonstration by direct
microscopic examination of BAL fluid or specific culture of the
following infectious agents: Legionella spp, mycobacteria, P
carinii, systemic fungi, and parasites.
Statistical Analysis
The 
2 test and Fisher’s Exact Test
were used to test BAL results from the first episode of each patient. A
value of p < 0.05 was considered significant.
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Results |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsReferences |
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The main reasons for admission to ICU were as follows: neurologic emergencies in 17 patients (32.1%); respiratory failure in 14 (26.4%); cardiocirculatory emergencies in 10 (18.9%); septic shock in 2; other infections in 4; hematologic diseases in 3; renal failure in 2; diabetes in 1; and acute abdomen in 1. Fifty-eight of 62 BALs (93.5%) were performed under antibiotics; the other 4 were performed 24 to 72 h after suspension of antibiotic therapy.
Five patients (9.4%) were hospitalized with CAP. On average, BAL was performed for treatment failure on the ninth day after hospitalization (range, 3 to 22 days). Among the 14 patients hospitalized for respiratory failure, 5 had interstitial pneumonia and 4 of these had AIDS; their mean time of hospitalization until BAL performance was 17.6 days (range, 5 to 49 days).
Seven patients underwent two bronchoscopies, and one patient had three, each bronchoscopy being performed for a different episode of treatment failure. Mean time between these BAL was 8.7 days (range, 5 to 15 days).
Fifty-one of the 62 BALs (82.3%) were performed on 42 intubated patients receiving mechanical ventilation, corresponding to 79.2% of the 53 patients; mean intubation time was 11.2 days (range, 1 to 37 days).
The empiric antibiotic regimens most used by the service were penicillin, ampicillin, or third-generation cephalosporin with or without macrolide for CAP; ceftazidime, ciprofloxacin, or imipenem with or without vancomycin for nosocomial pneumonia; sulfamethoxazole-trimethoprim for interstitial infiltrates in immunosuppressed patients; and clindamycin with or without third-generation cephalosporin for aspiration pneumonia.
Positivity of BAL
Forty-two of 62 BALs (67.8%) presented
> 104 cfu/mL in BAL quantitative culture. The
three BALs (4.8%) that presented between 103 and
104 cfu/mL were also considered positive and
guided a change of therapy. Total positivity was 45 of 62 (72.6%); 42
of these 45 positive episodes (93.3%) had
> 104 cfu/mL. There were no cases of bacterial
growth with < 103 cfu/mL. Seventeen cases
(27.4%) did not present bacterial growth.
Causes
The most frequent infectious agents were Acinetobacter
baumannii (38.7%), Staphylococcus aureus (19.3%), and
Pseudomonas aeruginosa (17.7%). Ten of the 12 isolates of
S aureus, representing 16.1% of all BALs, were
methicillin-resistant (MRSA), and two were methicillin-sensitive
Staphylococcus aureus (MSSA).
A baumannii was identified in isolation in a majority of cases. P aeruginosa and MRSA were most frequently identified in association with other pathogens, as were other bacteria (Table 1 ).
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There were two cases of pneumocystosis associated with bacterial infection in patients with AIDS. A patient with interstitial pneumonia and AIDS had disseminated strongyloidiasis diagnosed in one episode of pneumonia treatment failure, in which BAL identified Strongyloides stercoralis larvae and E coli; 7 days later, a second BAL was performed for another episode of treatment failure, showing growth of A baumannii with persistence of larvae in the BAL cytologic examination.
Considering 104 cfu/mL as the cutoff and including the cases with bacterial growth between 103 and 104 cfu/mL, 21 of all 45 positive BALs (46.7%) presented more than one isolate, which means polymicrobial infections. The most frequently encountered pathogen associations were between two different strains of A baumannii and between P aeruginosa and MRSA, with three cases of each association.
Eight patients underwent two or more bronchoscopies for treatment failure, and one of these had three BALs (Table 2 ). Mean time between these lavages was 8.7 days (range, 5 to 15 days). Four of the first eight BALs and seven of the nine BALs performed subsequently were positive, yielding a total of 11 of 17 BALs (64.7%) that were positive. Change of therapy guided by BAL culture results occurred in 9 of the 17 cases (52.3%). In the two cases that presented the same agent in the second BAL (A baumannii in case 5 and P aeruginosa in case 7), the strains and their sensitivities were different. Antibiotic therapy was changed in both cases, and the patients were discharged from the ICU.
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2 test) (Table 3)
. The
three BALs with growth between 103 and
104 cfu/mL were considered positives for the
purpose of therapy change. Only three patients (4.8%)—two positives
and one negative—died before BAL results were known. The other eight
patients continued with the empiric therapy adopted between procedure
and BAL fluid results.
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In one case with growth of S aureus, the antibiotic therapy (imipenem) empirically introduced in association with vancomycin was suspended. No antibiotics were suspended in the BAL-negative episodes of this study because it was not considered safe for clinically unstable patients and patients with other infections.
Outcome
The mean time between BAL and outcome (death or discharge from
ICU) was 20 days, whereas the mean interval between hospital admission
and outcome was 34.2 days. Twenty-three of 53 patients (43.4%) died.
Mortality was analyzed considering only the first BAL performed on each
patient. There was no difference between total mortality and mortality
rates for positive and negative cases. Patients for whom antibiotic
therapy was changed on the basis of BAL culture showed lower mortality
compared with other groups (Table 4
). However, there was no significant statistical difference
(p = 0.17, Fisher’s Exact Test).
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Discussion |
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TOPAbstractIntroductionMaterials and MethodsResultsDiscussionConclusionsReferences |
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The impact of BAL was studied in the management of episodes of pneumonia with treatment failure in a medical ICU. Treatment failure of pneumonia was studied by Örtqvist et al16 in 1990 and classified as early therapeutic failure (no clinical response in 72 h) or late therapeutic failure (initial response followed after 72 h by deterioration). Diagnostic bronchoscopy was performed on 18 patients with CAP and provided a diagnosis in 41% of the cases. Although treatment failure is a frequent clinical problem in ICUs, it has not been studied as often.
Treatment failure is caused by four mechanisms: agent resistance; other concomitant infections; noninfectious processes (such as atelectasia, pulmonary thromboembolism, congestive heart failure, ARDS); and host factors (prolonged mechanical ventilation, age > 60 years, chronic respiratory disease, unrecognized immunosuppression).4 5 The purpose of this study was to investigate and rule out the first mechanism by using BAL, a sensitive and specific technique in pneumonia diagnosis, for etiologic diagnosis of agents possibly resistant to previous treatment and guidance of specific therapy.
In this study, pneumonia was diagnosed by clinical variables only. A study performed with BAL and PSB in patients with presumed pneumonia receiving mechanical ventilation used autopsies as a gold standard and showed the presence of pneumonia in only 67% of the cases.17 Andrews et al18 reported that in patients with acute diffuse lung injury and suspected pneumonia receiving mechanical ventilation, 29% of cases were misdiagnosed by comparing clinical variables for pneumonia diagnosis with autopsy findings. Besides the possibility of overdiagnosis and overtreatment, empiric treatment based on clinical diagnosis is a frequent medical practice in the management of pneumonia. Guidelines for CAP management proposed in 1993 by the American Thoracic Society (ATS)1 and in 1998 by the Infectious Diseases Society of America4 as well as the ATS Consensus on Hospital-Acquired Pneumonias in 19955 suggested empiric antibiotic regimens for different situations. Concerns are greater in VAP, as previous antimicrobial therapy may lead to resistant bacterial and fungi infection and potentially increased morbidity and mortality.19 20 However, undue suspension may result in protracted illness, prolonged ventilation and ICU stay, and possibly death.15 Some authors propose different diagnostic methods to avoid these risks.7 14 21 Similarly, it would be logical to use a sensitive and specific method validated for pneumonia diagnosis, such as BAL, in treatment failures to identify etiologic agents and guide therapy.
Some variables may interfere in the positivity of a BAL fluid examination. Because it is a complex procedure placing severe demands on the bronchoscopy service, the examination is not always performed as soon as it is prescribed. The amount of fluid retrieved, sample conditioning, and time of transportation to the laboratory may influence positivity.13 BAL performance in the presence of antibiotics may produce false-negatives, inhibiting the growth of fastidious agents such as Streptococcus pneumoniae, Haemophilus influenzae, and anaerobes. Soweine and colleagues22 studied how the results of BAL and PSB cultures were affected by the presence and timing of previous antibiotics in patients with suspected VAP receiving mechanical ventilation, and proposed lower thresholds for the analysis. Approximately 70% of the 62 BALs performed in this study presented quantitative cultures considered positive, even though 58 of 62 BALs (93.5%) were performed while using antibiotics.
A threshold of 104 cfu/mL is the most accepted cutoff for positivity in BAL quantitative culture.5 7 11 Forty-two of 62 BALs (67.7%), equivalent to 93.3% (42 of 45) of all positive episodes, presented growth of > 104 cfu/mL in BAL quantitative culture. According to some authors, counts > 103 cfu/mL could be considered positives in cases with a compatible clinical picture under antibiotic therapy.7 22 The three BALs (4.8%) with growth between 104 and 103 cfu/mL were also considered positives for the purpose of changing antibiotic therapy. Besides quantitative culture, other examinations may detect additional agents, especially if patients have some degree of immunosuppression. Unusual or unsuspected agents such as P carinii can cause treatment failure. A study of 385 patients admitted to the hospital for CAP identified HIV infection in 46%, and 19% were unaware of HIV status at the time of admission. P carinii was diagnosed in 12.7% of the patients.23 In the present study, two patients had pneumocystosis, and one patient with disseminated strongyloidiasis had two episodes of treatment failure with persistence of larvae in BAL.
Bacterial growth under antibiotics is expected to involve mainly strains resistant to antibiotic regimens. In this study, 37 of 45 positives had bacteria resistant in vitro to the failed regimens. Seven patients had treatment that was not adequate to the isolate. The most frequently encountered pathogens in this study (A baumannii, P aeruginosa, and MRSA) are the etiologic agents usually found in late-onset nosocomial pneumonia (pneumonia diagnosed after 5 days of hospitalization) according to the Nosocomial Pneumonia Consensus of the ATS.5 In this study, the mean duration of hospitalization until BAL was 14.2 days. Only one case was diagnosed involving an anaerobe (B fragilis). S pneumoniae and H influenzae, most commonly isolated in CAP or early-onset nosocomial pneumonias (nosocomial pneumonias diagnosed within 5 days of hospital admission), were not isolated in any of the cases. Only two of the six cases diagnosed within 5 days of admission had negative BAL. These should be empirically covered by the antibiotic regimens used, so there is little likelihood of a false-negative in the case of such agents. Approximately 45% of infections were polymicrobial, a proportion compatible with the literature on nosocomial pneumonia.20 24 25 The most common associations were between P aeruginosa and MRSA, and between two distinct strains of A baumannii.
A change of therapy was guided by BAL results in 54.8% of all episodes (34 of 62) and in 75.6% of positive episodes (34 of 45). The agents that resulted most frequently in a therapy change were the Gram-negative A baumannii (83.3%) and P aeruginosa (75.0%). A study with suspected VAP showed a change of antibiotic regimen in 35% of all cases and suspension of antibiotic therapy in 17%.9 Other researchers changed the antibiotic prescription based on BAL or PSB cultures in 66 of 92 bronchoscoped VAP episodes (71.7%), with different changes of antibiotics (complete change, addition, or partial discontinuation of antibiotic therapy) in 48 episodes (52.1%) and discontinuation of treatment with all antibiotics in 18 (19.6%).15
Kirtland et al26 demonstrated in their study that BAL quantitative culture had a sensitivity of 63%, a specificity of 96%, and a positive predictive factor of 91% in recognizing sterile lung parenchyma in patients who died while being ventilated. Sterile lung parenchyma so recognized would indicate absence of infection in patients not receiving antibiotics and, in patients receiving antibiotics, would at least indicate no need to change antibiotics and in some instances, facilitate a decision to stop antimicrobial therapy. In a study with 138 patients with presumed VAP to evaluate implementation of bronchoscopic techniques (BAL and PSB), Bonten et al9 withheld therapy in 48 of the 66 patients in whom VAP diagnosis was not microbiologically confirmed (all 37 negatives and 11 of 29 less than culture threshold), without higher recurrence or mortality rates. Heyland et al15 described antibiotic therapy discontinuation in only 9 of 34 negatives (26.5%), with no growth in cultures from BAL or PBS. Sanchez-Nieto et al27 reported that antibiotic therapy was not withheld in 13 cases without significant bacterial growth in BAL, PBS, or quantitative endotracheal aspirate (QEA) cultures. There was no suspension of antibiotics in the BAL-negative episodes of this study because it was not considered safe for patients who were in clinically unstable condition or had other infections. Negatives mainly directed the attention toward other problems such as extrapulmonary infections and noninfectious complications.
Overall mortality in this study was 43.4%. No differences in mortality were found among positives, positives with therapy change, and negatives (46.7%). In a nonrandomized, prospective study of suspected VAP, Heyland and colleagues15 found a lower mortality rate in the group that underwent bronchoscopy for BAL or PSB compared with control subjects (18.5% vs 34.7%). Both groups were similar in terms of the duration of mechanical ventilation and ICU stay after BAL. Other studies did not find that therapy change based on BAL reduced mortality in VAP, even compared with other techniques.27 28 At the 1999 ATS meeting, Fagon and Chastre29 presented a multicenter randomized controlled trial for suspected VAP comparing 204 patients managed with invasive bronchoscopic techniques (BAL and PSB) with 209 patients managed with a noninvasive strategy (clinical evaluation, QEA, and ATS guidelines for selection of antibiotics). They showed that evaluation of patients using an invasive diagnostic strategy was associated with an improvement in multiorgan dysfunction, reduced antibiotic consumption, and reduced mortality.
The positives in this study were divided into two groups according to the number of pathogens. The analysis found a decrease in mortality that was not statistically significant (p = 0.06) for patients with one pathogen (6 of 21; 28.6%) compared with patients with polymicrobial infection (10 of 17; 58.8%). Mortality decreased to 46.1% (6 of 13) in the subgroup with polymicrobial infection that changed therapy based on BAL culture. This difference was also not statistically significant (p = 0.1). Identification of more than one pathogen may signify a worse prognosis for the patient, and BAL-targeted therapy may have improved outcomes, but the study was unable to produce statistically significant results on the difference owing to an insufficient number of patients.
However, mortality evaluation is not a satisfactory variable for medical ICU patients with many comorbidities, such as the patients in this study. Different studies show that mortality attributable to nosocomial pneumonia varies between 33% and 50%, indicating that at least half of hospitalized patients die of causes other than pneumonia.6 12 24 The patients in this study had a prolonged hospital and ICU stay, and they were therefore exposed to additional risks, such as wound scars, catheter-related infections, thrombosis, drug toxicity, and malnutrition.
Although the study group was heterogeneous, it was representative of the population of a medical ICU with treatment failure as a common denominator. This situation poses a dilemma for intensive care specialists: Should antibiotic therapy be suspended or changed? Will outcomes be changed by a different empiric antimicrobial regimen or treatment based on a diagnostic procedure? Is BAL advisable, or should easier and cheaper techniques such as QEA be preferred?
There is considerable controversy about whether quantitative invasive diagnostic procedures such as BAL or PSB should be used in the initial workup of patients with suspected nosocomial pneumonia.24 Some authors describe more frequent changes of antibiotic prescription and enhanced ability to narrow the spectrum or discontinue antibiotic therapy based on BAL or PSB cultures in VAP.9 15 27 28 29 This approach could permit cost savings despite procedural costs.30 QEA may be an easily performed and costless noninvasive diagnostic tool in VAP. BAL and QEA have similar diagnostic accuracy, but BAL has a higher specificity than QEA.17 Jourdain et al31 found only 40% concordance between QEA- and PSB-positive cultures and pointed out the advantage of bronchoscopic techniques compared with QEA in VAP diagnosis. In a randomized, controlled study of suspected VAP, Sanchez-Nieto et al27 did not find significant differences between invasive (BAL, PSB) and noninvasive (QEA) diagnostic methods in regard to mortality, ICU stay duration, and total duration of mechanical ventilation. However, treatment failure was not specifically analyzed, and there was no suspension of antibiotic therapy in negative cases. More recently, Fagon et al30 demonstrated that bronchoscopic management of VAP patients resulted in better outcomes (improved multiorgan dysfunction, reduced antibiotic consumption and mortality) compared with a clinical strategy using QEA and ATS guidelines for antibiotic selection.
The present study suggests BAL may be a sensitive method for diagnosis in cases of pneumonia with treatment failure and may be useful in guiding therapy even if performed during antibiotic treatment. Other diagnostic techniques were not evaluated. The institution in question processes only bronchoscopic samples for quantitative culture. QEA may possibly be helpful to identify treatment failure in cases of pneumonia and to guide therapy, given that it has been shown to help identify VAP. However, because QEA is less specific than BAL; it would be risky to suspend antibiotic therapy in negative cases based only on this technique. Because BAL is more specific, it can help physicians make decisions more confidently in cases of treatment failure, including decisions to suspend antibiotic therapy in negative stable cases without extrapulmonary infections. Heyland and coworkers15 measured this confidence in their study on invasive diagnostic techniques in VAP. A stepped approach using QEA for triage followed by BAL in negative or worsening cases could be cost-effective and deserves future testing.
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Acknowledgements |
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Footnotes |
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Received for publication November 19, 1999. Accepted for publication May 18, 2000.
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  R. Menendez and A. Torres Treatment Failure in Community-Acquired Pneumonia Chest, October 1, 2007; 132(4): 1348 - 1355. [Abstract] [Full Text] [PDF]
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 M. Woodhead, F. Blasi, S. Ewig, G. Huchon, M. Leven, A. Ortqvist, T. Schaberg, A. Torres, G. van der Heijden, and T. J. M. Verheij Guidelines for the management of adult lower respiratory tract infections Eur. Respir. J., December 1, 2005; 26(6): 1138 - 1180. [Abstract] [Full Text] [PDF]
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