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(Chest. 2003;124:2239-2243.)
© 2003 American College of Chest Physicians

Incidence, Etiology, and Outcome of Nosocomial Pneumonia in ICU Patients Requiring Percutaneous Tracheotomy for Mechanical Ventilation*

Jordi Rello, MD, PhD; Carmen Lorente, MD; Emili Diaz, MD; Maria Bodi, MD, PhD; Carmen Boque, MD, PhD; Albert Sandiumenge, MD and Josep Maria Santamaria, MD

* From the Critical Care (Drs. Rello, Lorente, Diaz, Bodi, Boque, and Sandiumenge), and Microbiology (Dr. Santamaria) Departments, Joan XXIII University Hospital, University Rovira & Virgili, Tarragona, 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
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 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Objective: To determine the epidemiology of pneumonia in patients with tracheotomy receiving short-term mechanical ventilation.

Design: Observational prospective study.

Setting: A 14-bed medical-surgical ICU.

Subjects: Ninety-nine critically ill acute patients requiring percutaneous dilatational tracheotomy for mechanical ventilation.

Interventions: Tracheal aspirate obtained 48 h before tracheotomy.

Measurements and main results: Eighteen patients (18.1%) acquired pneumonia (median of 7 days after tracheotomy). Pseudomonas aeruginosa was the most frequently identified pathogen, found in eight of the episodes (four not documented by prior tracheal colonization), followed by other Gram-negative bacilli. The development of ventilator-associated pneumonia (VAP) was not anticipated by any clinical variable. A positive tracheal aspirate (TA) culture result obtained before tracheotomy was associated with a risk of acquiring pneumonia of 19.7%, whereas sterile TA cultures were associated with a risk of 14.3% (p > 0.20). VAP prolonged ICU stay or the ventilation period for a median of 19 days and 15 days, respectively. Overall mortality was 34.3%, but the presence of VAP did not increase the mortality rate.

Conclusions: Percutaneous tracheotomy in patients receiving short-term mechanical ventilation predisposes to pneumonia. Pneumonia was associated with prolonged ventilation and ICU stay, but was not associated with increased mortality. Pseudomonas is a common pathogen after tracheotomy, and this observation should be considered in selecting an antibiotic regimen, because TA obtained prior to the tracheotomy often failed to identify this pathogen.

Key Words: epidemiology • incidence • outcome • Pseudomonas aeruginosa • tracheotomy • ventilator-associated pneumonia


   Introduction
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 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Nosocomial pneumonia is the most common infection in intubated patients. Its epidemiology has been extensively studied over the past decade.1 2 In a classic study, Niederman et al3 evaluated aspects related to nutrition and airway colonization in tracheotomized patients; however, these authors investigated a domiciliary population of patients with long-term tracheotomies. In a further study, Kollef et al2 analyzed if tracheotomy may or may not be associated with an increased risk of pneumonia in the ICU. More recently, a French retrospective study4 improved our understanding of the predisposing factors for pneumonia in patients receiving mechanical ventilation requiring surgical tracheotomy for weaning, but tracheotomies are often performed for other reasons in critically ill patients. Currently, percutaneous dilatational tracheotomies have emerged as the preferred technique in some ICUs, but no study has investigated specifically pneumonia under these conditions. In addition, a consensus conference report3 suggested the need to evaluate the epidemiology of ventilator-associated pneumonia (VAP) in patients with tracheotomy; however, more than a decade later, information on the impact of tracheotomy in patients with short ventilation periods remains scarce.

We conducted a prospective observational study to assess the incidence, etiology, and impact on outcome of nosocomial pneumonia acquired during short-term mechanical ventilation in critically ill acute patients who underwent percutaneous dilatational tracheotomy in general ICUs. A primary goal was to evaluate the infectious complications associated with tracheotomy in patients receiving short-term mechanical ventilation. We tried to identify the association between bacterial colonization prior to the tracheotomy and development of VAP, in order to guide and improve our management strategies. We specifically focused on risk factors associated with the procedure and previous tracheal colonization. A secondary objective was to evaluate the impact of these infections on outcome. It remains uncertain whether the epidemiology of this complication in patients who underwent a tracheotomy is different compared with patients with intubation.

Our primary hypothesis was that the findings of a tracheal aspirate (TA) obtained prior to the tracheotomy would identify the etiologic pathogen of the pneumonia. A secondary hypothesis was that mortality would be independent of the development of pneumonia in a population of patients receiving short-term mechanical ventilation with a tracheotomy.


   Materials and Methods
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 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
Study Population
The study was conducted in a 14-bed medical-surgical ICU at a teaching hospital from January 2000 until June 2002. All patients who required tracheotomy during the ICU stay were eligible for study. Patients were excluded if the tracheotomy was performed prior to ICU admission. Surgical tracheotomies were performed by an otorhinolaryngologic surgical specialist in the operating room, and these patients were also excluded. Percutaneous tracheotomies were performed by the ICU staff (C.B., M.B., E.D., A.S.) using a blind-stick technique. Chest radiographs and WBC counts were obtained daily. Chest radiographs were evaluated by the medical staff. All patients had a nasogastric tube in place and received ranitidine, pantoprazol, or sucralfate. Selective decontamination of the digestive tract was not used.

A worksheet including demographics, and characteristics before tracheotomy, on the day of tracheotomy and after tracheotomy was prospectively recorded by the same investigator (C.L.). A TA was obtained and cultured semiquantitatively 48 h before the tracheotomy was performed. Patients receiving an antibiotic regimen received an extra dose at the start the procedure, and a single dose of amoxicillin-clavulanate was recommended for patients who were not receiving antimicrobial agents. Two separate blood culture samples were obtained immediately after the procedure was completed and then 15 min later. Clinical progress was observed until ICU discharge or death. Subsequent episodes of pneumonia after ICU discharge were not studied. ICU follow-up was limited empirically to 60 days.

Diagnosis of Pneumonia
Pneumonia was defined as the presence of new and persistent pulmonary opacities in the chest radiographs plus presence of signs of local (purulent respiratory secretions) and systemic signs of inflammatory response (WBC count > 10,000/µL, rise in WBC count > 20% in the presence of leukocytosis, or fever). Fever was defined as two or more consecutive determinations > 38°C degrees. Fiberoptic bronchoscopic examination using a protective specimen brush was performed to identify the causative pathogen. Bacteriologic processing and identification methods have been reported elsewhere.5 Thresholds for identification of etiologic pathogens were 1,000 cfu/mL for protected specimen brush and 1,000,000 cfu/mL for TA. Empiric broad-spectrum antimicrobial therapy was started following a patient-based strategy,6 in which a respiratory sample was obtained within 6 h of the onset of pneumonia. Once the culture results were known, the antimicrobial regimen was adjusted on the basis of sensitivity testing of the identified microorganisms.

Definitions
A nasogastric tube was considered present when it was maintained until 3 days after the tracheotomy. Sedation was considered present if it was maintained > 24 h after tracheotomy. The APACHE (acute physiology and chronic health evaluation) II score was calculated with the values obtained within the first 24 h of ICU admission and within the 24 h prior to the tracheotomy. Criteria to diagnose coma, COPD, steroid use, prior antibiotic exposure, and other variables have been reported elsewhere.7 8 Diagnosis of infection of the tracheotomy stoma was based on Centers for Disease Control and Prevention criteria.9

Statistical Analysis
All results are expressed as a ratio of total patients, or medians. Continuous variables were compared using the Student t test. Qualitative variables were compared using the Fisher exact test (two-tailed) and the {chi}2 test with Yates correction, when necessary, using CIA statistical software (Version 1.2; British Medical Journal; London, UK). Development of pneumonia was considered the dependent variable in the analysis; p < 0.05 was chosen as significant.


   Results
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 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
A total of 796 consecutive patients received intubation and mechanical ventilation over the study period, representing 6,833 ventilation-days. One hundred ten of these patients (13.8%) underwent tracheotomies. Eleven patients underwent a surgical tracheotomy in the operating room due to existence of contraindications for percutaneous tracheotomy: morbid obesity (n = 4), unstable cervical fracture n = 3), uncertainty in identifying the anatomic landmarks (n = 3), and emergency surgical airway management (n = 1). One episode (9%) of pneumonia caused by Pseudomonas aeruginosa developed among the 11 patients excluded by surgical tracheotomy. The remaining 99 patients underwent percutaneous tracheotomy. All these interventions were performed in the ICU. Percutaneous tracheotomies were indicated in 61 patients (61.6%) due to difficulty of weaning, in 29 patients (29.2%) due to a decrease in the consciousness level, and in 9 patients (9.0%) by bronchoplegia. Extubation in 31 patients (31.3%) was unsuccessful prior to tracheotomy.

The procedures were performed a median of 13 days (range, 1 to 29 days) after ICU admission; characteristics are shown in Table 1 . Median age was 62 years (range, 19 to 90 years), and 75 patients (75.7%) were men. Median PO2/fraction of inspired oxygen ratio was 276 mm Hg (range, 116 to 536 mm Hg). In our study population, 16 patients (16.1%) with COPD required tracheotomy. The median APACHE II score of these patients was 16 (range, 3 to 33) on ICU admission and 12 (range, 3 to 24) on development of pneumonia. Seventy-five patients (75.8%) required sedation > 3 days after the tracheotomy was performed. Univariate analysis was unable to identify significant associations between any factor and pneumonia. We analyzed pretracheotomy variables (age, gender, APACHE II at ICU admission, steroid use, cranioencephalic trauma, surgery, COPD, ARDS, cardiopulmonary resuscitation, prior pneumonia, prior infection, prior antibiotic use), during the procedure (indication for tracheotomy, presence of fever, APACHE II, PO2/fraction of inspired oxygen, concomitant antibiotic use, steroid use), and posttracheotomy (presence of a nasogastric tube, structural coma, sedation > 48 h, bleeding). All the factors analyzed were nonsignificant. Similarly, there was no relationship between duration of ICU stay prior to tracheotomy and development of pneumonia.


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  		Table 1.. Characteristics of 110 Patients Studied

 
Overall, 80 patients (80.8%) received antibiotics during ventilation prior to tracheotomy. Thirty patients received prior antibiotic regimens containing antipseudomonal coverage, and 4 of them acquired pneumonia. All patients received antibiotic prophylaxis for tracheotomy. Twenty-two patients acquired pneumonia prior to the tracheotomy. Thirty-three patients acquired other nosocomial infections. These infections were not significantly associated with subsequent differences in the risk of pneumonia after tracheotomy.

Eighteen patients (18.1%) acquired VAP after the percutaneous tracheotomy. These episodes occurred a median of 7 days (range, 1 to 35 days) after the procedure (Table 2 ). Most episodes (n = 130) developed within the first week after tracheotomy, and 5 of these episodes were caused by P aeruginosa. The median onset of pneumonia was 20 days after ICU admission. One patient had an episode of pneumonia caused by methicillin-resistant Staphylococcus aureus (MRSA) after weaning and was not included in our analysis. Another patient acquired bacteremia due to P aeruginosa during the procedure. The same strain was isolated from their TA. No additional antibiotics were prescribed, and follow-up was free of complications. No patients presented with deep-wound infection. No episodes of relapse were identified in this study population over the follow-up period (60 days).


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  		Table 2.. Etiology of Pneumonia*

 
Identification of the causative agent was possible in the 18 cases. P aeruginosa (n = 8), S aureus (n = 2; one of them MRSA), Proteus mirabilis (n = 2), Klebsiella pneumoniae (n = 2), Acinetobacter baumannii (n = 2), Escherichia coli (n = 1), and Haemophilus influenzae (n = 1) were identified as the responsible pathogens. Five episodes (E coli, methicillin-sensitive S aureus [MSSA], H influenzae, and P aeruginosa in two) developed in patients without prior antibiotic exposure. The TA obtained before tracheotomy identified different organisms (MRSA, Enterobacter cloacae, S aureus, Aspergillus fumigatus) in only four cases (< 25%) [Table 2 ]. In 9 of 13 episodes that developed within the first week of tracheotomy, the etiology was anticipated by pretracheotomy (48 h) TA (Table 2) . P aeruginosa was not identified in the pretracheotomy TA in four of eight cases. No additional information was provided by TA performed immediately after the tracheotomy was performed.

The most frequent isolates colonizing patients prior to tracheotomy were nonfermentative Gram-negative bacilli. A baumannii was identified colonizing 17 patients, but only 1 of them acquired pneumonia. P aeruginosa was identified in 15 patients, and 4 of them acquired pneumonia. S aureus was isolated in 12 cases, 4 of which were MRSA. Less frequent bacteria were P mirabilis (n = 5), E cloacae (n = 3), coagulase-negative staphylococci (n = 2), and miscellaneous flora (< 4 patients) in the other 39 patients. Two samples showed polymicrobial isolates. Candida albicans was isolated in four cases, and none were followed by pneumonia. Finally, the TA was sterile in only 13 patients (13.1%). A positive TA culture result obtained before tracheotomy was associated with a risk of developing pneumonia of 19.7%, whereas sterile TA cultures were associated with a risk of 14.3% (p > 0.20).

Thirty-four patients (34.7%) died; infection was active in seven deaths (20.5%). Mortality was similar (33.3%, p > 0.20) to that in patients who did not acquire pneumonia. The period of mechanical ventilation was significantly longer (15 days, p < 0.05) in survivors who acquired pneumonia. The length of stay for pneumonia survivors was significantly higher (19 days, p < 0.05) for patients without pneumonia.


   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
This study investigated the epidemiology of pneumonia and other infectious complications in patients receiving short-term mechanical ventilation requiring tracheotomy in the ICU. In contrast with intubated patients, this subset of patients has been investigated rarely in the literature.10 A unique aspect of this study is that all patients underwent percutaneous tracheotomy. Our findings suggest that the risk of transient bacteremia or wound infections is marginal. The risk of pneumonia was estimated to be 18%, and P aeruginosa was the dominant pathogen. The majority of episodes occurred within the first week after tracheotomy. Interestingly, nearly 90% of patients had tracheal colonization prior to the procedure, but we could not relate pretracheotomy culture results to the bacteriology of subsequent pneumonias in two thirds of episodes.

These observations are important and not only of academic interest. Performing percutaneous tracheotomies a median of 13 days after ICU admission exposed our patients to an increment in the risk of acquiring pneumonia, particularly within the first week after the procedure. Our current findings suggest the need to select an antipseudomonal agent for prophylaxis of patients receiving mechanical ventilation who require tracheotomies. This contrast with current clinical practice in many institutions.4 P aeruginosa was responsible for one half of the pneumonia episodes, suggesting the need for antipseudomonal antibiotics in the empiric regimen of these patients, at least in our institution. A delay in prescribing adequate antibiotic therapy in patients with VAP has been associated with increased mortality rates and costs.7 11 12 Four of the eight episodes caused by P aeruginosa were not anticipated by TA performed 48 h before tracheotomy or during the procedure; this emphasizes the need for administering broad-spectrum antibiotic therapy to all patients with tracheotomy who acquire VAP. Seven of these 18 patients with VAP (Table 2) were candidates for de-escalation to minimize further selection of resistance and improving cost-effectiveness. Further studies analyzing virulence factors, such as type III intoxication proteins,13 may improve our understanding of why some strains were associated with pneumonia and others were not. Indeed, type III secretion has been reported significantly associated with higher mortality rates or relapses13 in patients with VAP caused by P aeruginosa.

Nonfermentative Gram-negative bacilli colonization was documented in one third of intubated patients before tracheotomy. Seventeen patients had A baumannii, and 15 others had P aeruginosa. Interestingly, persistent colonization by Pseudomonas was followed by pneumonia in four cases, but A baumannii colonization was followed by infection in one patient alone. Similar observations were found for E cloacae, coagulase-negative staphylococci, and C albicans. This suggests that these isolates should be considered nonpathogenic in patients with airway colonization.

The impact of VAP on outcome remains controversial. Our study suggests that the development of pneumonia in this series was not associated with increased mortality. Other reports11 12 have shown that mortality is associated with delayed antibiotic therapy rather than with development of pneumonia in critically ill patients; however, development of pneumonia prolonged ICU stay by 2 weeks, suggesting that the economic implications of this complication are important. This is consistent with other reports1 11 12 14 15 on the epidemiology of pneumonia in intubated patients.

Our study has several limitations. First, it was performed in a single ICU and the case-mix, treatments, indications for tracheotomy and clinical practices may not be generalizable to other settings. For example, all patients received antibiotic prophylaxis prior to the tracheotomy, and this may influence the findings. Second, the sample was relatively small, a fact that limits our ability to detect all possible differences between the study groups of interest. A type II error cannot be ruled out. Third, we used clinical criteria to establish the diagnosis of pneumonia. Though this may be considered a limitation, previous studies15 have demonstrated that clinically diagnosed pneumonia reflects the population of patients in clinical practice. Fourth, many patients receiving long-term ventilation through a tracheotomy acquire pneumonia weeks or even longer after the onset of tracheotomy. This subgroup of patients was out of the scope of this study. Consequently, implications for patients receiving long-term ventilation may be different. Such study and the epidemiology of recurrent episodes of pneumonia should be investigated in populations with long-term follow-up. Finally, no serial colonization culture samples were collected. It is evident that colonization may change, partly due to antibiotic use, but a recent study16 documented that routine surveillance may not be predictive to identify pathogens of VAP in intubated patients.

In summary, our study demonstrated that a large proportion of VAP developed within the first week after tracheotomy, P aeruginosa being the predominant pathogen. In our study population, baseline characteristics, and variables associated with the procedure and posttracheotomy were unable to predict the development of this complication. Finally, pneumonia after tracheotomy was associated with increased costs (doubling the length of stay and ventilation period in survivors) but did not influence crude mortality.


   Acknowledgements
 
We wish to thank Marta Roque for statistical support, Carmen Ardanuy for microbiologic support, and Michael Maudsley for editing the manuscript.


   Footnotes
 
Abbreviations: APACHE = acute physiology and chronic health evaluation; MRSA = methicillin-resistant Staphylococcus aureus; MSSA = methicillin-sensitive Staphylococcus aureus; TA = tracheal aspirate; VAP = ventilator-associated pneumonia

Supported in part with grants from Comissio Interdepartmental Recerca i Technologica (SGR2001-414) and Distincio a la Promocio de la Recerca Universitaria (Dr. Rello).

Received for publication November 6, 2002. Accepted for publication April 28, 2003.


   References
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 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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