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(Chest. 1999;115:178-183.)
© 1999 American College of Chest Physicians

The Role of Anaerobes in Patients With Ventilator-associated Pneumonia and Aspiration Pneumonia*

A Prospective Study

Paul E. Marik, MD, FCCP and Pamela Careau, MT, (ASCP)

* From the Medical and Surgical Intensive Care Unit (Dr. Marik) and CliniTech Services (Ms. Careau), St. Vincent Hospital, Worcester, MA.


   Abstract
TOP
 Abstract
Introduction
 Materials and Methods
 Results
 Discussion
 References
 
Context: Aspiration of oropharyngeal material, with its high concentration of anaerobic bacteria, has been implicated in the pathogenesis of both ventilator-associated pneumonia (VAP) and aspiration pneumonitis (AP). Consequently, patients with these disorders are usually treated with antimicrobial agents with anaerobic activity.

Objective: To determine the incidence of anaerobic bacteria in patients with VAP and AP.

Design: Prospective, nonrandomized, interventional study.

Setting: University-affiliated community teaching hospital.

Patients and interventions: We performed sequential blind protected specimen brush (PSB) sampling and mini-BAL in 143 patients with 185 episodes of suspected VAP and 25 patients with AP who required mechanical ventilation. Quantitative aerobic and anaerobic cultures were performed on all specimens. Pneumonia was considered to be present when either > 500 cfu/mL cultured from blind PSB sampling or > 5,000 cfu/mL cultured from mini-BAL were present.

Results: Using the predefined criteria, bacterial pneumonia was diagnosed in 63 of 185 suspected VAP episodes (34%) and 12 of 25 patients with AP (48%). At least one dose of an antibiotic was given in the 24 h prior to bacteriologic sampling in 106 suspected VAP episodes (57%) and in 12 patients with AP (48%). More than one pathogen was isolated from 11 VAP and four AP patients. Pseudomonas aeruginosa, Staphylococcus aureus, and enteric Gram-negative organisms were isolated most frequently from patients with VAP. In the patients with AP, enteric Gram-negative organisms were isolated in patients with GI disorders and Streptococcus pneumoniae and Haemophilus influenzae predominated in patients with "community-acquired" aspiration. Only one anaerobic organism was isolated from the entire group of patients; Veillonella paravula was isolated from a blind PSB specimen in a patient with suspected aspiration pneumonia.

Conclusion: Despite painstaking effort, we were able to isolate only one anaerobic organism (nonpathogenic) from this group of patients. The spectrum of aerobes in patients with VAP was similar to that reported in the literature. The organisms found in patients with AP was a reflection of the organisms likely to colonize the oropharynx. The use of antibiotics with anaerobic coverage may not be necessary in patients with suspected VAP and AP. Furthermore, penicillin G and clindamycin may not be the antibiotics of choice in patients with AP.

Key Words: anaerobes • aspiration pneumonitis • diagnosis • mechanical ventilation • protected specimen brush sampling • ventilator-associated pneumonia


   Introduction
TOP
 Abstract
 Introduction
Materials and Methods
 Results
 Discussion
 References
 
Ventilator-associated pneumonia (VAP) and aspiration pneumonitis (AP) represent a spectrum of aspiration "syndromes." Both are common problems encountered in the ICU, with VAP occurring in approximately 25% of patients undergoing mechanical ventilation,1 ,2 ,3 ,4 ,5 and AP commonly occurring in

patients admitted to the ICU with an altered level of consciousness.6 AP follows macroaspiration of oropharyngeal and/or gastric contents in patients with an altered level of consciousness, dysphagia, or bowel obstruction.6 ,7 ,8 VAP is widely believed to result from the microaspiration of oropharyngeal material colonized by pathogenic microorganisms.9 ,10 ,11 ,12 ,13 Although anaerobic bacteria are frequently isolated from the oropharyngeal flora,14 their pathogenetic role in VAP and AP is unclear. Many studies have failed to isolate anaerobic bacteria in patients with VAP.15 ,16 ,17 ,18 The microbiology of aspiration pneumonitis is based on studies performed in the 1970s using transtracheal aspiration.19 ,20 ,21 ,22 These studies suggested that anaerobic bacteria were the major pulmonary pathogens. Based on these studies, most patients with AP are currently treated with either penicillin G or clindamycin.7 ,8 ,23 ,24 ,25 However, a recently published study questions the validity of this treatment approach.6

Isolation of anaerobic bacteria requires adequate transport conditions and specific growth media. Many of the recent studies investigating the microbiology of VAP have not specifically taken these measures.15 ,16 ,17 ,18 Transtracheal aspiration may result in a large number of false-positive results.26 Furthermore, transtracheal aspiration cannot be performed in intubated patients. Protected specimen brush (PSB) sampling has been recommended as the method of choice in isolating anaerobes in ventilated patients.27 The aim of this study was to determine, using strictly controlled culture conditions, the pathogenetic role of anaerobic bacteria in patients with suspected VAP and in patients with AP who required endotracheal intubation.


   Materials and Methods
TOP
 Abstract
 Introduction
 Materials and Methods
Results
 Discussion
 References
 
This study was conducted between June 1996 and August 1997 in the Medical and Surgical ICUs at St. Vincent Hospital, Worcester, MA. This study was approved by our Institutional Review Board. As both blind PSB sampling and mini-BAL are considered to be within the standard of care in our ICUs, the Institutional Review Board waived the need for informed consent. Patients were eligible for inclusion in this study if they had been mechanically ventilated for more than 48 h and were suspected to have VAP based on clinical grounds. The clinical suspicion of VAP was based on recent and persistent pulmonary infiltrates on the chest radiograph and at least two of the following three clinical criteria: fever > 38.5°C, leukocytosis (> 10 x 109/L), and purulent tracheal secretions.5 ,28 ,29 In addition, patients who required endotracheal intubation and mechanical ventilation as a consequence of AP were included in the study. The criteria for aspiration were those defined by Lorber and Swenson20 and Bartlett et al22 : namely, the presence of alveolar infiltrates on the chest radiograph and either witnessed aspiration or risk factors for aspiration (ie, altered level of consciousness, dysphagia, or intestinal obstruction).

All patients underwent sequential blind PSB sampling and mini-BAL as previously reported.30 ,31 Briefly, patients were preoxygenated at 80 to 100% oxygen throughout the procedure and monitored by continuous pulse oximetry. Midazolam was used for sedation as needed. No local anesthesia was used. Blind PSB sampling was performed first. Utilizing a standard microbiology specimen brush (Microvasive No 1650; Boston Scientific Corp; Watertown, MA), the catheter was inserted through the endotracheal tube and advanced "blindly" to approximately 35 cm or until resistance was met. A specimen was obtained by expressing and retracting the inner catheter and brush in the standard fashion. The brush was then placed in 1 mL of thioglycolate broth (Remel; Lenexa, KS).

Subsequently, a mini-BAL specimen was obtained using a BAL catheter (No. 140; Ballard Medical Products; Draper, UT). The BAL catheter was inserted through the adapter into the endotracheal tube. With the catheter just protruding into the endotracheal tube, wide-bore suction tubing was connected to the end of the catheter. The catheter stopcock was then opened to suction, the pressure adjusted to 40 to 60 mm Hg, and the stopcock then closed. The catheter was then advanced into the mainstem bronchus of the lung suspected to have pneumonia by orienting the directional tip. The tip of the catheter was flushed with 2 mL of sterile physiologic saline solution. The inner catheter was then advanced until resistance confirmed a wedge position. A Luki sputum trap (Davis & Geck; Wayne, NJ) was placed in line with the catheter and wide-bore suction tubing. With the inner catheter in a wedged position, 20 mL of sterile physiologic saline solution was instilled into the lung and allowed to dwell for approximately 20 s. The stopcock was then turned into the open position, allowing aspiration of lavage fluid. If no return was obtained, another 20-mL aliquot was injected and suctioned. This procedure was repeated until at least 2 to 3 mL of return was obtained. No attempt was made to radiographically determine in which lobe of the lung the blind PSB/mini-BAL sampling was performed.

Microbiologic Processing
The respiratory specimens were transported immediately by hand, and processed by our microbiology laboratory within 20 min of sampling. Quantitative culture was performed on the blind PSB and mini-BAL specimens using the calibrated loop method.27 After gently vortexing the samples, each specimen was inoculated onto two sets of media using first a 0.01-mL and then a 0.1-mL calibrated loop. Final organism dilutions were 1:100 and 1:10, respectively. Routine sets of culture media inoculated included 5% sheep blood agar plates, chocolate agar plates, MacConkey agar plates and CDC anaerobic blood agar plates (Remel). Blood and MacConkey agar plates were incubated at 35°C in a 5% CO2 incubator for a total of 48 h.

Specimens submitted for anaerobic culture were inoculated on prereduced commercial media, which are maintained prior to inoculation in jars flushed with nitrogen gas (anaerobic holding jars). After inoculation, agar media was immediately placed into a self-contained jar with a commercial gas-generating system and an anaerobic indicator strip (BBL anaerobic GasPak Plus; Becton Dickinson Microbiology Systems; Sparks, MD). The indicator is monitored throughout the culture process. Anaerobic cultures are incubated in monitored 35 to 37°C incubators for 48 h prior to first examination. Negative cultures are incubated for an additional 3 days. For quality control, various anaerobic organisms are periodically subcultured in the same manner. Recovery of these organisms validates the ability of the system to recover a variety of anaerobic species.

All organisms recovered from cultures were quantitated. Those bacterial isolates recognized as potential respiratory pathogens and recovered at the 10 cfu/mL threshold were identified as completely as possible using either the Vitek System (BioMerieux Vitek; Hazelwood, MO) or standard manual laboratory procedures. Anaerobic organisms were identified using the Innovative Diagnostic Systems (Remel). Antibiotic susceptibility testing was performed using either the Vitek System or by the Kirby-Bauer disk diffusion method for aerobic and microaerophilic organisms. No antibiotic testing was performed on anaerobic organisms.

Data Collection and Analysis
In patients who were investigated for repeat episodes of suspected VAP, each episode was recorded separately. The patients' basic demographic data, major admitting diagnoses, acute physiology and chronic health evaluation II score, WBC count, radiographic changes, and concurrent antibiotics were recorded in a computerized database (Access 97; Microsoft; Redmond, WA). For the purposes of this study, patients with either > 500 cfu/mL cultured from blind PSB sampling or > 5,000 cfu/mL cultured from mini-BAL were considered to have pneumonia.5 The patients' antibiotic regimens were tailored according to the sensitivities of the pathogen(s) isolated. In patients with negative cultures, the decision to continue or stop the antibiotics was made by the patient's attending physician.

At the end of the data collection, summary statistics were compiled to allow a description of the study population. {chi}2 analysis was used to compare categorical data. Unless otherwise stated, all data are expressed as mean ± SD, with statistical significance declared for p values of 0.05 or less.


   Results
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
Discussion
 References
 
During the study period, 185 paired specimens from 143 patients with suspected VAP and 25 paired specimens from 25 patients with AP were obtained. One patient with bacteriologically proven AP subsequently underwent blind PSB sampling /mini-BAL for suspected VAP (the cultures were negative). The clinical characteristics of both groups of patients are listed in Table 1 . Blind PSB sampling and mini-BAL were performed within 24 h of the suspected episode of aspiration in the patients with AP. Blind PSB sampling and mini-BAL were performed 5 ± 4 days after endotracheal intubation in the patients with suspected VAP.


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  		Table 1. Clinical Features of Patients with Suspected VAP and AP

 
Using the predefined quantitative culture thresholds, bacterial pneumonia was confirmed in 63 of the 185 suspected VAP episodes (34%) and in 12 of the 25 patients with AP (48%). One patient had two distinct episodes of VAP, each with different organisms. At least one dose of an antibiotic had been given in the 24 h prior to bacteriologic sampling in 106 suspected VAP episodes (57%) and in 12 AP patients (48%). The 106 patients with suspected VAP received the following antibiotics (with number in parentheses) prior to bacteriologic sampling: ceftazidime (n = 67), aztreonam (n = 16), ceftriaxone (n = 15), gentamicin (n = 8), vancomycin (n = 16), and clindamycin (n = 63). The 12 patients with suspected AP all received clindamycin in the 24 h prior to blind PSB sampling /mini-BAL. In the group of patients with suspected VAP, pneumonia was diagnosed in 32 instances in which an antibiotic had been given in the previous 24 h, compared with 31 instances in which no antibiotic had been given (30 vs 39%, respectively; not significant). Similarly, in the group of patients with AP, a bacterial pathogen was isolated in five patients who had received a dose of an antibiotic in the previous 24 h and seven patients who had not (42 vs 54%, respectively; not significant).

More than one pathogen was isolated from 11 VAP and four AP patients. The bacterial isolates from both groups of patients are listed in Table 2 . Pseudomonas aeruginosa, Staphylococcus aureus, and enteric Gram-negative organisms were isolated most frequently from the patients with VAP. In the patients with AP, enteric Gram-negative organisms were isolated in patients with GI disorders, and Streptococcus pneumoniae and Haemophilus influenzae predominated in patients with "community-acquired" aspiration. The isolates in patients with AP grouped according to their primary disease are listed in Table 3 . Only one anaerobic organism was isolated from the entire group of patients studied; Veillonella paravula was isolated from a blind PSB specimen in a patient with suspected AP.


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  		Table 2. Isolates Recovered From Patients With VAP and AP

 

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  		Table 3. Isolates in Patients With AP According to Primary Disease

 

   Discussion
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
References
 
Anaerobic bacteria are considered to be common pulmonary pathogens, and they are believed to play a major role in aspiration and nosocomial pneumonia.8 ,23 ,25 ,32 These beliefs are based on a handful of studies conducted in the 1970s, when transtracheal aspiration was used for the collection of "uncontaminated" respiratory secretions 19 ,20 ,21 ,22 ,32 Consequently, antimicrobial agents with anaerobic coverage have been recommended in patients with aspiration pneumonia and nosocomial pneumonia.7 ,8 ,23 ,24 ,25 The results of our study question this common clinical practice. Despite painstaking effort, we recovered only a single nonpathogenic anaerobe from a diverse population of hospitalized ICU patients with suspected pneumonia.

A number of studies using bronchoscopically directed PSB sampling and anaerobic culture media have failed to isolate anaerobic bacteria in patients suspected to have VAP or have reported an incidence of less than 2%.15 ,16 ,17 ,18 However, in all these studies, physiologic saline solution or Ringer's lactate was used as the transport media. It has been suggested that this low yield may be related to the fact that anaerobes are unlikely to survive in these solutions.27 Doré et al33 recently reported the results of a study in which they performed bronchoscopically directed PSB sampling in patients with suspected VAP. Anaerobic transport broth and anaerobic culture media were used to promote the recovery of anaerobic bacteria. These authors recovered anaerobic bacteria in 23% of patients with VAP. The major anaerobic strains that they isolated were Prevotella melaninogenica, Fusobacterium nucleatum, and V parvula. While Prevotella and Fusobacterium spp are regarded as pulmonary pathogens, Veillonella spp are considered to be nonpathogenic.34 ,35 The disparate finding between this study and our present study is unclear. On the day of the PSB sampling, 47% of the patients in the study by Doré et al were receiving antimicrobial therapy, but none were reported to be receiving clindamycin. It is noteworthy that 35% of the patients in whom these authors isolated an anaerobe were receiving antibiotics at the time of microbiologic sampling. The only apparent difference in study design is that the PSB sampling in our study was performed "blind" (nondirected), while in the study by Doré et al, sampling was performed through a bronchoscope. The dependent segments of the right lower lobe are predominantly involved in aspiration syndromes, and the blind technique will likely sample these segments.6 ,24 ,36 We and others have previously demonstrated an excellent concordance between the two techniques and this factor seems unlikely to account for the different findings.15 ,30 ,37

Mier et al6 performed bronchoscopy and PSB sampling in a group of intubated ICU patients with aspiration pneumonia. As in our study, anaerobic transport media and strict anaerobic culture techniques were employed. These investigators failed to isolate a single anaerobe; the spectrum of aerobic organisms recovered was remarkably similar to that recovered in our study. The results of our study differ markedly from the findings of Bartlett and others, whose studies in the 1970s form the basis for current therapy.7 ,19 ,20 ,21 ,22 ,23 ,24 ,25 These studies used transtracheal aspirates to obtain "uncontaminated" pulmonary secretions. It is possible that the organisms recovered by transtracheal aspiration represent oropharyngeal flora that contaminated the trachea during the procedure (due to aspiration) or bacteria that have colonized the trachea, rather than representing true pulmonary pathogens. With PSB sampling, however, uncontaminated lower respiratory tract secretions are obtained.28 ,38 This postulate is supported by a study by Moser et al,26 who demonstrated discrepancies between bacteria recovery by transtracheal aspiration and by transthoracic needle aspiration in dogs with experimental pneumonia.

Less than 50% of patients with either suspected VAP or AP in our study had bacteriologically proven infection. This observation has been well documented in previous studies.6 ,18 ,28 ,30 ,39 Furthermore, these studies have demonstrated that it is not possible, on clinical grounds alone, to determine which patients have bacterial pneumonia. In our study, the right lower lobe was the most commonly involved site. This is not surprising, as the dependent areas of the right lower lobe are the most frequently involved bronchopulmonary segments in patients with aspiration syndromes.6 ,24 ,36

In order to increase the diagnostic sensitivity of blind PSB sampling and mini-BAL, we used a lower quantitative threshold than has traditionally been used.15 ,16 ,17 ,18 This is in keeping with observations of a number of recent studies and is unlikely to have changed the findings of our study. Timsit and colleagues5 have demonstrated that the classic PSB threshold of 1,000 cfu/mL has a sensitivity of only 67%. When these investigators lowered the threshold to 500 cfu/mL, the sensitivity increased to 81% with only a moderate decrease in specificity. Similarly, Dreyfuss et al40 followed 29 patients with suspected VAP who had a PSB culture between 10 and 1,000 cfu/mL. Repeat PSB sampling in 12 of these patients isolated the same organism that was found in the first PSB specimen in a concentration of > 1,000 cfu/mL, and these patients were subsequently treated for pneumonia.

The results of our study suggest that while anaerobes are quantitatively important oropharyngeal commensals, these organisms may be unimportant pulmonary pathogens in patients with VAP and aspiration pneumonia. The bacteriology of these syndromes reflects the aerobic organisms that are likely to colonize the patients at the time of aspiration. These results imply that antimicrobial agents with anaerobic coverage may no longer be required in the treatment of these patients. Furthermore, penicillin G and clindamycin, the traditional antimicrobials of choice in patients with AP, provide inadequate antimicrobial coverage. A major limitation of our study is that 35% of our patients had received an antibiotic with anaerobic activity in the 24 h prior to microbiologic sampling. Furthermore, it is possible that anaerobic bacteria were missed during the sampling procedure or not identified by culture grown out despite our rigorous efforts. We hope the findings of our study will spur clinical trials examining the specific utility of adding anaerobic drugs to the standard antibacterial regimens used in patients with suspected VAP or aspiration pneumonia.


   Acknowledgements
 
ACKNOWLEDGMENT: The authors acknowledge with gratitude the excellent work done by the Respiratory Therapy Department at St. Vincent Hospital and the CliniTech microbiology technicians.


   Footnotes
 
For editorial comment see page 8.

Supported by the St. Vincent Hospital Critical Care Research Fund. The authors have no financial involvement with any of the products mentioned.

Correspondence to: Paul E. Marik, MD, FCCP, Department of Critical Care, St. Vincent Hospital, 25 Winthrop St, Worcester, MA 01604; e-mail: pmarik@ultranet.com

Abbreviations: AP = aspiration pneumonitis; PSB = protected specimen brush; VAP = ventilator-associated pneumonia

Received for publication April 16, 1998. Accepted for publication July 21, 1998.


   References
TOP
 Abstract
 Introduction
 Materials and Methods
 Results
 Discussion
 References
 

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Arch Intern Med, July 10, 2000; 160(13): 1926 - 1936.
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R. Robert, G. Grollier, M. Hira, and P. Dore
A Role for Anaerobic Bacteria in Patients With Ventilatory Acquired Pneumonia : Yes or No?
Chest, April 1, 2000; 117(4): 1214 - 1215.
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