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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)

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 (nonpatho-
genic) 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. (CHEST 1999; 115:178–183)

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

Abbreviations: AP 5 aspiration pneumonitis; PSB 5 protected specimen brush; VAP 5 ventilator-associated pneumonia

V entilator-associated pneumonia (VAP) and aspi-


ration pneumonitis (AP) represent a spectrum of
encountered in the ICU, with VAP occurring in
approximately 25% of patients undergoing mechan-
aspiration “syndromes.” Both are common problems ical ventilation,1–5 and AP commonly occurring in

*From the Medical and Surgical Intensive Care Unit (Dr. Marik) For editorial comment see page 8
and CliniTech Services (Ms. Careau), St. Vincent Hospital, Worces-
ter, MA.
Supported by the St. Vincent Hospital Critical Care Research patients admitted to the ICU with an altered level of
Fund. The authors have no financial involvement with any of the
products mentioned. consciousness.6 AP follows macroaspiration of oro-
Manuscript received April 16, 1998; revision accepted July 21, pharyngeal and/or gastric contents in patients with
1998. an altered level of consciousness, dysphagia, or
Correspondence to: Paul E. Marik, MD, FCCP, Department of
Critical Care, St. Vincent Hospital, 25 Winthrop St, Worcester, bowel obstruction.6 – 8 VAP is widely believed to
MA 01604; e-mail: pmarik@ultranet.com result from the microaspiration of oropharyngeal

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material colonized by pathogenic microorgan- endotracheal tube and advanced “blindly” to approximately 35
isms.9 –13 Although anaerobic bacteria are frequently cm or until resistance was met. A specimen was obtained by
expressing and retracting the inner catheter and brush in the
isolated from the oropharyngeal flora,14 their patho- standard fashion. The brush was then placed in 1 mL of
genetic role in VAP and AP is unclear. Many studies thioglycolate broth (Remel; Lenexa, KS).
have failed to isolate anaerobic bacteria in patients Subsequently, a mini-BAL specimen was obtained using a BAL
with VAP.15–18 The microbiology of aspiration pneu- catheter (No. 140; Ballard Medical Products; Draper, UT). The
monitis is based on studies performed in the 1970s BAL catheter was inserted through the adapter into the endo-
tracheal tube. With the catheter just protruding into the endo-
using transtracheal aspiration.19 –22 These studies tracheal tube, wide-bore suction tubing was connected to the end
suggested that anaerobic bacteria were the major of the catheter. The catheter stopcock was then opened to
pulmonary pathogens. Based on these studies, most suction, the pressure adjusted to 40 to 60 mm Hg, and the
patients with AP are currently treated with either stopcock then closed. The catheter was then advanced into the
penicillin G or clindamycin.7,8,23–25 However, a re- mainstem bronchus of the lung suspected to have pneumonia by
orienting the directional tip. The tip of the catheter was flushed
cently published study questions the validity of this with 2 mL of sterile physiologic saline solution. The inner
treatment approach.6 catheter was then advanced until resistance confirmed a wedge
Isolation of anaerobic bacteria requires adequate position. A Luki sputum trap (Davis & Geck; Wayne, NJ) was
transport conditions and specific growth media. placed in line with the catheter and wide-bore suction tubing.
Many of the recent studies investigating the micro- With the inner catheter in a wedged position, 20 mL of sterile
physiologic saline solution was instilled into the lung and allowed
biology of VAP have not specifically taken these to dwell for approximately 20 s. The stopcock was then turned
measures.15–18 Transtracheal aspiration may result in into the open position, allowing aspiration of lavage fluid. If no
a large number of false-positive results.26 Further- return was obtained, another 20-mL aliquot was injected and
more, transtracheal aspiration cannot be performed suctioned. This procedure was repeated until at least 2 to 3 mL
in intubated patients. Protected specimen brush of return was obtained. No attempt was made to radiographically
determine in which lobe of the lung the blind PSB/mini-BAL
(PSB) sampling has been recommended as the sampling was performed.
method of choice in isolating anaerobes in ventilated
patients.27 The aim of this study was to determine, Microbiologic Processing
using strictly controlled culture conditions, the
pathogenetic role of anaerobic bacteria in patients The respiratory specimens were transported immediately by
with suspected VAP and in patients with AP who hand, and processed by our microbiology laboratory within 20
min of sampling. Quantitative culture was performed on the blind
required endotracheal intubation. PSB and mini-BAL specimens using the calibrated loop meth-
od.27 After gently vortexing the samples, each specimen was
inoculated onto two sets of media using first a 0.01-mL and then
Materials and Methods a 0.1-mL calibrated loop. Final organism dilutions were 1:100
and 1:10, respectively. Routine sets of culture media inoculated
This study was conducted between June 1996 and August 1997 included 5% sheep blood agar plates, chocolate agar plates,
in the Medical and Surgical ICUs at St. Vincent Hospital, MacConkey agar plates and CDC anaerobic blood agar plates
Worcester, MA. This study was approved by our Institutional (Remel). Blood and MacConkey agar plates were incubated at
Review Board. As both blind PSB sampling and mini-BAL are 35°C in a 5% CO2 incubator for a total of 48 h.
considered to be within the standard of care in our ICUs, the Specimens submitted for anaerobic culture were inoculated on
Institutional Review Board waived the need for informed con- prereduced commercial media, which are maintained prior to
sent. Patients were eligible for inclusion in this study if they had inoculation in jars flushed with nitrogen gas (anaerobic holding
been mechanically ventilated for more than 48 h and were jars). After inoculation, agar media was immediately placed into
suspected to have VAP based on clinical grounds. The clinical a self-contained jar with a commercial gas-generating system and
suspicion of VAP was based on recent and persistent pulmonary an anaerobic indicator strip (BBL anaerobic GasPak Plus; Becton
infiltrates on the chest radiograph and at least two of the Dickinson Microbiology Systems; Sparks, MD). The indicator is
following three clinical criteria: fever . 38.5°C, leukocytosis monitored throughout the culture process. Anaerobic cultures
(. 10 3 109/L), and purulent tracheal secretions.5,28,29 In addi- are incubated in monitored 35 to 37°C incubators for 48 h prior
tion, patients who required endotracheal intubation and mechan- to first examination. Negative cultures are incubated for an
ical ventilation as a consequence of AP were included in the additional 3 days. For quality control, various anaerobic organ-
study. The criteria for aspiration were those defined by Lorber isms are periodically subcultured in the same manner. Recovery
and Swenson20 and Bartlett et al22: namely, the presence of of these organisms validates the ability of the system to recover a
alveolar infiltrates on the chest radiograph and either witnessed variety of anaerobic species.
aspiration or risk factors for aspiration (ie, altered level of All organisms recovered from cultures were quantitated. Those
consciousness, dysphagia, or intestinal obstruction). bacterial isolates recognized as potential respiratory pathogens
All patients underwent sequential blind PSB sampling and and recovered at the 10 cfu/mL threshold were identified as
mini-BAL as previously reported.30,31 Briefly, patients were completely as possible using either the Vitek System (BioMerieux
preoxygenated at 80 to 100% oxygen throughout the procedure Vitek; Hazelwood, MO) or standard manual laboratory proce-
and monitored by continuous pulse oximetry. Midazolam was dures. Anaerobic organisms were identified using the Innovative
used for sedation as needed. No local anesthesia was used. Blind Diagnostic Systems (Remel). Antibiotic susceptibility testing was
PSB sampling was performed first. Utilizing a standard microbi- performed using either the Vitek System or by the Kirby-Bauer
ology specimen brush (Microvasive No 1650; Boston Scientific disk diffusion method for aerobic and microaerophilic organisms.
Corp; Watertown, MA), the catheter was inserted through the No antibiotic testing was performed on anaerobic organisms.

CHEST / 115 / 1 / JANUARY, 1999 179

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Data Collection and Analysis Table 1—Clinical Features of Patients with Suspected
VAP and AP
In patients who were investigated for repeat episodes of
suspected VAP, each episode was recorded separately. The VAP AP
patients’ basic demographic data, major admitting diagnoses, (n 5 143) (n 5 25)
acute physiology and chronic health evaluation II score, WBC
count, radiographic changes, and concurrent antibiotics were Age, yr 67 6 15 58 6 21
recorded in a computerized database (Access 97; Microsoft; Male:female ratio 1.8:1 1:1
Redmond, WA). For the purposes of this study, patients with APACHE II score* 16 6 5 12 6 3
either . 500 cfu/mL cultured from blind PSB sampling or WBC count, 3 109/L† 14.8 6 3.4 13.2 6 2.7
. 5,000 cfu/mL cultured from mini-BAL were considered to Lobes involved†
have pneumonia.5 The patients’ antibiotic regimens were tailored Right lower lobe 119 21
according to the sensitivities of the pathogen(s) isolated. In Right middle lobe 3 —
patients with negative cultures, the decision to continue or stop Left lower lobe 22 1
the antibiotics was made by the patient’s attending physician. Bilateral 41 3
At the end of the data collection, summary statistics were Primary diagnoses
compiled to allow a description of the study population. x2 COPD/pneumonia 38 1
analysis was used to compare categorical data. Unless otherwise Post-bowel surgery 21 —
stated, all data are expressed as mean 6 SD, with statistical Congestive heart failure 23 1
significance declared for p values of 0.05 or less. Sepsis syndrome/septic shock 15 —
Cerebrovascular accident 12 2
Post-peripheral vascular surgery 11 —
Post-thoracic surgery 6 —
Results Head injury 6 1
Drug overdose 2 6
During the study period, 185 paired specimens Delirium tremens 1 5
from 143 patients with suspected VAP and 25 paired Seizures 1 4
specimens from 25 patients with AP were obtained. Small bowel obstruction 3 3
One patient with bacteriologically proven AP subse- Other 4 2
quently underwent blind PSB sampling /mini-BAL *APACHE 5 acute physiology and chronic health evaluation.
for suspected VAP (the cultures were negative). The †n 5 185 for VAP, ie, 185 episodes of suspected VAP in 143 patients.
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 an antibiotic in the previous 24 h and seven
of aspiration in the patients with AP. Blind PSB patients who had not (42 vs 54%, respectively; not
sampling and mini-BAL were performed 5 6 4 days significant).
after endotracheal intubation in the patients with More than one pathogen was isolated from 11 VAP
suspected VAP. and four AP patients. The bacterial isolates from
Using the predefined quantitative culture thresh- both groups of patients are listed in Table 2. Pseudo-
olds, bacterial pneumonia was confirmed in 63 of the monas aeruginosa, Staphylococcus aureus, and en-
185 suspected VAP episodes (34%) and in 12 of the teric Gram-negative organisms were isolated most
25 patients with AP (48%). One patient had two frequently from the patients with VAP. In the pa-
distinct episodes of VAP, each with different organ- tients with AP, enteric Gram-negative organisms
isms. At least one dose of an antibiotic had been were isolated in patients with GI disorders, and
given in the 24 h prior to bacteriologic sampling in Streptococcus pneumoniae and Haemophilus influ-
106 suspected VAP episodes (57%) and in 12 AP enzae predominated in patients with “community-
patients (48%). The 106 patients with suspected VAP acquired” aspiration. The isolates in patients with AP
received the following antibiotics (with number in grouped according to their primary disease are listed
parentheses) prior to bacteriologic sampling: ceftazi- in Table 3. Only one anaerobic organism was isolated
dime (n 5 67), aztreonam (n 5 16), ceftriaxone from the entire group of patients studied; Veillonella
(n 5 15), gentamicin (n 5 8), vancomycin (n 5 16), paravula was isolated from a blind PSB specimen in
and clindamycin (n 5 63). The 12 patients with a patient with suspected AP.
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 Discussion
diagnosed in 32 instances in which an antibiotic had
been given in the previous 24 h, compared with 31 Anaerobic bacteria are considered to be common
instances in which no antibiotic had been given (30 pulmonary pathogens, and they are believed to play
vs 39%, respectively; not significant). Similarly, in a major role in aspiration and nosocomial pneumo-
the group of patients with AP, a bacterial pathogen nia.8,23,25,32 These beliefs are based on a handful of
was isolated in five patients who had received a dose studies conducted in the 1970s, when transtracheal

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Table 2—Isolates Recovered From Patients With VAP gested that this low yield may be related to the fact
and AP that anaerobes are unlikely to survive in these solu-
VAP Isolates AP Isolates tions.27 Doré et al33 recently reported the results of
(n 5 74) (n 5 17) a study in which they performed bronchoscopically
P aeruginosa 16 — directed PSB sampling in patients with suspected
MSSS 15 2 VAP. Anaerobic transport broth and anaerobic cul-
Enterobacter spp 8 3 ture media were used to promote the recovery of
S pneumoniae 5 2
anaerobic bacteria. These authors recovered anaer-
MRSA 4 —
Streptococcus agalactiae 4 — obic bacteria in 23% of patients with VAP. The major
H influenzae 3 2 anaerobic strains that they isolated were Prevotella
Stenotrophomonas maltophilia 3 — melaninogenica, Fusobacterium nucleatum, and V
Acinetobacter baumannii 3 —
parvula. While Prevotella and Fusobacterium spp
Klebsiella pneumoniae 3 2
Escherichia coli 1 2 are regarded as pulmonary pathogens, Veillonella
Flavobacterium spp — 2 spp are considered to be nonpathogenic.34,35 The
Serratia sp 1 1 disparate finding between this study and our present
V paravula† — 1 study is unclear. On the day of the PSB sampling,
Other 8 —
47% of the patients in the study by Doré et al were
*MSSS 5 methicillin-sensitive S aureus; MRSA 5 methicillin-resis- receiving antimicrobial therapy, but none were re-
tant S aureus. ported to be receiving clindamycin. It is noteworthy
†Nonpathogenic anaerobe.
that 35% of the patients in whom these authors
isolated an anaerobe were receiving antibiotics at the
time of microbiologic sampling. The only apparent
aspiration was used for the collection of “uncontam- difference in study design is that the PSB sampling
inated” respiratory secretions 19 –22,32 Consequently, in our study was performed “blind” (nondirected),
antimicrobial agents with anaerobic coverage have while in the study by Doré et al, sampling was
been recommended in patients with aspiration pneu- performed through a bronchoscope. The dependent
monia and nosocomial pneumonia.7,8,23–25 The re- segments of the right lower lobe are predominantly
sults of our study question this common clinical involved in aspiration syndromes, and the blind
practice. Despite painstaking effort, we recovered technique will likely sample these segments.6,24,36
only a single nonpathogenic anaerobe from a diverse We and others have previously demonstrated an
population of hospitalized ICU patients with sus- excellent concordance between the two techniques
pected pneumonia. and this factor seems unlikely to account for the
A number of studies using bronchoscopically di- different findings.15,30,37
rected PSB sampling and anaerobic culture media Mier et al6 performed bronchoscopy and PSB
have failed to isolate anaerobic bacteria in patients sampling in a group of intubated ICU patients with
suspected to have VAP or have reported an inci- aspiration pneumonia. As in our study, anaerobic
dence of less than 2%.15–18 However, in all these transport media and strict anaerobic culture tech-
studies, physiologic saline solution or Ringer’s lactate niques were employed. These investigators failed to
was used as the transport media. It has been sug- isolate a single anaerobe; the spectrum of aerobic

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

No. of Patients* CAP‡ Bacterial Isolates (n 5 17)

Drug overdose 6 (1) 6 S aureus, V paravula†


Seizures 4 (2) 4 Enterobacter spp, H influenzae
Delirium tremens 5 (3) 4 S pneumoniae (2), H influenzae, S aureus, K pneumoniae
Small bowel obstruction 3 (3) 1 E coli (2), Enterobacter spp, Flavobacterium spp
Cerebrovascular accident 2 —
COPD/pneumonia 1 1
Congestive heart failure 1 1
Head injury 1 (1) — Serratia spp
Liver failure 1 (1) — K pneumoniae
Ileus post-bowel surgery 1 (1) — Flavobacterium spp, Enterobacter spp
*Number with bacterial pneumonia in parentheses.
†Nonpathogenic anaerobe.
‡CAP 5 community-acquired pneumonia. Aspiration pneumonitis suspected within 72 h of admission to hospital.

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organisms recovered was remarkably similar to that with anaerobic coverage may no longer be required
recovered in our study. The results of our study in the treatment of these patients. Furthermore,
differ markedly from the findings of Bartlett and penicillin G and clindamycin, the traditional antimi-
others, whose studies in the 1970s form the basis for crobials of choice in patients with AP, provide
current therapy.7,19 –25 These studies used transtra- inadequate antimicrobial coverage. A major limita-
cheal aspirates to obtain “uncontaminated” pulmo- tion of our study is that 35% of our patients had
nary secretions. It is possible that the organisms received an antibiotic with anaerobic activity in the
recovered by transtracheal aspiration represent oro- 24 h prior to microbiologic sampling. Furthermore,
pharyngeal flora that contaminated the trachea dur- it is possible that anaerobic bacteria were missed
ing the procedure (due to aspiration) or bacteria that during the sampling procedure or not identified by
have colonized the trachea, rather than representing culture grown out despite our rigorous efforts. We
true pulmonary pathogens. With PSB sampling, hope the findings of our study will spur clinical trials
however, uncontaminated lower respiratory tract examining the specific utility of adding anaerobic
secretions are obtained.28,38 This postulate is sup- drugs to the standard antibacterial regimens used in
ported by a study by Moser et al,26 who demon- patients with suspected VAP or aspiration pneumonia.
strated discrepancies between bacteria recovery by
ACKNOWLEDGMENT: The authors acknowledge with grati-
transtracheal aspiration and by transthoracic needle tude the excellent work done by the Respiratory Therapy De-
aspiration in dogs with experimental pneumonia. partment at St. Vincent Hospital and the CliniTech microbiology
Less than 50% of patients with either suspected technicians.
VAP or AP in our study had bacteriologically proven
infection. This observation has been well docu-
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