Anaerobe 18 (2012) 235e239

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Anaerobe
journal homepage: www.elsevier.com/locate/anaerobe

Clinical microbiology

Anaerobic bacterial infection of the lung

John G. Bartlett*
Johns Hopkins University, School of Medicine, 1830 East Monument Street, Rm 447, Baltimore, MD 21202, United States

a r t i c l e i n f o a b s t r a c t

Article history: Anaerobic bacteria are relatively frequent pathogens in pulmonary infections that are associated with
Received 5 September 2011 aspiration and its associated complications including aspiration pneumonitis, lung abscess, necrotizing
Received in revised form pneumonia and empyema. These conditions have been studied since the early 1900’s and substantial
5 December 2011
data with important clinical and microbiologic information are now readily available. However, the
Accepted 7 December 2011
Available online 27 December 2011
reports of these infections in the past 20 years have been sparse in number and much of the previous
information relevant to this topic seems much less visible or apparent. The purpose of this report is to
summarize the previous data and to celebrate the enormous contributions of Dr. Sydney Finegold to
Keywords:
Lung abscess
this topic.
Empyema Ó 2012 Published by Elsevier Ltd.
Aspiration pneumonia
Anaerobic pleuropulmonary disease

1. Introduction comprehensive report on the pathophysiology of lung abscess done

Anaerobic bacteria are frequent pathogens in pulmonary infec-
tions associated with aspiration and its complications including
aspiration pneumonitis, lung abscess, necrotizing pneumonia and
empyema. These conditions have been studied since the early
1900’s and substantial data with important clinical and microbio-
logic information are now readily available. However, reports of
these infections in the past 20 years have been sparse in number
and much of the previous information relevant to this topic seems
less visible or apparent. The purpose of this report is to summarize
the previous data and to celebrate the enormous contributions of
Dr. Sydney Finegold to this topic.
2. History
Some of the historical highlights of critical observations
regarding anaerobic bacterial infections of the lung and pleural
space are summarized in Table 1. The first apparent report on this
topic is the short review of “fetid infections” by Veillon published in
1893 [1]. A more comprehensive review of these infections is the
report of 14 cases of patients with empyema involving anaerobes by
Guillemot et al. in 1904 [2]. Perhaps the most comprehensive report
in the pre-penicillin era was by David Smith from Duke who auth-
ored several papers dealing with Fuso-spirochetal diseases of the
lungs in the period 1927e30. The most important of these was the
* Tel.: þ1 410 955 7634; fax: þ1 410 614 8488.
E-mail address: jb@jhmi.edu.
in experimental animals including mice, guinea pigs, rabbits and
dogs [3]. This investigator noted that the bacteria observed in lung
abscess cases at autopsy resembled those in the gingival crevice, and
he postulated aspiration as the mechanism of infection at a time
when contagion was the presumed cause of most infections. The
study involved a tracheal challenge with gingival crevice bacteria
including four anaerobic species: “spirochetes, fusiform bacilli,
anaerobic streptococci and vibrios.” It was noted that three or all
four microbes were required to produce a typical lung abscess in the
experimental animals. Further, cultures of the lung yielded mixed
growth of spirochetes, fusiforms bacilli and streptococci that were
readily apparent on stain and with anaerobic culture. This is one of
the very early studies of bacterial synergy, and to our knowledge, the
first to define the pathophysiology of primary lung abscess.
The next important contribution in studies of these infections
was the description of transtracheal aspiration by Pecora et al. [4] in
1962. Their report did not use anaerobic culture techniques, but
provided a method to bypass the upper airways to obtain an
uncontaminated specimen from the lower respiratory tract that
eventually proved vital in studies of the bacteriology of pulmonary
infections, particularly those involving anaerobic bacteria.
The first publication with a PubMed search for “anaero-
bes þ lung” is a comprehensive review of 70 cases from Wadsworth
Hospital and a literature review and compilation of 348 cases in the
literature through 1970 which was published in 1972 [5]. This
report emphasized the frequency of lung abscess, necrotizing
pneumonia and lung infections complicated by empyema as the
dominant clinical categories.

1075-9964/$ e see front matter Ó 2012 Published by Elsevier Ltd.

doi:10.1016/j.anaerobe.2011.12.004
236 J.G. Bartlett / Anaerobe 18 (2012) 235e239
Table 1
Historic highlights.
Year Highlight
1893 1st report e Veillon [1]
1904 1st comprehensive report (14 cases of
putrid empyema) e Guillemot et al. [2]
1927 Reproduction of aspiration pneumonia with
progression to abscess using inoculation of
gingival crevice bacteria e Smith [3]
1962 Description of transtracheal aspiration as
a method to obtain uncontaminated pulmonary
secretions e Pecora et al. [4]
1972 Description of 70 cases of anaerobic
pleuropulmonary infection e Bartlett and Finegold [5]
1983 Randomized trial showing utility of
clindamycin vs. penicillin for putrid lung
abscess e Levison et al. [6]
With regard to treatment, there were relatively few formal
studies of various antibacterial agents for patients with anaerobic
lung infections, possibly related to the difficulty of obtaining valid
specimens for meaningful anaerobic culture. Perhaps the most
outstanding contribution in terms of study design and meaningful
conclusions that had substantial impact on the field was the
comparative trial of penicillin vs. clindamycin in the treatment of
lung abscess involving anaerobic bacteria by Levison et al. [6]. This
showed clindamycin was clearly superior to penicillin despite the
fact that penicillin was generally regarded as the preferred drug for
the previous three decades. A subsequent randomized trial
comparing clindamycin vs. penicillin in 37 patients with lung abscess
or necrotizing pneumonia showed almost identical results [7].
3. Pathophysiology
The usual source of anaerobic bacteria causing lung infections is
the oral cavity especially the gingival crevice based on the previously
reviewed data from D.T. Smith [3]. This is an area where the
concentrations of anaerobic bacteria approach the geometric limits
with which bacteria occupy space, about 1012/gm [8]. Most of the
patients have a condition that predisposes to aspiration as a result
of reduced consciousness or dysphagia [9,10]. Thus, common ante-
cedent events or populations include illicit drug abuse, alcohol abuse,
seizures, anesthesia, esophageal lesions, neurologic disorders
resulting in compromised consciousness or dysphagia, etc. The usual
segments involved are those that are dependent in the recumbent
position which include the superior segments of the lower lobes and
posterior of the upper lobes. Aspiration in the upright position favors
the lower lobes. Other predisposing conditions include obstructing
lesions such as tumors, or foreign bodies such as the aspirated peanut.
4. Clinical features
The first stage of this infection is pneumonitis that may be acute,
subacute or chronic. This is one form of “aspiration pneumonia”
which represents one of the three commonly recognized forms of
“aspiration pneumonia.” (The other two are foreign body aspiration
resulting in obstruction and aspiration of gastric acid resulting in
the equivalent of a chemical burn of the lung, so nicely described by
Mendelson [10,11]).
The subsequent evolution of studies of this pulmonary infection
is highly variable, but a characteristic feature in many cases is tissue
necrosis resulting in lung abscess, necrotizing pneumonia or an
empyema. According to the previously noted studies by Smith [3]
necrosis with abscess formation usually requires 6e7 days after
the bacterial challenge. Note that patients seen before this time will
present with a pulmonary infiltrate, usually in a dependent
pulmonary segment, and they may appear much like other patients
with community-acquired pneumonia [12,13]. Comparisons of 46
patients with pneumonitis caused by anaerobic bacteria established
by transtracheal aspiration were compared to 46 with pneumo-
coccal pneumonia. This showed similar clinical features including
fever, leukocytosis and pulmonary infiltrates. Differences were that
those with anaerobic pneumonitis were less acutely ill, they did not
have a shaking chill and 20% subsequently had pulmonary abscesses.
Most patients present for clinical care later in the disease course
when they have advanced to the suppurative complications char-
acterized as primary lung abscess, necrotizing pneumonia or an
empyema secondary to a bronchopleural fistula [10]. Characteristic
features of these infections are the necrosis of tissue, chronicity of
the course, the common antecedent event or typical risk for aspi-
ration in the host and putrid drainage which is generally considered
diagnostic of infections involving anaerobes. Some of the clinical
features are summarized in Table 2 which includes 193 patients
with anaerobic lung infections. The composite findings include an
antecedent predisposition to aspiration and typical clinical features
of pneumonitis. The features that specifically suggest involvement
with anaerobic bacteria include the predisposition to aspiration,
the rather chronic course of most of these infections, pulmonary
necrosis, and/or putrid sputum, breath or empyema fluids.
It should be emphasized that anaerobes are now forgotten
potential pathogens in pulmonary infection, both community-
acquired and nosocomial pneumonia. Most are not acknowledged
as important pathogens in contemporary guidelines on community-
acquired pneumonia, no diagnostic studies are recommended to
detect them and treatment guidelines ignore them [14]. It is not
clear that this is wrong, since the guidelines are based on clinical
response data from the Medicare database with over 13,000 records
from CAP patients. Nevertheless, there are clinical settings that in
which anaerobes are clearly important. The clinical clues that
specifically suggest anaerobic infection are pulmonary with:
1) Putrid discharge (sputum, pleural fluid, breath); 2) Infection
associated with aspiration that is often presumed based on predis-
position to aspiration and imaging showing infection in a dependent
segment and 3) Infection associated necrosis of tissue with abscess
formation, necrotizing pneumonia or a bronchopleural fistula
underlying an empyema.
Recovery rates of anaerobic bacteria in selected syndromes are
summarized in Table 3. This review is limited to cases for the
designated category in which specimens devoid of upper airway
contamination (see below) were used and anaerobic cultures were
done. No attempt was made to evaluate the quality of the anaerobic
microbiology, and it was not always clear that he microbiology
specimens were obtained before antibiotic treatment.
5. Specimen sources
Diagnostic studies for the etiology of all forms of common
pulmonary infections have become uncommon in contemporary
Table 2
Clinical features of pulmonary infections involving anaerobic bacteriaa.
Numberb Pneumonitis 79 Abscess 83 Empyema 51 Total 213
Age (yrs) 60 52 49 51
Peak fever ( F) 102.6 102.1 102.4 102.4
WBC ( 1000/mL) 13.7 15.0 21.6 15.0
Duration six (days) 3 14 15 7
Weight loss (Yes) 3% 43% 55% 30%
Putrid discharge 4% 49% 63% 32%
Mortality 4% 4% 6% 4%
a
Categories are mutually exclusive.
b
All figures are median values.
 J.G. Bartlett / Anaerobe 18 (2012) 235e239 237

Table 3 sputum specimen in a tea strainer and then washing it with a jet of
Microbiology of lung abscess aspiration and empyema. tap water could reduce contaminants in the salivary envelope of the
Condition Frequency expectorated specimen by 100e1000-fold; it was also shown that
Lung abscess AnO2/total pts combining the wash procedure with quantitation produced good
Bartlett, 1993 [10] 53/57 (93%) results. The problem was that microbiologists found the procedure
Beerens, 1965 [15] 22/26 (85%) unacceptable due to the widespread contamination from the wash
Brook, 1979 [16] 9/10 (90%)
procedure and the tedious requirement for quantitation. More
Guidol, 1990 [7] 37/41 (90%)
Wang [17] 18/46 (39%)a recently, Hunter et al. [42] used gas liquid chromatography to
De `[18] 13/13 (100%) detect the characteristic volatile fatty acids of anaerobic bacteria in
Mori, 1993 [19] 24/55 (45%) healthy persons and those with lung disease. The results showed 7
Takayanagi [20] 32/122 (26%) of 83 specimens had GLC patterns indicating the presence of
Aspiration pneumonia anaerobic bacteria in high concentration. These 7 specimens were
Bartlett, 1979 [13] 61/70 (87%) obtained from 11 patients with either pulmonary abscess or
Gonzalez, 1975 [21] 17/17 (100%)
empyemas, and no positive results were obtained in 72 patients
Lorber, 1974 [22] 29/47 (62%)
Brook, 1980 [23] 69/74 (93%) with other conditions [27]. This suggested efficacy with this rather
Tokuyasu, 2010 [24] 16/38 (50%) simple method, but there were no follow-up studies after the initial
report in 1985.
Empyema
Bartlett, 1974 [25] 63/83 (76%) My impression is that pleural fluid and transthoracic needle
Beerens, 1965 [15] 23/45 (51%) aspiration remain possibly the only specimen sources that are
Sullivan, 1973 [26] 42/482 (9%) currently available for meaningful anaerobic culture in patients
Varkey, 1981 [28] 28/72 (39%)
with pulmonary infections since transtracheal aspirations are no
Mavroudis, 1981 [28] 25/100 (25%)
Grant, 1985 [29] 26.90 (29%)
longer done, fiberoptic bronchoscopy specimens are rarely handled
Lammer, 1985 [30] 20/70 (29%) in the appropriate fashion and the GLC method has not been vali-
Boyanova, 2004 [31] 146/198 (74%) dated. The newer molecular techniques and antigen detection
Brook 1993 [32] 70/197 (36%) methods used to identify pathogens in pulmonary infections seem
Meskell 2006 [33] 67/336 (20%)
unlikely to be applicable to anaerobic infections where specimens
a
Klebsiella pneumoniae accounted for 21%, which appears to be a well estab- are almost invariably associated with contamination [34]. The
lished, poorly understood microbiological pattern for lung abscesses in patients
exception is pleural fluid. A recent report from Japan used analysis
from Taiwan.
of pleural fluid specimens from 42 febrile patients and applied
a clone library method using amplified fragments of the 16S ribo-
medicine so that empiricism now reigns as the management somal RNA gene with universal primers [43]. The specimens were
standard even by the IDSA/ATS Guidelines [14]. The important also cultured using conventional anaerobic and aerobic methods.
advance that is anticipated to correct this relies on molecular Of the 42 specimens, 16 amplified 16S rDNA and 7 (43%) of these
diagnostics or antigen detection using nasopharyngeal swabs or indicated anaerobes including 6 that were not detected by routine
expectorated sputum as samples, which will not be applicable to cultivation. The authors concluded that their results show anaer-
anaerobes [34]. It has never been easy to get specimens from obes are more frequent in pleural fluid samples than found with
patients with pulmonary infections that are valid for meaningful conventional cultures. Given the impracticality of this method, it
anaerobic culture due to the contamination resulting from passage appears that recognition of anaerobic pulmonary infections in the
through the upper airways. The notable exception is empyema absence of empyema will generally require clinical skills that define
fluid, but for infections restricted to the lung parenchyma, the this probability.
methods that have been used historically to confirm the diagnosis
include transtracheal aspiration [35], fiberoptic bronchoscopy with 6. Microbiology
quantitation using the protected brush [36] or BAL and trans-
thoracic needle aspiration [7,15]. Microbiology results for anaerobic bacteria are summarized in
Transtracheal aspiration was done extensively in studies of Table 4 which combines reports from two large studies with
anaerobic pulmonary infections in the 1970’s and early 1980’s, but a combined total of nearly 400 cases and over 1000 anaerobic
the technique has subsequently been almost completely excluded isolates [9,44]. The major organisms identified in these infections
from medical practice due to concerns about patient safety [37] and
patient acceptance. With regard to bronchoscopy, the usual
methods are inadequate for valid anaerobic culture due to instru-
Table 4
ment contamination that inevitably yields large concentrations of Bacteriology of anaerobic pulmonary infections.
oral flora [38]. The double lumen catheter with a distal plug was
Bartlett [9] Finegold [44]
developed using an in vitro testing of various catheter designs by
filling of the inner channel with saliva and obtaining the culture Period reviewed 1968e75 1975e85
No. of cases 193 196
with a marker organism (Serratia marcescens) [39]. The conclusion Total anaerobes 461 656
from this work was that the double catheter and quantitative Bacteroides
cultures were required and that the lidocaine used for topical B. melaninogenicus 76 46
anesthesia had antibacterial properties that made rapid culturing B. intermedius e 60
B. urealyticus e 18
important [40]. The results of this work resulted in the final product
Bacteroides (other) 75 180
that is now commercially available and has been tested in patients F. nucleatum 56 58
with good results [36]. Quantitative culture with broncho-alveolar Peptostreptococcus 87 66
lavage (BAL) may be successful in defining the role of anaerobes in GPC (other) e 39
the lower airways, but there are no published data to support this. Gram pos bacilli
Clostridia 18 20
Expectorated sputum has been tested using a wash and quan- Other 50 146
titative method [41]. This work showed that placing a purulent
238 J.G. Bartlett / Anaerobe 18 (2012) 235e239
are recognized as the “big three”: Bacteroides melaninogenicus,
Fusobacterium nucleatum and anaerobic Streptococci. Many of these
infections are mixed, and the predominant non-anaerobes are
microaerophilic streptococci. Earlier studies had relatively high
yields of Bacteroides fragilis, but some of these were probably
erroneously identified since B. fragilis has been rare in the more
recent reports.
7. Treatment
The major issues are antibiotic selection and adequate drainage
of empyemas. With regard to antibiotic selection, clindamycin has
been a favored drug for treatment of anaerobic pulmonary infec-
tions since the previously cited comparative trial by Levison et al.
[6] This trial was subsequently confirmed by another comparative
trial by Gudiol et al. [7] that also demonstrated the superiority of
clindamycin vs. penicillin in patients with lung abscess. These trials
show the recipients of clindamycin had higher cure rates, reduced
duration of fever and reduced duration of putrid sputum. The
published experience with clindamycin for aspiration pneumonia
and lung abscess is robust and supportive [45,46].
Betalactamebetalactamase inhibitor combinations also show
appropriate in vitro activity and had done well in clinical trials with
both oral [47] and parenteral formulations [48]. A randomized
comparative clinical trial of ampicillin/sulbactam vs. clindamycin in
70 patients with aspiration pneumonia or lung abscess showed
similar clinical and microbiologic responses [45]. A non-
comparative trial with amoxicillin-clavulanate proved uniformly
successful in 40 patients with lung abscess [47].
More recent studies with moxifloxacin have shown good results
in anaerobic pulmonary infections compared to clindamycin [48]
and to ampicillin/sulbactam [49]. As expected carbapenems are
also effective. One anecdotal report showed a good outcome in
a prospective study of meropenem for 62 elderly patients (mean
age 86.6 years) [50].
Metronidazole performs poorly in pulmonary infections despite
an extraordinary record in the treatment of anaerobes at other
anatomical sites. One comparative trial with clindamycin had to be
discontinued when 4 of 6 patients with lung abscess or necrotizing
pneumonia failed metronidazole [51]. Another trial showed treat-
ment failures in 5 of 11 patients with anaerobic lung abscess [52].
The presumed explanation is the lack of activity vs. aerobic and
microaerophilic streptococci. If accurate, this could easily be cor-
rected by adding a betalactam. Other agents have good in vitro
activity vs. oral anaerobes, but limited published experience in
bacteriologically confirmed cases. These include tigecycline, cef-
triaxone, ceftaroline and azithromycin [53e55].
8. Summary
Pulmonary infections frequently involve anaerobic bacteria,
presumably as a result of aspiration. It is probable that the great
majority are not recognized as anaerobic infections but respond to
the empiric treatment used for community-acquired pneumonia.
Clinical features that distinguish these infections in some cases are
an associated condition that predisposes to aspiration, infection in
a dependent segment, indolent course and late complications that
include lung abscess, necrotizing pneumonia, empyema and putrid
discharge. The microbiologic diagnosis requires a specimen that is
devoid of upper airway flora coupled with good anaerobic micro-
biology. The preferred treatment consists of drugs that are effective
against anaerobes and have clinical trials to support efficacy e
clindamycin, a betalactam/betalactamase combination or a carba-
penem. Empyemas require drainage. Recognition of anaerobic
infections in the lung appear to have hit a zenith in the period
1972e1985 and recognition is now rare.
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