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Anaerobe 18 (2012) 235e239

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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
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

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

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

236 J.G. Bartlett / Anaerobe 18 (2012) 235e239

Table 1 pulmonary segment, and they may appear much like other patients
Historic highlights. with community-acquired pneumonia [12,13]. Comparisons of 46
Year Highlight patients with pneumonitis caused by anaerobic bacteria established
1893 1st report e Veillon [1] by transtracheal aspiration were compared to 46 with pneumo-
1904 1st comprehensive report (14 cases of coccal pneumonia. This showed similar clinical features including
putrid empyema) e Guillemot et al. [2] fever, leukocytosis and pulmonary infiltrates. Differences were that
1927 Reproduction of aspiration pneumonia with
those with anaerobic pneumonitis were less acutely ill, they did not
progression to abscess using inoculation of
gingival crevice bacteria e Smith [3] have a shaking chill and 20% subsequently had pulmonary abscesses.
1962 Description of transtracheal aspiration as Most patients present for clinical care later in the disease course
a method to obtain uncontaminated pulmonary when they have advanced to the suppurative complications char-
secretions e Pecora et al. [4] acterized as primary lung abscess, necrotizing pneumonia or an
1972 Description of 70 cases of anaerobic
pleuropulmonary infection e Bartlett and Finegold [5]
empyema secondary to a bronchopleural fistula [10]. Characteristic
1983 Randomized trial showing utility of features of these infections are the necrosis of tissue, chronicity of
clindamycin vs. penicillin for putrid lung the course, the common antecedent event or typical risk for aspi-
abscess e Levison et al. [6] 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 regard to treatment, there were relatively few formal with anaerobic lung infections. The composite findings include an
studies of various antibacterial agents for patients with anaerobic antecedent predisposition to aspiration and typical clinical features
lung infections, possibly related to the difficulty of obtaining valid of pneumonitis. The features that specifically suggest involvement
specimens for meaningful anaerobic culture. Perhaps the most with anaerobic bacteria include the predisposition to aspiration,
outstanding contribution in terms of study design and meaningful the rather chronic course of most of these infections, pulmonary
conclusions that had substantial impact on the field was the necrosis, and/or putrid sputum, breath or empyema fluids.
comparative trial of penicillin vs. clindamycin in the treatment of It should be emphasized that anaerobes are now forgotten
lung abscess involving anaerobic bacteria by Levison et al. [6]. This potential pathogens in pulmonary infection, both community-
showed clindamycin was clearly superior to penicillin despite the acquired and nosocomial pneumonia. Most are not acknowledged
fact that penicillin was generally regarded as the preferred drug for as important pathogens in contemporary guidelines on community-
the previous three decades. A subsequent randomized trial acquired pneumonia, no diagnostic studies are recommended to
comparing clindamycin vs. penicillin in 37 patients with lung abscess detect them and treatment guidelines ignore them [14]. It is not
or necrotizing pneumonia showed almost identical results [7]. clear that this is wrong, since the guidelines are based on clinical
response data from the Medicare database with over 13,000 records
3. Pathophysiology from CAP patients. Nevertheless, there are clinical settings that in
which anaerobes are clearly important. The clinical clues that
The usual source of anaerobic bacteria causing lung infections is specifically suggest anaerobic infection are pulmonary with:
the oral cavity especially the gingival crevice based on the previously 1) Putrid discharge (sputum, pleural fluid, breath); 2) Infection
reviewed data from D.T. Smith [3]. This is an area where the associated with aspiration that is often presumed based on predis-
concentrations of anaerobic bacteria approach the geometric limits position to aspiration and imaging showing infection in a dependent
with which bacteria occupy space, about 1012/gm [8]. Most of the segment and 3) Infection associated necrosis of tissue with abscess
patients have a condition that predisposes to aspiration as a result formation, necrotizing pneumonia or a bronchopleural fistula
of reduced consciousness or dysphagia [9,10]. Thus, common ante- underlying an empyema.
cedent events or populations include illicit drug abuse, alcohol abuse, Recovery rates of anaerobic bacteria in selected syndromes are
seizures, anesthesia, esophageal lesions, neurologic disorders summarized in Table 3. This review is limited to cases for the
resulting in compromised consciousness or dysphagia, etc. The usual designated category in which specimens devoid of upper airway
segments involved are those that are dependent in the recumbent contamination (see below) were used and anaerobic cultures were
position which include the superior segments of the lower lobes and done. No attempt was made to evaluate the quality of the anaerobic
posterior of the upper lobes. Aspiration in the upright position favors microbiology, and it was not always clear that he microbiology
the lower lobes. Other predisposing conditions include obstructing specimens were obtained before antibiotic treatment.
lesions such as tumors, or foreign bodies such as the aspirated peanut.
5. Specimen sources
4. Clinical features
Diagnostic studies for the etiology of all forms of common
The first stage of this infection is pneumonitis that may be acute, pulmonary infections have become uncommon in contemporary
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 Table 2
Clinical features of pulmonary infections involving anaerobic bacteriaa.
resulting in obstruction and aspiration of gastric acid resulting in
the equivalent of a chemical burn of the lung, so nicely described by Numberb Pneumonitis 79 Abscess 83 Empyema 51 Total 213
Mendelson [10,11]). Age (yrs) 60 52 49 51
The subsequent evolution of studies of this pulmonary infection Peak fever ( F) 102.6 102.1 102.4 102.4
WBC ( 1000/mL) 13.7 15.0 21.6 15.0
is highly variable, but a characteristic feature in many cases is tissue
Duration six (days) 3 14 15 7
necrosis resulting in lung abscess, necrotizing pneumonia or an Weight loss (Yes) 3% 43% 55% 30%
empyema. According to the previously noted studies by Smith [3] Putrid discharge 4% 49% 63% 32%
necrosis with abscess formation usually requires 6e7 days after Mortality 4% 4% 6% 4%
the bacterial challenge. Note that patients seen before this time will a
Categories are mutually exclusive.
present with a pulmonary infiltrate, usually in a dependent 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.
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
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, infections in the lung appear to have hit a zenith in the period
Fusobacterium nucleatum and anaerobic Streptococci. Many of these 1972e1985 and recognition is now rare.
infections are mixed, and the predominant non-anaerobes are
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