Annals of Otology, Rhinology & Laryngology 120(11):707-712.

2011 Annals Publishing Company. All rights reserved.

Microbiology of Acute and Chronic Maxillary Sinusitis

in Smokers and Nonsmokers
Itzhak Brook, MD, MSc; Jeffrey N. Hausfeld, MD
Objectives: We evaluated the microbiology of sinus aspirates of smokers and nonsmokers with acute and chronic maxillary sinusitis.

Methods: Cultures were obtained from 458 patients, 244 (87 smokers and 157 nonsmokers) of whom had acute maxillary sinusitis and 214 (84 smokers and 130 nonsmokers) of whom had chronic maxillary sinusitis, between 2001 and
2007.

Results: A greater number of Staphylococcus aureus, methicillin-resistant S aureus (MRSA), and beta-lactamaseproducing bacteria (BLPB) were found in the 87 smokers with acute sinusitis than in the nonsmokers with acute sinusitis (p
< 0.005, p < 0.025, and p < 0.05, respectively). A greater number of these organisms were found in the 84 smokers with
chronic sinusitis than in the nonsmokers (p < 0.01, p < 0.025, and p < 0.001, respectively). Eighty-five BLPB isolates
were recovered from 73 patients (30%) with acute sinusitis. These included Moraxella catarrhalis, S aureus, Haemophilus influenzae, Prevotella spp, and Fusobacterium spp; 40 BLPB isolates were found in smokers, and 45 in nonsmokers
(p < 0.05). One hundred twenty-five BLPB isolates were recovered from 91 patients (43%) with chronic sinusitis, including M catarrhalis, Bacteroides fragilis group, S aureus, H influenzae, Prevotella spp, and Fusobacterium spp; 69 BLPB
isolates were found in smokers, and 56 in nonsmokers (p < 0.001). Antimicrobial therapy had been administered in the
past month to 130 patients (28%; 60 smokers and 70 nonsmokers; p < 0.025). Both MRSA and BLPB were isolated more
often from these individuals (p < 0.025). However, the higher isolation rates of MRSA and BLPB in smokers were independent of previous antimicrobial therapy.
Conclusions: These data illustrate a greater frequency of isolation of S aureus, MRSA, and BLPB in patients with acute
and chronic sinusitis who smoke.
Key Words: beta-lactamase, methicillin resistance, sinusitis, smoking, Staphylococcus aureus.

ington, DC. The patients were consecutively seen in

the outpatient clinic between January 1, 2001, and
January 1, 2007, and had a diagnosis of acute or
chronic bacterial maxillary sinusitis.

INTRODUCTION

Smoking has a significant impact on the oropharyngeal bacterial flora of children, as well as adults.1
Active smokers and those exposed to secondhand
smoke are at increased risk of bacterial infections
such as sinusitis,2 tuberculosis, pneumonia, and legionnaires disease; bacterial vaginosis and sexually
transmitted diseases; Helicobacter pylori infection;
periodontitis; meningitis; otitis media; and postsurgical and nosocomial infections.3

The patients with acute infection had symptoms

that had lasted between 10 and 30 days, and those
with chronic infection had had symptoms for more
than 90 days. None of those with chronic sinusitis
had had previous sinus surgery. Smokers were defined as individuals who had smoked at least 10 cigarettes a day for the past 5 years. The determination
was based on the patients own history.

No previous study has compared the microbiology of sinus aspirates obtained from smokers to that
of those obtained from nonsmokers. This retrospective study evaluated the microbiology of sinus aspirates of smokers and nonsmokers who had acute or
chronic maxillary sinusitis.

The patients complaints included facial pain,

frontal headache, purulent nasal discharge, fever,
and malaise. Radiography with occipitomental (Waters view), lateral, oblique, and verticomental views
or computed tomography was performed. Sinusitis was defined radiographically as complete sinus
opacity, ie, an air-fluid level or mucous membrane
thickening of at least 6 mm in the maxillary sinus.

PATIENTS and METHODS

The population studied was a middle-class one residing in suburban locations in the vicinity of Wash-

From the Department of Pediatrics, Georgetown University School of Medicine, Washington, DC.
Correspondence: Itzhak Brook, MD, MSc, 4431 Albemarle St NW, Washington, DC 20016.

707

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Brook & Hausfeld, Smoking & Sinusitis

For the Waters view, mucosal thickening of the maxillary sinuses was measured as the shortest distance
from the air-mucosal interface to the most lateral
part of the maxillary sinus wall. Specimens were obtained through endoscopy, and the sinus secretions
were collected with calcium alginatetipped microswabs. The study was granted Institutional Review
Board approval.

Cultures were obtained endoscopically before

therapy with calcium alginate swabs that were immediately plated into media supportive of the growth of
aerobic and anaerobic bacteria. The methods of specimen collection, transportation, and microbiological
evaluation were previously described.4 Specimens
were processed semiquantitatively, and organisms
were identified by standard methods.5 Beta-lactamase activity was determined by use of the chromogenic cephalosporin analog 87/312 method.6
Staphylococcus aureus isolates were screened
for oxacillin resistance by the Clinical Laboratory
Standard Institute disk diffusion method.7 Overnight cultures from blood agar plate were suspended
in Mueller-Hinton broth to the turbidity of 0.5 McFarland and plated on Mueller-Hinton agar, and a
1-g oxacillin disc was placed with the inoculum.
Zone diameters were measured and recorded after
a 24-hour incubation at 35C (susceptible, equal to
or less than 13 mm; intermediate, between 11 and
12 mm; and resistant, equal to or less than 10 mm).
Methicillin-resistant S aureus (MRSA) strains were
not typed.

All isolates of Streptococcus pneumoniae were

screened for penicillin susceptibility with a 1-g oxacillin disk by the Kirby-Bauer disk diffusion method. Intermediate resistance to penicillin was defined
as a minimal inhibitory concentration of 0.1 to 1.0
g/mL, and high resistance to penicillin was defined
as a minimal inhibitory concentration of at least 2.0
g/mL.
Included in the final analysis were only patients
whose culture showed bacterial growth. Statistical
significance was calculated by Fishers exact test
(2-sided) unadjusted.
RESULTS

We evaluated 458 patients (244 with acute and

214 with chronic maxillary sinusitis) after exclusion
of an additional 110 patients (62 with acute and 48
with chronic sinusitis) whose culture did not show
any bacterial growth. The patients ages ranged from
18 to 75 years (mean, 42 years 4 months); 265 were
male. No differences were noted in the age distribution, ethnicity, or gender of the patients.

708

TABLE 1. BACTERIOLOGY OF 244 PATIENTS WITH

ACUTE MAXILLARY SINUSITIS

Smokers Nonsmokers Total
Bacteria
(N = 87) (N = 157) (N = 244)
Aerobic bacteria
-Hemolytic streptococci 4
9
13
Streptococcus pneumoniae 25
54
79
Intermediate resistance 7
8
15
to penicillin
High resistance to
3
4
7
penicillin
Group F streptococcus
2
4
6
Streptococcus pyogenes
4
7
11
Staphylococcus aureus 8* (6)
4 (3)
12 (9)
(methicillin-resistant)
Staphylococcus aureus 7 (4)
4 (1)
11 (5)
(methicillin-sensitive)
Staphylococcus
4 (2)
4 (1)
8 (3)
epidermidis
Haemophilus influenzae 16 (9)
37 (8)
53 (17)
Moraxella catarrhalis 15 (15)
29 (29)
44 (44)
Klebsiella pneumoniae
2
1
3
Pseudomonas aeruginosa 1
1
2
Proteus mirabilis
2
1
3
Escherichia coli
1
1
Subtotal aerobes
90 (36) 156 (42)
246 (78)
Anaerobic bacteria
Peptostreptococcus spp
6
15
21
Veillonella parvula
2
2
Eubacterium spp
1
2
3
Propionibacterium acnes 2
3
5
Fusobacterium spp
1 (1)
2
3 (1)
Fusobacterium nucleatum
2 (1)
2 (1)
Bacteroides spp
1 (1)
1
2 (1)
Prevotella
2 (1)
2 (1)
4 (2)
melaninogenica
Prevotella oralis
2 (1)
2 (1)
Prevotella oris-buccae
2 (1)
2 (1)
Prevotella intermedia
2
2
Porphyromonas
1
2
3
asaccharolytica
Subtotal anaerobes
18 (4)
33 (3)
51 (7)
Total
108 (40) 189 (45)
297 (85)

Numbers within parentheses indicate number of beta-lactamase

producing bacteria.
*Difference between smokers and nonsmokers, p < 0.025.
Difference between smokers and nonsmokers, p < 0.05.

Acute Sinusitis. Of the 244 patients, 87 were

smokers and 157 were nonsmokers. A total of 297
isolates were recovered (1.2 per specimen): 246 aerobic and facultative (1.0 per specimen) and 51 anaerobic (0.2 per specimen; Table 1). The number of
isolates varied from 1 to 3. Antimicrobial therapy
was administered to 45 patients (24%) in the month
before sample collection.
Aerobic and facultative organisms only were re-

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Brook & Hausfeld, Smoking & Sinusitis

covered in 213 instances (87%), anaerobes only

were recovered in 15 (6%), and mixed aerobic and
anaerobic bacteria were recovered in 16 (7%). The
predominant aerobic bacteria were S pneumoniae
(79 isolates; 15 were intermediately resistant and 7
highly resistant to penicillin), Haemophilus influenzae (53), Moraxella catarrhalis (44), and S aureus
(23, including 12 that were methicillin-resistant; Table 1).
The predominant anaerobes were gram-negative
bacilli (15 isolates, including 10 Prevotella, 3 Porphyromonas spp, and 2 Bacteroides spp), Peptostreptococcus spp (21), and Fusobacterium spp (5).
Eighty-five beta-lactamaseproducing bacteria
(BLPB) were recovered from 73 patients (30%; Table 1). These included all 44 M catarrhalis isolates,
14 of the 23 (61%) S aureus isolates, 17 of the 53
(32%) H influenzae isolates, 4 of the 10 (40%) Prev
otella spp isolates, and 2 of the 5 (40%) Fusobacterium spp isolates. Forty BLPB isolates were found
in smokers, and 45 in nonsmokers (p < 0.05).
A greater number of S aureus, MRSA, methicillin-sensitive S aureus, and BLPB isolates were
found in smokers than in nonsmokers (p < 0.005, p
< 0.025, p < 0.05, and p < 0.05, respectively; Table
1). No other differences were noted in the recovery
of isolates between smokers and nonsmokers.
Chronic Sinusitis. Of the 214 patients, 84 were
smokers and 130 were nonsmokers. A total of 591
isolates were recovered (2.8 per specimen): 211 aerobic and facultative (1.0 per specimen) and 380 anaerobic (1.8 per specimen; Table 2). The number of
isolates varied from 1 to 5. Antimicrobial therapy
was administered to 85 patients (40%) in the month
before sample collection.
Aerobic and facultative organisms only were recovered in 42 instances (19%), anaerobes only in 59
(28%), and mixed aerobic and anaerobic bacteria
were recovered in 113 (52%). The predominant aerobic bacteria were S aureus (38 isolates, including
18 that were methicillin-resistant), microaerophilic
streptococci (22), M catarrhalis (16), H influenzae
(13), S pneumoniae (10 isolates, 3 of which were
intermediately resistant and 2 of which were highly resistant to penicillin), Proteus mirabilis (12),
Pseudomonas aeruginosa (11), Klebsiella pneumoniae (10), and Escherichia coli (7; Table 2).
The predominant anaerobes were gram-negative
bacilli (157 isolates, including 100 Prevotella spp,
28 Porphyromonas asaccharolytica, and 15 Bacteroides fragilis group), Peptostreptococcus spp (118),
and Fusobacterium spp (57).

709

TABLE 2. BACTERIOLOGY OF 214 PATIENTS

WITH CHRONIC MAXILLARY SINUSITIS

Smokers Nonsmokers Total
Bacteria
(N = 84) (N = 130) (N = 214)
Aerobic bacteria
-Hemolytic streptococci 14
21
35
Microaerophilic
8
14
22
streptococci
Streptococcus pneumoniae 4
6
10
Intermediate resistance 2
1
3
to penicillin
High resistance to
1
1
2
penicillin
Group F streptococcus
2
7
9
Group G streptococcus
3
4
7
Streptococcus pyogenes
5
7
12
Staphylococcus aureus 13* (8)
5 (1)
18 (9)
(methicillin-resistant)
Staphylococcus aureus 11 (9)
9 (3)
20 (12)
(methicillin-sensitive)
Staphylococcus
4 (2)
4 (1)
8 (3)
epidermidis
Haemophilus influenzae 5 (3)
8 (6)
13 (9)
Moraxella catarrhalis
6 (6)
10 (10)
16 (16)
Klebsiella pneumoniae
5
5
10
Pseudomonas aeruginosa 4
7
11
Proteus mirabilis
5
7
12
Escherichia coli
3
4
7
Subtotal aerobes
93 (28*) 118 (21)
211 (49)
Anaerobic bacteria
Peptostreptococcus spp
44
74
118
Veillonella parvula
4
11
15
Eubacterium spp
3
6
9
Propionibacterium acnes 11
13
24
Fusobacterium spp
10 (4)
12 (4)
22 (8)
Fusobacterium nucleatum 15 (7)
20 (5)
35 (12)
Bacteroides spp
5 (1)
9 (3)
14 (4)
Bacteroides fragilis group 5 (5)
10 (10)
15 (15)
Prevotella
13 (8)
15 (3)
28 (11)
melaninogenica
Prevotella oralis
7 (3)
11 (2)
18 (5)
Prevotella oris-buccae 11 (2)
13 (2)
24 (4)
Prevotella intermedia
10 (5)
20 (2)
30 (7)
Porphyromonas
12 (6)
16 (4)
28 (10)
asaccharolytica
Subtotal anaerobes
150 (41) 230 (35)
380 (76)
Total
243 (69) 348 (56) 591 (125)

Numbers within parentheses indicate number of beta-lactamase

producing bacteria.
*Difference between smokers and nonsmokers, p < 0.025.
Difference between smokers and nonsmokers, p < 0.001.

We recovered 125 BLPB isolates from 91 patients

(43%). These included all 16 M catarrhalis and 15 B
fragilis group isolates, 21 of the 38 (55%) S aureus
isolates, 9 of the 13 (69%) H influenzae isolates, 27
of the 100 (27%) Prevotella spp isolates, and 20 of
the 77 (29%) Fusobacterium spp isolates. Sixty-

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Brook & Hausfeld, Smoking & Sinusitis

nine BLPB isolates were found in smokers, and 56

in nonsmokers (p < 0.001).
A greater number of S aureus, MRSA, and BLPB
isolates were found in smokers than in nonsmokers
(p < 0.01, p < 0.025, and p < 0.001, respectively;
Tables 1 and 2). No other differences were noted in
the recovery of isolates between smokers and nonsmokers.
Effect of Previous Antimicrobial Therapy on Isolation of MRSA and BLPB. Antimicrobial therapy
had been administered in the past month to 130 patients (28%; 60 smokers and 70 nonsmokers; p <
0.025). MRSA was isolated more often from previously treated individuals (14 of 130 patients, or
11%) than from those not previously treated (16 of
328, or 5%; p < 0.025); 10 of these 14 MRSA isolates were from smokers, and 4 from nonsmokers (p
< 0.05). BLPB were also isolated more frequently
in those recently treated with antibiotics (58 of 130
patients, or 45%) than in those not treated (106 of
328, or 32%; p < 0.025); 34 of these 58 BLPB isolates were from smokers, and 24 from nonsmokers (p < 0.025). The antimicrobials administered to
the patients were amoxicillin (45 instances), fluoroquinolones (34), extended-spectrum macrolides
(21), amoxicillin-clavulanate (18), and cephalospo
rins (12). The antimicrobials administered to the 14
patients in whom MRSA was isolated were fluoroquinolones (8 instances), extended-spectrum macrolides (5), and cephalosporins and amoxicillin-clav
ulanate (1).
DISCUSSION

Our study confirms the predominance of S pneumoniae, H influenzae, M catarrhalis, group A beta-hemolytic streptococci, and S aureus in community-acquired acute sinusitis in adults.8 Similarly, S
aureus and anaerobic bacteria (Prevotella, Porphyromonas, Fusobacterium, and Peptostreptococcus
spp) were found to be the main isolates in chronic
sinusitis.9

Our data also illustrate that although similar organisms were recovered in acute and chronic sinusitis in smokers and nonsmokers, S aureus, MRSA,
and BLPB were more frequently recovered from
those who smoked. The higher isolation rates of
MRSA and BLPB in smokers were independent of
previous antimicrobial therapy.

We previously found a statistically significant

higher number of antibiotic-resistant organisms in
the sinuses of smokers who had acute sinusitis and
had undergone failed antimicrobial therapy, as compared to their susceptibility before therapy.10 In con-

710

trast to our previous study,10 in which we compared

recovery of organisms in 20 patients with sinusitis
before therapy to that after therapy, in this study we
evaluated the isolation of organisms in smokers and
nonsmokers in a larger number of individuals. Even
though smokers often receive antimicrobial therapy
for respiratory infections, the higher rates of isolation of MRSA and BLPB were independent of their
recent exposure to these antimicrobial agents.11

Adults who smoke have an increased risk of respiratory tract infections, including sinusitis,3,12 and
of oral colonization by potentially pathogenic bacteria.13,14 These phenomena were explained by enhanced bacterial binding to epithelial cells of smokers,15 and by the low number of aerobic and anaerobic organisms with inhibitory activity against bacterial pathogens (interfering organisms) in the oral
cavity of smokers.16,17 The high number of pathogens and the low number of interfering organisms
found in smokers revert to normal levels after complete cessation of smoking.1 Tobacco smoke also
compromises the antibacterial function of leukocytes, including neutrophils, monocytes, T cells, and
B cells, providing a mechanistic explanation for increased infection risk.18 It is therefore not surprising
that smokers are more often exposed than nonsmokers to antimicrobial therapies, which subsequently
lead to greater acquisition of antimicrobial resistance, as was illustrated in our study.

The major BLPB recovered from our patients were

S aureus, H influenzae, M catarrhalis, and Prevo
tella, Porphyromonas, and Fusobacterium spp. The
recovery rate of aerobic and anaerobic BLPB in the
oropharynx has increased in recent years, and these
organisms were isolated in one study in more than
half of patients with head and neck infections, including sinusitis.19 BLPB can be involved directly
in the infection, protecting not only themselves from
the activity of penicillins, but also penicillin-susceptible organisms. This protection can occur when the
enzyme beta-lactamase is secreted into the infected tissue or abscess fluid in sufficient quantities to
break the penicillins beta-lactam ring before it can
kill the susceptible bacteria.20 The actual activity of
the enzyme beta-lactamase and the phenomenon of
shielding have been demonstrated in fluids from
acutely and chronically inflamed sinuses.21
An increase in the recovery of MRSA was previously noted in various respiratory infections,22 including acute and chronic sinusitis,23 as well as in
the nasal mucosa of normal individuals.24 Smoking
was found to be a risk factor for nasal colonization
with MRSA.25
The presence of MRSA in the infected sinus may

711

Brook & Hausfeld, Smoking & Sinusitis

not only lead to failure of antimicrobial therapy, but

can also serve as a potential source for the spread
of these organisms to other body sites, as well as an
origin for dissemination to other individuals. Furthermore, MRSA that also produces beta-lactamase
can survive treatment with beta-lactam antibiotics
and continue to protect penicillin-susceptible pathogens from penicillins.20
The association between previous use of antimicrobial therapy and increased isolation of MRSA has
been noticed in community- and hospital-acquired
infections,26,27 as well as in patients with sinusitis.26
Like Gerencer,28 we found that the majority of patients with sinusitis infected with MRSA who were
previously treated with antimicrobials had been
treated with either a fluoroquinolone or an extended-spectrum macrolide antibiotic. Since almost all
strains of MRSA are resistant to these agents, it is
possible that these classes of antibiotics may be creating an environment within the sinuses that is particularly conducive to MRSA growth.
Treatment of sinus infection in smokers may
be more challenging than such treatment in nonsmokers. The higher rates of recovery of S aureus,
MRSA, and BLPB in these patients may require the
administration of antimicrobials effective against
these bacteria, as well as other potential aerobic
and anaerobic pathogens. Antimicrobials effective
against aerobic and anaerobic BLPB are amoxicillin
plus clavulanic acid, moxifloxacin, and the carba
penems. Clindamycin is effective against anaerobic
BLPB, but has no activity against H influenzae.
Although vancomycin represents the gold standard of therapy for MRSA infections, reports of increasing in vitro resistance to vancomycin,29 combined with reports of clinical failures (with this and

711

other antistaphylococcal agents), underscore the

need for alternative therapies. Older agents with favorable in vitro activity available in both oral and
intravenous dose forms include trimethoprim-sulfamethoxazole and clindamycin. Limited clinical
data exist to support their routine use as initial therapy in the treatment of MRSA infections. However,
these and other options (eg, tetracyclines) are being
re-explored in the setting of increasing concern over
MRSA acquired in the community setting. Newer
treatment options for MRSA include linezolid, quinupristin-dalfopristin, daptomycin, and tigecycline.

Culture-directed oral and topical antibiotic therapy

has been effectively utilized in treatment of MRSA,
as well as BLPB-associated sinusitis.28 Even though
the gold standard of obtaining such a culture is
through a surgical specimen or punctures,30 cultures
obtained through meatal endoscopy have been repeatedly shown to provide adequate results.31 Topical application of antibiotics to the sinus membranes
offers the potential benefit of a high concentration
of the drug at the site of infection. Such topical antibiotics include gentamicin, tobramycin, vancomycin, ciprofloxacin, and mupirocin.
Further prospective studies and continuous monitoring of the rates of recovery of S aureus, MRSA,
and BLPB in smokers who present with acute and
chronic sinusitis are indicated. The results of our
study, which demonstrated the increased role of
MRSA and BLPB in sinusitis in smokers, underscore the need to have a greater index of suspicion
for the presence of S aureus, MRSA, and BLPB in
smokers with sinusitis, and highlight the importance
of performing routine endoscopic cultures, especially in cases that fail to respond to empiric antimicrobial therapy.

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