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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.
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
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 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
708
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.
708
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)
709
709
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)
710
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.
710
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.
711
711
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