Annals of Otology. Rhinology & Laryngology 120(11):7O7-7I2. 2011 Annals Publishing Company. All rights reserved.

Microbiology of Acute and Chronic Maxillary Sinusitisin 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 maxil-lary sinusitis.

Methods: Cultures were obtained from 458 patients, 244 (87 smokers and 157 nonsmokers) of whom had acute maxil-lary sinusitis and 214 (84 smokers and 130 nonsmokers) of whom had chronic maxillary sinusitis, between 2001 and2007.

Results: A greater number of Staphylococcus aureus, methicillin-resistant 5 aureus (MRSA), and beta-lactamase-pro-ducing 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 withchronic sinusitis than in the nonsmokers (p < 0.01, p < 0.025, and p < 0.001, respectively). Eighty-five BLPB isolateswere recovered from 73 patients (30%) with acute sinusitis. These included Moraxella catarrhalis, S aureus, Haemophi-lus 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, includ-ing M caarr/ia/, Bacteroides fragilis group, S aureus, H influenzae, Prevotella spp, and Fusobacterium spp; 69 BLPBisolates were found in smokers, and 56 in nonsmokers (p < 0.001). Antimicrobial therapy had been administered in thepast month to 130 patients (28%; 60 smokers and 70 nonsmokers; p < 0.025). Both MRSA and BLPB were isolated moreoften from these individuals (p < 0.025). However, the higher isolation rates of MRSA and BLPB in smokers were inde-pendent of previous antimicrobial therapy.

Conclusions: These data illustrate a greater frequency of isolation of S aureus, MRSA, and BLPB in patients with acuteand chronic sinusitis who smoke.Key Words: beta-lactamase, methicillin resistance, sinusitis, smoking, Staphylococcus aureus.

INTRODUCTIONSmoking has a significant impact on the oropha-

ryngeal bacterial fiora of children, as well as adults.'Active smokers and those exposed to secondhandsmoke are at increased risk of bacterial infectionssuch as sinusitis,^ tuberculosis, pneumonia, and le-gionnaires disease; bacterial vaginosis and sexuallytransmitted diseases; Helicobacter pylori infection;periodontitis; meningitis; otitis media; and postsur-gical and nosocomial infections.^

No previous study has compared the microbiol-ogy of sinus aspirates obtained from smokers to thatof those obtained from nonsmokers. This retrospec-tive study evaluated the microbiology of sinus aspi-rates of smokers and nonsmokers who had acute orchronic maxillary sinusitis.

PATIENTS AND METHODSThe population studied was a middle-class one re-

siding in suburban locations in the vicinity of Wash-

ington, DC. The patients were consecutively seen inthe outpatient clinic between January 1, 2001, andJanuary 1, 2007, and had a diagnosis of acute orchronic bacterial maxillary sinusitis.

The patients with acute infection had symptomsthat had lasted between 10 and 30 days, and thosewith chronic infection had had symptoms for morethan 90 days. None of those with chronic sinusitishad had previous sinus surgery. Smokers were de-fined as individuals who had smoked at least 10 cig-arettes a day for the past 5 years. The determinationwas based on the patient's own history.

The patients' complaints included facial pain,frontal headache, purulent nasal discharge, fever,and malaise. Radiography with occipitomental (Wa-ters view), lateral, oblique, and verticomental viewsor computed tomography was performed. Sinus-itis was defined radiographically as complete sinusopacity, ie, an air-fluid level or mucous membranethickening of at least 6 mm in the maxillary sinus.

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 Brook & Hausfeld, Smoking & Sinusitis

For the Waters view, mucosal thickening of the max-illary sinuses was measured as the shortest distancefrom the air-mucosal interface to the most lateralpart of the maxillary sinus wall. Specimens were ob-tained through endoscopy, and the sinus secretionswere collected with calcium alginate-tipped micro-swabs. The study was granted Institutional ReviewBoard approval.

Cultures were obtained endoscopically beforetherapy with calcium alginate swabs that were imme-diately plated into media supportive of the growth ofaerobic and anaerobic bacteria. The methods of spec-imen collection, transportation, and microbiologicalevaluation were previously described ."* Specimenswere processed semiquantitatively, and organismswere identified by standard methods.^ Beta-lacta-mase activity was determined by use of the chro-mogenic cephalosporin analog 87/312 method.^

Staphylococcus qureus isolates were screenedfor oxacillin resistance by the Clinical LaboratoryStandard Institute disk diffusion method.'' Over-night cultures from blood agar plate were suspendedin Mueller-Hinton broth to the turbidity of 0.5 Mc-Farland and plated on Mueller-Hinton agar, and al-^ig oxacillin disc was placed with the inoculum.Zone diameters were measured and recorded aftera 24-hour incubation at 35C (susceptible, equal toor less than 13 mm; intermediate, between 11 and12 mm; and resistant, equal to or less than 10 mm).Methicillin-resistant S aureus (MRSA) strains werenot typed.

All isolates of Streptococcus pneumoniae werescreened for penicillin susceptibility with a 1 -\ig ox-acillin disk by the Kirby-Bauer disk diffusion meth-od. Intermediate resistance to penicillin was definedas a minimal inhibitory concentration of 0.1 to 1.0|j,g/mL, and high resistance to penicillin was definedas a minimal inhibitory concentration of at least 2.0|a,g/mL.

Included in the final analysis were only patientswhose culture showed bacterial growth. Statisticalsignificance was calculated by Fisher's exact test(2-sided) unadjusted.

RESULTS,We evaluated 458 patients (244 with acute and

214 with chronic maxillary sinusitis) after exclusionof an additional 110 patients (62 with acute and 48with chronic sinusitis) whose culture did not showany bacterial growth. The patients' ages ranged from18 to 75 years (mean, 42 years 4 months); 265 weremale. No differences were noted in the age distribu-tion, ethnicity, or gender of the patients.

TABLE 1. BACTERIOLOGY OF 244 PATIENTS WITHACUTE MAXILLARY SINUSITIS

BacteriaAer^ obic bacteria

a-Hemolytic streptococci

Smokers(N = 87)

4Streptococcus pneumoniae 25

Intermediate resistanceto penicillin

High resistance topenicillin

Group F streptococcusStreptococcus pyogenesStaphylococcus aureus

(methicillin-resistant)Staphylococcus aureus

(methicillin-sensitive)Staphylococcus

epidermidisHaemophilus influenzaeMoraxella catarrhalisKlebsiella pneumoniaePseudomonas aeruginosaProteus mirabilisFscherichia coli

Subtotal aerobesAnaerobic bacteria

Peptostreptococcus sppVeillonella prvulaEubacterium sppPropionibacterium acnesFusobacterium spp

7

3

24

8* (6)

7t(4)4(2)

16(9)15(15)

2! 1

2

90 (36t)

6212

1(1)Fusobacterium nucleatumBacteroides sppPrevotella

melaninogenicaPrevotella oralisPrevotella oris-buccaePrevotella intermediaPorphyromonas

asaccharolyticaSubtotal anaerobesTotal

1(1)2(1)

2(1)

1

18(4)108 (40t)

Numbers within parentheses indicateproducing bacteria.

Nonsmokers(N = 157)

9548

4

47

4(3)

4(1)

4(1)

37(8)29 (29)

1111

156 (42)

15

232

2(1)1

2(1)

2(1)

22

33(3)189 (45)

Total(N = 244)

137915

7

611

12(9)

11(5)

8(3)

53(17)44(44)

3231

246 (78)

21235

3(1)2(1)2(1)4(2)

2(1)2(1)

23

51(7)297 (85)

number of beta-lactamase-

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

Acute Sinusitis. Of the 244 patients, 87 weresmokers and 157 were nonsmokers. A total of 297isolates were recovered (1.2 per specimen): 246 aer-obic and facultative ( 1.0 per specimen) and 51 an-aerobic (0.2 per specimen; Table 1). The number ofisolates varied from 1 to 3. Antimicrobial therapywas administered to 45 patients (24%) in the monthbefore sample collection.

Aerobic and facultative organisms only were re-

Brook & Hausfeld, Smoking & Sinusitis 709

covered in 213 instances (87%), anaerobes onlywere recovered in 15 (6%), and mixed aerobic andanaerobic bacteria were recovered in 16 (7%). Thepredominant aerobic bacteria were S pneumoniae(79 isolates; 15 were intermediately resistant and 7highly resistant to penicillin), Haemophilus influen-zae (53), Moraxella catarrhalis (44), and S aureus(23, including 12 that were methicillin-resistant; Ta-ble 1).

The predominant anaerobes were gram-negativebacilli (15 isolates, including 10 Prevotella, 3 Por-phyromonas spp, and 2 Bacteroides spp), Pepto-streptococcus spp (21), and Fusobacterium spp (5).

Eighty-five beta-lactamase-producing bacteria(BLPB) were recovered from 73 patients (30%; Ta-ble 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 th 5 (40%) Fusobacte-rium spp isolates. Forty BLPB isolates were foundin smokers, and 45 in nonsmokers (p < 0.05).

A greater number of S aureus, MRSA, methi-cillin-sensitive S aureus, and BLPB isolates werefound in smokers than in nonsmokers (p < 0.005, p< 0.025, p < 0.05, and p < 0.05, respectively; Table1). No other differences were noted in the recoveryof isolates between smokers and nonsmokers.

Chronic Sinusitis. Of the 214 patients, 84 weresmokers and 130 were nonsmokers. A total of 591isolates were recovered (2.8 per specimen): 211 aer-obic and facultative (1.0 per specimen) and 380 an-aerobic (1.8 per specimen; Table 2). The number ofisolates varied from 1 to 5. Antimicrobial therapywas administered to 85 patients (40%) in the monthbefore sample collection.

Aerobic and facultative organisms only were re-covered in 42 instances (19%), anaerobes only in 59(28%), and mixed aerobic and anaerobic bacteriawere recovered in 113 (52%). The predominant aer-obic bacteria were S aureus (38 isolates, including18 that were methicillin-resistant), microaerophilicstreptococci (22), M catarrhalis {16), H influenzae(13), S pneumoniae (10 isolates, 3 of which wereintermediately resistant and 2 of which were high-ly resistant to penicillin), Proteus mirabilis (12),Pseudomonas aeruginosa (11), Klebsiella pneumo-niae (10), and Escherichia coli (7; Table 2).

The predominant anaerobes were gram-negativebacilli (157 isolates, including 100 Prevotella spp,28 Porphyromonas asaccharolytica, and 15 Bacte-roides fragilis group), Peptostreptococcus spp (118),and Fusobacterium spp (57).

TABLE 2. BACTERIOLOGY OF 214 PATIENTSWITH CHRONIC MAXILLARY SINUSITIS

Smokers Nonsmokers TotalBacteria (N = 84) (N = 30} (N = 214)Aerobic bacteria

a-Hemolytic streptococci 14Microaerophilic 8

streptococciStreptococcus pneumoniae 4

Intermediate resistance 2to penicillin

High resistance to 1penicillin

Group F streptococcus 2Group G streptococcus 3Streptococcus pyogenes 5Staphylococcus aureus 13* (8)

(methicillin-resistant)Staphylococcus aureus 11 (9)

(methicillin-sensitive)Staphylococcus 4 (2)

epidermidisHaemophilus influenzae 5 (3)Moraxella catarrhalis 6 (6)Klebsiella pneumoniae 5Pseudomonas aeruginosa 4Proteus mirabilis 5Escherichia coli 3

Subtotal aerobes 93 (28*)Anaerobic bacteria

Peptostreptococcus spp 44Veillonella prvula 4Eubacterium spp 3Propionibacterium acnes 11Fusobacterium spp 10 (4)Fusobacterium nucleatum 15 (7)Bacteroides spp 5(1)Bacteroides fragilis group 5 (5)Prevotella 13 (8)

melaninogenicaPrevotella oralis 1 (3)Prevotella oris-buccae 11 (2)Prevotella intermedia 10 (5)Porphyromonas 12 (6)

asaccharolyticaSubtotal anaerobes 150(41) 230(35) 380(76)Total 243(691) 348(56) 591(125)

Numbers within parentheses indicate number of beta-lactamase-producing bacteria.

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

We recovered 125 BLPB isolates from 91 patients(43%). These included all 16 M catarrhalis and 15 fragilis group isolates, 21 of the 38 (55%) S aureusisolates, 9 of the 13 (69%) H influenzae isolates, 27of the 100 (27%) Prevotella spp isolates, and 20 ofthe 77 (29%) Fusobacterium spp isolates. Sixty-

2114

61

1

747

5(1)

9(3)

4(1)

8(6)10(10)5774

118(21)

7411613

12(4)20(5)9(3)10(10)15(3)

11(2)13(2)20(2)16(4)

3522

103

2

9712

18(9)

20(12)

8(3)

13(9)16(16)1011127

211 (49)

11815924

22(8)35(12)14(4)15(15)28(11)

18(5)24(4)30(7)28(10)

710 Brook & Hausfeld, Smoking & Sinusitis

nine BLPB isolates were found in smokers, and 56in nonsmokers (p < 0.001).

A greater number of S aureus, MRSA, and BLPBisolates 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 inthe recovery of isolates between smokers and non-smokers.

Effect of Previous Antimicrobial Therapy on Iso-lation of MRSA and BLPB. Antimicrobial therapyhad been administered in the past month to 130 pa-tients (28%; 60 smokers and 70 nonsmokers; p