The prevalence of bacterial infection in acute rhinosinusitis: A systematic review and meta-analysis Stephanie Shintani Smith, MD, MS1,2; Elisabeth Henderson Ference, MD1; Charlesnika T. Evans, PhD, MPH2, 3; Bruce K. Tan, MD1; Robert C. Kern, MD1; Rakesh K. Chandra, MD1

1 Department of Otolaryngology – Head and Neck Surgery, Northwestern University Feinberg School of Medicine, Chicago, IL, USA; 2 Center for Healthcare Studies, Northwestern University Feinberg School of Medicine, Chicago, IL, USA; 3 Department of Veterans Affairs, Center for Management of Complex Chronic Care, Edward Hines Jr. VA Hospital, Hines, IL, USA

Running title: Bacterial infection in acute rhinosinusitis Funding: Supported by an institutional award from the Agency for Healthcare Research and Quality, T-32 HS 000078 (S.S.S., PI: Jane L. Holl, MD MPH), the National Institutes of Health/National Institute of Deafness and Communications Disorders 1K23DC012067 and the American College of Surgeons/ Triological Society (B.K.T.), and the Department of Otolaryngology, Northwestern University Feinberg School of Medicine (S.S.S. and B.K.T.). Disclosures: The authors have no other funding, financial relationships, or conflicts of interest to disclose. Presentations: Presented at the Triological Society meeting at COSM, April 10-14, 2013, in Orlando, FL, USA. Corresponding Author: Stephanie Shintani Smith, MD Northwestern University Department of Otolaryngology – Head & Neck Surgery 676 North St. Clair, Suite 15-200, Chicago, IL 60640 312-695-8182 (office)

312-695-7851 (fax)

[email protected]

This article has been accepted for publication and undergone full peer review but has not been through the copyediting, typesetting, pagination and proofreading process which may lead to differences between this version and the Version of Record. Please cite this article as doi: 10.1002/lary.24709

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Abstract

Key words: systematic review, meta-analysis, acute rhinosinusitis, bacterial infection, antral puncture, endoscopic middle meatus culture Objective: To systematically assess the prevalence of bacterial infection in adults with acute rhinosinusitis (ARS) Data Sources: PubMed and CINAHL databases Review Methods: Electronic databases were systematically searched for relevant studies published up to June 2012.Results: 29 articles, evaluating a total of 9,595 patients with a clinical diagnosis of ARS, were included in the study. 14 (48%) studies required radiographic confirmation of sinusitis, 1 (3%) required evidence of purulence, 10 (35%) required both for inclusion in the study population, and 4 (14%) required neither. The random effects model estimate of prevalence of bacterial growth on all cultures was 53.7% (CI 48.4%-59.0%), ranging from 52.5% (CI 46.7%-58.3%) in studies requiring radiographic confirmation of sinusitis to 61.1% (CI 54.0%-68.1%) in studies requiring neither radiographic evidence nor purulence on exam. Studies which obtained cultures from antral swab had a prevalence of bacterial growth of 61.0% (CI 54.7%-67.2%), while those utilizing endoscopic meatal sampling had a prevalence of 32.9% (CI 19.0%-46.8%). Conclusion: Few studies evaluate the recovery of bacteria via culture in adults with a diagnosis of ABRS or ARS based on clinical criteria alone. With radiographic and/or endoscopic confirmation, antral puncture and endoscopically guided cultures produce positive bacterial cultures in approximately half of patients. Opportunities exist to improve diagnostic accuracy for bacterial infection in ARS.

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Introduction Acute rhinosinusitis (ARS) is among the most common conditions encountered by primary care providers, and ARS is one of the most common reasons for antibiotic prescriptions, with antibiotics prescribed in 82-88% of patient visits for ARS.1-4 A growing body of evidence suggests that antibiotics do not confer a distinct benefit in the majority of ARS cases,5-8 and guidelines do not recommend antibiotics for most cases of ARS.9-15 This is largely because only a small proportion of viral sinus infections is believed to progress to acute bacterial rhinosinusitis.9,10,16 In scientific literature, however, the reported prevalence of bacterial infection in ARS ranges widely, from 0.5% to 86%, depending on the population studied and the diagnostic methods used to confirm bacterial sinusitis. 13,16-24 ARS, as defined by the American Academy of Otolaryngology--Head and Neck Surgery Foundation clinical practice guideline, is defined by up to 4 weeks of purulent nasal drainage accompanied by nasal obstruction and/or facial pain/pressure/fullness.9 In ARS, an inflammatory reaction to a viral upper respiratory infection characterizes most cases. Viral, postviral, and bacterial ARS show considerable overlap in inflammatory mechanisms and clinical presentation.7 The pathophysiology involves interplay between a predisposing condition (e.g. allergic rhinitis, septal deformity, concha bullosa, primary ciliary dyskinesia, immune deficiency, and environmental factors), infection, and consequent inflammatory response in the sinonasal mucosa. Viruses attach to host cells via intermolecular interaction between nucleocapsids (naked viruses) or viral membranes (enveloped viruses) and the host cell receptor.7 The inflammatory response involves edema, fluid extravasation, and mucus production. The inflammatory cascade involves T-helper type 1 cytokine polarization associated with tumor necrosis factor-β and interferon-γ. Proinflammatory cytokines such as interleukin (IL)-1β, IL-6, and IL-8 are potent chemoattractive agents for neutrophils.25 Mucosal inflammation may lead to obstruction of normal sinus outflow tracts. This obstruction impedes normal ventilation and

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drainage, leading to a lower partial pressure of oxygen, decreased ciliary clearance, and stasis of secretions. A secondary bacterial infection may develop. The prevalence of bacterial infection in patients with clinically diagnosed ARS is not well defined given the difficulty distinguishing viral from bacterial infection. The clinical features of viral and bacterial ARS are similar. There are no clinical findings, including a change in the color or character of nasal discharge17, that predict whether ARS is of bacterial origin. Common imaging modalities are neither sufficiently sensitive nor specific. Several imaging, clinical, and laboratory tests have been used to increase the likelihood of a correct diagnosis of bacterial ARS.26-28 Culture of intrasinusal secretions from sinus puncture is considered the most widely accepted and gold standard method to define ABRS, 26,29-31 but is not routinely feasible due to patient perceived of real discomfort of this invasive procedure.32 A recent meta-analysis revealed that endoscopically directed middle meatal cultures (EMMC) is a highly sensitive and accurate culture method for acute ABRS and may be more sensitive than maxillary sinus taps given the presence of pathogenic bacteria not found on antral lavage. The authors stated that EMMC is a viable, and possibly preferred, culture method for determining antimicrobial efficacy and bacterial resistance patterns.24 With the detrimental effects of inappropriate antibiotic prescribing in mind, the primary objective of this study was to review the literature to assess the prevalence of bacterial infection in adults with clinically diagnosed ARS who undergo culture from antral puncture or endoscopically directed middle meatus culture. A secondary objective was to compare the prevalence of bacterial infection in adults with clinically diagnosed ARS by method of culture: antral puncture vs. EMMC. We hypothesized bacterial recovery would be same between antral puncture and EMMC. Information regarding prevalence of bacterial infection in ARS and culture methods could direct efforts to improve the quality and quantity of antibiotic prescribing. Materials and methods 4 John Wiley & Sons

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This review was conducted based on the 2009 Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines.33 We searched PubMed and Ovid MEDLINE and CINAHL from date of database inception to June 12, 2012. For MEDLINE, we used search terms "acute sinusitis"[All Fields] OR "acute rhinosinusitis"[All Fields] OR "acute bacterial sinusitis"[All Fields] OR "acute bacterial rhinosinusitis"[All Fields] OR "viral rhinosinusitis"[All Fields] OR "viral sinusitis"[All Fields] AND ("humans"[MeSH Terms] AND English[lang]). For CINAHL, we searched boolean/phrases "acute sinusitis" or "acute rhinosinusitis" or "acute bacterial sinusitis" or "acute bacterial rhinosinusitis" or “viral sinusitis” or “viral rhinosinusitis.” We subsequently reviewed reference lists of review articles and other relevant publications for additional studies to include. A single patient was considered the unit of analysis in the study. Eligibility criteria were participants aged ≥13years with ARS by clinical, radiographic, or endoscopic diagnosis; English language; original research; experimental, quasi-experimental, or observational study designs; intervention with antral puncture or maxillary aspiration prior to antibiotic treatment; measurable outcome with bacterial culture; N14

91

Prospective

series)

18-18

351

Prospective

NA

>=18

290

Prospective

NA

Sweden, Finland, Carenfelt, 1990

43

Drug

Iceland

Canada, Germany, Desrosiers, 2008

Greece, Portugal,

61

Drug

Turkey

Germany, Gauger, 1990

Hadley, 2010

44

62

Drug

Switzerland

21-65

41

Prospective

NA

Drug

U.S.

>=18

374

Prospective

NA

Drug

U.S.

adults

78

Prospective

NA

Drug

U.S.

>=15

81

Prospective

NA

Drug

Thailand

17-68

48

Prospective

NA

Culture and Hamory, 1979

Huck, 1993

42

63

Jareoncharsi, 2004

64

Johnson, 1999

65

Drug

U.S.

≥18

322

Prospective

NA

Johnson, 2008

66

Drug

U.S.

≥18

184

Prospective

NA

Drug

U.S.

≥15

13

Prospective

NA

Jones, 1985

67

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4 (case-

Diagnostic Joniau, 2005

68

technique

Belgium

>=16

24

Prospective

control)

69

Drug

Croatia

15-50

70

Prospective

NA

≥18

452

Prospective

NA

18-80

543

Prospective

NA

≥18

538

Prospective

NA

Klapan, 1999

Belgium, France, Germany, Great Britain, Greece, Lithuania, Spain, Klossek, 2003

70

Drug

Sweden

U.S. Mexico, Lopez Sisniega, 2007

71

Argentina, Drug

Europe

U.S., India, Europe, Latin 72

Murray, 2005

Drug

America

Finland, Germany, Belgium,

4 (case

Switzerland, Penttila, 1997

Poole, 2006

74

73

Culture

Spain, Austria

>13

569

Prospective

series)

Drug

U.S.

≥18

780

Prospective

NA

≥12

342

Prospective

NA

Canada, Greece, Hungary, Italy, Lithuania, Poland, Romania, Spain, 75

Riffer, 2005

Drug

U.S.

4 (case-

Savolainen, 1989

76

Culture

Finland

18-28

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310

Prospective

control)

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4 (case

Enzyme Shinogi, 2001

77

assay

Japan

15-71

11

Prospective

series)

≥18

447

Prospective

NA

France, Germany, Greece, Israel, Lithuania, Spain, Siegert, 2003

78

Drug

Sweden

Finland, France, Germany, Greece, Israel, Siegert, 2000

79

Drug

Spain, Sweden

≥18

493

Prospective

NA

80

Drug

U.S.

>=18

28

Prospective

NA

Sydnor, 1998

4 (case-

Diagnostic 81

Talbot, 2001

technique

U.S.

>=18

46

Prospective

control)

Van

4 (case

Cauwenberge, 1976

41

Culture

Belgium

NS

69

Retrospective

series)

≥18

100

Prospective

NA

Belgium, France, van den

Germany, 82

Wijngaart, 1992

Drug

Netherlands

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Purulence Required

Diagnostic Method

Basis for ARS Clinical Diagnosis Purulent discharge or purulence in the

Diagnostic Radiography Required

Author (year)

Symptom duration, days

Supplemental Table 2. Diagnostic criteria of studies included in final data set

Notes

nasal cavity on exam and ≥1 major criterion (facial pain/pressure/tightness, facial congestion/fullness, or nasal obstruction/blockage) or ≥2 minor criteria (nonvascular headache, cough, change in perception of smell, sore Anon, 2006

59

throat, tooth pain, earache, halitosis, periorbital swelling, and fever).

3-28

Yes

Yes

AP

≥1 of the following: spontaneous facial pain, facial pain after pressure and/or facial tightness over any sinus site, purulent rhinorrhea, or cough; plus ≥2 of the following: fever, headache, nasal Arrieta, 2007

23

congestion, halitosis, change in

AP/

perception of smell, or lacrimation.

7-28

Yes

No

EMMC

Study

Berg, 1988

60

Carenfelt, 1990

43

Clinical symptoms and signs of sinusitis

participants

indicating diagnostic and therapeutic

were not

puncture with prevailing antral secretion

consecutive or

at aspiration.

0-90

No

No

AP

randomized.

Local pain, purulent ongoing nasal

Required

discharge, pus in the nasal cavity, and

suppuration on

at least one maxillary sinus with

pretreatment

suppuration at pretreatment aspiration

1-90

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No

Yes

AP

aspiration.

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(discolored, yellow-green, mucoid, or nonviscous).

Purulent rhinorrhea, plus 2 major sign/symptom (facial pain/pressure/tightness over the maxillary sinuses; nasal congestion/obstruction; hyposmia/anosmia; fever) or 2 minor signs/symptoms (headache, halitosis, Desrosiers, 2008

61

Gauger, 1990

44

dental pain, ear pressure/fullness, cough, fatigue).

7-28

Yes

Yes

EMMC

0-8

No

No

AP

7-28

Yes

No

AP

0-21

No

No

AP

0-14

Yes

No

AP

Acute bacterial sinusitis; diagnostic basis not specified.

Two major symptoms (purulent anterior or posterior nasal discharge and unilateral facial pain or malar Hadley, 2010

62

tenderness), or ≥1 major and 1 minor symptom (frontal headache or fever).

Not specified; the complaints of the patients included facial pain, purulent Hamory, 1979

42

Huck, 1993

63

nasal discharge, and, less commonly, headache and feverishness or malaise.

Facial pain and/or purulent nasal discharge.

Outpatients with acute or acute exacerbation of chronic sinusitis based

Did not

on clinical symptoms and signs ( i.e.

separate ARS

Jareon-

nasal obstruction, purulent nasal

from

charsi,

discharge or postnasal drip, impairment

exacerbation of

2004

64

of sense of smell, foul smell and

0-28

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Yes

Yes

AP

CRS

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headache) plus mucopurulent discharge in the middle meatus of maxillary ostium on nasal endoscopy.

Did not

Johnson, 1999

65

Clinical signs and symptoms of

separate ARS

sinusitis; plus ≥2 of the following: fever;

from acute

leukocytosis; symptoms consistent with

exacerbation of

sinus infection; or physical findings.

0-28

Yes

No

AP

CRS

S. pneumoniae, H. influenzae, or M. catarrhalsis were the only pathogens studied; this

Johnson, 2008

66

Clinically confirmed acute bacterial

was a pooled

maxillary sinusitis with the presence of

analysis of two

at least 1 major and 1 symptom.

7-28

Yes

No

EMMC

Yes

No

AP

industry trials

Clinically diagnosed acute maxillary Jones, 1985

67

sinusitis (rhinorrhea, nasal obstruction,

unknow

facial pressure).

n

Clinical signs and symptoms of acute bacterial maxillary sinusitis (facial/dental Joniau, 2005

68

pain, rhinorrhea, nasal obstruction, and/or hyposmia).

AP/ 0-21

Yes

No

EMMC

Signs and symptoms consistent with sinusitis, not otherwise specified, plus

Klapan, 1999

69

nasal endoscopy showing complete

AP performed

obstruction of the ostiomeatal complex

"when maxillary

or partial obstruction with purulent

sinus puncture

discharge.

0-28

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Yes

Yes

AP

was indicated"

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≥2 of the following: nasal congestion, post-nasal drainage, frequent coughing or throat clearing, frontal headache, Klossek, 2003

70

molar tenderness/pain, purulent nasal drainage.

AP/ 0-28

Yes

No

EMMC

5-28

Yes

Yes

AP

7-28

Yes

Yes

AP

1) facial pain/tenderness ≥1 maxillary areas; 2) ≥2 of the following: fever, leukocytosis, nasal congestion, postnasal drainage, frequent coughing, and headache; 3) ≥1 of the following Lopez

physical examination findings: purulent

Sisniega,

discharge from the maxillary sinus

2007

71

orifice, nose, or back of the throat.

Facial pain, pressure, and/or tightness over ≥1 maxillary sinus combined with purulent discharge from the nose or the maxillary sinus orifice and/or the posterior pharynx, plus ≥2 of the following: fever, leukocytosis, frequent Murray, 2005

72

coughing, headache, nasal congestion, or postnasal drainage.

Required positive yield of

Penttila, 1997

73

Poole, 2006

74

Clinical symptoms and signs, purulent

secretions on

nasal discharge, and a positive yield of

antral puncture

secretion in puncture from at least one

for study

maxillary sinus.

0-21

Yes

Yes

AP

inclusion.

1) ≥1 of the following: purulent

Does not

rhinorrhea; facial pain, tenderness,

distinguish AP

pressure, or tightness over the maxillary sinuses or periorbital region;

0-28

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Yes

Yes

AP/

vs. EMMC

EMMC

results

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congestion; maxillary tooth pain; 2) visible nasal purulence on physical or endoscopic exam.

1) Purulent nasal discharge, and 2) ≥2 relevant signs and symptoms (facial pain or facial pressure over one or both Riffer, 2005

75

maxillary sinus areas, nasal congestion, and fever)

AP/ 7-28

Yes

Yes

EMMC

Military hospital with predominantly male study population (297 Savolainen, 1989

76

male, 13

Suspected acute maxillary sinusitis confirmed by sinus puncture.

0-21

Yes

Yes

AP

1-28

Yes

No

AP

female)

Clinical history, clinical symptoms, and findings in the nasal cavity that resolved with medical therapy leaving no Shinogi, 2001

77

significant mucosal damage after 4 weeks.

AP yielded 33/114 positive cultures; EMMC yielded 103/333 Siegert, 2003

78

Siegert, 2000

79

≥1 major symptom, plus ≥2 minor symptoms

0-28

Yes

No

AP/

positive

EMMC

cultures.

Acute bacterial sinusitis was diagnosed

Authors do not

either bacteriologically or clinically on

distinguish

the basis of radiological paranasal sinus

between

X-ray together with two or more of the

unknow

following symptoms; nasal congestion,

n

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Yes

No

AP/

endoscopic

EMMC

swab,

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post- nasal drainage, frequent coughing

cannulation of

or throat clearing, frontal headache,

the middle

malar tenderness or pain and purulent

meatus, or

nasal discharge.

sinus puncture

≥2 signs/symptoms (fever, headache, Sydnor, 1998

80

Talbot, 2001

81

purulent rhinorrhea, facial pain, malar tenderness, dental pain)

AP/ 0-28

Yes

No

Sinus pain, rhinorrhea, facial swelling, sensation of nasal or sinus congestion.

EMMC

AP/ 0-30

Yes

No

EMMC

Included some inpatients; Van

"pathogenic

Cauwen-

Not

bacteria" were

berge,

speci-

counted for

1976

41

Not specified.

fied.

No

No

AP

cultures

Does not Symptoms consistent with an acute and

distinguish

van den

uncomplicated paranasal sinus infection

Not

between

Wijngaart,

likely to be caused by organisms

speci-

inpatients and

susceptible to cefprozil.

fied.

1992

82

Yes

No

AP

outpatients.

Abbreviations: AP=Antral puncture; EMMC=Endoscopic middle meatus culture; ARS=Acute rhinosinusitis; CRS=Chronic Rhinosinusitis.

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Systematic Review Flowchart 215x279mm (300 x 300 DPI)

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Bacterial growth based on objective diagnostic criteria (n = number of studies)

254x190mm (300 x 300 DPI)

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Bacteria growth based on method of culture (n = number of studies)

254x190mm (300 x 300 DPI)

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Prevalence of bacterial infection in acute rhinosinusitis 254x190mm (300 x 300 DPI)

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The prevalence of bacterial infection in acute rhinosinusitis: a Systematic review and meta-analysis.

To systematically assess the prevalence of bacterial infection in adults with acute rhinosinusitis (ARS)...
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