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
The Laryngoscope
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.
2 John Wiley & Sons
Page 2 of 37
Page 3 of 37
The Laryngoscope
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
3 John Wiley & Sons
The Laryngoscope
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
Page 4 of 37
Page 5 of 37
The Laryngoscope
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
24 John Wiley & Sons
Page 25 of 37
The Laryngoscope
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
25 John Wiley & Sons
310
Prospective
control)
The Laryngoscope
Page 26 of 37
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
26 John Wiley & Sons
Page 27 of 37
The Laryngoscope
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
27 John Wiley & Sons
No
Yes
AP
aspiration.
The Laryngoscope
Page 28 of 37
(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
28 John Wiley & Sons
Yes
Yes
AP
CRS
Page 29 of 37
The Laryngoscope
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
29 John Wiley & Sons
Yes
Yes
AP
was indicated"
The Laryngoscope
Page 30 of 37
≥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
30 John Wiley & Sons
Yes
Yes
AP/
vs. EMMC
EMMC
results
Page 31 of 37
The Laryngoscope
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
31 John Wiley & Sons
Yes
No
AP/
endoscopic
EMMC
swab,
The Laryngoscope
Page 32 of 37
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.
32 John Wiley & Sons
The Laryngoscope
Systematic Review Flowchart 215x279mm (300 x 300 DPI)
John Wiley & Sons
Page 34 of 37
Page 35 of 37
The Laryngoscope
Bacterial growth based on objective diagnostic criteria (n = number of studies)
254x190mm (300 x 300 DPI)
John Wiley & Sons
The Laryngoscope
Bacteria growth based on method of culture (n = number of studies)
254x190mm (300 x 300 DPI)
John Wiley & Sons
Page 36 of 37
Page 37 of 37
The Laryngoscope
Prevalence of bacterial infection in acute rhinosinusitis 254x190mm (300 x 300 DPI)
John Wiley & Sons