AMER IC AN JOURNAL OF OT OLA RYNGOLOGY–H E A D A N D NE CK M E D ICI N E AN D S U RGE RY X X (2 0 1 5) XXX –XXX
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Original contribution
Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review☆ Thunchai Thanasumpun, MD a , Pete S. Batra, MD, FACS b,⁎ a
Department of Otolaryngology-Head and Neck Surgery Faculty of Medicine Vajira Hospital, University of Bangkok Metropolis Navamindradhiraj, Bangkok, Thailand b Department of Otorhinolaryngology-Head and Neck Surgery, Rush University Medical Center, Chicago, Illinois
ARTI CLE I NFO
A BS TRACT
Article history:
Background: Culture-directed antibiotic therapy represents an important component in the
Received 4 February 2015
management paradigm of chronic rhinosinusitis (CRS). The objective of this study was to systematically review the literature to assess culture yield of the most common aerobic and anaerobic pathogens. Methods: A total of 43 studies between 1975 and 2010 were included. Results: The composite data comprised 3528 patients with 6005 total culture specimens. The cultures were obtained in operating room in 33 (76.7%) and clinic in 10 (23.3%) of the studies, respectively. The most common site of culture was the maxillary sinus in 18 (41.9%) of the studies. The most common assay techniques reported were swab in 19 (44.2%) and aspirate in 12 (27.9%) studies. The most common gram positive aerobes reported were coagulase negative Staphylococcus and Staphylococcus aureus in 630 (34.7%) and 481 (26.5%) of the cultures, respectively. The most common gram negative aerobes included Haemophilus influenzae and Pseudomonas aeruginosa in 245 (27.0%) and 198 (21.6%) cultures, respectively. The most common anaerobes reported were Peptostreptococcus species in 156 (19.6%) and Bacteroides species in 153 (19.2%) cultures. Conclusion: This study provides a composite snapshot of the literature accrued on the microbiology of CRS. It should serve to apprise clinicians on the most common aerobic and anaerobic organisms in CRS patients when employing culture-directed antimicrobial therapy. © 2015 Elsevier Inc. All rights reserved.
1.
Introduction
Chronic rhinosinusitis (CRS) represents an inflammatory disorder of at least 3 months’ duration caused by a multitude of etiologies, including microbes (viruses, bacteria, fungi), biofilm, Staphylococcus superantigen, ciliary dysfunction, and derange-
ments in innate and adaptive immunity [1]. The role of infection as a potential pathophysiologic mechanism in CRS has been a source of considerable debate and, at times, controversy in rhinology. Nonetheless, bacterial superinfection is commonly observed during acute exacerbations of CRS contributing to ongoing recalcitrant CRS [2]. Though empiric
☆ Disclosures: TT: none. PSB: Advisory Board (Merck). These data were presented as an oral presentation at the IFOS meeting in Seoul, South Korea held June 1st–5th, 2013. ⁎ Corresponding author at: Department of Otorhinolaryngology-Head and Neck Surgery, Rush University Medical Center, 1611 W. Harrison St., Suite 550, Chicago, IL, 60612. Tel.: +1 312 942 7182; fax: + 1 312 942 6653. E-mail address: [email protected] (P.S. Batra).
http://dx.doi.org/10.1016/j.amjoto.2015.04.010 0196-0709/© 2015 Elsevier Inc. All rights reserved.
Please cite this article as: Thanasumpun T, Batra PS, Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review, Am J Otolaryngol–Head and Neck Med and Surg (2015), http://dx.doi.org/10.1016/j.amjoto.2015.04.010
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antimicrobial therapy is often employed in this setting, the emergence of atypical bacterial pathogens and concerns for drug resistance, especially in the setting of post-endoscopic sinus surgery (ESS) refractory CRS, warrant the need for sinus cultures to guide targeted antibiotic therapy [3]. Rigid nasal endoscopy facilitates the capability of concurrent diagnostic visualization and to aspirate or swab purulence to identify the offending microorganism, to guide selection of appropriate antibiotics, and minimize risk of bacterial resistance. The microbiology of CRS is polymicrobial with assays demonstrating a wide range of bacteria. The predominant organisms reported include Staphylococcus aureus, coagulasenegative Staphylococcus (CNS), and various gram-negative rods, such as Pseudomonas aeruginosa, Escherichia coli, and Stenotrophomonas maltophilia [4]. The accrued literature on microbiology of CRS is quite disparate, reporting culture yield in the clinic and operative setting, various sinonasal subsites, and different assay techniques. With this in mind, the present study reviewed the available evidence base of microbiologic studies in CRS to better understand overall culture yield of the most common aerobic and anaerobic bacteria.
2.
Materials and methods
For this systematic review, the clinical indicator was endoscopically-derived bacterial cultures in CRS. The population of interest was adults with CRS without nasal polyps and acute exacerbation on CRS (AECRS). The objective of the review was to ascertain the prevalence of microorganisms yielded by endoscopic cultures based on clinical setting, paranasal sinus subsite, and assay technique. Criteria for inclusion into the evidence base review were as follows: 1. Index disease of (1) CRS without nasal polyposis or (2) acute exacerbation of CRS 2. No systemic or topical antibiotics received at least 1 week prior to culture 3. Cultures, regardless of the assay technique, were performed under endoscopic guidance
2.1.
inclusion and were also excluded. Four studies included both external cultures from maxillary taps and sterile cultures obtained during endoscopic sinus surgery [5,8,12,16]. These were included as the individual reported culture data were in congruence with the more recent endoscopically derived cultures. A total of 43 full-length articles were included for further systematic review and analysis (Fig. 1) [3,5–46].
2.3.
Data collection
Salient data collated from the studies included number of patients in each study, patient age, gender distribution, history of previous surgery, total culture specimens (positive and negative), number of isolates per positive culture separated by collecting method (swab, aspirate, and mucosal biopsy), and diagnostic yield of the most common aerobic and anaerobic organisms.
3.
Results
A total of 43 studies were accrued for the data analysis. Patients with CRS without polyps and CRS with/without polyps were reported in 40 (93.2%) and 3 (6.8%) studies, respectively. A total of 36 studies (83.7%) reported cultures in patients without previous surgery. The location of the specimen collection was the ambulatory clinic and operative suite in 10 (23.3%) and 33 (76.7%) studies, respectively. Twenty-three studies (53.5%) reported single site of culture, while 20 studies (46.5%) reported multiple sites. The reported culture technique was as follows: swab in 19 (44.2%), aspirate in 12 (27.9%), and mucosal biopsy in 2 (4.7%) series. Table 1 illustrates the salient characteristics of the 43 studies. A total of 3528 patients with median age of 36 years (range, 6–50 years) were accrued from the 43 studies. The gender of the patient group was 1932 males (60%) and 1288 females (40%). The total number of specimens collected from each site was 6005, with positive culture specimens being noted in 3826 cases (63.7%). A total of 6152 organisms were isolated in these
Literature search
Studies for inclusion were identified on PubMed (www.ncbi. nlm.nih.gov/pubmed) through search of the English language literature between 1975 to March 2010. Search terms included chronic sinusitis and microbiology, chronic sinusitis and bacteria, chronic sinusitis and culture, chronic sinusitis and aerobic culture, chronic sinusitis and anaerobic culture.
2.2.
Selection criteria for article inclusion
The PubMed search identified 205 abstracts available for further review. After removing 60 duplicates, a total of 145 citations remained. Both authors screened all abstracts independently. During the title and abstract screening, 77 citations were excluded leaving 68 citations for full-text review. An additional 25 studies did not fulfill the criteria for
Fig. 1 – Flowchart of literature retrieval in systematic review.
Please cite this article as: Thanasumpun T, Batra PS, Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review, Am J Otolaryngol–Head and Neck Med and Surg (2015), http://dx.doi.org/10.1016/j.amjoto.2015.04.010
AMER IC AN JOURNAL OF OT OLA RYNGOLOGY–H E A D A N D NE CK M E D ICI N E AN D S U RGE RY X X (2 0 1 5) XXX –XXX
Table 1 – Salient characteristics of the 43 studies. Clinical characteristic
Categories
No. Percent studies
Diagnosis of CRS subset
CRS Acute exacerbation of CRS CRS w/ or w/o polyps CRS or Acute exacerbation of CRS No Yes Not assigned Maxillary sinus Middle meatus Multiple Ethmoid cavity Operating Room Clinic Swab Aspirate Swab/Aspirate Swab/Aspirate/Mucosal biopsy Mucosal biopsy Swab/Mucosal biopsy Aspirate/Mucosal biopsy
37 3 2 1
86.0% 7.0% 4.7% 2.3%
36 6 1 18 12 9 4 33 10 19 12 4 3
83.7% 14.0% 2.3% 41.9% 27.9% 20.9% 9.3% 76.7% 23.3% 44.2% 27.9% 9.3% 7.0%
2 2 1
4.7% 4.7% 2.3%
Previous Surgery
Site of Culture
Specimen Collection Site Technique
positive culture specimens. The median number of organisms isolated by swab, aspirate, mucosal biopsy, and not separated by technique was 1.3, 1.3, 1.7, and 3.3, respectively (Table 2). The most common aerobic gram positive bacteria identified by culture included, CNS, S. aureus, and Streptococcus viridans, while the most common aerobic gram negative organisms included Haemophilus influenzae, P. aeruginosa, and Klebsiella pneumoniae. The most common anaerobes included Peptostreptococcus species, Bacteroides species, and Propionibacterium acnes (Table 3).
4.
Discussion
CRS is characterized by a protracted inflammatory process persisting for 3 months or longer. Despite the existing controversy on the role of bacteria in the central pathophysiology of CRS, it is likely that bacteria can serve as an important disease modifier in a subset of patients. Though acute rhinosinusitis (ARS) is characterized by predictably common
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acute pathogens (S. pneumoniae, H. influenzae, Moraxella catarrhalis), the microbiology of CRS can be varied. As chronicity develops, the bacteriology shifts from predominantly gram positive to gram negative bacteria as well as aerobic and facultative species being gradually replaced by anaerobes over time. The most common organisms in CRS include S. aureus, CNS, gram negative rods (GNRs), especially P. aeruginosa, and anaerobic bacteria. Empiric antimicrobial therapy is often being targeted against these offending pathogens; however, concern of atypical pathogens and emergence of drug resistance necessitate the need for sinus cultures to guide accurate treatment. The available literature on this topic can be conflicting with varied yields reported from different sinonasal sites by multiple assay techniques from both the operating room and ambulatory clinic setting. The current study examines the available evidence base of microbiologic studies in CRS to better understand culture yield of the most common bacteria. Historically, direct aspiration of the maxillary sinus during aseptic technique has served as a historical gold standard for obtaining purulence for accurate identification of causative pathogens with least amount of contamination. However, the procedure is invasive and may result in nasal discomfort, pain, and bleeding. Alternately, endoscopic-assisted cultures may be used to assay the microbiology of the paranasal sinuses. The data suggest endoscopically-guided cultures (EGCs) correlate well with culture taken directly from the maxillary sinus by antral tap. A recent study compared yield by endoscopic middle meatal aspiration and direct antral tap cultures before ESS, noting association between techniques was strong to moderate in 81.25% of cases [36]. Similarly, weighted pooled data in a meta-analysis by Dubin et al. demonstrated that endoscopic middle meatal culture correlated with maxillary sinus aspirates per culture and per isolate in 73% and 82%, respectively [47]. The pooled microbiologic data demonstrated that gram positive aerobes, followed by gram negative aerobes and anaerobes predominate in patients with CRS and AECRS. The two most common gram positive aerobes represented CNS and S. aureus in 34.7% and 26.5%, respectively. On the other hand, the most common gram negative aerobes included H. influenzae, P. aeruginosa, K. pneumoniae and E. coli in 26.7%, 21.6%, 10.9%, and 10.7%, respectively. Multiple studies have individually reported similar culture yield in CRS patients.
Table 2 – Salient features of the 43 studies. Label
Number of studies
Age (years) No. of patients Male Female Total culture specimens Positive culture specimens Negative culture specimens No. isolated per positive specimen: swab No. isolated per positive specimen: aspirate No. isolated per positive specimen: mucosal biopsy No. isolated per positive specimen: not separated by technique
37 43 39 39 43 39 39 25 13 6 3
Total of all studies 3528 1932 1288 6005 3826 1703
Median
Minimum
Maximum
36 52 31 24 91 54 16 1.3 1.3 1.7 3.3
6.3 6 4 2 12 12 0 0.7 0.7 1.2 2.1
50.4 419 268 151 609 442 181 4.2 4 3.8 3.3
Please cite this article as: Thanasumpun T, Batra PS, Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review, Am J Otolaryngol–Head and Neck Med and Surg (2015), http://dx.doi.org/10.1016/j.amjoto.2015.04.010
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Table 3 – Most common aerobic and anaerobic bacteria from the cultures. Type Total
Organism
Coagulase negative Staphylococcus Staphylococcus aureus Haemophilus influenzae Streptococcus viridans Pseudomonas aeruginosa Streptococcus pneumoniae Peptostreptococcus species Bacteroides species Alpha hemolytic Streptococcus Propionibacterium acnes Gram Positive Coagulase negative Aerobes Staphylococcus Staphylococcus aureus Streptococcus viridans Streptococcus pneumoniae Alpha hemolytic Streptococcus Corynebacterium species Beta-hemolytic Group A Streptococcus Streptococcus pyogenes Diphtheria bacillus Micrococcus Gram Negative Haemophilus influenzae Aerobes Pseudomonas aeruginosa Klebsiella pneumoniae Escherichia coli Moraxella (Branhamella) catarrhalis Haemophilus parainfluenzae Enterobacter aerogenes Proteus mirabilis Klebsiella oxytoca Stenotrophomonas maltophilia Anaerobes Peptostreptococcus species Bacteroides species Propionibacterium acnes Peptococcus species Bacteroides melaninogenicus Propionibacterium species Bacteroides fragilis Fusobacterium species Fusobacterium nucleatum Clostridium species
Bacterial Percent Count 630
24.8%
481 245 233 198 179 156 153 135
18.9% 9.6% 9.2% 7.8% 7.0% 6.1% 6.0% 5.3%
131 630
5.2% 34.7%
481 233 179 135
26.5% 12.8% 9.9% 7.4%
69 31
3.8% 1.7%
24 20 16 245 198 100 98 64
1.3% 1.1% 0.9% 26.7% 21.6% 10.9% 10.7% 7.0%
52 47 47 37 30 156 153 131 108 62 60 41 31 29 26
5.7% 5.1% 5.1% 4.0% 3.3% 19.6% 19.2% 16.4% 13.6% 7.8% 7.5% 5.1% 3.9% 3.6% 3.3%
Nadel et al. reported 507 EGC cultures of 256 patients with CRS and AECRS [3]. The results were compared to a control group of 50 cultures from healthy volunteers. GNRs were present in 27% of cultures and were more commonly seen in patients with prior sinus surgery or using irrigations. CNS occurred with the same incidence in patients and controls but was more prevalent in cultures obtained intraoperatively and in patients taking systemic steroids. S. aureus occurred at similar rates in patients and controls but grew heavily in CRS patients and exhibited only light growth in controls. Cincik and Ferguson obtained EGCs in 77 patients with CRS and AECRS [48]. The results illustrated a preponderance of
S. aureus, typical acute pathogens, and P. aeruginosa. There were no significant difference in frequency of pathogens between CRS and AECRS; however, acute pathogens (S. pneumoniae, H. influenzae, M. catarrhalis) usually emerged in episodes of AECRS. Bhattacharyya et al. determined the microbiology of exacerbations of CRS in 125 patients during post-ESS period [49]. Gram positive cocci (GPC) were recovered from 37.9% of the 290 culture specimens, with S. aureus and CNS being the most common organisms. GNRs constituted 14.8% of the isolates, with P. aeruginosa in 7.2% of cases. Klossek et al. obtained EGCs in 394 CRS patients; aerobes predominated, most commonly being S. aureus(18.6%), followed by CNS(23.9%) and S. viridians(10%) [2]. Finegold et al. performed an open-label multicenter study determining the bacteriology of chronic maxillary sinusitis in adults [50]. A total of 134 organisms isolated from 150 patients were considered pathogens. The most frequent aerobic pathogens were Streptococcus species (21.4%), H. influenzae (15.7%), P. aeruginosa (15.7%), and S. aureus and M. catarrhalis (10% each). Anaerobic bacteria constitute a predominant component of oropharyngeal mucous membranes bacterial flora, and represent a common source of bacterial infections of endogenous origin of upper respiratory tract and head and neck region. Although the association of anaerobes with CRS has been well reported, their role in pathogenicity is not fully understood. Studies in CRS utilizing proper culture technique have recovered anaerobes in 25%–56% of isolates [8,51]. Nord posits that these mixed groups of bacteria may interact synergistically, enhancing and prolonging the overall virulence of infection [51]. Anaerobic bacteria may further contribute to persistence of infection through their proposed ability to protect susceptible organisms by the production of beta-lactamases. CRS caused by anaerobes is a particular concern given that a variety of complications have been associated, including mucoceles, osteomyelitis, and intracranial abscess formation [52]. The pooled analysis corroborates that anaerobes represent important micro-organisms in CRS [53–55]. The most prevalent anaerobic bacteria were Peptostreptococcus species, followed by Bacteroides species and P. acnes. Nadel et al. assayed anaerobic bacteria in 47 of 106 cultures, with P.acnes being the most predominate anaerobe [3]. Klossek et al. recovered 159 anaerobic isolates in 101 patients, most commonly being Propionibacterium (32.1%), followed by Prevotella (18.2%) and Fusobacterium (8.8%) [2]. Finegold et al. identified 64 anaerobic isolates from 114 CRS patients [50]. The most commonly isolated anaerobes were Prevotella species (31.1%), anaerobic streptococci (21.9%), and Fusobacterium species (15.6%). These aforementioned studies attest to the prevalence of anaerobes in the CRS patient. Nonetheless, these results should be viewed with caution as “non-inflamed maxillary sinuses” can be colonized by a variety of anaerobes. Brook reported 33 anaerobic isolates in 12 patients (2.75 per specimen), with predominant organisms including Bacteroides species, anaerobic gram-positive cocci, and Fusobacterium species [54]. This pooled analysis should serve to apprise the clinician of the most common aerobic and anaerobic organisms in the CRS patient. It also underscores the microbiologic diversity and the potential polymicrobial nature of infectious exacerbations of CRS, especially in the setting of previous sinus surgery. Thus, endoscopically-derived cultures remain an
Please cite this article as: Thanasumpun T, Batra PS, Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review, Am J Otolaryngol–Head and Neck Med and Surg (2015), http://dx.doi.org/10.1016/j.amjoto.2015.04.010
AMER IC AN JOURNAL OF OT OLA RYNGOLOGY–H E A D A N D NE CK M E D ICI N E AN D S U RGE RY X X (2 0 1 5) XXX –XXX
imperative to accurately identify potential pathogens and to monitor drug resistance patterns. Important limitations of this data must be highlighted. The mere presence of these bacteria in cultures does not imply causality. In the carefully selected patient, an infectious exacerbation of specific bacteria may serve as an important disease modifier of the underlying sinonasal inflammatory process. However, this important fact cannot be discerned from this pooled data. The accrued data also are unable to account for patient and assay variables inherent to these studies. In fact, patient factors, such as age, gender, disease duration and extent, and concurrent medical therapy, and assay factors, including sample collection techniques, site of specimen, inoculation media, specimen transport method, and time between collection and cultivation of the sample could have greatly altered the organisms and their respective yield. These discrepancies could only be reconciled through large prospective databases that carefully control these potential factors, preferably in multicenter studies. Nonetheless, this preliminary database should serve to provide a template of the available microbiologic data to guide future studies.
5.
Conclusion
The present analysis provides a composite of the previous microbiologic studies to date. It serves to highlight the most common aerobic and anaerobic micro-organisms assayed in patients with CRS or acute exacerbations of CRS. Coagulase negative Staphylococcus and S. aureus represent the most common gram positive aerobes, while H. influenzae and P. aeruginosa signify the most common gram negative aerobes. Anaerobes comprise an important component of the polymicrobial flora, most commonly by Peptostreptococcus species and Bacteroides species. Though the exact role of these pathogens in the pathophysiology remains to be elucidated, they are frequently cultured in the CRS patient and may play an important role as disease modifiers. Importantly, establishment of the correct microbiology of CRS by endoscopically-derived cultures is imperative to guide accurate antimicrobial therapy, especially given concerns for antibiotic resistance in the recalcitrant patient.
Acknowledgments The authors are grateful to Liyue Tong, MS from the Department of Clinical Sciences at UT Southwestern Medical Center for the data analysis.
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Please cite this article as: Thanasumpun T, Batra PS, Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review, Am J Otolaryngol–Head and Neck Med and Surg (2015), http://dx.doi.org/10.1016/j.amjoto.2015.04.010
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Original contribution
Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review☆ Thunchai Thanasumpun, MD a , Pete S. Batra, MD, FACS b,⁎ a
Department of Otolaryngology-Head and Neck Surgery Faculty of Medicine Vajira Hospital, University of Bangkok Metropolis Navamindradhiraj, Bangkok, Thailand b Department of Otorhinolaryngology-Head and Neck Surgery, Rush University Medical Center, Chicago, Illinois
ARTI CLE I NFO
A BS TRACT
Article history:
Background: Culture-directed antibiotic therapy represents an important component in the
Received 4 February 2015
management paradigm of chronic rhinosinusitis (CRS). The objective of this study was to systematically review the literature to assess culture yield of the most common aerobic and anaerobic pathogens. Methods: A total of 43 studies between 1975 and 2010 were included. Results: The composite data comprised 3528 patients with 6005 total culture specimens. The cultures were obtained in operating room in 33 (76.7%) and clinic in 10 (23.3%) of the studies, respectively. The most common site of culture was the maxillary sinus in 18 (41.9%) of the studies. The most common assay techniques reported were swab in 19 (44.2%) and aspirate in 12 (27.9%) studies. The most common gram positive aerobes reported were coagulase negative Staphylococcus and Staphylococcus aureus in 630 (34.7%) and 481 (26.5%) of the cultures, respectively. The most common gram negative aerobes included Haemophilus influenzae and Pseudomonas aeruginosa in 245 (27.0%) and 198 (21.6%) cultures, respectively. The most common anaerobes reported were Peptostreptococcus species in 156 (19.6%) and Bacteroides species in 153 (19.2%) cultures. Conclusion: This study provides a composite snapshot of the literature accrued on the microbiology of CRS. It should serve to apprise clinicians on the most common aerobic and anaerobic organisms in CRS patients when employing culture-directed antimicrobial therapy. © 2015 Elsevier Inc. All rights reserved.
1.
Introduction
Chronic rhinosinusitis (CRS) represents an inflammatory disorder of at least 3 months’ duration caused by a multitude of etiologies, including microbes (viruses, bacteria, fungi), biofilm, Staphylococcus superantigen, ciliary dysfunction, and derange-
ments in innate and adaptive immunity [1]. The role of infection as a potential pathophysiologic mechanism in CRS has been a source of considerable debate and, at times, controversy in rhinology. Nonetheless, bacterial superinfection is commonly observed during acute exacerbations of CRS contributing to ongoing recalcitrant CRS [2]. Though empiric
☆ Disclosures: TT: none. PSB: Advisory Board (Merck). These data were presented as an oral presentation at the IFOS meeting in Seoul, South Korea held June 1st–5th, 2013. ⁎ Corresponding author at: Department of Otorhinolaryngology-Head and Neck Surgery, Rush University Medical Center, 1611 W. Harrison St., Suite 550, Chicago, IL, 60612. Tel.: +1 312 942 7182; fax: + 1 312 942 6653. E-mail address: [email protected] (P.S. Batra).
http://dx.doi.org/10.1016/j.amjoto.2015.04.010 0196-0709/© 2015 Elsevier Inc. All rights reserved.
Please cite this article as: Thanasumpun T, Batra PS, Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review, Am J Otolaryngol–Head and Neck Med and Surg (2015), http://dx.doi.org/10.1016/j.amjoto.2015.04.010
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antimicrobial therapy is often employed in this setting, the emergence of atypical bacterial pathogens and concerns for drug resistance, especially in the setting of post-endoscopic sinus surgery (ESS) refractory CRS, warrant the need for sinus cultures to guide targeted antibiotic therapy [3]. Rigid nasal endoscopy facilitates the capability of concurrent diagnostic visualization and to aspirate or swab purulence to identify the offending microorganism, to guide selection of appropriate antibiotics, and minimize risk of bacterial resistance. The microbiology of CRS is polymicrobial with assays demonstrating a wide range of bacteria. The predominant organisms reported include Staphylococcus aureus, coagulasenegative Staphylococcus (CNS), and various gram-negative rods, such as Pseudomonas aeruginosa, Escherichia coli, and Stenotrophomonas maltophilia [4]. The accrued literature on microbiology of CRS is quite disparate, reporting culture yield in the clinic and operative setting, various sinonasal subsites, and different assay techniques. With this in mind, the present study reviewed the available evidence base of microbiologic studies in CRS to better understand overall culture yield of the most common aerobic and anaerobic bacteria.
2.
Materials and methods
For this systematic review, the clinical indicator was endoscopically-derived bacterial cultures in CRS. The population of interest was adults with CRS without nasal polyps and acute exacerbation on CRS (AECRS). The objective of the review was to ascertain the prevalence of microorganisms yielded by endoscopic cultures based on clinical setting, paranasal sinus subsite, and assay technique. Criteria for inclusion into the evidence base review were as follows: 1. Index disease of (1) CRS without nasal polyposis or (2) acute exacerbation of CRS 2. No systemic or topical antibiotics received at least 1 week prior to culture 3. Cultures, regardless of the assay technique, were performed under endoscopic guidance
2.1.
inclusion and were also excluded. Four studies included both external cultures from maxillary taps and sterile cultures obtained during endoscopic sinus surgery [5,8,12,16]. These were included as the individual reported culture data were in congruence with the more recent endoscopically derived cultures. A total of 43 full-length articles were included for further systematic review and analysis (Fig. 1) [3,5–46].
2.3.
Data collection
Salient data collated from the studies included number of patients in each study, patient age, gender distribution, history of previous surgery, total culture specimens (positive and negative), number of isolates per positive culture separated by collecting method (swab, aspirate, and mucosal biopsy), and diagnostic yield of the most common aerobic and anaerobic organisms.
3.
Results
A total of 43 studies were accrued for the data analysis. Patients with CRS without polyps and CRS with/without polyps were reported in 40 (93.2%) and 3 (6.8%) studies, respectively. A total of 36 studies (83.7%) reported cultures in patients without previous surgery. The location of the specimen collection was the ambulatory clinic and operative suite in 10 (23.3%) and 33 (76.7%) studies, respectively. Twenty-three studies (53.5%) reported single site of culture, while 20 studies (46.5%) reported multiple sites. The reported culture technique was as follows: swab in 19 (44.2%), aspirate in 12 (27.9%), and mucosal biopsy in 2 (4.7%) series. Table 1 illustrates the salient characteristics of the 43 studies. A total of 3528 patients with median age of 36 years (range, 6–50 years) were accrued from the 43 studies. The gender of the patient group was 1932 males (60%) and 1288 females (40%). The total number of specimens collected from each site was 6005, with positive culture specimens being noted in 3826 cases (63.7%). A total of 6152 organisms were isolated in these
Literature search
Studies for inclusion were identified on PubMed (www.ncbi. nlm.nih.gov/pubmed) through search of the English language literature between 1975 to March 2010. Search terms included chronic sinusitis and microbiology, chronic sinusitis and bacteria, chronic sinusitis and culture, chronic sinusitis and aerobic culture, chronic sinusitis and anaerobic culture.
2.2.
Selection criteria for article inclusion
The PubMed search identified 205 abstracts available for further review. After removing 60 duplicates, a total of 145 citations remained. Both authors screened all abstracts independently. During the title and abstract screening, 77 citations were excluded leaving 68 citations for full-text review. An additional 25 studies did not fulfill the criteria for
Fig. 1 – Flowchart of literature retrieval in systematic review.
Please cite this article as: Thanasumpun T, Batra PS, Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review, Am J Otolaryngol–Head and Neck Med and Surg (2015), http://dx.doi.org/10.1016/j.amjoto.2015.04.010
AMER IC AN JOURNAL OF OT OLA RYNGOLOGY–H E A D A N D NE CK M E D ICI N E AN D S U RGE RY X X (2 0 1 5) XXX –XXX
Table 1 – Salient characteristics of the 43 studies. Clinical characteristic
Categories
No. Percent studies
Diagnosis of CRS subset
CRS Acute exacerbation of CRS CRS w/ or w/o polyps CRS or Acute exacerbation of CRS No Yes Not assigned Maxillary sinus Middle meatus Multiple Ethmoid cavity Operating Room Clinic Swab Aspirate Swab/Aspirate Swab/Aspirate/Mucosal biopsy Mucosal biopsy Swab/Mucosal biopsy Aspirate/Mucosal biopsy
37 3 2 1
86.0% 7.0% 4.7% 2.3%
36 6 1 18 12 9 4 33 10 19 12 4 3
83.7% 14.0% 2.3% 41.9% 27.9% 20.9% 9.3% 76.7% 23.3% 44.2% 27.9% 9.3% 7.0%
2 2 1
4.7% 4.7% 2.3%
Previous Surgery
Site of Culture
Specimen Collection Site Technique
positive culture specimens. The median number of organisms isolated by swab, aspirate, mucosal biopsy, and not separated by technique was 1.3, 1.3, 1.7, and 3.3, respectively (Table 2). The most common aerobic gram positive bacteria identified by culture included, CNS, S. aureus, and Streptococcus viridans, while the most common aerobic gram negative organisms included Haemophilus influenzae, P. aeruginosa, and Klebsiella pneumoniae. The most common anaerobes included Peptostreptococcus species, Bacteroides species, and Propionibacterium acnes (Table 3).
4.
Discussion
CRS is characterized by a protracted inflammatory process persisting for 3 months or longer. Despite the existing controversy on the role of bacteria in the central pathophysiology of CRS, it is likely that bacteria can serve as an important disease modifier in a subset of patients. Though acute rhinosinusitis (ARS) is characterized by predictably common
3
acute pathogens (S. pneumoniae, H. influenzae, Moraxella catarrhalis), the microbiology of CRS can be varied. As chronicity develops, the bacteriology shifts from predominantly gram positive to gram negative bacteria as well as aerobic and facultative species being gradually replaced by anaerobes over time. The most common organisms in CRS include S. aureus, CNS, gram negative rods (GNRs), especially P. aeruginosa, and anaerobic bacteria. Empiric antimicrobial therapy is often being targeted against these offending pathogens; however, concern of atypical pathogens and emergence of drug resistance necessitate the need for sinus cultures to guide accurate treatment. The available literature on this topic can be conflicting with varied yields reported from different sinonasal sites by multiple assay techniques from both the operating room and ambulatory clinic setting. The current study examines the available evidence base of microbiologic studies in CRS to better understand culture yield of the most common bacteria. Historically, direct aspiration of the maxillary sinus during aseptic technique has served as a historical gold standard for obtaining purulence for accurate identification of causative pathogens with least amount of contamination. However, the procedure is invasive and may result in nasal discomfort, pain, and bleeding. Alternately, endoscopic-assisted cultures may be used to assay the microbiology of the paranasal sinuses. The data suggest endoscopically-guided cultures (EGCs) correlate well with culture taken directly from the maxillary sinus by antral tap. A recent study compared yield by endoscopic middle meatal aspiration and direct antral tap cultures before ESS, noting association between techniques was strong to moderate in 81.25% of cases [36]. Similarly, weighted pooled data in a meta-analysis by Dubin et al. demonstrated that endoscopic middle meatal culture correlated with maxillary sinus aspirates per culture and per isolate in 73% and 82%, respectively [47]. The pooled microbiologic data demonstrated that gram positive aerobes, followed by gram negative aerobes and anaerobes predominate in patients with CRS and AECRS. The two most common gram positive aerobes represented CNS and S. aureus in 34.7% and 26.5%, respectively. On the other hand, the most common gram negative aerobes included H. influenzae, P. aeruginosa, K. pneumoniae and E. coli in 26.7%, 21.6%, 10.9%, and 10.7%, respectively. Multiple studies have individually reported similar culture yield in CRS patients.
Table 2 – Salient features of the 43 studies. Label
Number of studies
Age (years) No. of patients Male Female Total culture specimens Positive culture specimens Negative culture specimens No. isolated per positive specimen: swab No. isolated per positive specimen: aspirate No. isolated per positive specimen: mucosal biopsy No. isolated per positive specimen: not separated by technique
37 43 39 39 43 39 39 25 13 6 3
Total of all studies 3528 1932 1288 6005 3826 1703
Median
Minimum
Maximum
36 52 31 24 91 54 16 1.3 1.3 1.7 3.3
6.3 6 4 2 12 12 0 0.7 0.7 1.2 2.1
50.4 419 268 151 609 442 181 4.2 4 3.8 3.3
Please cite this article as: Thanasumpun T, Batra PS, Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review, Am J Otolaryngol–Head and Neck Med and Surg (2015), http://dx.doi.org/10.1016/j.amjoto.2015.04.010
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Table 3 – Most common aerobic and anaerobic bacteria from the cultures. Type Total
Organism
Coagulase negative Staphylococcus Staphylococcus aureus Haemophilus influenzae Streptococcus viridans Pseudomonas aeruginosa Streptococcus pneumoniae Peptostreptococcus species Bacteroides species Alpha hemolytic Streptococcus Propionibacterium acnes Gram Positive Coagulase negative Aerobes Staphylococcus Staphylococcus aureus Streptococcus viridans Streptococcus pneumoniae Alpha hemolytic Streptococcus Corynebacterium species Beta-hemolytic Group A Streptococcus Streptococcus pyogenes Diphtheria bacillus Micrococcus Gram Negative Haemophilus influenzae Aerobes Pseudomonas aeruginosa Klebsiella pneumoniae Escherichia coli Moraxella (Branhamella) catarrhalis Haemophilus parainfluenzae Enterobacter aerogenes Proteus mirabilis Klebsiella oxytoca Stenotrophomonas maltophilia Anaerobes Peptostreptococcus species Bacteroides species Propionibacterium acnes Peptococcus species Bacteroides melaninogenicus Propionibacterium species Bacteroides fragilis Fusobacterium species Fusobacterium nucleatum Clostridium species
Bacterial Percent Count 630
24.8%
481 245 233 198 179 156 153 135
18.9% 9.6% 9.2% 7.8% 7.0% 6.1% 6.0% 5.3%
131 630
5.2% 34.7%
481 233 179 135
26.5% 12.8% 9.9% 7.4%
69 31
3.8% 1.7%
24 20 16 245 198 100 98 64
1.3% 1.1% 0.9% 26.7% 21.6% 10.9% 10.7% 7.0%
52 47 47 37 30 156 153 131 108 62 60 41 31 29 26
5.7% 5.1% 5.1% 4.0% 3.3% 19.6% 19.2% 16.4% 13.6% 7.8% 7.5% 5.1% 3.9% 3.6% 3.3%
Nadel et al. reported 507 EGC cultures of 256 patients with CRS and AECRS [3]. The results were compared to a control group of 50 cultures from healthy volunteers. GNRs were present in 27% of cultures and were more commonly seen in patients with prior sinus surgery or using irrigations. CNS occurred with the same incidence in patients and controls but was more prevalent in cultures obtained intraoperatively and in patients taking systemic steroids. S. aureus occurred at similar rates in patients and controls but grew heavily in CRS patients and exhibited only light growth in controls. Cincik and Ferguson obtained EGCs in 77 patients with CRS and AECRS [48]. The results illustrated a preponderance of
S. aureus, typical acute pathogens, and P. aeruginosa. There were no significant difference in frequency of pathogens between CRS and AECRS; however, acute pathogens (S. pneumoniae, H. influenzae, M. catarrhalis) usually emerged in episodes of AECRS. Bhattacharyya et al. determined the microbiology of exacerbations of CRS in 125 patients during post-ESS period [49]. Gram positive cocci (GPC) were recovered from 37.9% of the 290 culture specimens, with S. aureus and CNS being the most common organisms. GNRs constituted 14.8% of the isolates, with P. aeruginosa in 7.2% of cases. Klossek et al. obtained EGCs in 394 CRS patients; aerobes predominated, most commonly being S. aureus(18.6%), followed by CNS(23.9%) and S. viridians(10%) [2]. Finegold et al. performed an open-label multicenter study determining the bacteriology of chronic maxillary sinusitis in adults [50]. A total of 134 organisms isolated from 150 patients were considered pathogens. The most frequent aerobic pathogens were Streptococcus species (21.4%), H. influenzae (15.7%), P. aeruginosa (15.7%), and S. aureus and M. catarrhalis (10% each). Anaerobic bacteria constitute a predominant component of oropharyngeal mucous membranes bacterial flora, and represent a common source of bacterial infections of endogenous origin of upper respiratory tract and head and neck region. Although the association of anaerobes with CRS has been well reported, their role in pathogenicity is not fully understood. Studies in CRS utilizing proper culture technique have recovered anaerobes in 25%–56% of isolates [8,51]. Nord posits that these mixed groups of bacteria may interact synergistically, enhancing and prolonging the overall virulence of infection [51]. Anaerobic bacteria may further contribute to persistence of infection through their proposed ability to protect susceptible organisms by the production of beta-lactamases. CRS caused by anaerobes is a particular concern given that a variety of complications have been associated, including mucoceles, osteomyelitis, and intracranial abscess formation [52]. The pooled analysis corroborates that anaerobes represent important micro-organisms in CRS [53–55]. The most prevalent anaerobic bacteria were Peptostreptococcus species, followed by Bacteroides species and P. acnes. Nadel et al. assayed anaerobic bacteria in 47 of 106 cultures, with P.acnes being the most predominate anaerobe [3]. Klossek et al. recovered 159 anaerobic isolates in 101 patients, most commonly being Propionibacterium (32.1%), followed by Prevotella (18.2%) and Fusobacterium (8.8%) [2]. Finegold et al. identified 64 anaerobic isolates from 114 CRS patients [50]. The most commonly isolated anaerobes were Prevotella species (31.1%), anaerobic streptococci (21.9%), and Fusobacterium species (15.6%). These aforementioned studies attest to the prevalence of anaerobes in the CRS patient. Nonetheless, these results should be viewed with caution as “non-inflamed maxillary sinuses” can be colonized by a variety of anaerobes. Brook reported 33 anaerobic isolates in 12 patients (2.75 per specimen), with predominant organisms including Bacteroides species, anaerobic gram-positive cocci, and Fusobacterium species [54]. This pooled analysis should serve to apprise the clinician of the most common aerobic and anaerobic organisms in the CRS patient. It also underscores the microbiologic diversity and the potential polymicrobial nature of infectious exacerbations of CRS, especially in the setting of previous sinus surgery. Thus, endoscopically-derived cultures remain an
Please cite this article as: Thanasumpun T, Batra PS, Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review, Am J Otolaryngol–Head and Neck Med and Surg (2015), http://dx.doi.org/10.1016/j.amjoto.2015.04.010
AMER IC AN JOURNAL OF OT OLA RYNGOLOGY–H E A D A N D NE CK M E D ICI N E AN D S U RGE RY X X (2 0 1 5) XXX –XXX
imperative to accurately identify potential pathogens and to monitor drug resistance patterns. Important limitations of this data must be highlighted. The mere presence of these bacteria in cultures does not imply causality. In the carefully selected patient, an infectious exacerbation of specific bacteria may serve as an important disease modifier of the underlying sinonasal inflammatory process. However, this important fact cannot be discerned from this pooled data. The accrued data also are unable to account for patient and assay variables inherent to these studies. In fact, patient factors, such as age, gender, disease duration and extent, and concurrent medical therapy, and assay factors, including sample collection techniques, site of specimen, inoculation media, specimen transport method, and time between collection and cultivation of the sample could have greatly altered the organisms and their respective yield. These discrepancies could only be reconciled through large prospective databases that carefully control these potential factors, preferably in multicenter studies. Nonetheless, this preliminary database should serve to provide a template of the available microbiologic data to guide future studies.
5.
Conclusion
The present analysis provides a composite of the previous microbiologic studies to date. It serves to highlight the most common aerobic and anaerobic micro-organisms assayed in patients with CRS or acute exacerbations of CRS. Coagulase negative Staphylococcus and S. aureus represent the most common gram positive aerobes, while H. influenzae and P. aeruginosa signify the most common gram negative aerobes. Anaerobes comprise an important component of the polymicrobial flora, most commonly by Peptostreptococcus species and Bacteroides species. Though the exact role of these pathogens in the pathophysiology remains to be elucidated, they are frequently cultured in the CRS patient and may play an important role as disease modifiers. Importantly, establishment of the correct microbiology of CRS by endoscopically-derived cultures is imperative to guide accurate antimicrobial therapy, especially given concerns for antibiotic resistance in the recalcitrant patient.
Acknowledgments The authors are grateful to Liyue Tong, MS from the Department of Clinical Sciences at UT Southwestern Medical Center for the data analysis.
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Please cite this article as: Thanasumpun T, Batra PS, Endoscopically-derived bacterial cultures in chronic rhinosinusitis: A systematic review, Am J Otolaryngol–Head and Neck Med and Surg (2015), http://dx.doi.org/10.1016/j.amjoto.2015.04.010
