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Microbiology and choice of antimicrobial therapy for acute sinusitis complicated by subperiosteal abscess in children
International Journal of Pediatric Otorhinolaryngology 84 (2016) 21–26
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International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Review Article
Microbiology and choice of antimicrobial therapy for acute sinusitis complicated by subperiosteal abscess in children Itzhak Brook * Department of Pediatrics, Georgetown University School of Medicine, Washington, DC, USA
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 January 2016 Received in revised form 17 February 2016 Accepted 18 February 2016 Available online 26 February 2016
Objectives: Review past studies of the microbiology of subperiosteal abscesses (SPOA) complicating sinusitis in children and their implications of the antimicrobials administered to treat the infection. Methods: Literature search was conducted of the Cochrane Library, EMBASE, TRIP, EMBASE, and MEDLINE databases from their inception. Results: The most common pathogens isolated from studies of SPOA complicating sinusitis are aerobic (Streptococcus pneumoniae, Streptococcus spp., Haemophilus spp., Eikenella corrodens), anaerobic (Peptostreptococcus, Fusobacterium, Prevotella, Porphyromonas, Bacteroides, and Veillonella spp.), and micoaerophilic streptococci (Streptococcus anginosus/Streptococcus milleri group), all members of the oropharyngeal flora. S. pneumoniae and S. aureus were more frequently recovered in children >7 years old, while polymicrobial aerobic–anaerobic flora were more often isolated from those >15 years. The introduction of pneumococcal vaccine reduced the rate of isolation of S. pneumoniae, and correlated with increase of recovery of S. aureus including methicillin resistant strains, as well as Streptococcus pyogenes and S. anginosus/milleri group. Conclusions: The microbiology and consequently the treatment of respiratory infections including sinusitis and its complications has evolved over the past decades. Establishing the microbiology of SPOA by obtaining appropriate cultures for both aerobic and anaerobic bacteria are essential for proper antimicrobial selection. ß 2016 Elsevier Ireland Ltd. All rights reserved.
Keywords: Subperiosteal abscesses Acute sinusitis Microbiology Anaerobic bacteria Staphylococcus aureus Sinusitis
Contents 1. 2. 3. 4. 5.
Introduction . . . . . . . . . Materials and methods Results . . . . . . . . . . . . . Discussion . . . . . . . . . . Conclusions . . . . . . . . . References . . . . . . . . . .
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1. Introduction Sinusitis can cause local and systemic complications. Subperiosteal abscess (SPOA) is an uncommon complication of acute sinusitis in children. The majority of local complications including
* Correspondence to: 4431 Albemarle St. NW, Washington, DC 20016, USA. Tel.: +1 202 364 4253. E-mail address: [email protected] http://dx.doi.org/10.1016/j.ijporl.2016.02.022 0165-5876/ß 2016 Elsevier Ireland Ltd. All rights reserved.
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SPOA are anatomically linked to the paranasal sinuses [1]. The rates of these complications are not known, but it is estimated that they occur in about 5% of patients hospitalized for sinusitis. Numerous studies evaluated the microbiology of SPOA over the past 5 decades [2–27]. Establishing the bacterial etiology of SPOA is important in understanding the pathophysiology of the infection and enables the appropriate choice of antimicrobial therapy. The microbiology and consequently the treatment of respiratory infections including sinusitis and its complications have evolved over the past decades. The changes in microbiology were
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I. Brook / International Journal of Pediatric Otorhinolaryngology 84 (2016) 21–26
associated with the introduction of vaccinations against Haemophilus influenzae and Streptococcus pneumoniae, and the growing resistance to antimicrobials [17,27]. This review presents past studies of the microbiology of SPOA complicating sinusitis in children and their implications of antimicrobials administered to treat the infection. 2. Materials and methods A literature search was conducted of the Cochrane Library, EMBASE, TRIP, and MEDLINE databases from their inception (1993 for the Cochrane Library, 1980 for EMBASE, 1997 for TRIP, and 1966 for MEDLINE) through October 25, 2015. The following search terms were used: sinusitis, complications, SPOA, microbiology, S. pneumoniae, H. influenzae, Staphylococcus aureus, and anaerobic bacteria. Results of these searches were closely evaluated, and articles and documents that were not pertinent or redundant were excluded. This review was focused on the microbiology of SPOA in children. 3. Results Many studies have investigated the microbiology of SPOA [2–27]. Four studies also included adults [12,18,23,25] (Table 1). Schramm et al., [2,3] evaluated 32 children and adults with SPOA. The predominate isolates were Stapylococcus, Streptococcus and Bacteroides spp. Brook et al. [4] studied 8 children with periorbital cellulitis and other complications of sinusitis. SPOA was present in two children who had ethmoiditis. Anaerobic bacteria were isolated from the infected sinuses in all the patients and no aerobic organisms were found. The isolates recovered from the sinuses of the two children with SPOA were Fusobacterium nucleatum, Prevotella oralis, Prevotella melaninogenica, Peptostreptococcus spp., Veillonella parvula, and microaerophilic streptococci. Skau et al. [5] reported 12 children, 3 with intracranial and 9 with orbital complications of ethmoidal and frontal sinusitis. SPOA was found in 6 patients; two each had Bacteroides spp., and alpha streptococci, and one each had Peptostreptococci and beta-hemolytic streptococci. Spires and Smith [6] studied 241 children with periorbital or orbital soft-tissue infections treated from 1962 to 1986. Two hundred twenty-six children (94%), half <1 year of age, had periorbital soft-tissue infections. Orbital infections occurred in 15 (6%) children, 11 (5%) had orbital cellulitis (9 associated with sinusitis), 3 (1.2%) had SPOA (2 associated with sinusitis), and one had cavernous sinus thrombosis. One child with SPOA developed brain abscess. The organisms recovered in those with a sinus etiology were Staphylococcus spp. (20 isolates), Streptococcus spp., and anaerobes (4 each), and H. influenzae [1]. Williams and Harrison [7] reports 16 children with SPOA associated with acute sinusitis. The recovered organisms were Streptococcus milleri (6 isolates); H. influenzae, anaerobic cocci, and S. aureus (2 each); and Streptococcus group F, Streptococcus pyogenes, and S. pneumoniae (one each). Williams and Carruth [8] described 18 children with orbital infections secondary to sinusitis. Two had intracranial complications and 9 had SPOA. No organisms were isolated from 5 of the 15 patients, S. aureus, H. influenzae and S. milleri were identified in 3 each, and Bacteroides spp. in one. Skedros et al. [9] reviewed 21 children seen from 1983 to 1990 who had surgical intervention for SPOA. The organisms recovered included: 8 (38% of abscesses) S. pneumoniae, 7 (33%) S. pyogenes, and 3 (14%) H. influenzae. Anaerobes (Fusobacterium, Bacteroides, and Peptostreptococcus spp., mixed with Eikenella and Actinobacter spp.) were isolated from a single patient. However,
adequate methodologies for transportation and cultivation of anaerobes were not employed in this study. Arjmand et al. [10] reported on 18 children with SPOA complicating sinusitis treated from 1983 to 1992. Organisms were isolated from 13 (72%) of the patients; eight of them had polymicrobial flora including four with aerobic and anaerobic bacteria. Staphylococcus or Streptococcus spp. accounted for all single organism infections. The predominate aerobic isolates were Streptococcus and Staphylococcus spp., S. pneumoniae and H. influenzae. The most common anaerobes were Fusobacterium and Bacteroides spp. Harris [11] reviewed the records of 37 patients with SPOA admitted between 1977 and 1992. Variations in the microbiology of SPOA appear to be age-associated. Among 12 patients <9 years, two had bacterial growth of S. pneumoniae and S. aureus. The organisms found in 12 of 16 of 9–14 years old patients where Streptococcus spp. (alpha and beta hemolytic groups A, C and D), Stapylococcus spp., H. influenzae, M. catarrhalis, Eikenella corrodens, Klebsiella pneumoniae, Prevottela intermedia and V. parvula. Polymicrobial aerobic–anaerobic infection occurred in all of individuals >15 years. The organism recovered were Streptococcus spp. (alpha and beta hemolytic groups A, B and D), Stapylococcus spp., E. corrodens; microaerophilic streptococci, V. parvula, Bacteroides fragilis, and Prevotella, Porphyromonas, Fusobacterium, and Peptostreptococcus spp. Brook and Frazier [12] using strict methodology for identification of aerobic and anaerobic bacteria studied the microbiology of pus aspirates from eight adults with SPOA and their corresponding infected sinuses. Polymicrobial flora was found in all instances, and the number of isolates varied from two to five. Anaerobes were recovered from all specimens. The predominant isolates were Peptostreptococcus, Prevotella, and Fusobacterium spp, S. aureus, and microaerophilic streptococci. Concordance in the microbiological findings between SPOA and the corresponding infected sinus was found in all instances. However, certain organisms were only present at one site and not the other. Fourteen beta-lactamaseproducing organisms were present in nine specimens. Even though no children were included in this study, it illustrates that utilization of appropriate methodology for the recovery of anaerobes can lead to their recovery. Herrmann and Forsen [13] evaluated 74 children seen from 1990 to 2002 with orbital complications of acute sinusitis. There were no intracranial complications in children admitted for orbital complications of acute sinusitis that were <7 years, in contrast to 4 of 43 (9.3%) of patients >7 years had such a complication. All intraoperative cultures obtained from the 4 patients (two had SPOA) with intracranial extension were polymicrobial. The isolates included group C streptococci, E. corrodens, Haemophillus parainfluenzae, Streptococcus viridans, Staphylococcus epidermidis, Fusobacterium necrophorum, B. fragilis, and S. milleri. Nageswaran et al. [14] studied 41 children with orbital cellulitis seen from 1992 to 2002, 34 (83%) of whom had SPOA and/or orbital abscess. The predominate aerobes were Streptococcus spp. (alpha and groups A and C beta-hemolytic, and non-hemolytic), S. aureus, H. influenzae, E. corrodens, and M. cattarhalis. The commonest anaerobes were Peptostreptococcus and Bacteroides spp. Oxford and McClay [15] evaluated the microbiology of 21 children with SPOA complicating acute sinusitis seen between 1995 and 2002. The predominate isolates were 7 (33%) S. milleri group, 6 (29%) S. aureus, 3 (14%) S. pneumoniae, 2 (9.5%) each of alpha hemolytic streptococci and Eikenella spp., and H. influenzae, and one (5%) each of Bacteroides, Propionibacterium, Porphyromonas, and Peptstreptococcus spp. Sinclair et al. [16] reviewed 39 children seen between 1996 to 2005 that had surgical drainage of a SPOA complicating acute sinusitis. The predominate isolates were Streptococcus spp. (20 isolates, including 6 Streptococcus
I. Brook / International Journal of Pediatric Otorhinolaryngology 84 (2016) 21–26
23
Table 1 Studies of the microbiology of subperiosteal abscesses complicating of sinusitis in children. Author(s)
Year
Number patients
Microbiology
Comments
Schramm et al. [2,3]
32
Skau et al. [5]
1984
6
Spires & Smith [6]
1986
3
Williams & Harrison [7]
1991
16
Williams& Carruth [8]
1992
9
Skedros et al. [9]
1993
21
Arjmand et al. [10]
1993
18
Harris [11]
1994
37
Brook and Frazier [12]
1996
8
Herrmann and Forsen [13]
2004
2
Nageswaran et al. [14]
2006
34
Oxford & McClay [15]
2006
21
Sinclair & Berkowitz [16] Sulte´sz et al. [17]
2007 2009
39 4
Liao et al. [18]
2010
19 adults 11 children
Soon [19] Fanella et al. [20] Huang et al. [21]
2011 2011 2011
3 12 64
Eviatar et al. [22]
2012
22
Ketenci et al. [23]
2013
36
˜ a et al. [24] Pen
2013
273
ˇ et al. [25] Sˇuchan Stokken et al. [26]
2014 2014
8 8
Liao & Harris [27]
2015
67
Stapylococcus spp. Streptococcus spp. Bacteroides spp. Fusobacterium nucleatum P. oralis, P. melaninogenica Peptostreptococcus spp. V. parvula, Microaerophilic streptococci Bacteroides spp., Peptostreptococcus spp. beta- and alpha hemolytic streptococci. Streptococcus spp. Staphylococcus spp. H. influenzae, Anaerobes S. milleri, H. influenzae, S. aureus streptococcus group F, S. pyogenes, S. pneumoniae, Peptostreptococcus spp. S. aureus, H. influenzae S. milleri, Bacteroides spp S. pneumoniae, S. pyogenes H. influenza, Eikenella spp., Actinobacter spp., Fusobacterium, Bacteroides, and Peptostreptococcus spp., Streptococcus & Staphylococcus spp., S. pneumoniae, H. influenzae, Fusobacterium spp., Bacteroides spp. S. pneumoniae, S. aureus, Streptococcus spp. Stapylococcus spp., H influenzae, M. catarrhalis, E. corrodens, K. pneumoniae, P. intermedia, V. parvula, Prevotella spp., Porphyromonas spp., B. fragilis, Fusobacterium spp., Peptostreptococcus spp., V. parvula, and microaerophilic streptococci were isolated. Peptostreptococcus spp, Prevotella spp, Fusobacterium spp, S. aureus, microaerophilic streptococci Group C streptococci, E. corrodens, H. parainfluenzae, S. viridans, S. epidermidis, F. necrophorum, B.fragilis, S. milleri. Streptococcus spp., S. aureus, H. influenzae, E. corrodens, M. cattarhalis, Peptostreptococcus spp.,Bacteroides spp. S. milleri group, S. aureus, S. pneumoniae, S. viridans, Eikenella spp., H. influenzae, Bacteroides spp., Propionibacterium spp., Porphyromonas spp., Peptstreptococcus spp. Streptococcus spp., S. aureus, Haemophillus spp. S. pneumoniae, S. aureus, S. epidermidis, H. influenzae, S. viridans Beta-hem. Strep groups A and C, S. anginosus/ milleri, S. aureus, S. epidermidis, H. influenzae, H. aphrophilus, P. acnes, Klebsiella, Morganella, Serratia, Peptostreptococcus, Prevotella, Porphyromonas, and Fusobacterium spp. S. aureus S. aureus, S. viridans, S. pyogenes. S. aureus, S. viridans, and coagulase-negative staphylococci H. influenzae, M. catarrhalis, S. pneumoniae, S. aureus. S. epidermidis, S. viridans S. millerii, S. pneumoniae, S. aureus, K. pneumonia, P. mirabilis, S. pyogenes, Bacteroides spp. Peptosptreptococcus spp., Fusobactrium spp. S. pneumoniae, S. viridans, S. aureus, MRSA, H.influenzae, S.pyogenes, S. intermedius, E. corrodens S. epidermidis, S. aureus ‘‘Anaerobic bacteria’’, S. milleri, S. epidermidis, Propionobacterium spp H influenzae, S. pneumoniae, S. pyogenes, S. aureus, S. anginosus group,
Children & adultsa
Brook et al. [4]
1978, 1982 1980
a
2
Polymicrobial flora
Single case of polymicrobial aerobic– anaerobic flora Polymicrobial flora in 8 children
S. pneumoniae and S. aureus in <9 years, Polymicrobial aerobic–anaerobic in >15 years
Adults with maxillary sinusitis, polymicrobial flora was found in all abscesses Simultaneous intracranial and SPOA. Polymicrobial flora
Children and adults.a Microbiology results combined
One newborn
Polymicrobial flora in 33%. Streptococci common in children and anaerobes in adultsa S. pneumoniae eliminated by PCV7 vaccination, and S. aureus, including MRSA increased Adultsa and children
Comparison between 1977–1992 to 2002– 2012: increase in S. anginosus group, S. aureus and MRSA
Several studies included also adults.
intermedius, and 4 S. pneumoniae), S. aureus (3), and Haemophillus spp. (2 H. influenzae, and one H. parainfluenzae). Sulte´sz et al. [17] reviewed 157 children with secondary complications of acute bacterial sinusitis treated between
1997 and 2006. Orbital complications were observed in 150 patients: 126 had preseptal cellulitis, 9 orbital cellulitis, 4 SPOA, and 11 orbital abscess. The bacterial isolates included 42 (28% of the children) S. pneumoniae, 32 (21%) S. aureus, 30 (20%)
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S. epidermidis, 27 (18%) H. influenzae, and 23 (15%) alpha-hemolytic streptococci. Liao et al. [18] assessed the bacteriology of orbital and SPOA secondary to sinusitis in 28 adults and 18 children treated between 1994 and 2008. SPOS was present in 30 patients and orbital abscesses in 16. Whereas aerobic culture results were available for all patients, anaerobic cultures were not uniformly performed. No organisms or only skin flora (S. epidermidis, diphtheroids, and Propionibacterium acnes) were found in 12 patients. Polymicrobial flora was detected in 15 (33%) individuals from either abscess or concurrent sinus cultures. Streptococci (6 S. anginosis/milleri, 6 S. viridans, 3 group C and one group A beta-hemolytic streptococci) were isolated in 17 (37%) patients, S. aureus in 13 (28.3%, including 3 methicillin resistant S. aureus or MRSA), gramnegative bacilli (including H. influenzae, Haemophilus aphrophilus, and Klebsiella, Morganella, and Serratia spp.) in 8 (17.4%), and anaerobes (Peptostreptococcus, Prevotella, Porphyromonas, and Fusobacterium spp.) in 9 (19.6%). Of the 10 patients with both sinus and abscess cultures, five had a concordance of organisms between culture sites. The authors concluded that since S. aureus was the single most common pathogen recovered and one fourth of them were MRSA, treatment with an antibiotic active against this organism should be included in the initial broad-spectrum antimicrobial treatment regimen of orbital and SPOA of sinusitis origin until culture results are available. Soon [18] describes 3 children with SPOA secondary to acute sinusitis between 2004 and 2009. A 38-day-old newborn had methicillin-resistant coagulase-negative Staphylococcal bacteremia, an ocular infection due to Acinetobacter, and SPOA caused by S. aureus. Fanella et al. [20] studied 38 children with orbital cellulitis seen between 1997 and 2008. SPOA occurred in 12 (31.5%), and only eight patients (21%) required surgery. The rates of admissions for orbital cellulitis increased after the introduction of PCV7. The mean number of orbital cellulitis cases per 1000 admissions before PCV7 licensure, after licensure and before full provincial funding, and after licensure and full funding – were 0.39, 0.53 and 0.90, respectively. S. pyogenes was recovered from the blood culture of one patient. Cultures of abscesses were obtained in eight cases, following up to nine days of antibiotic therapy. Three cultures were sterile, while two had positive gram stains (gram-negative bacilli and grampositive cocci) with negative cultures. Organisms isolated were one each of methicillin-susceptible S. aureus, S. viridans and S. pyogenes. It is not known if adequate methods for the recovery of anaerobic bacteria were employed in the study. Of the 22 children who had received antibiotics before admission, only two had positive cultures. Huang et al. [21] reviewed 64 children diagnosed with periorbital cellulitis and SPOA associated with sinusitis between 1996 and 2007. Thirty patients (47%) had surgical drainage, and 34 (53%) received antibiotic therapy only. The significant factors associated with abscess formation were age of 6 years or less, proptosis, fever, and a white blood cell count >11,100 cells/ microliter. In patients who underwent surgical drainage, the most frequently cultured organisms were S. aureus, S. viridans, and S. epidermidis, and 29% of the patients had polymicrobial flora. It is unknown if adequate methods for the recovery of anaerobes were employed in the study. Eviatar et al. [22] investigated the microbiology of SPOA and the adjacent involved paranasal sinuses in children from 1992 to 2009. Endoscopic drainage of the abscesses were performed in 29 (13.8%) and bacterial culture were obtained in 22. Organisms were recovered from the sinuses of 17 children (77%) and from the SPOA in 18 children (82%). In 13 children (59%), both sinus and abscess
culture results were available with correlation found in 4 (31%) instances. H. influenzae, M. catarrhalis and S. pneumoniae were recovered from 5 sinuses and 4 abscesses. S. aureus and S. epidermidis were recovered from 3 sinuses and 7 abscesses, and 6 S. viridans were recovered from 4 sinuses and 5 abscesses. Polymicrobial flora was detected in 3 sinuses and 3 abscesses. P. intermedia was isolated from one sinus. No organisms were found if 4 (18%) SPOA. Ketenci et al. [23] evaluated the microbiology in 36 patients with SPOA secondary to acute sinusitis from 1998 to 2011. Microorganisms were recovered in 12 (33%) patients; three individuals had polymicrobial infection. The aerobic isolates were S. millerii (3 isolates); S. pneumoniae, S. aureus, and K. pneumoniae (2 each); and Proteus mirabilis, and S. pyogenes (1 each). The anaerobes isolates were Bacteroides and Peptosptreptococcus spp. (2 each), and Fusobactrium spp. (1). The commonest microbial isolates were streptococci in children and anaerobes in adults. ˜ a et al. [24] determined if the characteristics of orbital Pen complications (orbital cellulitis and/or SPOA) of acute sinusitis in children have changed in the post-Pneumococcal Conjugate Vaccine 7 (PCV7) era, by comparing 128 patients seen before and 145 after 2003. The bacteriological methods used in the study were not reported and it is not known if adequate methods for the recovery of anaerobic bacteria were employed. A significant decrease in S. pneumoniae and S. viridans in surgically obtained sinus or blood cultures were observed (22.4% vs. 0% [P < .001] and 12.24% vs. 0% [P = .005], respectively) after 2003. An increase in S. aureus was seen in the post-PCV7 group (20.4% vs. 42.37% [P = .02]). MRSA was isolated only in the post-PCV7 group (P = .002). The pre-PCV7 group had a significantly longer hospital stay than the post-PCV7 group (7.15 days vs. 5.47 days [P = .004]). The authors concluded that although universal PCV7 vaccination has eliminated S. pneumoniae as an etiologic pathogen in acute sinusitis complications, there has been a parallel and significant increase in S. aureus, including an increase in the prevalence of MRSA associated with orbital infections related to acute sinusitis. ˇ et al. [25] evaluated the microbiology of orbital Sˇuchan complications of sinusitis in 8 pediatric and adult patients. The sources of orbital complication was ethmoid (62.5%), maxillary (25%) and frontal (12.5%) sinusitis. Pansinusitis occurred in 6 (75%) individuals. S. epidermidis and S. aureus were recovered in 4 (50%) of cases. Stokken et al. [26] compared 27 children with a complication of acute bacterial sinusitis (ABS) to 77 with chronic sinusitis (CS). Within the ABS group, the orbital complications included: 15 with preseptal cellulitis (26%), 5 with orbital cellulitis (8.7%), 8 with SPOA (14%), and 5 with an orbital abscess (8.7%). Cultures were obtained intra-operatively in 26 patients with complications of ABS. The predominate microorganism in the ABS group was S. anginosis/milleri. Five patients had polymicrobial infections with both anaerobic and aerobic pathogens. Twenty-one patients in the CRS group had cultures that grew pathogenic organisms. The predominant microorganisms included S. aureus and S. pneumoniae. It is not known if adequate methods for the recovery of anaerobic bacteria were employed in the study. Liao and Harris [27] compared culture results of 26 children with SPOA treated from 1977 through 1992, to 41 treated from 2002 to 2012. H. influenzae was recovered from 2 of 26 (8%) in the earlier series, and from 3 of 41 (7%) in the later series. In the earlier series, S. pneumoniae was recovered from 1 of 26 patients (4%), and from 5 of 41 patients (12%) in the later series. There was increased representation over time of the Streptococcus anginosus/milleri group – in 3 of 26 cases (12%) in the early series versus 10 of 41 cases (24%) in the later series, and of S. aureus – in 3 of 26 cases (12%) versus 7 of 41 cases (17%). MRSA was not reported in the early series but accounted for 4 of 7 S. aureus cases (57%) in the
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later one. Also increased was S. pyogenes – in 1 of 26 cases (4%) versus 5 of 41 cases (12%). In general, positive culture results in the 1977 through 1992 series were more diverse, with respect to both aerobic and anaerobic pathogens, than in the later cohort. 4. Discussion The orbit is susceptible to contiguous spread of infection from the sinuses as it is surrounded by sinuses on three sides. Sinusitis is responsible for at least three fourth of orbital infections including SPOA [3], and these may be the first and only presenting sign of sinus involvement [1]. The orbit is bordered by the ethmoid cells and maxillary sinus and separated from them by thin bony plates (called the lamina papyracea), which contain bony dehiscences. Infections can penetrate the thin bones or spread through the bony dehiscence [1,4]. Infection can also spread through the anterior and posterior ethmoid foraminas. Another mechanism of extension is through the valve less ophthalmic venous system. This extensive venous and lymphatic communication between the sinuses and the surrounding structures allows flow in either direction, thus enabling retrograde thrombophlebitis and spread of the infection [1,4]. Chandler et al. [28] categorized orbital complications into five separate stages according to the severity: inflammatory edema and preseptal cellulites, orbital cellulites, SPOA, orbital abscess, and cavernous sinus thrombosis. SPOA is often a progression of orbital cellulitis, and forms beneath the periosteum of the ethmoid, frontal, and maxillary bone. The most common pathogens isolated from studies of SPOA complicating sinusitis are aerobic and anaerobic members of the oropharyngeal flora (Table 1). Concordance in the microbiological findings between SPOA and the corresponding infected sinus supports the etiological source of these organisms [12,17]. S. pneumoniae and S. aureus were more frequently recovered in children younger >7 years, while polymicrobial aerobic–anaerobic flora was were more often isolated from those >15 years [11,23]. Studies done prior to the introduction of pneumococcal vaccine showed the predominance in younger children of S. pneumoniae and H. influenzae [6,7,11,24,27]. The introduction of pneumococcal vaccine reduced S. pneumoniae rate of isolation, and correlated with increase recovery of S. aureus and MRSA [17,27]. This tendency was also evident in studies of acute [29] and chronic [30] sinusitis in children and adults. Increased recovery of S. anginosus/ milleri group [23,26,27] and S. pyogenes [27] was also observed. Since anaerobic bacteria predominate in the oropharyngeal flora outnumbering aerobes 10 to one [31], it is not surprising that they were recovered in studies that employed adequate methods for their isolation [4,6,9,12–15,18,23]. The anaerobes isolated were members of the oral flora [31] and included Peptostreptococcus spp., anaerobic gram negative bacilli (Prevotella, Porphyromonas, and Bacteroides spp.), and Fusobacterium and Veillonella spp. Microaerophilic streptococci and Streptococcal species all members of the oral flora were also recovered. (Table 1) Of interest is the consistent isolation of E. corrodens, and S. anginosus/milleri group. E. corrodens, a gram-negative coccobacillus, is a facultative anaerobe and member of the oral flora. It is often resistant to first generation cephalosporins, macrolydes and clindamycin [32]. The unique characteristic of the S. anginosus/ milleri group is their ability to cause abscesses [33]. Both S. anginosus/milleri group and E. corrodens often participate in polymicrobial infections including abscesses. Although appropriate selection of antimicrobial therapy is of primary importance in the management of SPOA, surgical drainage may be required. Delay in surgical drainage can be associated with high morbidity and mortality [4,34]. Surgical drainage may be necessary in many patients to ensure adequate therapy
25
andcomplete resolution of infection. Surgical drainage of the concomitant sinus infection and any orbital collection of pus should also be performed concomitantly. Periodontal abscess or any other dental lesion should also be drained and/or corrected [35]. Establishing a microbiological diagnosis is important in planning the appropriate antimicrobial therapy. Empirical antimicrobial treatment of SPOA should cover all potential pathogens. However, obtaining adequate cultures for aerobic and anaerobic bacteria whenever possible can establish the precise microbiology and susceptibility of the isolates enabling adequate choice of antimicrobial therapy. Needle aspiration guided by CT may provide this important information. This is especially important in the era of increased microbial resistance to antimicrobials. The most effective available oral antibiotics are amoxicillinclavulanate, and the fluoroquinolones (levofloxacin, moxifloxacin) [36]. The systemic use of fluoroquinolones has not been approved in children younger than 18 years. Although concerns remain regarding the adverse musculoskeletal effects of fluoroquinolones in children, their use in the pediatric population has increased. Parenteral agents include the combination of beta-lactam/betalactamase inhibitor (e.g., ampicillin-sulbactam, amoxicillin-clavulanate, piperacillin-tazobactam), carbapenems (i.e. imipenem, meropenem), ceftriaxone or cefotaxime plus coverage for anaerobic bacteria (addition of metronidazole or clindamycin).. Therapy should also include antimicrobials effective against S. aureus including MRSA (i.e. vancomycin, or linezolid) and gramnegative aerobic and facultative bacilli including P. aeruginosa (an aminoglycoside, ceftazidime, cefipime, or a fluroquinolone) when they are suspected or isolated. 5. Conclusions Early recognition and appropriate surgical and medical therapy are essential to ensure recovery. Establishing the microbiology and antimicrobial susceptibility by obtaining appropriate cultures for both aerobic and anaerobic bacteria are essential for proper antimicrobial selection for the treatment of SPOA. References [1] I. Brook, Microbiology and antimicrobial treatment of orbital and intracranial complications of sinusitis in children and their management, Int. J. Pediatr. Otorhinolaryngol. 73 (2009) 1183–1186. [2] V.L. Schramm, E.N. Myers, J.S. Kennerdell, Orbital complications of acute sinusitis: evaluation, management, and outcome, Otolaryngology 86 (1978) 221–230. [3] V.L. Schramm Jr., H.D. Curtin, J.S. Kennerdell, Evaluation of orbital cellulitis and results of treatment, Laryngoscope 92 (1982) 732–738. [4] I. Brook, E.M. Friedman, W.J. Rodriguez, G. Controni, Complications of sinusitis in children, Pediatrics 66 (1980) 568–572. [5] N.K. Skau, K.O. Nielsen, O. Osgaard, I.L. Mølgaard, E. Peitersen, Intracranial and orbital complications of ethmoidal and frontal sinusitis, Acta Otolaryngol. (Stokh.) (Suppl. 412) (1984) 91–94. [6] J.R. Spires, R.J. Smith, Bacterial infections of the orbital and periorbital soft-tissues in children, Laryngoscope 96 (1986) 763–767. [7] B.J. Williams, H.C. Harrison, Subperiosteal abscesses of the orbit due to sinusitis in childhood, Aust. N. Z. J. Ophthalmol. (1991) 29–36. [8] S.R. Williams, J.A. Carruth, Orbital infection secondary to sinusitis in children: diagnosis and management, Clin. Otolaryngol. Allied Sci. 17 (1992) 550–557. [9] D.G. Skedros, J. Haddad Jr., C.D. Bluestone, H.D. Curtin, Subperiosteal orbital abscess in children: diagnosis, microbiology, and management, Laryngoscope 103 (1993) 28–32. [10] E.M. Arjmand, R.P. Lusk, H.R. Muntz, Pediatric sinusitis and subperiosteal orbital abscess formation: diagnosis and treatment, Otolaryngol. Head Neck Surg. 109 (1993) 886–894. [11] G.J. Harris, Subperiosteal abscess of the orbit. Age as a factor in the bacteriology and response to treatment, Ophthalmology 101 (1994) 585–595. [12] I. Brook, E.H. Frazier, Microbiology of subperiosteal orbital abscess and associated maxillary sinusitis, Laryngoscope 106 (1996) 1010–1013. [13] B.W. Herrmann, J.W. Forsen Jr., Simultaneous intracranial and orbital complications of acute rhinosinusitis in children, Int. J. Pediatr. Otorhinolaryngol. 68 (May (5)) (2004) 619–625. [14] S. Nageswaran, C.R. Woods, D.K. Benjamin Jr., L.B. Givner, A.K. Shetty, Orbital cellulitis in children, Pediatr. Infect. Dis. J. 25 (2006) 695–699.
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[15] L.E. Oxford, J. McClay, Medical and surgical management of subperiosteal orbital abscess secondary to acute sinusitis in children, Int. J. Pediatr. Otorhinolaryngol. 70 (2006) 1853–1861. [16] C.F. Sinclair, R.G. Berkowitz, Prior antibiotic therapy for acute sinusitis in children and the development of subperiosteal orbital abscess, Int. J. Pediatr. Otorhinolaryngol. 71 (2007) 1003–1006. [17] M. Sulte´sz, Z. Csa´ka´nyi, T. Majoros, Z. Farkas, G. Katona, Acute bacterial rhinosinusitis and its complications in our pediatric otolaryngological department between 1997 and 2006, Int. J. Pediatr. Otorhinolaryngol. 73 (2009) 1507–1512. [18] S. Liao, M.L. Durand, M.J. Cunningham, Sinogenic orbital and subperiosteal abscesses: microbiology and methicillin-resistant Staphylococcus aureus incidence, Otolaryngol. Head Neck Surg. 143 (2010) 392–396. [19] V.T. Soon, Pediatric subperiosteal orbital abscess secondary to acute sinusitis: a 5-year review, Am. J. Otolaryngol. 32 (2011) 62–68. [20] S. Fanella, A. Singer, J. Embree, Presentation and management of pediatric orbital cellulitis, Can. J. Infect. Dis. Med. Microbiol. 22 (2011) 97–100. [21] S.F. Huang, T.J. Lee, Y.S. Lee, C.C. Chen, S.C. Chin, N.C. Wang, Acute rhinosinusitisrelated orbital infection in pediatric patients: a retrospective analysis, Ann. Otol. Rhinol. Laryngol. 120 (2011) 185–190. [22] E. Eviatar, T. Lazarovitch, H. Gavriel, The correlation of microbiology growth between subperiosteal orbital abscess and affected sinuses in young children, Am. J. Rhinol. Allergy 26 (2012) 489–492. [23] I. Ketenci, Y. Unlu¨, A. Vural, H. Dog˘an, M.I. Sahin, E. Tuncer, Approaches to subperiosteal orbital abscesses, Eur. Arch. Otorhinolaryngol. 270 (2013) 1317–1327. [24] M.T. Pen˜a, D. Preciado, M. Orestes, S. Choi, Orbital complications of acute sinusitis: changes in the post-pneumococcal vaccine era, JAMA Otolaryngol. Head Neck Surg. 139 (2013) 223–227.
[25] M. Sˇuchanˇ, M. Hornˇa´k, L. Kaliarik, S. Krempaska´, T. Kosˇtialova´, J. Koval´, Orbital complications of sinusitis, Ces. Slov. Oftalmol. 70 (2014) 234–238. [26] J. Stokken, A. Gupta, P. Krakovitz, S. Anne, Rhinosinusitis in children: a comparison of patients requiring surgery for acute complications versus chronic disease, Am. J. Otolaryngol. 35 (2014) 641–646. [27] J.C. Liao, G.J. Harris, Subperiosteal abscess of the orbit: evolving pathogens and the therapeutic protocol, Ophthalmology 122 (2015) 639–647. [28] J.R. Chandler, D.J. Langenbrunner, E.F. Stevens, The pathogenesis of orbital complications in acute sinusitis, Laryngoscope 80 (1970) 1414–1428. [29] I. Brook, P.A. Foote, J.N. Hausfeld, Frequency of recovery of pathogens causing acute maxillary sinusitis in adults before and after introduction of vaccination of children with the 7-valent pneumococcal vaccine, J. Med. Microbiol. 55 (2006) 943–946. [30] I. Brook, P.A. Foote, J.N. Hausfeld, Increase in the frequency of recovery of meticillin-resistant Staphylococcus aureus in acute and chronic maxillary sinusitis, J. Med. Microbiol. 57 (2008) 1015–1017. [31] D.J. Hentges, The anaerobic microflora of the human body, Clin. Infect. Dis. 164 (1993) S175–S180. [32] T. Udaka, N. Hiraki, T. Shiomori, H. Miyamoto, T. Fujimura, T. Inaba, et al., Eikenella corrodens in head and neck infections, J. Infect. 54 (4) (2007) 343–348. [33] J. Gossling, Occurrence and pathogenicity of the Streptococcus milleri group, Rev. Infect. Dis. 10 (1988) 257–285. [34] I. Brook, Anaerobic Infections Diagnosis and Management. A Textbook, Informa Healthcare USA, Inc., New York, 2007. [35] I. Brook, E.M. Friedman, Intracranial complications of sinusitis in children: a sequela of periapical abscess, Ann. Otol. Rhinol. Laryngol. 91 (1982) 41–43. [36] I. Brook, Antimicrobial treatment of anaerobic infections, Expert Opin. Pharmacother. 12 (2011) 1691–1707.
Contents lists available at ScienceDirect
International Journal of Pediatric Otorhinolaryngology journal homepage: www.elsevier.com/locate/ijporl
Review Article
Microbiology and choice of antimicrobial therapy for acute sinusitis complicated by subperiosteal abscess in children Itzhak Brook * Department of Pediatrics, Georgetown University School of Medicine, Washington, DC, USA
A R T I C L E I N F O
A B S T R A C T
Article history: Received 7 January 2016 Received in revised form 17 February 2016 Accepted 18 February 2016 Available online 26 February 2016
Objectives: Review past studies of the microbiology of subperiosteal abscesses (SPOA) complicating sinusitis in children and their implications of the antimicrobials administered to treat the infection. Methods: Literature search was conducted of the Cochrane Library, EMBASE, TRIP, EMBASE, and MEDLINE databases from their inception. Results: The most common pathogens isolated from studies of SPOA complicating sinusitis are aerobic (Streptococcus pneumoniae, Streptococcus spp., Haemophilus spp., Eikenella corrodens), anaerobic (Peptostreptococcus, Fusobacterium, Prevotella, Porphyromonas, Bacteroides, and Veillonella spp.), and micoaerophilic streptococci (Streptococcus anginosus/Streptococcus milleri group), all members of the oropharyngeal flora. S. pneumoniae and S. aureus were more frequently recovered in children >7 years old, while polymicrobial aerobic–anaerobic flora were more often isolated from those >15 years. The introduction of pneumococcal vaccine reduced the rate of isolation of S. pneumoniae, and correlated with increase of recovery of S. aureus including methicillin resistant strains, as well as Streptococcus pyogenes and S. anginosus/milleri group. Conclusions: The microbiology and consequently the treatment of respiratory infections including sinusitis and its complications has evolved over the past decades. Establishing the microbiology of SPOA by obtaining appropriate cultures for both aerobic and anaerobic bacteria are essential for proper antimicrobial selection. ß 2016 Elsevier Ireland Ltd. All rights reserved.
Keywords: Subperiosteal abscesses Acute sinusitis Microbiology Anaerobic bacteria Staphylococcus aureus Sinusitis
Contents 1. 2. 3. 4. 5.
Introduction . . . . . . . . . Materials and methods Results . . . . . . . . . . . . . Discussion . . . . . . . . . . Conclusions . . . . . . . . . References . . . . . . . . . .
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1. Introduction Sinusitis can cause local and systemic complications. Subperiosteal abscess (SPOA) is an uncommon complication of acute sinusitis in children. The majority of local complications including
* Correspondence to: 4431 Albemarle St. NW, Washington, DC 20016, USA. Tel.: +1 202 364 4253. E-mail address: [email protected] http://dx.doi.org/10.1016/j.ijporl.2016.02.022 0165-5876/ß 2016 Elsevier Ireland Ltd. All rights reserved.
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SPOA are anatomically linked to the paranasal sinuses [1]. The rates of these complications are not known, but it is estimated that they occur in about 5% of patients hospitalized for sinusitis. Numerous studies evaluated the microbiology of SPOA over the past 5 decades [2–27]. Establishing the bacterial etiology of SPOA is important in understanding the pathophysiology of the infection and enables the appropriate choice of antimicrobial therapy. The microbiology and consequently the treatment of respiratory infections including sinusitis and its complications have evolved over the past decades. The changes in microbiology were
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I. Brook / International Journal of Pediatric Otorhinolaryngology 84 (2016) 21–26
associated with the introduction of vaccinations against Haemophilus influenzae and Streptococcus pneumoniae, and the growing resistance to antimicrobials [17,27]. This review presents past studies of the microbiology of SPOA complicating sinusitis in children and their implications of antimicrobials administered to treat the infection. 2. Materials and methods A literature search was conducted of the Cochrane Library, EMBASE, TRIP, and MEDLINE databases from their inception (1993 for the Cochrane Library, 1980 for EMBASE, 1997 for TRIP, and 1966 for MEDLINE) through October 25, 2015. The following search terms were used: sinusitis, complications, SPOA, microbiology, S. pneumoniae, H. influenzae, Staphylococcus aureus, and anaerobic bacteria. Results of these searches were closely evaluated, and articles and documents that were not pertinent or redundant were excluded. This review was focused on the microbiology of SPOA in children. 3. Results Many studies have investigated the microbiology of SPOA [2–27]. Four studies also included adults [12,18,23,25] (Table 1). Schramm et al., [2,3] evaluated 32 children and adults with SPOA. The predominate isolates were Stapylococcus, Streptococcus and Bacteroides spp. Brook et al. [4] studied 8 children with periorbital cellulitis and other complications of sinusitis. SPOA was present in two children who had ethmoiditis. Anaerobic bacteria were isolated from the infected sinuses in all the patients and no aerobic organisms were found. The isolates recovered from the sinuses of the two children with SPOA were Fusobacterium nucleatum, Prevotella oralis, Prevotella melaninogenica, Peptostreptococcus spp., Veillonella parvula, and microaerophilic streptococci. Skau et al. [5] reported 12 children, 3 with intracranial and 9 with orbital complications of ethmoidal and frontal sinusitis. SPOA was found in 6 patients; two each had Bacteroides spp., and alpha streptococci, and one each had Peptostreptococci and beta-hemolytic streptococci. Spires and Smith [6] studied 241 children with periorbital or orbital soft-tissue infections treated from 1962 to 1986. Two hundred twenty-six children (94%), half <1 year of age, had periorbital soft-tissue infections. Orbital infections occurred in 15 (6%) children, 11 (5%) had orbital cellulitis (9 associated with sinusitis), 3 (1.2%) had SPOA (2 associated with sinusitis), and one had cavernous sinus thrombosis. One child with SPOA developed brain abscess. The organisms recovered in those with a sinus etiology were Staphylococcus spp. (20 isolates), Streptococcus spp., and anaerobes (4 each), and H. influenzae [1]. Williams and Harrison [7] reports 16 children with SPOA associated with acute sinusitis. The recovered organisms were Streptococcus milleri (6 isolates); H. influenzae, anaerobic cocci, and S. aureus (2 each); and Streptococcus group F, Streptococcus pyogenes, and S. pneumoniae (one each). Williams and Carruth [8] described 18 children with orbital infections secondary to sinusitis. Two had intracranial complications and 9 had SPOA. No organisms were isolated from 5 of the 15 patients, S. aureus, H. influenzae and S. milleri were identified in 3 each, and Bacteroides spp. in one. Skedros et al. [9] reviewed 21 children seen from 1983 to 1990 who had surgical intervention for SPOA. The organisms recovered included: 8 (38% of abscesses) S. pneumoniae, 7 (33%) S. pyogenes, and 3 (14%) H. influenzae. Anaerobes (Fusobacterium, Bacteroides, and Peptostreptococcus spp., mixed with Eikenella and Actinobacter spp.) were isolated from a single patient. However,
adequate methodologies for transportation and cultivation of anaerobes were not employed in this study. Arjmand et al. [10] reported on 18 children with SPOA complicating sinusitis treated from 1983 to 1992. Organisms were isolated from 13 (72%) of the patients; eight of them had polymicrobial flora including four with aerobic and anaerobic bacteria. Staphylococcus or Streptococcus spp. accounted for all single organism infections. The predominate aerobic isolates were Streptococcus and Staphylococcus spp., S. pneumoniae and H. influenzae. The most common anaerobes were Fusobacterium and Bacteroides spp. Harris [11] reviewed the records of 37 patients with SPOA admitted between 1977 and 1992. Variations in the microbiology of SPOA appear to be age-associated. Among 12 patients <9 years, two had bacterial growth of S. pneumoniae and S. aureus. The organisms found in 12 of 16 of 9–14 years old patients where Streptococcus spp. (alpha and beta hemolytic groups A, C and D), Stapylococcus spp., H. influenzae, M. catarrhalis, Eikenella corrodens, Klebsiella pneumoniae, Prevottela intermedia and V. parvula. Polymicrobial aerobic–anaerobic infection occurred in all of individuals >15 years. The organism recovered were Streptococcus spp. (alpha and beta hemolytic groups A, B and D), Stapylococcus spp., E. corrodens; microaerophilic streptococci, V. parvula, Bacteroides fragilis, and Prevotella, Porphyromonas, Fusobacterium, and Peptostreptococcus spp. Brook and Frazier [12] using strict methodology for identification of aerobic and anaerobic bacteria studied the microbiology of pus aspirates from eight adults with SPOA and their corresponding infected sinuses. Polymicrobial flora was found in all instances, and the number of isolates varied from two to five. Anaerobes were recovered from all specimens. The predominant isolates were Peptostreptococcus, Prevotella, and Fusobacterium spp, S. aureus, and microaerophilic streptococci. Concordance in the microbiological findings between SPOA and the corresponding infected sinus was found in all instances. However, certain organisms were only present at one site and not the other. Fourteen beta-lactamaseproducing organisms were present in nine specimens. Even though no children were included in this study, it illustrates that utilization of appropriate methodology for the recovery of anaerobes can lead to their recovery. Herrmann and Forsen [13] evaluated 74 children seen from 1990 to 2002 with orbital complications of acute sinusitis. There were no intracranial complications in children admitted for orbital complications of acute sinusitis that were <7 years, in contrast to 4 of 43 (9.3%) of patients >7 years had such a complication. All intraoperative cultures obtained from the 4 patients (two had SPOA) with intracranial extension were polymicrobial. The isolates included group C streptococci, E. corrodens, Haemophillus parainfluenzae, Streptococcus viridans, Staphylococcus epidermidis, Fusobacterium necrophorum, B. fragilis, and S. milleri. Nageswaran et al. [14] studied 41 children with orbital cellulitis seen from 1992 to 2002, 34 (83%) of whom had SPOA and/or orbital abscess. The predominate aerobes were Streptococcus spp. (alpha and groups A and C beta-hemolytic, and non-hemolytic), S. aureus, H. influenzae, E. corrodens, and M. cattarhalis. The commonest anaerobes were Peptostreptococcus and Bacteroides spp. Oxford and McClay [15] evaluated the microbiology of 21 children with SPOA complicating acute sinusitis seen between 1995 and 2002. The predominate isolates were 7 (33%) S. milleri group, 6 (29%) S. aureus, 3 (14%) S. pneumoniae, 2 (9.5%) each of alpha hemolytic streptococci and Eikenella spp., and H. influenzae, and one (5%) each of Bacteroides, Propionibacterium, Porphyromonas, and Peptstreptococcus spp. Sinclair et al. [16] reviewed 39 children seen between 1996 to 2005 that had surgical drainage of a SPOA complicating acute sinusitis. The predominate isolates were Streptococcus spp. (20 isolates, including 6 Streptococcus
I. Brook / International Journal of Pediatric Otorhinolaryngology 84 (2016) 21–26
23
Table 1 Studies of the microbiology of subperiosteal abscesses complicating of sinusitis in children. Author(s)
Year
Number patients
Microbiology
Comments
Schramm et al. [2,3]
32
Skau et al. [5]
1984
6
Spires & Smith [6]
1986
3
Williams & Harrison [7]
1991
16
Williams& Carruth [8]
1992
9
Skedros et al. [9]
1993
21
Arjmand et al. [10]
1993
18
Harris [11]
1994
37
Brook and Frazier [12]
1996
8
Herrmann and Forsen [13]
2004
2
Nageswaran et al. [14]
2006
34
Oxford & McClay [15]
2006
21
Sinclair & Berkowitz [16] Sulte´sz et al. [17]
2007 2009
39 4
Liao et al. [18]
2010
19 adults 11 children
Soon [19] Fanella et al. [20] Huang et al. [21]
2011 2011 2011
3 12 64
Eviatar et al. [22]
2012
22
Ketenci et al. [23]
2013
36
˜ a et al. [24] Pen
2013
273
ˇ et al. [25] Sˇuchan Stokken et al. [26]
2014 2014
8 8
Liao & Harris [27]
2015
67
Stapylococcus spp. Streptococcus spp. Bacteroides spp. Fusobacterium nucleatum P. oralis, P. melaninogenica Peptostreptococcus spp. V. parvula, Microaerophilic streptococci Bacteroides spp., Peptostreptococcus spp. beta- and alpha hemolytic streptococci. Streptococcus spp. Staphylococcus spp. H. influenzae, Anaerobes S. milleri, H. influenzae, S. aureus streptococcus group F, S. pyogenes, S. pneumoniae, Peptostreptococcus spp. S. aureus, H. influenzae S. milleri, Bacteroides spp S. pneumoniae, S. pyogenes H. influenza, Eikenella spp., Actinobacter spp., Fusobacterium, Bacteroides, and Peptostreptococcus spp., Streptococcus & Staphylococcus spp., S. pneumoniae, H. influenzae, Fusobacterium spp., Bacteroides spp. S. pneumoniae, S. aureus, Streptococcus spp. Stapylococcus spp., H influenzae, M. catarrhalis, E. corrodens, K. pneumoniae, P. intermedia, V. parvula, Prevotella spp., Porphyromonas spp., B. fragilis, Fusobacterium spp., Peptostreptococcus spp., V. parvula, and microaerophilic streptococci were isolated. Peptostreptococcus spp, Prevotella spp, Fusobacterium spp, S. aureus, microaerophilic streptococci Group C streptococci, E. corrodens, H. parainfluenzae, S. viridans, S. epidermidis, F. necrophorum, B.fragilis, S. milleri. Streptococcus spp., S. aureus, H. influenzae, E. corrodens, M. cattarhalis, Peptostreptococcus spp.,Bacteroides spp. S. milleri group, S. aureus, S. pneumoniae, S. viridans, Eikenella spp., H. influenzae, Bacteroides spp., Propionibacterium spp., Porphyromonas spp., Peptstreptococcus spp. Streptococcus spp., S. aureus, Haemophillus spp. S. pneumoniae, S. aureus, S. epidermidis, H. influenzae, S. viridans Beta-hem. Strep groups A and C, S. anginosus/ milleri, S. aureus, S. epidermidis, H. influenzae, H. aphrophilus, P. acnes, Klebsiella, Morganella, Serratia, Peptostreptococcus, Prevotella, Porphyromonas, and Fusobacterium spp. S. aureus S. aureus, S. viridans, S. pyogenes. S. aureus, S. viridans, and coagulase-negative staphylococci H. influenzae, M. catarrhalis, S. pneumoniae, S. aureus. S. epidermidis, S. viridans S. millerii, S. pneumoniae, S. aureus, K. pneumonia, P. mirabilis, S. pyogenes, Bacteroides spp. Peptosptreptococcus spp., Fusobactrium spp. S. pneumoniae, S. viridans, S. aureus, MRSA, H.influenzae, S.pyogenes, S. intermedius, E. corrodens S. epidermidis, S. aureus ‘‘Anaerobic bacteria’’, S. milleri, S. epidermidis, Propionobacterium spp H influenzae, S. pneumoniae, S. pyogenes, S. aureus, S. anginosus group,
Children & adultsa
Brook et al. [4]
1978, 1982 1980
a
2
Polymicrobial flora
Single case of polymicrobial aerobic– anaerobic flora Polymicrobial flora in 8 children
S. pneumoniae and S. aureus in <9 years, Polymicrobial aerobic–anaerobic in >15 years
Adults with maxillary sinusitis, polymicrobial flora was found in all abscesses Simultaneous intracranial and SPOA. Polymicrobial flora
Children and adults.a Microbiology results combined
One newborn
Polymicrobial flora in 33%. Streptococci common in children and anaerobes in adultsa S. pneumoniae eliminated by PCV7 vaccination, and S. aureus, including MRSA increased Adultsa and children
Comparison between 1977–1992 to 2002– 2012: increase in S. anginosus group, S. aureus and MRSA
Several studies included also adults.
intermedius, and 4 S. pneumoniae), S. aureus (3), and Haemophillus spp. (2 H. influenzae, and one H. parainfluenzae). Sulte´sz et al. [17] reviewed 157 children with secondary complications of acute bacterial sinusitis treated between
1997 and 2006. Orbital complications were observed in 150 patients: 126 had preseptal cellulitis, 9 orbital cellulitis, 4 SPOA, and 11 orbital abscess. The bacterial isolates included 42 (28% of the children) S. pneumoniae, 32 (21%) S. aureus, 30 (20%)
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S. epidermidis, 27 (18%) H. influenzae, and 23 (15%) alpha-hemolytic streptococci. Liao et al. [18] assessed the bacteriology of orbital and SPOA secondary to sinusitis in 28 adults and 18 children treated between 1994 and 2008. SPOS was present in 30 patients and orbital abscesses in 16. Whereas aerobic culture results were available for all patients, anaerobic cultures were not uniformly performed. No organisms or only skin flora (S. epidermidis, diphtheroids, and Propionibacterium acnes) were found in 12 patients. Polymicrobial flora was detected in 15 (33%) individuals from either abscess or concurrent sinus cultures. Streptococci (6 S. anginosis/milleri, 6 S. viridans, 3 group C and one group A beta-hemolytic streptococci) were isolated in 17 (37%) patients, S. aureus in 13 (28.3%, including 3 methicillin resistant S. aureus or MRSA), gramnegative bacilli (including H. influenzae, Haemophilus aphrophilus, and Klebsiella, Morganella, and Serratia spp.) in 8 (17.4%), and anaerobes (Peptostreptococcus, Prevotella, Porphyromonas, and Fusobacterium spp.) in 9 (19.6%). Of the 10 patients with both sinus and abscess cultures, five had a concordance of organisms between culture sites. The authors concluded that since S. aureus was the single most common pathogen recovered and one fourth of them were MRSA, treatment with an antibiotic active against this organism should be included in the initial broad-spectrum antimicrobial treatment regimen of orbital and SPOA of sinusitis origin until culture results are available. Soon [18] describes 3 children with SPOA secondary to acute sinusitis between 2004 and 2009. A 38-day-old newborn had methicillin-resistant coagulase-negative Staphylococcal bacteremia, an ocular infection due to Acinetobacter, and SPOA caused by S. aureus. Fanella et al. [20] studied 38 children with orbital cellulitis seen between 1997 and 2008. SPOA occurred in 12 (31.5%), and only eight patients (21%) required surgery. The rates of admissions for orbital cellulitis increased after the introduction of PCV7. The mean number of orbital cellulitis cases per 1000 admissions before PCV7 licensure, after licensure and before full provincial funding, and after licensure and full funding – were 0.39, 0.53 and 0.90, respectively. S. pyogenes was recovered from the blood culture of one patient. Cultures of abscesses were obtained in eight cases, following up to nine days of antibiotic therapy. Three cultures were sterile, while two had positive gram stains (gram-negative bacilli and grampositive cocci) with negative cultures. Organisms isolated were one each of methicillin-susceptible S. aureus, S. viridans and S. pyogenes. It is not known if adequate methods for the recovery of anaerobic bacteria were employed in the study. Of the 22 children who had received antibiotics before admission, only two had positive cultures. Huang et al. [21] reviewed 64 children diagnosed with periorbital cellulitis and SPOA associated with sinusitis between 1996 and 2007. Thirty patients (47%) had surgical drainage, and 34 (53%) received antibiotic therapy only. The significant factors associated with abscess formation were age of 6 years or less, proptosis, fever, and a white blood cell count >11,100 cells/ microliter. In patients who underwent surgical drainage, the most frequently cultured organisms were S. aureus, S. viridans, and S. epidermidis, and 29% of the patients had polymicrobial flora. It is unknown if adequate methods for the recovery of anaerobes were employed in the study. Eviatar et al. [22] investigated the microbiology of SPOA and the adjacent involved paranasal sinuses in children from 1992 to 2009. Endoscopic drainage of the abscesses were performed in 29 (13.8%) and bacterial culture were obtained in 22. Organisms were recovered from the sinuses of 17 children (77%) and from the SPOA in 18 children (82%). In 13 children (59%), both sinus and abscess
culture results were available with correlation found in 4 (31%) instances. H. influenzae, M. catarrhalis and S. pneumoniae were recovered from 5 sinuses and 4 abscesses. S. aureus and S. epidermidis were recovered from 3 sinuses and 7 abscesses, and 6 S. viridans were recovered from 4 sinuses and 5 abscesses. Polymicrobial flora was detected in 3 sinuses and 3 abscesses. P. intermedia was isolated from one sinus. No organisms were found if 4 (18%) SPOA. Ketenci et al. [23] evaluated the microbiology in 36 patients with SPOA secondary to acute sinusitis from 1998 to 2011. Microorganisms were recovered in 12 (33%) patients; three individuals had polymicrobial infection. The aerobic isolates were S. millerii (3 isolates); S. pneumoniae, S. aureus, and K. pneumoniae (2 each); and Proteus mirabilis, and S. pyogenes (1 each). The anaerobes isolates were Bacteroides and Peptosptreptococcus spp. (2 each), and Fusobactrium spp. (1). The commonest microbial isolates were streptococci in children and anaerobes in adults. ˜ a et al. [24] determined if the characteristics of orbital Pen complications (orbital cellulitis and/or SPOA) of acute sinusitis in children have changed in the post-Pneumococcal Conjugate Vaccine 7 (PCV7) era, by comparing 128 patients seen before and 145 after 2003. The bacteriological methods used in the study were not reported and it is not known if adequate methods for the recovery of anaerobic bacteria were employed. A significant decrease in S. pneumoniae and S. viridans in surgically obtained sinus or blood cultures were observed (22.4% vs. 0% [P < .001] and 12.24% vs. 0% [P = .005], respectively) after 2003. An increase in S. aureus was seen in the post-PCV7 group (20.4% vs. 42.37% [P = .02]). MRSA was isolated only in the post-PCV7 group (P = .002). The pre-PCV7 group had a significantly longer hospital stay than the post-PCV7 group (7.15 days vs. 5.47 days [P = .004]). The authors concluded that although universal PCV7 vaccination has eliminated S. pneumoniae as an etiologic pathogen in acute sinusitis complications, there has been a parallel and significant increase in S. aureus, including an increase in the prevalence of MRSA associated with orbital infections related to acute sinusitis. ˇ et al. [25] evaluated the microbiology of orbital Sˇuchan complications of sinusitis in 8 pediatric and adult patients. The sources of orbital complication was ethmoid (62.5%), maxillary (25%) and frontal (12.5%) sinusitis. Pansinusitis occurred in 6 (75%) individuals. S. epidermidis and S. aureus were recovered in 4 (50%) of cases. Stokken et al. [26] compared 27 children with a complication of acute bacterial sinusitis (ABS) to 77 with chronic sinusitis (CS). Within the ABS group, the orbital complications included: 15 with preseptal cellulitis (26%), 5 with orbital cellulitis (8.7%), 8 with SPOA (14%), and 5 with an orbital abscess (8.7%). Cultures were obtained intra-operatively in 26 patients with complications of ABS. The predominate microorganism in the ABS group was S. anginosis/milleri. Five patients had polymicrobial infections with both anaerobic and aerobic pathogens. Twenty-one patients in the CRS group had cultures that grew pathogenic organisms. The predominant microorganisms included S. aureus and S. pneumoniae. It is not known if adequate methods for the recovery of anaerobic bacteria were employed in the study. Liao and Harris [27] compared culture results of 26 children with SPOA treated from 1977 through 1992, to 41 treated from 2002 to 2012. H. influenzae was recovered from 2 of 26 (8%) in the earlier series, and from 3 of 41 (7%) in the later series. In the earlier series, S. pneumoniae was recovered from 1 of 26 patients (4%), and from 5 of 41 patients (12%) in the later series. There was increased representation over time of the Streptococcus anginosus/milleri group – in 3 of 26 cases (12%) in the early series versus 10 of 41 cases (24%) in the later series, and of S. aureus – in 3 of 26 cases (12%) versus 7 of 41 cases (17%). MRSA was not reported in the early series but accounted for 4 of 7 S. aureus cases (57%) in the
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later one. Also increased was S. pyogenes – in 1 of 26 cases (4%) versus 5 of 41 cases (12%). In general, positive culture results in the 1977 through 1992 series were more diverse, with respect to both aerobic and anaerobic pathogens, than in the later cohort. 4. Discussion The orbit is susceptible to contiguous spread of infection from the sinuses as it is surrounded by sinuses on three sides. Sinusitis is responsible for at least three fourth of orbital infections including SPOA [3], and these may be the first and only presenting sign of sinus involvement [1]. The orbit is bordered by the ethmoid cells and maxillary sinus and separated from them by thin bony plates (called the lamina papyracea), which contain bony dehiscences. Infections can penetrate the thin bones or spread through the bony dehiscence [1,4]. Infection can also spread through the anterior and posterior ethmoid foraminas. Another mechanism of extension is through the valve less ophthalmic venous system. This extensive venous and lymphatic communication between the sinuses and the surrounding structures allows flow in either direction, thus enabling retrograde thrombophlebitis and spread of the infection [1,4]. Chandler et al. [28] categorized orbital complications into five separate stages according to the severity: inflammatory edema and preseptal cellulites, orbital cellulites, SPOA, orbital abscess, and cavernous sinus thrombosis. SPOA is often a progression of orbital cellulitis, and forms beneath the periosteum of the ethmoid, frontal, and maxillary bone. The most common pathogens isolated from studies of SPOA complicating sinusitis are aerobic and anaerobic members of the oropharyngeal flora (Table 1). Concordance in the microbiological findings between SPOA and the corresponding infected sinus supports the etiological source of these organisms [12,17]. S. pneumoniae and S. aureus were more frequently recovered in children younger >7 years, while polymicrobial aerobic–anaerobic flora was were more often isolated from those >15 years [11,23]. Studies done prior to the introduction of pneumococcal vaccine showed the predominance in younger children of S. pneumoniae and H. influenzae [6,7,11,24,27]. The introduction of pneumococcal vaccine reduced S. pneumoniae rate of isolation, and correlated with increase recovery of S. aureus and MRSA [17,27]. This tendency was also evident in studies of acute [29] and chronic [30] sinusitis in children and adults. Increased recovery of S. anginosus/ milleri group [23,26,27] and S. pyogenes [27] was also observed. Since anaerobic bacteria predominate in the oropharyngeal flora outnumbering aerobes 10 to one [31], it is not surprising that they were recovered in studies that employed adequate methods for their isolation [4,6,9,12–15,18,23]. The anaerobes isolated were members of the oral flora [31] and included Peptostreptococcus spp., anaerobic gram negative bacilli (Prevotella, Porphyromonas, and Bacteroides spp.), and Fusobacterium and Veillonella spp. Microaerophilic streptococci and Streptococcal species all members of the oral flora were also recovered. (Table 1) Of interest is the consistent isolation of E. corrodens, and S. anginosus/milleri group. E. corrodens, a gram-negative coccobacillus, is a facultative anaerobe and member of the oral flora. It is often resistant to first generation cephalosporins, macrolydes and clindamycin [32]. The unique characteristic of the S. anginosus/ milleri group is their ability to cause abscesses [33]. Both S. anginosus/milleri group and E. corrodens often participate in polymicrobial infections including abscesses. Although appropriate selection of antimicrobial therapy is of primary importance in the management of SPOA, surgical drainage may be required. Delay in surgical drainage can be associated with high morbidity and mortality [4,34]. Surgical drainage may be necessary in many patients to ensure adequate therapy
25
andcomplete resolution of infection. Surgical drainage of the concomitant sinus infection and any orbital collection of pus should also be performed concomitantly. Periodontal abscess or any other dental lesion should also be drained and/or corrected [35]. Establishing a microbiological diagnosis is important in planning the appropriate antimicrobial therapy. Empirical antimicrobial treatment of SPOA should cover all potential pathogens. However, obtaining adequate cultures for aerobic and anaerobic bacteria whenever possible can establish the precise microbiology and susceptibility of the isolates enabling adequate choice of antimicrobial therapy. Needle aspiration guided by CT may provide this important information. This is especially important in the era of increased microbial resistance to antimicrobials. The most effective available oral antibiotics are amoxicillinclavulanate, and the fluoroquinolones (levofloxacin, moxifloxacin) [36]. The systemic use of fluoroquinolones has not been approved in children younger than 18 years. Although concerns remain regarding the adverse musculoskeletal effects of fluoroquinolones in children, their use in the pediatric population has increased. Parenteral agents include the combination of beta-lactam/betalactamase inhibitor (e.g., ampicillin-sulbactam, amoxicillin-clavulanate, piperacillin-tazobactam), carbapenems (i.e. imipenem, meropenem), ceftriaxone or cefotaxime plus coverage for anaerobic bacteria (addition of metronidazole or clindamycin).. Therapy should also include antimicrobials effective against S. aureus including MRSA (i.e. vancomycin, or linezolid) and gramnegative aerobic and facultative bacilli including P. aeruginosa (an aminoglycoside, ceftazidime, cefipime, or a fluroquinolone) when they are suspected or isolated. 5. Conclusions Early recognition and appropriate surgical and medical therapy are essential to ensure recovery. Establishing the microbiology and antimicrobial susceptibility by obtaining appropriate cultures for both aerobic and anaerobic bacteria are essential for proper antimicrobial selection for the treatment of SPOA. References [1] I. Brook, Microbiology and antimicrobial treatment of orbital and intracranial complications of sinusitis in children and their management, Int. J. Pediatr. Otorhinolaryngol. 73 (2009) 1183–1186. [2] V.L. Schramm, E.N. Myers, J.S. Kennerdell, Orbital complications of acute sinusitis: evaluation, management, and outcome, Otolaryngology 86 (1978) 221–230. [3] V.L. Schramm Jr., H.D. Curtin, J.S. Kennerdell, Evaluation of orbital cellulitis and results of treatment, Laryngoscope 92 (1982) 732–738. [4] I. Brook, E.M. Friedman, W.J. Rodriguez, G. Controni, Complications of sinusitis in children, Pediatrics 66 (1980) 568–572. [5] N.K. Skau, K.O. Nielsen, O. Osgaard, I.L. Mølgaard, E. Peitersen, Intracranial and orbital complications of ethmoidal and frontal sinusitis, Acta Otolaryngol. (Stokh.) (Suppl. 412) (1984) 91–94. [6] J.R. Spires, R.J. Smith, Bacterial infections of the orbital and periorbital soft-tissues in children, Laryngoscope 96 (1986) 763–767. [7] B.J. Williams, H.C. Harrison, Subperiosteal abscesses of the orbit due to sinusitis in childhood, Aust. N. Z. J. Ophthalmol. (1991) 29–36. [8] S.R. Williams, J.A. Carruth, Orbital infection secondary to sinusitis in children: diagnosis and management, Clin. Otolaryngol. Allied Sci. 17 (1992) 550–557. [9] D.G. Skedros, J. Haddad Jr., C.D. Bluestone, H.D. Curtin, Subperiosteal orbital abscess in children: diagnosis, microbiology, and management, Laryngoscope 103 (1993) 28–32. [10] E.M. Arjmand, R.P. Lusk, H.R. Muntz, Pediatric sinusitis and subperiosteal orbital abscess formation: diagnosis and treatment, Otolaryngol. Head Neck Surg. 109 (1993) 886–894. [11] G.J. Harris, Subperiosteal abscess of the orbit. Age as a factor in the bacteriology and response to treatment, Ophthalmology 101 (1994) 585–595. [12] I. Brook, E.H. Frazier, Microbiology of subperiosteal orbital abscess and associated maxillary sinusitis, Laryngoscope 106 (1996) 1010–1013. [13] B.W. Herrmann, J.W. Forsen Jr., Simultaneous intracranial and orbital complications of acute rhinosinusitis in children, Int. J. Pediatr. Otorhinolaryngol. 68 (May (5)) (2004) 619–625. [14] S. Nageswaran, C.R. Woods, D.K. Benjamin Jr., L.B. Givner, A.K. Shetty, Orbital cellulitis in children, Pediatr. Infect. Dis. J. 25 (2006) 695–699.
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[15] L.E. Oxford, J. McClay, Medical and surgical management of subperiosteal orbital abscess secondary to acute sinusitis in children, Int. J. Pediatr. Otorhinolaryngol. 70 (2006) 1853–1861. [16] C.F. Sinclair, R.G. Berkowitz, Prior antibiotic therapy for acute sinusitis in children and the development of subperiosteal orbital abscess, Int. J. Pediatr. Otorhinolaryngol. 71 (2007) 1003–1006. [17] M. Sulte´sz, Z. Csa´ka´nyi, T. Majoros, Z. Farkas, G. Katona, Acute bacterial rhinosinusitis and its complications in our pediatric otolaryngological department between 1997 and 2006, Int. J. Pediatr. Otorhinolaryngol. 73 (2009) 1507–1512. [18] S. Liao, M.L. Durand, M.J. Cunningham, Sinogenic orbital and subperiosteal abscesses: microbiology and methicillin-resistant Staphylococcus aureus incidence, Otolaryngol. Head Neck Surg. 143 (2010) 392–396. [19] V.T. Soon, Pediatric subperiosteal orbital abscess secondary to acute sinusitis: a 5-year review, Am. J. Otolaryngol. 32 (2011) 62–68. [20] S. Fanella, A. Singer, J. Embree, Presentation and management of pediatric orbital cellulitis, Can. J. Infect. Dis. Med. Microbiol. 22 (2011) 97–100. [21] S.F. Huang, T.J. Lee, Y.S. Lee, C.C. Chen, S.C. Chin, N.C. Wang, Acute rhinosinusitisrelated orbital infection in pediatric patients: a retrospective analysis, Ann. Otol. Rhinol. Laryngol. 120 (2011) 185–190. [22] E. Eviatar, T. Lazarovitch, H. Gavriel, The correlation of microbiology growth between subperiosteal orbital abscess and affected sinuses in young children, Am. J. Rhinol. Allergy 26 (2012) 489–492. [23] I. Ketenci, Y. Unlu¨, A. Vural, H. Dog˘an, M.I. Sahin, E. Tuncer, Approaches to subperiosteal orbital abscesses, Eur. Arch. Otorhinolaryngol. 270 (2013) 1317–1327. [24] M.T. Pen˜a, D. Preciado, M. Orestes, S. Choi, Orbital complications of acute sinusitis: changes in the post-pneumococcal vaccine era, JAMA Otolaryngol. Head Neck Surg. 139 (2013) 223–227.
[25] M. Sˇuchanˇ, M. Hornˇa´k, L. Kaliarik, S. Krempaska´, T. Kosˇtialova´, J. Koval´, Orbital complications of sinusitis, Ces. Slov. Oftalmol. 70 (2014) 234–238. [26] J. Stokken, A. Gupta, P. Krakovitz, S. Anne, Rhinosinusitis in children: a comparison of patients requiring surgery for acute complications versus chronic disease, Am. J. Otolaryngol. 35 (2014) 641–646. [27] J.C. Liao, G.J. Harris, Subperiosteal abscess of the orbit: evolving pathogens and the therapeutic protocol, Ophthalmology 122 (2015) 639–647. [28] J.R. Chandler, D.J. Langenbrunner, E.F. Stevens, The pathogenesis of orbital complications in acute sinusitis, Laryngoscope 80 (1970) 1414–1428. [29] I. Brook, P.A. Foote, J.N. Hausfeld, Frequency of recovery of pathogens causing acute maxillary sinusitis in adults before and after introduction of vaccination of children with the 7-valent pneumococcal vaccine, J. Med. Microbiol. 55 (2006) 943–946. [30] I. Brook, P.A. Foote, J.N. Hausfeld, Increase in the frequency of recovery of meticillin-resistant Staphylococcus aureus in acute and chronic maxillary sinusitis, J. Med. Microbiol. 57 (2008) 1015–1017. [31] D.J. Hentges, The anaerobic microflora of the human body, Clin. Infect. Dis. 164 (1993) S175–S180. [32] T. Udaka, N. Hiraki, T. Shiomori, H. Miyamoto, T. Fujimura, T. Inaba, et al., Eikenella corrodens in head and neck infections, J. Infect. 54 (4) (2007) 343–348. [33] J. Gossling, Occurrence and pathogenicity of the Streptococcus milleri group, Rev. Infect. Dis. 10 (1988) 257–285. [34] I. Brook, Anaerobic Infections Diagnosis and Management. A Textbook, Informa Healthcare USA, Inc., New York, 2007. [35] I. Brook, E.M. Friedman, Intracranial complications of sinusitis in children: a sequela of periapical abscess, Ann. Otol. Rhinol. Laryngol. 91 (1982) 41–43. [36] I. Brook, Antimicrobial treatment of anaerobic infections, Expert Opin. Pharmacother. 12 (2011) 1691–1707.