- Email: [email protected]
Intraorbital and Intracranial Extension of Sinusitis: Comparative Morbidity
Intraorbital and Intracranial Extension of Sinusitis: Comparative Morbidity Veronica K. Goytia, MD, Carla M. Giannoni, MD, and Morven S. Edwards, MD Objectives We hypothesized that intracranial extension of sinusitis carries greater morbidity than extension confined to the orbit and that presenting features can raise suspicion for intracranial extension. Study design A retrospective review (1997 to 2006) identified 118 children with sinusitis complicated by intracranial extension or intraorbital extension. Presenting features and infecting organisms were compared using c2 or Fisher exact tests. Outcomes included duration of hospitalization, length of therapy and sequelae. Results Thirty-three children had intracranial extension and 85 had intraorbital extension. Children with intracranial extension were older (11.4 versus 7.6 years; P # .001), had more preadmission encounters (1.9 versus 1.3; P = .012), longer headache duration (9.5 versus 2.8 days; P = .009), and presented more often with vomiting (73% versus 28%; P < .001) than those with intraorbital extension. Children with intracranial extension also were hospitalized (26 versus 10 days; P < .001) and treated (36 versus 24 days; P = .001) longer. Four children (3%) had persistent sequelae. Conclusions Children with intracranial extension are hospitalized and treated longer than those with intraorbital extension of sinusitis but persistent sequelae are uncommon. Prolonged headache and protracted vomiting at presentation should alert caregivers to consider intracranial extension. (J Pediatr 2011;158:486-91).
D
espite availability of sophisticated diagnostic imaging modalities to delineate the extent of disease, complications of sinusitis carry the potential for serious consequences. Extension beyond the confines of the paranasal sinuses usually involves the orbit or central nervous system and can occur hematogenously, by contiguous spread, or by retrograde extension along the valveless diploic veins.1,2 Early recognition of intraorbital and intracranial extension of sinusitis can minimize the morbidity and the potential for a fatal outcome from these disease processes.2-7 Intracranial extension more often occurs in children older than 7 or 8 years of age than in younger children and in children of African American than of other ethnicities,8-14 but an attempt to define presenting features suggesting intracranial extension among children with complicated sinusitis previously has not been undertaken. Intraorbital extension of sinusitis can be classified according to severity.15,16 Poorly localizing processes such as inflammatory edema and medial abscesses of modest size can respond to medical therapy, but larger and nonmedially located abscesses can require surgical intervention.15 Our objectives were (1) to determine whether clinical features at presentation can alert caregivers to suspect intracranial extension of sinusitis; and (2) to determine whether intracranial extension is associated with greater morbidity and a higher risk for sequelae than is intraorbital extension of sinusitis.
Methods This was a retrospective study of patients with sinusitis from 3 months through 18 years of age admitted to Texas Children’s Hospital from January 1, 1997, through December 31, 2006. For the purpose of this report, sinusitis was defined by radiographic sinus opacification on imaging performed within 72 hours of hospital admission. Children with sinusitis and imaging showing postseptal orbital findings including proptosis, retroorbital phlegmon, lateral displacement of the medial rectus muscle, subperiostial phlegmon or abscess and intraorbital cellulitis or abscess, as defined by the Chandler classification17 but without extension beyond the orbit were considered to have intraorbital extension. Imaging evidence of intracranial extension was defined by radiographic evidence of epidural abscess, subdural empyema, dural enhancement, intracerebral abscess, venous sinus thrombosis or frontal bone osteomyelitis. Subjects were identified by search of International Classification of Diseases, 9th Edition codes for orbital phlegmon (376.0), orbital cellulitis/abscess (376.01), brain abscess/empyema (324.0), epidural abscess/empyema (324.1), subdural abscess/empyema (324.9), intracranial thrombosis (325.0), frontal bone osteomyelitis/Pott puffy tumor (730.0, 730.1, From the Section of Infectious Diseases, Department of Pediatrics (V.G., M.E.), and the Bobby R. Alford 730.2), and by review of the consultation records of the Infectious Disease SerDepartment of Otolaryngology-Head and Neck Surgery (C.G.), Baylor College of Medicine, Houston, TX
CT ESS MRI MRSA
Computed tomography Endoscopic sinus surgery Magnetic resonance imaging Methicillin-resistant Staphylococcus aureus
V.G. received partial funding through a scholarship from the Minnie L. Maffett Fund of the Texas Federation of Business and Professional Women’s Foundation, and M.E. is a consultant for Novartis Vaccines and Diagnostics. C.G. declares no conflicts of interest. 0022-3476/$ - see front matter. Copyright ª 2011 Mosby Inc. All rights reserved. 10.1016/j.jpeds.2010.09.011
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Vol. 158, No. 3 March 2011 vice. Children with periorbital/preseptal infections and/or phlegmon and those with uncomplicated sinusitis, underlying immunodeficiency, age younger than 3 months or an unavailable medical record were excluded. Records were reviewed for clinical and laboratory features. Microbiologic data were obtained through computerized records (Oacis, Dinmar, Inc, Petaluma, California) and crossreferenced with surgical intraoperative reports. Outcomes were obtained from charts and electronic medical records of outpatient visits. Data were recorded on a standardized form and entered into a Microsoft Excel spreadsheet (Microsoft Corp, Redmond, Washington). The study was approved by the Institutional Review Board for Human Subject Research for Baylor College of Medicine and Affiliated Hospitals, Houston, Texas. Descriptive statistical data analysis was performed using SPSS software (SPSS Inc, Chicago, Illinois). c2 or Fisher exact tests were used to compare independent proportions. The t test was used to compare means. A P value of < .05 was considered significant.
Results One hundred forty-five children were identified with intraorbital extension or intracranial extension of sinusitis during the 10-year interval (Figure). Twenty-seven were excluded for the reasons specified in the Figure. Children with periorbital/preseptal infections also were excluded. One hundred eighteen children comprised the study group, including 85 with intraorbital extension and 33 with intracranial extension. Fourteen children with intracranial extension also had orbital involvement. Two-thirds of patients with intracranial extension had two or more and one-third had three or more intracranial extension features. Boys had both intracranial extension and intraorbital extension more often than girls (overall ratio, 2.3:1; P < .001). The ethnic distribution (40% African American, 38% Caucasian, 15% Hispanic, 2% Asian, and 3% not specified) did not differ. At 40% of the group, African Americans were overrepresented compared with the proportion of their total hospital admissions (19%) for the study interval (P < .001). Subjects with intracranial extension were older (mean, 11.4 years; range, 4 months to 18 years) than those with intraorbital extension (mean, 7.3 years; range, 7 months to 18 years; P < .001). Three children with intracranial extension and 11 with intraorbital extension were admitted at their first healthcare system encounter. Among the remainder, 70% with intracranial extension and 65% with intraorbital extension had preadmission healthcare encounters (mean, 1.9 versus 1.3, respectively; P = .012) initiated a mean of 7 days (intracranial extension) compared with 2 days (intraorbital extension) before admission (P = .051). Children with intracranial extension often presented to a community or referral hospital for evaluation (48%), and 60% of those with intraorbital extension were evaluated by their primary care provider. Approximately 60% of children in each group received antibiotics
before admission. Primary care providers prescribed an antibiotic for 39% of children later admitted with intracranial extension and 40% of those with intraorbital extension. Hospital personnel prescribed an antibiotic for 67% of children with intracranial extension and 82% of those with intraorbital extension, often including an intramuscular dose of ceftriaxone. Clinical Features The median duration of symptoms before admission was 7 days (range, 1 to 60) for children with intracranial extension and 6 days (range, 1 to 30) for children with intraorbital extension (P = not significant). All children with intraorbital extension and 22 of 33 with intracranial extension presented with eye swelling. Children with intracranial extension had more prolonged headache duration and were more likely to report vomiting than those with intraorbital extension (Table I). Acute sinusitis had been diagnosed in only 8 children with intraorbital extension and 3 with intracranial extension. There were no differences between groups in history of upper respiratory infection, allergic rhinitis, otitis media, chronic sinusitis, behavioral change, or dental surgery or in findings of otitis media, aphasia, hemiparesis, neck stiffness, or seizures at presentation, when specified (data not shown). The initial examination findings in the 85 children with intraorbital extension and the 14 with intracranial extension who had orbital involvement included eye pain (68%), proptosis (57%), chemosis (32%), and limitation of extraocular movements (53% of children). Among these 99 children, 53 (54%) had at least one objective finding (proptosis, chemosis or limitation of extraocular movements) at presentation to suggest intraorbital involvement. One or more of these findings were noted in 3 of 19 children (16%) with intracranial extension who did not have orbital involvement. The mean admission white blood cell count was 15.6 109/L (range, 6.6 to 37.7) for children with intracranial extension and 14.8 109/L (range, 4.6 to 36.4) for those with intraorbital extension. Eighteen percent of children with intraorbital extension and 21% with intracranial extension had an admission white blood cell count exceeding 20 109/L. Inflammatory marker measurements did not differ significantly. The mean erythrocyte sedimentation rate was 91 mm/h (range, 41 to 113) for children with intracranial extension and 68 mm/h (range, 33 to 108) for those with intraorbital extension; mean C-reactive protein was 13.6 mg/dL (range, 1.1 to 30) for children with intracranial extension and 5.5 mg/dL (range, 0.6 to 17.7) for those with intraorbital extension. Contrast-enhanced computed tomography (CT) (n = 20), magnetic resonance imaging (MRI) (n = 1), or both (n = 8 children) were performed within 72 hours after admission for 29 of 33 children with intracranial extension; 78 of 85 children with intraorbital extension had contrastenhanced CT performed. Seven children with intraorbital extension and three of the remaining four with intracranial extension had a noncontrast CT; one child with intracranial 487
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Figure. Intraorbital or intracranial complications of sinusitis in 118 children.
extension had sinus radiographs only. The imaging findings pertaining to the orbit for the 14 children with intracranial extension included orbital cellulitis (n = 2), intraorbital phlegmon (n = 3), subperiosteal abscess (n = 5), orbital abscess (n = 3), and abscess in the extraconal space (1 child). The imaging findings in those with intraorbital extension are shown in the Figure. Among those with subperiosteal phlegmon, size was specified for 11 and 8 were #0.5 cm. Among those with subperiosteal abscess, size was specified for 19 and the median was 2.2 1.5 0.5 cm. The orbital abscess size, when specified, was 0.5 cm. Additional imaging studies were obtained for 94% and 42% of children with intracranial extension or intraorbital extension, respectively. The mean number of imaging studies was 5.4 for intracranial extension and 1.9 for intraorbital extension (P < .001). Most children had involvement of multiple sinuses. Greater than 90% of children had two or more sinuses involved; 58 (68%) with intraorbital extension and 27 (82%) with intracranial extension had opacification of three or 488
more sinuses. Children with intracranial extension more often had frontal sinus involvement than those with intraorbital extension (85% versus 34%; P # .001). Treatment All children received intravenous antibiotics. The most common initial regimen for children with intracranial extension was cefotaxime, vancomycin, and metronidazole (52% of the group). Regimens for intraorbital extension usually included cefotaxime and an anti-staphylococcal antibiotic. Cefuroxime alone or nafcillin plus cefotaxime were used as intraorbital extension regimens in the pre–methicillin-resistant Staphylococcus aureus (MRSA) era, but after 2002 the most common initial regimen for children with intraorbital extension was clindamycin or vancomycin plus cefotaxime. All microorganisms recovered, except for a Pseudomonas aeruginosa isolate, were susceptible to the regimen chosen. Antibiotic regimens were refined based on susceptibility data. The final full extent of infection was identified within 48 hours of hospitalization for 76 of 85 children with Goytia, Giannoni, and Edwards
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Table I. Presenting features in children with intraorbital or intracranial extension of sinusitis Feature
IOE (n = 85)
ICE (n = 33)
Fever (T $100.4F) Mean height Mean duration Headache Mean duration Vomiting Mean duration Upper respiratory infection Photophobia Trauma Diplopia
65/77 (84)* 102.4 3.0 days 41/51 (80) 2.8 days 15/54 (28) 2.4 days 66/76 (87) 7/18 (39) 6/55 (11) 12/33 (36)
26/31 (84)* 103.0 3.2 days 24/25 (96) 9.5 days† 19/26 (73)z 3.6 days 18/27 (67) 7/16 (44) 1/19 (5) 3/11 (27)
ICE, Intracranial extension of sinusitis; IOE, intraorbital extension of sinusitis; T, temperature. *Denominator represents number of patients for whom medical record provided specific data (%). †P = .009 compared with children with IOE. zP < .001 compared with children with IOE.
intraorbital extension, for 13 of 14 with intracranial extension who also had orbital infection and for 16 of 19 with intracranial extension who did not have orbital involvement. Delay until the third hospital day for nine children with intraorbital extension was due to an initial clinical impression of preseptal cellulitis (n = 8) and diagnosis of respiratory syncytial virus bronchiolitis with eye swelling (one child). Diagnosis was delayed until the fourth hospital day for a child with intracranial extension and orbital involvement because initial non-contrast CT did not delineate full disease extent. Two children with intracranial extension were considered to have viral gastroenteritis until day three when stupor or facial edema, respectively, developed. In another child, subdural empyema was appreciated on the day of hospitalization but frontal brain abscess was not diagnosed until the fifth hospital day. Thirty-two of 33 children with intracranial extension had a total of 87 (mean, 2.6; range, 0 to 7) and 46 of 85 with intraorbital extension had a total of 57 (mean, 1.3; range, 0 to 2) surgical procedures (P < .001). Children with intracranial extension more often had a multidisciplinary surgical approach (58% versus 24%; P = .003) or a second procedure (33% versus 0%; P < .001). Twenty-nine children with intracranial extension and 36 with intraorbital extension underwent endoscopic sinus surgery (ESS); 15 with intracranial extension had frontal sinus drainage procedures in conjunction with ESS. Orbital procedures, often performed in conjunction with ESS, included orbitotomy and drainage (eight patients with intracranial extension and 13 with intraorbital extension), external approach to drainage of orbital abscess (one patient with intracranial extension and 7 with intraorbital extension). External drainage of an eyelid abscess was performed for three children, one of whom had repeat drainage. Twenty-four neurosurgical procedures were performed for 17 children with intracranial extension. Microbiology Twenty-four of 32 children with intracranial extension had operative cultures from sinus (n = 27), orbital (n = 7), or in-
tracranial (16 children) sites yielding one or more organisms (Table II). Twenty-nine children with intraorbital extension had cultures from sinus or orbit that grew pathogens. Seven children, all with intraorbital extension and all admitted after 2002, had MRSA. One isolate was clindamycin-resistant. Severity of illness based on hospitalization did not differ between children with MRSA and those with methicillinsusceptible S aureus isolates (12.5 versus 16.5 days; P = not significant). Duration of Therapy and Outcome The mean hospital stay and duration of parenteral therapy were significantly longer for children with intracranial extension (Table III). Children with intraorbital extension who had a surgical procedure were hospitalized longer (mean, 11; range, 4 to 27 days) than those who had medical management (mean, 9; range, 4 to 23 days; P = .028). Among children with intraorbital extension who completed therapy orally, the common regimens were amoxicillinclavulanate (36%), clindamycin (23%), or clindamycin plus a cephalosporin (22% of children). There were no deaths. Eight of 85 children with intraorbital extension and one of 33 with intracranial extension had diplopia (n = 4) or gaze limitation (n = 5) at hospital discharge that resolved within 1 month for two with followup information. Persistent sequelae were evident in four children (3%). One child with intracranial extension and 1 with intraorbital extension had no light perception in the involved eye at the time of admission and they did not regain vision. One child with intraorbital extension had gaze limitation at age 1 year and another with intracranial extension had expressive aphasia and right foot paresis at a 16-month follow-up visit.
Discussion The diagnosis of intracranial extension complicating sinusitis is challenging. It occurs uncommonly and usually among children who are not known to have chronic sinusitis or other comorbidities.7,10 Some reports cite cerebral abscess as a common manifestation, and others describe epidural abscess or subdural empyema as occurring more often.5,18-20 Subdural empyema and epidural abscess were found in almost one-half and frontal bone osteomyelitis in one-fourth of our children. Multiple sites of involvement were common. We found that children with intraorbital extension or intracranial extension were equally likely to present with fever, headache, and vomiting, but identified prolonged duration of headache, often for more than a week, and persistent emesis as presenting features heightening suspicion for intracranial extension. Children in both groups often received medical care before admission, but those with intracranial extension were likely to attend an acute care center rather than the office of a primary caregiver and to have had encounters that did not lead to admission. Preadmission encounters resulted, for two-thirds of children, in prescription of antibiotic therapy.
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Table II. Culture results for children with intraorbital or intracranial extension of sinusitis Number of isolates in children with positive operative cultures* Microbe Gram-positive aerobes a-Hemolytic streptococciz b-Hemolytic streptococcix g-Hemolytic streptococci Methicillin-susceptible Staphylococcus aureus Methicillin-resistant Staphylococcus aureus{ Rothia mucilaginosa Gram-negative aerobes Haemophilus influenzae** Haemophilus parainfluenzae Klebsiella pneumoniae Pseudomonas aeruginosa Subtotal aerobes Anaerobes Bacteroides species Fusobacterium species†† Gemella morbillorum Peptostreptococcus specieszz Prevotella species Veillonella species Subtotal anaerobes Total isolates (isolates per patient)
†
IOE (n = 29)
ICE (n = 24)
6 10 9 7
9 5 13 7
7
0
1
0
5 1 1 0 47
2 2 0 1 39
0 0 0 2 2 0 4
1 2 1 6 4 1
51 (1.8)
15xx 54 (2.3)
ICE, Intracranial extension of sinusitis; IOE, intraorbital extension of sinusitis. *Includes endoscopic sinus, intraorbital, and intracranial culture sources. †Operative cultures from 17 and 8 of children in the IOE and ICE groups, respectively, were sterile. zIncludes Streptococcus pneumoniae (3 isolates). xIncludes group A Streptococcus (n = 5), group B Streptococcus (n = 1), group C Streptococcus (n = 4), group F Streptococcus (n = 4), and b-hemolytic Streptococcus, group not determined (1 isolate). {One isolate was clindamycin-resistant. **Includes nontypable Haemophilus influenzae (n = 6) and Haemophilus influenzae, type b (1 isolate). ††Includes Fusobacterium nucleatum (n = 1) and F necrophorum (1 isolate). zzIncludes Peptostreptococcus micros (n = 5), P prevotii (n = 1), and Peptostreptococcus species (2 isolates). xxP = .02.
Computed tomography provides excellent resolution of bony structures, globe, retro-orbital tissue, sinuses, and cranium and is the imaging modality of choice when complications of sinusitis are suspected.21,22 Contrast-enhanced CT of orbit and sinuses is sufficient for medical decision-making in children with intraorbital extension, whereas MRI offers increased sensitivity to identify the location and extent of intracranial pathology.21,23 Both studies usually are obtained in children with intracranial extension. A presumed diagnosis of viral gastroenteritis in two of our children with headache and emesis delayed imaging evaluation for intracranial extension. Although ethmoid involvement is associated with intraorbital extension and frontal sinusitis with intracranial extension of sinusitis, 90% of the children we evaluated had opacification of multiple sinuses.24-26 Approximately onehalf of those with intraorbital extension and all except one child with intracranial extension underwent drainage of purulent material. Approximately one-half with intracranial extension had neurosurgical drainage and one third required multiple drainage procedures. These patients can be too ill 490
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Table III. Medical treatment of children with intraorbital or intracranial extension of sinusitis Medical intervention Total hospital days Mean duration of total antibiotics (days)† Intravenous Total Patients receiving antibiotics at home Oral route Mean duration (days) IV route Mean duration (days)
IOE (n = 85)*
ICE (n = 33)
10
26
<.001
12 24 83 (98) 70 (84) 14 19 (23)z 11
35 36 17 (52) 6 (35) 13 11 (65) 21
.001 .001 .001 .009 NS .017 .034
P value
ICE, Intracranial extension of sinusitis; IOE, intraorbital extension of sinusitis. *Number of patients (%). †Inpatient and outpatient antibiotic therapy. zSix also had oral therapy.
to tolerate full ESS at the first encounter and limited culture and drainage can be performed initially with a more definitive procedure when the child is clinically stable. Operative cultures were sterile in approximately one fourth of children who had received preadmission antibiotics. A majority of positive cultures were polymicrobial, supporting the use of empirical broad-spectrum antibiotics.27 Broad-spectrum regimens were initiated, most often vancomycin, cefotaxime, and metronidazole when intracranial extension was suspected. The study interval embraced the emergence of community-acquired MRSA in Houston. Infections in children from whom MRSA was isolated were not uncommonly severe or prolonged by comparison with those in which MRSA was isolated. Others have reported neurologic outcomes in children and adolescents with intracranial complications of sinusitis. Among the 11 children with suppurative intracranial extension of sinusitis in the report of Kombogiorgas et al,28 five had persistent focal neurological deficits. Germiller et al20 reported one death and two patients who sustained permanent neurologic sequelae that included hemiparesis and cognitive deficits. Oxford and McClay14 reported persistent morbidity in 4% of their 104 children with intraorbital or intracranial extension of sinusitis. Our 3% overall rate of persistent sequelae is comparable with the latter report. Aggressive management may have contributed to the favorable outcomes we observed. Most children undergoing drainage had surgery within the first 48 hours of admission. Our findings are subject to the limitations inherent in a retrospective study and, although 118 children is a large series, the numbers are still relatively small. Differences in treatment for children in the groups could have resulted in ascertainment bias. Children with intraorbital extension were less likely than those with intracranial extension to undergo MRI. However, based on the hospital course and outcomes, it is unlikely that children were erroneously assigned into groups. Children with intracranial extension had longer courses of intravenous antibiotics, total therapy and hospital stays than those with intraorbital extension. Periorbital edema is shared Goytia, Giannoni, and Edwards
ORIGINAL ARTICLES
March 2011 by both intraorbital extension and intracranial extension, but infection in both sites, as defined by strict imaging criteria, is uncommon. Eye swelling combined with persistent headache and vomiting may be the most helpful finding in identifying children with intracranial extension in routine practice. Especially among older children, headache and emesis of sufficient severity to warrant hospitalization should warrant consideration of the diagnosis. Multispecialty participation by otolaryngologists, neurosurgeons, ophthalmologists, and infectious disease physicians is important so that children with these challenging infections can receive prompt, comprehensive treatment to optimize a favorable outcome. n The authors thank Edward O Mason, Jr, PhD, for assistance with the database search and Carol J. Baker, MD, for her insightful suggestions and review of the manuscript. Submitted for publication Dec 18, 2009; last revision received Jun 21, 2010; accepted Sep 2, 2010. Reprint requests: Dr Morven S. Edwards, MD, Texas Children’s Hospital, 1102 Bates Street, Suite 1120, Houston, TX 77030. E-mail: [email protected]
References 1. Reynolds DJ, Kodsi SR, Rubin SE, Rodgers IR. Intracranial infection associated with preseptal and orbital cellulitis in the pediatric patient. JAAPOS 2003;7:413-7. 2. Adame N, Hedlund G, Byington CL. Sinogenic intracranial empyema in children. Pediatrics 2005;116:e461-7. 3. Ong YK, Tan HKK. Suppurative intracranial complications of sinusitis in children. Int J Pediatr Otorhinolaryngol 2002;66:49-54. 4. Hyt€ onen M, Atula T, Pitk€aranta A. Complications of acute sinusitis in children. Acta Otolaryngol 2000;543:154-7. 5. Clayman GL, Adams GL, Paugh DR, Koopmann CF, Jr. Intracranial complications of paranasal sinusitis: a combined institutional review. Laryngoscope 1991;101:234-9. 6. Lerner DN, Choi SS, Zalzal GH, Johnson DL. Intracranial complications of sinusitis in childhood. Ann Otol Rhinol Laryngol 1995;104:288-93. 7. Rosenfeld EA, Rowley AH. Infectious intracranial complications of sinusitis, other than meningitis, in children: 12-year review. Clin Infect Dis 1994;18:750-4. 8. Bambakidis NC, Cohen AR. Intracranial complications of frontal sinusitis in children: Pott’s puffy tumor revisited. Pediatr Neurosurg 2001;35:82-9. 9. El-Hakim H, Malik AC, Aronyk K, Ledi E, Bhargava R. The prevalence of intracranial complications in pediatric frontal sinusitis. Int J Pediatr Otolaryngol 2006;70:1383-7.
10. Gallagher RM, Gross CW, Phillips CD. Suppurative intracranial complications of sinusitis. Laryngoscope 1998;108:1635-42. 11. Giannoni C, Sulek M, Friedman EM. Intracranial complications of sinusitis: a pediatric series. Am J Rhinol 1998;12:173-8. 12. Herrmann BW, Chung JC, Eisenbeis JF, Forsen JW, Jr. Intracranial complications of pediatric frontal rhinosinusitis. Am J Rhinol 2006; 20:320-4. 13. Johnson DL, Markle BM, Wiedermann BL, Hanahan L. Treatment of intracranial abscesses associated with sinusitis in children and adolescents. J Pediatr 1988;113:15-23. 14. Oxford LE, McClay JE. Complications of acute sinusitis in children. Otolaryngol Head Neck Surg 2005;133:32-7. 15. Wald ER. Acute sinusitis and orbital complications in children. Am J Otolaryngol 1983;4:424-7. 16. Garcia GH, Harris GJ. Criteria for nonsurgical management of subperiosteal abscess of the orbit: analysis of outcomes 1988-1998. Ophthalmology 2000;107:1454-8. 17. Chandler JR, Langenbrunner DJ, Stevens ER. The pathogenesis of orbital complications in acute sinusitis. Laryngoscope 1970;80:1414-28. 18. Giannoni CM, Stewart MG, Alford EL. Intracranial complications of sinusitis. Laryngoscope 1997;107:863-7. 19. Eufinger H, Machtens E. Purulent pansinusitis, orbital cellulitis, and rhinogenic intracranial complications. J Craniomaxillofac Surg 2001;29: 111-7. 20. Germiller JA, Monin DL, Sparano AM, Tom LWC. Intracranial complications of sinusitis in children and adolescents and their outcomes. Arch Otolaryngol Head Neck Surg 2006;132:969-76. 21. Younis RT, Anand VK, Davidson B. The role of computed tomography and magnetic resonance imaging in patients with sinusitis with complications. Laryngoscope 2002;112:224-9. 22. Younis RT, Lazar RH, Bustillo A, Anand VK. Orbital infection as a complication of sinusitis: are diagnostic and treatment trends changing? Ear Nose Throat J 2002;81:771-5. 23. Vazquez E, Creixell S, Carre~ no JC, Castellote A, Figueras C, Pumarola F, et al. Complicated acute pediatric bacterial sinusitis: imaging updated approach. Curr Probl Diagn Radiol 2004;33:127-45. 24. Ali A, Kurien M, Mathews SS, Mathew J. Complications of acute infective rhinosinusitis: experience from a developing country. Singapore Med J 2005;46:540-4. 25. Carter BL, Bankoff MS, Fisk JD. Computed tomographic detection of sinusitis responsible for intracranial and extracranial infections. Radiology 1983;147:739-42. 26. Wald ER, Pang D, Milmoe GJ, Schramm VL, Jr. Sinusitis and its complications in the pediatric patient. Pediatr Clin N Am 1981;28:777-96. 27. Herrmann BW, Forsen JW, Jr. Simultaneous intracranial and orbital complications of acute rhinosinusitis in children. Int J Pediatr Otorhinolaryngol 2004;68:619-25. 28. Kombogiorgas D, Seth R, Athwal R, Modha J, Singh J. Suppurative intracranial complications of sinusitis in adolescence: single institute experience and review of literature. Br J Neurosurg 2007;21:603-9.
Intraorbital and Intracranial Extension of Sinusitis: Comparative Morbidity
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D
espite availability of sophisticated diagnostic imaging modalities to delineate the extent of disease, complications of sinusitis carry the potential for serious consequences. Extension beyond the confines of the paranasal sinuses usually involves the orbit or central nervous system and can occur hematogenously, by contiguous spread, or by retrograde extension along the valveless diploic veins.1,2 Early recognition of intraorbital and intracranial extension of sinusitis can minimize the morbidity and the potential for a fatal outcome from these disease processes.2-7 Intracranial extension more often occurs in children older than 7 or 8 years of age than in younger children and in children of African American than of other ethnicities,8-14 but an attempt to define presenting features suggesting intracranial extension among children with complicated sinusitis previously has not been undertaken. Intraorbital extension of sinusitis can be classified according to severity.15,16 Poorly localizing processes such as inflammatory edema and medial abscesses of modest size can respond to medical therapy, but larger and nonmedially located abscesses can require surgical intervention.15 Our objectives were (1) to determine whether clinical features at presentation can alert caregivers to suspect intracranial extension of sinusitis; and (2) to determine whether intracranial extension is associated with greater morbidity and a higher risk for sequelae than is intraorbital extension of sinusitis.
Methods This was a retrospective study of patients with sinusitis from 3 months through 18 years of age admitted to Texas Children’s Hospital from January 1, 1997, through December 31, 2006. For the purpose of this report, sinusitis was defined by radiographic sinus opacification on imaging performed within 72 hours of hospital admission. Children with sinusitis and imaging showing postseptal orbital findings including proptosis, retroorbital phlegmon, lateral displacement of the medial rectus muscle, subperiostial phlegmon or abscess and intraorbital cellulitis or abscess, as defined by the Chandler classification17 but without extension beyond the orbit were considered to have intraorbital extension. Imaging evidence of intracranial extension was defined by radiographic evidence of epidural abscess, subdural empyema, dural enhancement, intracerebral abscess, venous sinus thrombosis or frontal bone osteomyelitis. Subjects were identified by search of International Classification of Diseases, 9th Edition codes for orbital phlegmon (376.0), orbital cellulitis/abscess (376.01), brain abscess/empyema (324.0), epidural abscess/empyema (324.1), subdural abscess/empyema (324.9), intracranial thrombosis (325.0), frontal bone osteomyelitis/Pott puffy tumor (730.0, 730.1, From the Section of Infectious Diseases, Department of Pediatrics (V.G., M.E.), and the Bobby R. Alford 730.2), and by review of the consultation records of the Infectious Disease SerDepartment of Otolaryngology-Head and Neck Surgery (C.G.), Baylor College of Medicine, Houston, TX
CT ESS MRI MRSA
Computed tomography Endoscopic sinus surgery Magnetic resonance imaging Methicillin-resistant Staphylococcus aureus
V.G. received partial funding through a scholarship from the Minnie L. Maffett Fund of the Texas Federation of Business and Professional Women’s Foundation, and M.E. is a consultant for Novartis Vaccines and Diagnostics. C.G. declares no conflicts of interest. 0022-3476/$ - see front matter. Copyright ª 2011 Mosby Inc. All rights reserved. 10.1016/j.jpeds.2010.09.011
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Vol. 158, No. 3 March 2011 vice. Children with periorbital/preseptal infections and/or phlegmon and those with uncomplicated sinusitis, underlying immunodeficiency, age younger than 3 months or an unavailable medical record were excluded. Records were reviewed for clinical and laboratory features. Microbiologic data were obtained through computerized records (Oacis, Dinmar, Inc, Petaluma, California) and crossreferenced with surgical intraoperative reports. Outcomes were obtained from charts and electronic medical records of outpatient visits. Data were recorded on a standardized form and entered into a Microsoft Excel spreadsheet (Microsoft Corp, Redmond, Washington). The study was approved by the Institutional Review Board for Human Subject Research for Baylor College of Medicine and Affiliated Hospitals, Houston, Texas. Descriptive statistical data analysis was performed using SPSS software (SPSS Inc, Chicago, Illinois). c2 or Fisher exact tests were used to compare independent proportions. The t test was used to compare means. A P value of < .05 was considered significant.
Results One hundred forty-five children were identified with intraorbital extension or intracranial extension of sinusitis during the 10-year interval (Figure). Twenty-seven were excluded for the reasons specified in the Figure. Children with periorbital/preseptal infections also were excluded. One hundred eighteen children comprised the study group, including 85 with intraorbital extension and 33 with intracranial extension. Fourteen children with intracranial extension also had orbital involvement. Two-thirds of patients with intracranial extension had two or more and one-third had three or more intracranial extension features. Boys had both intracranial extension and intraorbital extension more often than girls (overall ratio, 2.3:1; P < .001). The ethnic distribution (40% African American, 38% Caucasian, 15% Hispanic, 2% Asian, and 3% not specified) did not differ. At 40% of the group, African Americans were overrepresented compared with the proportion of their total hospital admissions (19%) for the study interval (P < .001). Subjects with intracranial extension were older (mean, 11.4 years; range, 4 months to 18 years) than those with intraorbital extension (mean, 7.3 years; range, 7 months to 18 years; P < .001). Three children with intracranial extension and 11 with intraorbital extension were admitted at their first healthcare system encounter. Among the remainder, 70% with intracranial extension and 65% with intraorbital extension had preadmission healthcare encounters (mean, 1.9 versus 1.3, respectively; P = .012) initiated a mean of 7 days (intracranial extension) compared with 2 days (intraorbital extension) before admission (P = .051). Children with intracranial extension often presented to a community or referral hospital for evaluation (48%), and 60% of those with intraorbital extension were evaluated by their primary care provider. Approximately 60% of children in each group received antibiotics
before admission. Primary care providers prescribed an antibiotic for 39% of children later admitted with intracranial extension and 40% of those with intraorbital extension. Hospital personnel prescribed an antibiotic for 67% of children with intracranial extension and 82% of those with intraorbital extension, often including an intramuscular dose of ceftriaxone. Clinical Features The median duration of symptoms before admission was 7 days (range, 1 to 60) for children with intracranial extension and 6 days (range, 1 to 30) for children with intraorbital extension (P = not significant). All children with intraorbital extension and 22 of 33 with intracranial extension presented with eye swelling. Children with intracranial extension had more prolonged headache duration and were more likely to report vomiting than those with intraorbital extension (Table I). Acute sinusitis had been diagnosed in only 8 children with intraorbital extension and 3 with intracranial extension. There were no differences between groups in history of upper respiratory infection, allergic rhinitis, otitis media, chronic sinusitis, behavioral change, or dental surgery or in findings of otitis media, aphasia, hemiparesis, neck stiffness, or seizures at presentation, when specified (data not shown). The initial examination findings in the 85 children with intraorbital extension and the 14 with intracranial extension who had orbital involvement included eye pain (68%), proptosis (57%), chemosis (32%), and limitation of extraocular movements (53% of children). Among these 99 children, 53 (54%) had at least one objective finding (proptosis, chemosis or limitation of extraocular movements) at presentation to suggest intraorbital involvement. One or more of these findings were noted in 3 of 19 children (16%) with intracranial extension who did not have orbital involvement. The mean admission white blood cell count was 15.6 109/L (range, 6.6 to 37.7) for children with intracranial extension and 14.8 109/L (range, 4.6 to 36.4) for those with intraorbital extension. Eighteen percent of children with intraorbital extension and 21% with intracranial extension had an admission white blood cell count exceeding 20 109/L. Inflammatory marker measurements did not differ significantly. The mean erythrocyte sedimentation rate was 91 mm/h (range, 41 to 113) for children with intracranial extension and 68 mm/h (range, 33 to 108) for those with intraorbital extension; mean C-reactive protein was 13.6 mg/dL (range, 1.1 to 30) for children with intracranial extension and 5.5 mg/dL (range, 0.6 to 17.7) for those with intraorbital extension. Contrast-enhanced computed tomography (CT) (n = 20), magnetic resonance imaging (MRI) (n = 1), or both (n = 8 children) were performed within 72 hours after admission for 29 of 33 children with intracranial extension; 78 of 85 children with intraorbital extension had contrastenhanced CT performed. Seven children with intraorbital extension and three of the remaining four with intracranial extension had a noncontrast CT; one child with intracranial 487
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Figure. Intraorbital or intracranial complications of sinusitis in 118 children.
extension had sinus radiographs only. The imaging findings pertaining to the orbit for the 14 children with intracranial extension included orbital cellulitis (n = 2), intraorbital phlegmon (n = 3), subperiosteal abscess (n = 5), orbital abscess (n = 3), and abscess in the extraconal space (1 child). The imaging findings in those with intraorbital extension are shown in the Figure. Among those with subperiosteal phlegmon, size was specified for 11 and 8 were #0.5 cm. Among those with subperiosteal abscess, size was specified for 19 and the median was 2.2 1.5 0.5 cm. The orbital abscess size, when specified, was 0.5 cm. Additional imaging studies were obtained for 94% and 42% of children with intracranial extension or intraorbital extension, respectively. The mean number of imaging studies was 5.4 for intracranial extension and 1.9 for intraorbital extension (P < .001). Most children had involvement of multiple sinuses. Greater than 90% of children had two or more sinuses involved; 58 (68%) with intraorbital extension and 27 (82%) with intracranial extension had opacification of three or 488
more sinuses. Children with intracranial extension more often had frontal sinus involvement than those with intraorbital extension (85% versus 34%; P # .001). Treatment All children received intravenous antibiotics. The most common initial regimen for children with intracranial extension was cefotaxime, vancomycin, and metronidazole (52% of the group). Regimens for intraorbital extension usually included cefotaxime and an anti-staphylococcal antibiotic. Cefuroxime alone or nafcillin plus cefotaxime were used as intraorbital extension regimens in the pre–methicillin-resistant Staphylococcus aureus (MRSA) era, but after 2002 the most common initial regimen for children with intraorbital extension was clindamycin or vancomycin plus cefotaxime. All microorganisms recovered, except for a Pseudomonas aeruginosa isolate, were susceptible to the regimen chosen. Antibiotic regimens were refined based on susceptibility data. The final full extent of infection was identified within 48 hours of hospitalization for 76 of 85 children with Goytia, Giannoni, and Edwards
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Table I. Presenting features in children with intraorbital or intracranial extension of sinusitis Feature
IOE (n = 85)
ICE (n = 33)
Fever (T $100.4F) Mean height Mean duration Headache Mean duration Vomiting Mean duration Upper respiratory infection Photophobia Trauma Diplopia
65/77 (84)* 102.4 3.0 days 41/51 (80) 2.8 days 15/54 (28) 2.4 days 66/76 (87) 7/18 (39) 6/55 (11) 12/33 (36)
26/31 (84)* 103.0 3.2 days 24/25 (96) 9.5 days† 19/26 (73)z 3.6 days 18/27 (67) 7/16 (44) 1/19 (5) 3/11 (27)
ICE, Intracranial extension of sinusitis; IOE, intraorbital extension of sinusitis; T, temperature. *Denominator represents number of patients for whom medical record provided specific data (%). †P = .009 compared with children with IOE. zP < .001 compared with children with IOE.
intraorbital extension, for 13 of 14 with intracranial extension who also had orbital infection and for 16 of 19 with intracranial extension who did not have orbital involvement. Delay until the third hospital day for nine children with intraorbital extension was due to an initial clinical impression of preseptal cellulitis (n = 8) and diagnosis of respiratory syncytial virus bronchiolitis with eye swelling (one child). Diagnosis was delayed until the fourth hospital day for a child with intracranial extension and orbital involvement because initial non-contrast CT did not delineate full disease extent. Two children with intracranial extension were considered to have viral gastroenteritis until day three when stupor or facial edema, respectively, developed. In another child, subdural empyema was appreciated on the day of hospitalization but frontal brain abscess was not diagnosed until the fifth hospital day. Thirty-two of 33 children with intracranial extension had a total of 87 (mean, 2.6; range, 0 to 7) and 46 of 85 with intraorbital extension had a total of 57 (mean, 1.3; range, 0 to 2) surgical procedures (P < .001). Children with intracranial extension more often had a multidisciplinary surgical approach (58% versus 24%; P = .003) or a second procedure (33% versus 0%; P < .001). Twenty-nine children with intracranial extension and 36 with intraorbital extension underwent endoscopic sinus surgery (ESS); 15 with intracranial extension had frontal sinus drainage procedures in conjunction with ESS. Orbital procedures, often performed in conjunction with ESS, included orbitotomy and drainage (eight patients with intracranial extension and 13 with intraorbital extension), external approach to drainage of orbital abscess (one patient with intracranial extension and 7 with intraorbital extension). External drainage of an eyelid abscess was performed for three children, one of whom had repeat drainage. Twenty-four neurosurgical procedures were performed for 17 children with intracranial extension. Microbiology Twenty-four of 32 children with intracranial extension had operative cultures from sinus (n = 27), orbital (n = 7), or in-
tracranial (16 children) sites yielding one or more organisms (Table II). Twenty-nine children with intraorbital extension had cultures from sinus or orbit that grew pathogens. Seven children, all with intraorbital extension and all admitted after 2002, had MRSA. One isolate was clindamycin-resistant. Severity of illness based on hospitalization did not differ between children with MRSA and those with methicillinsusceptible S aureus isolates (12.5 versus 16.5 days; P = not significant). Duration of Therapy and Outcome The mean hospital stay and duration of parenteral therapy were significantly longer for children with intracranial extension (Table III). Children with intraorbital extension who had a surgical procedure were hospitalized longer (mean, 11; range, 4 to 27 days) than those who had medical management (mean, 9; range, 4 to 23 days; P = .028). Among children with intraorbital extension who completed therapy orally, the common regimens were amoxicillinclavulanate (36%), clindamycin (23%), or clindamycin plus a cephalosporin (22% of children). There were no deaths. Eight of 85 children with intraorbital extension and one of 33 with intracranial extension had diplopia (n = 4) or gaze limitation (n = 5) at hospital discharge that resolved within 1 month for two with followup information. Persistent sequelae were evident in four children (3%). One child with intracranial extension and 1 with intraorbital extension had no light perception in the involved eye at the time of admission and they did not regain vision. One child with intraorbital extension had gaze limitation at age 1 year and another with intracranial extension had expressive aphasia and right foot paresis at a 16-month follow-up visit.
Discussion The diagnosis of intracranial extension complicating sinusitis is challenging. It occurs uncommonly and usually among children who are not known to have chronic sinusitis or other comorbidities.7,10 Some reports cite cerebral abscess as a common manifestation, and others describe epidural abscess or subdural empyema as occurring more often.5,18-20 Subdural empyema and epidural abscess were found in almost one-half and frontal bone osteomyelitis in one-fourth of our children. Multiple sites of involvement were common. We found that children with intraorbital extension or intracranial extension were equally likely to present with fever, headache, and vomiting, but identified prolonged duration of headache, often for more than a week, and persistent emesis as presenting features heightening suspicion for intracranial extension. Children in both groups often received medical care before admission, but those with intracranial extension were likely to attend an acute care center rather than the office of a primary caregiver and to have had encounters that did not lead to admission. Preadmission encounters resulted, for two-thirds of children, in prescription of antibiotic therapy.
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Table II. Culture results for children with intraorbital or intracranial extension of sinusitis Number of isolates in children with positive operative cultures* Microbe Gram-positive aerobes a-Hemolytic streptococciz b-Hemolytic streptococcix g-Hemolytic streptococci Methicillin-susceptible Staphylococcus aureus Methicillin-resistant Staphylococcus aureus{ Rothia mucilaginosa Gram-negative aerobes Haemophilus influenzae** Haemophilus parainfluenzae Klebsiella pneumoniae Pseudomonas aeruginosa Subtotal aerobes Anaerobes Bacteroides species Fusobacterium species†† Gemella morbillorum Peptostreptococcus specieszz Prevotella species Veillonella species Subtotal anaerobes Total isolates (isolates per patient)
†
IOE (n = 29)
ICE (n = 24)
6 10 9 7
9 5 13 7
7
0
1
0
5 1 1 0 47
2 2 0 1 39
0 0 0 2 2 0 4
1 2 1 6 4 1
51 (1.8)
15xx 54 (2.3)
ICE, Intracranial extension of sinusitis; IOE, intraorbital extension of sinusitis. *Includes endoscopic sinus, intraorbital, and intracranial culture sources. †Operative cultures from 17 and 8 of children in the IOE and ICE groups, respectively, were sterile. zIncludes Streptococcus pneumoniae (3 isolates). xIncludes group A Streptococcus (n = 5), group B Streptococcus (n = 1), group C Streptococcus (n = 4), group F Streptococcus (n = 4), and b-hemolytic Streptococcus, group not determined (1 isolate). {One isolate was clindamycin-resistant. **Includes nontypable Haemophilus influenzae (n = 6) and Haemophilus influenzae, type b (1 isolate). ††Includes Fusobacterium nucleatum (n = 1) and F necrophorum (1 isolate). zzIncludes Peptostreptococcus micros (n = 5), P prevotii (n = 1), and Peptostreptococcus species (2 isolates). xxP = .02.
Computed tomography provides excellent resolution of bony structures, globe, retro-orbital tissue, sinuses, and cranium and is the imaging modality of choice when complications of sinusitis are suspected.21,22 Contrast-enhanced CT of orbit and sinuses is sufficient for medical decision-making in children with intraorbital extension, whereas MRI offers increased sensitivity to identify the location and extent of intracranial pathology.21,23 Both studies usually are obtained in children with intracranial extension. A presumed diagnosis of viral gastroenteritis in two of our children with headache and emesis delayed imaging evaluation for intracranial extension. Although ethmoid involvement is associated with intraorbital extension and frontal sinusitis with intracranial extension of sinusitis, 90% of the children we evaluated had opacification of multiple sinuses.24-26 Approximately onehalf of those with intraorbital extension and all except one child with intracranial extension underwent drainage of purulent material. Approximately one-half with intracranial extension had neurosurgical drainage and one third required multiple drainage procedures. These patients can be too ill 490
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Table III. Medical treatment of children with intraorbital or intracranial extension of sinusitis Medical intervention Total hospital days Mean duration of total antibiotics (days)† Intravenous Total Patients receiving antibiotics at home Oral route Mean duration (days) IV route Mean duration (days)
IOE (n = 85)*
ICE (n = 33)
10
26
<.001
12 24 83 (98) 70 (84) 14 19 (23)z 11
35 36 17 (52) 6 (35) 13 11 (65) 21
.001 .001 .001 .009 NS .017 .034
P value
ICE, Intracranial extension of sinusitis; IOE, intraorbital extension of sinusitis. *Number of patients (%). †Inpatient and outpatient antibiotic therapy. zSix also had oral therapy.
to tolerate full ESS at the first encounter and limited culture and drainage can be performed initially with a more definitive procedure when the child is clinically stable. Operative cultures were sterile in approximately one fourth of children who had received preadmission antibiotics. A majority of positive cultures were polymicrobial, supporting the use of empirical broad-spectrum antibiotics.27 Broad-spectrum regimens were initiated, most often vancomycin, cefotaxime, and metronidazole when intracranial extension was suspected. The study interval embraced the emergence of community-acquired MRSA in Houston. Infections in children from whom MRSA was isolated were not uncommonly severe or prolonged by comparison with those in which MRSA was isolated. Others have reported neurologic outcomes in children and adolescents with intracranial complications of sinusitis. Among the 11 children with suppurative intracranial extension of sinusitis in the report of Kombogiorgas et al,28 five had persistent focal neurological deficits. Germiller et al20 reported one death and two patients who sustained permanent neurologic sequelae that included hemiparesis and cognitive deficits. Oxford and McClay14 reported persistent morbidity in 4% of their 104 children with intraorbital or intracranial extension of sinusitis. Our 3% overall rate of persistent sequelae is comparable with the latter report. Aggressive management may have contributed to the favorable outcomes we observed. Most children undergoing drainage had surgery within the first 48 hours of admission. Our findings are subject to the limitations inherent in a retrospective study and, although 118 children is a large series, the numbers are still relatively small. Differences in treatment for children in the groups could have resulted in ascertainment bias. Children with intraorbital extension were less likely than those with intracranial extension to undergo MRI. However, based on the hospital course and outcomes, it is unlikely that children were erroneously assigned into groups. Children with intracranial extension had longer courses of intravenous antibiotics, total therapy and hospital stays than those with intraorbital extension. Periorbital edema is shared Goytia, Giannoni, and Edwards
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March 2011 by both intraorbital extension and intracranial extension, but infection in both sites, as defined by strict imaging criteria, is uncommon. Eye swelling combined with persistent headache and vomiting may be the most helpful finding in identifying children with intracranial extension in routine practice. Especially among older children, headache and emesis of sufficient severity to warrant hospitalization should warrant consideration of the diagnosis. Multispecialty participation by otolaryngologists, neurosurgeons, ophthalmologists, and infectious disease physicians is important so that children with these challenging infections can receive prompt, comprehensive treatment to optimize a favorable outcome. n The authors thank Edward O Mason, Jr, PhD, for assistance with the database search and Carol J. Baker, MD, for her insightful suggestions and review of the manuscript. Submitted for publication Dec 18, 2009; last revision received Jun 21, 2010; accepted Sep 2, 2010. Reprint requests: Dr Morven S. Edwards, MD, Texas Children’s Hospital, 1102 Bates Street, Suite 1120, Houston, TX 77030. E-mail: [email protected]
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