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Subdural empyema in bacterial meningitis

Kin K. Jim, MSc Matthijs C. Brouwer, MD, PhD Arie van der Ende, PhD Diederik van de Beek, MD, PhD

ABSTRACT

Objective: To evaluate the occurrence, treatment, and outcome of subdural empyema complicating community-acquired bacterial meningitis in adults.

Methods: Case series from a prospective nationwide cohort study from Dutch hospitals from 2006 to 2011. Results: Subdural empyema was diagnosed in 28 of 1,034 episodes (2.7%), and was present on
admission in 10 episodes and diagnosed during admission in 18. Predisposing conditions were present in 26 patients (93%), and consisted of otitis or sinusitis in 21 patients (75%). In all these patients the otitis or sinusitis spread to the subdural space. Twenty-three patients (82%) presented with neurologic symptoms (paresis, focal seizures, dysesthesia contralateral to the empyema). Streptococcus pneumoniae was identified in 26 patients (93%) and Streptococcus pyogenes in 1 (3%); 1 patient had negative CSF cultures. Clinical course was frequently complicated with seizures (50%), focal neurologic abnormalities (54%), and hearing impairment (39%), causing an unfavorable outcome in 19 episodes (68%). Neurosurgical evacuation of the empyema was performed in 5 patients, all with considerable midline shift.

Correspondence & reprint requests to Dr. van de Beek: d.vandebeek@amc.uva.nl

Conclusions: Although rare, subdural empyema must be considered in patients with communityacquired bacterial meningitis and otitis or sinusitis, focal neurologic deficits, or epileptic seizures. S pneumoniae is the predominant causative organism and neurosurgical intervention should be regarded as first-choice therapy in patients with empyema causing midline shift and focal neurologic abnormalities or a decreased level of consciousness. Neurology 2012;79:21332139
GLOSSARY
ADC 5 apparent diffusion coefficient; DWI 5 diffusion-weighted imaging; NRLBM 5 Netherlands Reference Laboratory for Bacterial Meningitis.

Bacterial meningitis is a life-threatening disease that requires immediate medical attention. The predominant causative pathogens are Streptococcus pneumoniae and Neisseria meningitidis in adults, causing 80%85% of all cases, with mortality rates varying from 19% to 37% for S pneumoniae and 3%13% for N meningitidis.14 Community-acquired bacterial meningitis is associated with serious intracranial complications such as cerebral infarctions, hydrocephalus, subdural empyema, and cerebral abscess, which can be life-threatening and may require neurosurgical treatment.2,3,510 Subdural empyema has only been reported as an uncommon complication of community-acquired bacterial meningitis in adults.24,9,11,12 We investigated the occurrence, treatment, and outcome of subdural empyemas in adults with community-acquired bacterial meningitis.
METHODS We included adults (defined as patients older than 16 years of age) who had bacterial meningitis and were listed in the database of the Netherlands Reference Laboratory for Bacterial Meningitis (NRLBM) from March 2006 to November 2011 in a nationwide prospective cohort study. The NRLBM receives CSF and blood isolates from approximately 90% of all patients with CSF culturepositive bacterial meningitis in the Netherlands (population, 16.7 million).2,11,12 The NRLBM provided daily updates of the names of the hospitals where patients with bacterial meningitis had been admitted in the preceding 26 days and the names of physicians. Physicians were contacted, and informed consent was obtained from all participating patients or their legally authorized representatives. Physicians could also contact the investigators without report of the NRLBM for inclusion of patients. Episodes
From the Departments of Neurology (K.K.J., M.C.B., D.v.d.B.) and Medical Microbiology (A.v.d.E.) and The Netherlands Reference Laboratory for Bacterial Meningitis (A.v.d.E.), Center of Infection and Immunity Amsterdam (CINIMA), Academic Medical Center, University of Amsterdam, Amsterdam, the Netherlands. Study funding: Funding information is provided at the end of the article. Go to Neurology.org for full disclosures. Disclosures deemed relevant by the authors, if any, are provided at the end of this article. 2012 American Academy of Neurology 2133

CME

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Table 1

Clinical and laboratory features in 28 adult bacterial meningitis patients with subdural empyemasa
Values 58 (14) 19/28 (68) 26/28 (93) 21/28 (75) 3/28 (11) 8/28 (29)

Clinical characteristics Mean age, y (SD) Male Predisposing conditions Otitis or sinusitis Pneumonia Immunocompromised stateb Symptoms and signs on admission Duration of symptoms >24 h Headache Nausea Neck stiffness Seizures Temperature 38C

18/28 (64) 23/27 (85) 10/26 (38) 20/28 (71) 2/27 (7) 22/28 (79)

Score on Glasgow Coma Scale (GCS) 10 (812) GCS score <14 indicating altered mental status GCS score <8 indicating coma Focal neurologic deficits Aphasia Ataxia Paresis Cranial nerve palsyc CSF valuesd Leukocyte count, cells/mm3 Protein, g/L CSF-blood glucose ratio Microbiologic findings Positive CSF Gram staine Positive blood culture CSF culture Streptococcus pneumoniae Streptococcus pyogenes Negative
a

23/28 (82)

6/28 (21) 11/28 (39) 4/14 (29) 1/11 (9) 7/28 (25) 3/26 (12)

2,133 (4154,665) 3.1 (1.65.7) 0.04 (0.000.29)

22/24 (92) 20/24 (83)

dL [1.9 mmol/L], a ratio of CSF glucose to blood glucose of less than 0.23, a protein level of more than 220 mg/dL, or a leukocyte count of more than 2,000/mL)13 and the clinical presentation was compatible with bacterial meningitis. Patients were considered immunocompromised if they used immunosuppressive drugs or had a history of splenectomy, diabetes mellitus, alcoholism, cancer, or HIV infection. Patients with hospital-associated meningitis (defined as meningitis that occurred during hospitalization or within 1 week of discharge) including neurosurgery patients, and patients with a neurosurgical device, or neurotrauma within 1 month of the onset of meningitis were excluded. Case-record forms were used to collect data on patient history, symptoms and signs on admission, clinical course, and outcome. Treatment information regarding antimicrobial treatment and (neuro)surgical interventions was collected. At discharge, all patients underwent neurologic examination performed by a neurologist, and the outcome was graded according to the Glasgow Outcome Scale. The Glasgow Outcome Scale is a well-validated instrument with good interobserver agreement.14 A favorable outcome was defined as a score of 5, and an unfavorable outcome as a score of 14. Patients were classified as having subdural empyema if reported by the treating physician and cranial imaging showed a crescent- or ellipse-shaped fluid collection in the subdural space. We chose to classify all subdural fluid collections as empyemas, as subdural effusion is a sterile fluid collection, mostly found in chronic disease.15 The differentiation between subdural empyema and effusion is difficult even with contrast-enhanced CT or MRI, and therefore one can also read subdural empyema or effusion when we use subdural empyema. Cranial radiologic imaging was collected and independently re-evaluated by 2 investigators (K.K.J., M.C.B.). Midline shift was measured, and the volume of the empyema was calculated using the ABC/2 method.16 To check for underreporting by physicians, we evaluated 150 consecutive patients who underwent cranial imaging in whom subdural empyema was not reported. None of these patients had subdural empyema. The Mann-Whitney U test was used to identify differences between episodes with and without subdural empyema with respect to continuous variables, and dichotomous variables were compared with use of the x2 test. Pearson correlation test was used to identify correlations between continuous variables. All tests were 2-tailed and a p value ,0.05 was considered significant. Statistical analyses were performed with use of IBM SPSS Statistics, version 19.0.0.

Standard protocol approvals, registrations, and patient consents.


The study was approved by the ethics committee of the Academic Medical Center, Amsterdam.

26/28 (93) 1/28 (4) 1/28 (4)

Data are number/number evaluated (%) and continuous values are median (interquartile range) unless otherwise stated. b Immunocompromise was defined as the use of immunosuppressive drugs or a history of splenectomy, diabetes mellitus, alcoholism, cancer, or HIV infection. c Oculomotor nerve in 2 patients, abducens and facial nerve in 1 patient each. d CSF leukocyte count was determined in 28 patients, CSFblood glucose ratio in 27 patients, and CSF protein concentration in 26 patients. e Gram-positive cocci in 21 (88%) and Gram-negative rods in 1 (4%).

reported by physicians with negative CSF cultures could also be included if CSF results showed at least one individual predictor of bacterial meningitis (defined as a glucose level of less than 34 mg/
2134 Neurology 79 November 20, 2012

RESULTS From March 2006 to November 2011, we included 1,034 patients with bacterial meningitis. A total of 678 (66%) episodes were caused by S pneumoniae, 107 (10%) by N meningitidis, and 165 (16%) by other bacteria. A total of 79 patients had negative CSF cultures but at least one individual CSF marker of bacterial meningitis. Subdural empyema was diagnosed in 28 of 1,034 episodes of bacterial meningitis (2.7%) and in 3.1% of 916 patients in whom cranial imaging was performed. Subdural empyema was present on admission in 10 patients (38%). In the remaining 18 patients (64%) the empyema was detected during hospitalization with a median time to detection of 5 days after admission (range 238 days). The mean age at diagnosis was 58 years (range, 2581; table 1). Predisposing conditions for bacterial

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meningitis were present in 26 of 28 patients (93%) and consisted of otitis, sinusitis, pneumonia, or an immunocompromised state. Of the patients with predisposing conditions, 21 had otitis or sinusitis (75%). On admission, 23 patients (82%) had an altered mental status (defined by a score on the Glasgow Coma Scale below 14) and 6 patients (21%) were comatose (Glasgow Coma Scale score ,8). Focal neurologic deficits were present on admission in 11 (39%) patients. The classic meningitis triad of neck stiffness, fever, and altered mental status was present in 13 patients (46%). Of the 10 patients diagnosed with subdural empyema on admission, 7 (70%) had a subacute presentation with symptoms for more than 24 hours. Focal neurologic abnormalities were present in 6 of these 10 patients (60%). Twenty-five patients (89%) presented with neurologic symptoms (paresis, focal seizures, dysesthesia) on the contralateral side of the empyema or effusion. Patients with subdural empyema were more likely to have predisposing conditions on admission (93% vs 54%; p , 0.001; table 2), especially otitis or sinusitis (75% vs 31%; p , 0.001), than patients without subdural empyema. Furthermore, they were more likely to present with a paresis on admission (25% vs 9%; p 5 0.007) than patients without subdural empyema. Lumbar puncture was performed on admission in all patients. At least one individual CSF finding predictive of bacterial meningitis (a glucose level of less than 34 mg/dL [1.9 mmol/L], a ratio of CSF glucose to blood glucose of less than 0.23, a protein level of
Table 2 Clinical and laboratory features in adults with and without subdural empyema among 1,034 episodes of bacterial meningitisa
Episodes with subdural empyema (n 5 28) 58 (14) 26/28 (93) 21/28 (75) Episodes without subdural empyema (n 5 1,006) 57 (18) 548/1,006 (55) 314/1,005 (31)

Characteristic Age, y, mean (SD) Predisposing conditions Otitis or sinusitis Symptoms and signs on admission Headache Focal neurologic deficits Paresis Neurologic complications Focal neurologic abnormalities Seizures Hearing impairment Causative organism Streptococcus pneumoniae Outcome Unfavorable outcome
a

p Value 0.836 ,0.001 ,0.001

23/27 (85) 11/28 (39) 7/28 (25)

734/877 (84) 283/1,006 (28) 87/921 (9)

0.836 0.197 0.007

15/28 (54)

189/930 (20)

,0.001 ,0.001 0.045

14/28 (50) 11/28 (39)

100/1,003 (10) 193/840 (23)

26/28 (93)

652/1,006 (65)

0.002

19/28 (68)

383/1,003 (38)

,0.001

Data are number/number evaluated (%).

more than 220 mg/dL, or a leukocyte count of more than 2,000/mm3) was present in all patients with subdural empyema. Eleven patients deteriorated clinically within 8 hours of initial lumbar puncture, but transtentorial cerebral herniation with pupil dilation and abnormal posturing was not observed. The deterioration consisted of (increase in) hemiparesis in 6 patients, respiratory failure in 4, and seizures in 4. Cranial imaging was repeated following deterioration in 10 of 11 patients and did not show radiologic signs of transtentorial cerebral herniation. Gram staining of CSF was done in 24 patients (86%) and showed presence of bacteria in 22 patients (92%). CSF cultures showed S pneumoniae in 26 patients, Streptococcus pyogenes in 1 patient, and 1 patient had a negative CSF culture. The incidence of subdural empyema in patients with pneumococcal meningitis presenting with otitis or sinusitis was 17 of 224 (8%). Patients with subdural empyema were more likely to have S pneumoniae as the causative microorganism compared to patients without empyema (93% vs 65%; p 5 0.002). Conversely, patients with pneumococcal meningitis are more likely to have subdural empyema than patients with meningitis due to another microorganism (3.8% vs 0.6%, p , 0.001). The subdural empyema was located at the left convexity in 12 patients, right convexity in 14 patients, and bilateral in 2 patients (figures 1 and 2). Cranial imaging was available for re-evaluation in 25 of 28 patients. The median volume of the subdural empyema was 16.7 mL (range 1.6129 mL). The subdural empyema caused a mass effect in 21 of 25 patients (84%), resulting in midline shift in 19 patients (76%). Median midline shift measured 3.0 mm (range 1.010.7 mm), and midline shift over 4 mm occurred more often in patients under 60 years (p 5 0.016). The degree of midline shift was strongly correlated to the volume of the empyema (coefficient 0.533, p 5 0.02). Cranial MRI was performed in 7 patients and included diffusionweighted imaging (DWI) and apparent diffusion coefficient (ADC) imaging in 4. On all these 4 MRIs the subdural fluid collection showed a DWI hyperintense and ADC hypointense signal (figure 2). This pattern is typical for subdural empyema, in contrast to subdural effusions, which are hypointense on DWI.17 Other abnormalities on cranial imaging were sinusitis or mastoiditis in 23 patients (82%), generalized cerebral edema in 8 patients (28%), and cerebral abscess and infarction each in 2 patients (7%). Meningioma, sinus thrombosis, hydrocephalus, and intracerebral hemorrhage were each identified in 1 patient (3%). In all 21 patients with mastoiditis the subdural empyema developed on the same side. Initial antimicrobial treatment consisted of a combination of amoxicillin/penicillin and third-generation cephalosporins for 9 patients (32%), monotherapy
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Figure 1

CTs of empyema complicating bacterial meningitis

Axial CT of patient with bacterial meningitis with bilateral subdural empyema (A), temporal subdural empyema (B), frontal subdural empyema adjacent to intracerebral abscess causing brain shift (C), and parafalcine subdural empyema (D).

penicillin or amoxicillin in 10 patients (36%), monotherapy with a third-generation cephalosporin in 7 patients (25%), and monotherapy carbapenem and a combination of penicillin and carbapenem each in 1 patient (4%). All patients received microbiologically adequate initial antimicrobial therapy. The median duration of antimicrobial treatment in surviving patients was 17 days (range 1162). The duration of treatment was not associated with the size of the empyema, with the causative microorganism, or with whether neurosurgical removal of the empyema was performed. None of the patients had a relapse of symptoms after discontinuation of antimicrobial therapy. Adjunctive steroids were administered in 25 patients (89%). Dexamethasone, given 10 mg every 6 hours for 4 days started before or with the first dose of antibiotics, was given in 24 patients (86%).
2136 Neurology 79 November 20, 2012

Nine patients underwent surgical treatment: craniectomy for evacuation of subdural empyema in 5 patients, mastoidectomy in 4 patients, paracentesis in 3, and 1 patient required an external ventricular drain for treatment of a hydrocephalus. All 5 patients who underwent craniectomy survived, of whom 3 had neurologic sequelae at discharge. The performance of craniectomy was associated with the degree of midline shift (p 5 0.01), but not with the volume of the empyema (p 5 0.41). Complications developed during clinical course in 27 of 28 patients (96%; table 3). Neurologic complications occurred in all 27 and systemic complications in 11. Focal neurologic abnormalities developed in 15 patients (54%), seizures in 14 (50%), and hearing impairment in 11 (39%). In 10 of 11 episodes (91%) that were complicated by hearing impairment, otitis was

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Figure 2

MRIs of empyema complicating bacterial meningitis

Axial (A) and sagittal (B) T1-weighted gadolinium-enhanced MRI of patients with parafalcine subdural empyema (arrows/asterisks), and diffusion-weighted (C) and apparent diffusion coefficient (D)weighted MRI of a subdural empyema over the left convexity (arrows).

diagnosed on admission. Five patients died (18%) and 19 had an unfavorable outcome (68%; table 3). A higher rate of unfavorable outcome was observed in patients with subdural empyema compared to patients with meningitis without subdural fluid collection (68% vs 38%; p , 0.001). Thirteen of 23 survivors had neurologic sequelae on discharge (57%).
DISCUSSION Our study shows that subdural empyema complicates 2.7% of adult cases of communityacquired bacterial meningitis but is associated with a high rate of unfavorable outcome (68%). Subdural fluid collection has been reported previously to occur in 1% 3.4%.3,4,18 Important clues for the diagnosis of empyema were otitis or sinusitis, focal neurologic deficits, or epileptic seizures. For patients with meningitis who develop neurologic complications during admission, cranial imaging to detect subdural empyema is indicated.3,19 MRI with DWI remains the preferred imaging modality

for detecting subdural empyema. DWI and diffusion on the ADC map have proven to be valuable in evaluation of intracranial pyogenic processes (abscess and empyema). Furthermore, DWI can distinguish subdural empyema from reactive subdural effusion.17 The incidence of subdural empyema in patients with pneumococcal meningitis presenting with otitis was high (8%). In all patients with otitis or sinusitis the bacteria spread from the mastoid or sinus to the adjacent subdural space causing the subdural empyema. Because of the increased risk of empyema in patients with otitis or sinusitis, consultation of an ear, nose, and throat specialist is warranted early during clinical course in all patients with bacterial meningitis. Only a minority of patients underwent neurosurgical evacuation of the empyema. In our series, midline shift was associated with the decision to evacuate the empyema and increased shift was associated with younger age rather than thickness or volume of the empyema.
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Table 3

Complications and outcome in 28 adult bacterial meningitis patients with subdural empyemaa
Values 27/28 (97) 19/28 (68) 15/28 (54) 11/28 (39) 14/28 (50) 4/28 (14) 2/28 (7) 1/28 (4) 13/28 (46) 4/28 (14) 7/28 (25) 4/28 (15)

Clinical characteristics Neurologic complications Impairment of consciousness Focal neurologic deficits Hearing impairment Seizures Cerebrovascular complicationsb Cerebral abscess Hydrocephalus Systemic complications Pneumonia Respiratory failure Otherc Glasgow Outcome Scale 1) Death 2) Vegetative state 3) Severe disability 4) Moderate disability 5) Complete recovery Neurologic sequelae
a
d

5 (17) 0 1 (3) 13 (46) 9 (32) 13/28 (46)

Data are number/number evaluated (%). Cerebral infarction in 2, sinus thrombosis in 1, and intracranial hemorrhage in 1. c Osteomyelitis, hyponatremia, rhabdomyolysis, and deep venous thrombosis of the arm each occurred in 1 patient. d Hemiparesis in 9 patients, sensory change in 7 patients, cognitive impairment in 6, cranial nerve palsy in 6, ataxia and aphasia both occurred in 1 patient.
b

This may well be explained by age-related cerebral atrophy. In our study, all 5 patients with subdural empyema who underwent craniectomy survived, albeit with neurologic sequelae at discharge in 3 of them. Nevertheless, neurosurgical intervention should be regarded as firstchoice therapy in patients with empyema causing midline shift and focal neurologic abnormalities or a decreased level of consciousness. A substantial number of patients deteriorated in the first 8 hours after lumbar puncture, developing seizures, respiratory failure, and hemiparesis contralateral to the empyema. These symptoms may be explained by local expansion of the empyema but could also be the result of brain shift following the lumbar puncture, although no transtentorial cerebral herniation was observed on cranial imaging. Patients with subdural empyema should be carefully monitored following lumbar puncture, as the empyema could expand and cause brain shift. In our study, the median duration of antimicrobial treatment in surviving patients was only 17 days, and
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was not associated with the size of the empyema, midline shift, or whether the empyema was neurosurgically evacuated. The optimal duration of antimicrobial treatment for patients with subdural empyema or effusion has not been established in trials or comparative studies, but general recommendations are to treat patients with empyema for 34 weeks if an empyema has been evacuated, and even longer if the patient is conservatively treated.20 This indicates that subdural empyemas do not trigger Dutch physicians to prolong antimicrobial treatment, but also that relatively short courses of antibiotics do not result in microbiologic treatment failures in these patients. Our study has several important limitations. First, cranial imaging was not performed in all patients in the cohort and cases of subdural fluid collection might have been missed. This could have led to an underestimation of the incidence of subdural empyema or effusion. Furthermore, subdural empyemas that remain subclinical may go undetected, which may lead to an overestimation of the severity of the disorder in our study. Asymptomatic subdural collections may resolve without neurosurgical intervention. Second, culture-negative patients are underrepresented in our study. Negative CSF cultures occur in 11% 30% of patients with bacterial meningitis.1,2,4 These patients were only included if the treating physician contacted the investigators, which occurred in 11% of the episodes.21 Third, the diagnosis subdural effusion or subdural empyema was classified by the treating physician, and therefore it is unclear if the differentiation between subdural empyema and subdural effusion always occurred in a similar fashion. To differentiate between subdural empyema and subdural effusion contrast-enhanced cranial imaging is necessary. Some patients did not undergo contrast-enhanced cranial imaging, and therefore the differentiation between empyema and effusion may not have been accurate in all cases. Although rare, subdural empyema must be considered in patients with community-acquired bacterial meningitis and otitis or sinusitis, focal neurologic deficits, or epileptic seizures. S pneumoniae is the predominant causative organism and patients are at high risk of developing seizures and unfavorable outcome (68%). Therefore, early diagnosis of empyema is necessary and neurosurgical intervention should be regarded as first-choice therapy in patients with empyema causing midline shift and focal neurologic abnormalities or a decreased level of consciousness.

AUTHOR CONTRIBUTIONS
Kin K. Jim, Matthijs Brouwer, and Diederik van de Beek performed the data analyses and wrote the manuscript. Arie van der Ende wrote the manuscript. Diederik van de Beek was the principal investigator of the study and provided funding.

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STUDY FUNDING
D.v.d.B. is supported by grants from the Netherlands Organization for Health Research and Development (ZonMw; NWO-Vidi grant 2010), the Academic Medical Center (AMC Fellowship 2008), and the European Research Council (ERC Starting Grant 2011).

10.

11. 12.

DISCLOSURE
The authors report no disclosures relevant to the manuscript. Go to Neurology.org for full disclosures.

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