This document describes a study of 28 cases of subdural empyema that occurred as a complication of community-acquired bacterial meningitis in adults. The main findings were:
1) Subdural empyema occurred in 2.7% of bacterial meningitis cases and was usually caused by Streptococcus pneumoniae spreading from a predisposing condition like otitis or sinusitis.
2) Patients with subdural empyema often presented with focal neurological deficits, seizures, or altered mental status and were more likely to have complications affecting outcome.
3) Neurosurgical evacuation of large empyemas causing significant midline shift was associated with a more favorable outcome in
2. 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/
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 1–4.
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 effu-
sion 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 under-
went 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 Med-
ical Center, Amsterdam.
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 pneumo-
niae, 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 bac-
terial 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 dur-
ing hospitalization with a median time to detection
of 5 days after admission (range 2–38 days).
The mean age at diagnosis was 58 years (range,
25–81; table 1). Predisposing conditions for bacterial
Table 1 Clinical and laboratory features in 28
adult bacterial meningitis patients with
subdural empyemasa
Clinical characteristics Values
Mean age, y (SD) 58 (14)
Male 19/28 (68)
Predisposing conditions 26/28 (93)
Otitis or sinusitis 21/28 (75)
Pneumonia 3/28 (11)
Immunocompromised stateb
8/28 (29)
Symptoms and signs on admission
Duration of symptoms >24 h 18/28 (64)
Headache 23/27 (85)
Nausea 10/26 (38)
Neck stiffness 20/28 (71)
Seizures 2/27 (7)
Temperature ‡ 38°C 22/28 (79)
Score on Glasgow Coma Scale (GCS) 10 (8–12)
GCS score <14 indicating altered
mental status
23/28 (82)
GCS score <8 indicating coma 6/28 (21)
Focal neurologic deficits 11/28 (39)
Aphasia 4/14 (29)
Ataxia 1/11 (9)
Paresis 7/28 (25)
Cranial nerve palsyc
3/26 (12)
CSF valuesd
Leukocyte count, cells/mm3
2,133 (415–4,665)
Protein, g/L 3.1 (1.6–5.7)
CSF-blood glucose ratio 0.04 (0.00–0.29)
Microbiologic findings
Positive CSF Gram staine
22/24 (92)
Positive blood culture 20/24 (83)
CSF culture
Streptococcus pneumoniae 26/28 (93)
Streptococcus pyogenes 1/28 (4)
Negative 1/28 (4)
a
Data are number/number evaluated (%) and continuous values
are median (interquartile range) unless otherwise stated.
b
Immunocompromise was defined as the use of immuno-
suppressive 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, CSF-
blood glucose ratio in 27 patients, and CSF protein con-
centration in 26 patients.
e
Gram-positive cocci in 21 (88%) and Gram-negative rods
in 1 (4%).
2134 Neurology 79 November 20, 2012
ª 2012 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
3. meningitis were present in 26 of 28 patients (93%)
and consisted of otitis, sinusitis, pneumonia, or an
immunocompromised state. Of the patients with pre-
disposing conditions, 21 had otitis or sinusitis (75%).
On admission, 23 patients (82%) had an altered men-
tal 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 def-
icits 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 neuro-
logic abnormalities were present in 6 of these 10 patients
(60%). Twenty-five patients (89%) presented with neu-
rologic 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 pre-
dictive 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
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 clin-
ically within 8 hours of initial lumbar puncture, but
transtentorial cerebral herniation with pupil dilation
and abnormal posturing was not observed. The dete-
rioration 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 pres-
ence 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 com-
pared 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 micro-
organism (3.8% vs 0.6%, p , 0.001).
The subdural empyema was located at the left con-
vexity 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 empy-
ema was 16.7 mL (range 1.6–129 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 1.0–10.7
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 diffusion-
weighted imaging (DWI) and apparent diffusion coeffi-
cient (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 sinus-
itis 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 combi-
nation of amoxicillin/penicillin and third-generation
cephalosporins for 9 patients (32%), monotherapy
Table 2 Clinical and laboratory features in adults with and without subdural
empyema among 1,034 episodes of bacterial meningitisa
Characteristic
Episodes with
subdural
empyema (n 5 28)
Episodes without
subdural
empyema (n 5 1,006) p Value
Age, y, mean (SD) 58 (14) 57 (18) 0.836
Predisposing conditions 26/28 (93) 548/1,006 (55) ,0.001
Otitis or sinusitis 21/28 (75) 314/1,005 (31) ,0.001
Symptoms and signs on
admission
Headache 23/27 (85) 734/877 (84) 0.836
Focal neurologic deficits 11/28 (39) 283/1,006 (28) 0.197
Paresis 7/28 (25) 87/921 (9) 0.007
Neurologic complications
Focal neurologic
abnormalities
15/28 (54) 189/930 (20) ,0.001
Seizures 14/28 (50) 100/1,003 (10) ,0.001
Hearing impairment 11/28 (39) 193/840 (23) 0.045
Causative organism
Streptococcus pneumoniae 26/28 (93) 652/1,006 (65) 0.002
Outcome
Unfavorable outcome 19/28 (68) 383/1,003 (38) ,0.001
a
Data are number/number evaluated (%).
Neurology 79 November 20, 2012 2135
ª 2012 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
4. penicillin or amoxicillin in 10 patients (36%), mono-
therapy 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 11–62). 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 ther-
apy. Adjunctive steroids were administered in 25 pa-
tients (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%).
Nine patients underwent surgical treatment: cra-
niectomy 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 perfor-
mance 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 compli-
cations 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
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).
2136 Neurology 79 November 20, 2012
ª 2012 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
5. diagnosed on admission. Five patients died (18%) and
19 had an unfavorable outcome (68%; table 3). A high-
er 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 neu-
rologic sequelae on discharge (57%).
DISCUSSION Our study shows that subdural empy-
ema complicates 2.7% of adult cases of community-
acquired 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 epi-
leptic 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 empy-
ema). 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 bac-
teria 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 empy-
ema and increased shift was associated with younger
age rather than thickness or volume of the empyema.
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/as-
terisks), and diffusion-weighted (C) and apparent diffusion coefficient (D)–weighted MRI of a subdural empyema over the left
convexity (arrows).
Neurology 79 November 20, 2012 2137
ª 2012 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
6. This may well be explained by age-related cerebral atro-
phy. In our study, all 5 patients with subdural empyema
who underwent craniectomy survived, albeit with neu-
rologic sequelae at discharge in 3 of them. Nevertheless,
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.
A substantial number of patients deteriorated in
the first 8 hours after lumbar puncture, developing
seizures, respiratory failure, and hemiparesis contra-
lateral to the empyema. These symptoms may be ex-
plained by local expansion of the empyema but could
also be the result of brain shift following the lumbar
puncture, although no transtentorial cerebral hernia-
tion was observed on cranial imaging. Patients with
subdural empyema should be carefully monitored fol-
lowing 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
was not associated with the size of the empyema, mid-
line shift, or whether the empyema was neurosurgi-
cally evacuated. The optimal duration of antimicrobial
treatment for patients with subdural empyema or effu-
sion has not been established in trials or comparative
studies, but general recommendations are to treat pa-
tients with empyema for 3–4 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 treat-
ment 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 empy-
ema 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 collec-
tions 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 differenti-
ation 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 consid-
ered in patients with community-acquired bacterial
meningitis and otitis or sinusitis, focal neurologic def-
icits, or epileptic seizures. S pneumoniae is the pre-
dominant causative organism and patients are at high
risk of developing seizures and unfavorable outcome
(68%). Therefore, early diagnosis of empyema is nec-
essary 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.
Table 3 Complications and outcome in 28 adult
bacterial meningitis patients with
subdural empyemaa
Clinical characteristics Values
Neurologic complications 27/28 (97)
Impairment of consciousness 19/28 (68)
Focal neurologic deficits 15/28 (54)
Hearing impairment 11/28 (39)
Seizures 14/28 (50)
Cerebrovascular complicationsb
4/28 (14)
Cerebral abscess 2/28 (7)
Hydrocephalus 1/28 (4)
Systemic complications 13/28 (46)
Pneumonia 4/28 (14)
Respiratory failure 7/28 (25)
Otherc
4/28 (15)
Glasgow Outcome Scale
1) Death 5 (17)
2) Vegetative state 0
3) Severe disability 1 (3)
4) Moderate disability 13 (46)
5) Complete recovery 9 (32)
Neurologic sequelaed
13/28 (46)
a
Data are number/number evaluated (%).
b
Cerebral infarction in 2, sinus thrombosis in 1, and intra-
cranial 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.
2138 Neurology 79 November 20, 2012
ª 2012 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.
7. 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 Euro-
pean Research Council (ERC Starting Grant 2011).
DISCLOSURE
The authors report no disclosures relevant to the manuscript. Go to
Neurology.org for full disclosures.
Received April 23, 2012. Accepted in final form July 31, 2012.
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