Empiema Subdural Meningitis 2012

8/13/2019 Empiema Subdural Meningitis 2012

1/7

Kin K. Jim, MSc

Matthijs C. Brouwer,

MD, PhD

Arie van der Ende, PhD

Diederik van de Beek,

MD, PhD

Correspondence & reprint

requests to Dr. van de Beek:

[email protected]

CME

Subdural empyema in bacterial meningitis

ABSTRACT

Objective: To evaluate the occurrence, treatment, and outcome of subdural empyema complicat-

ing 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%) pre-

sented with neurologic symptoms (paresis, focal seizures, dysesthesia contralateral to the empy-

ema). Streptococcus pneumoniae was identified in 26 patients (93%) and Streptococcus

pyogenesin 1 (3%); 1 patient had negative CSF cultures. Clinical course was frequently compli-

cated with seizures (50%), focal neurologic abnormalities (54%), and hearing impairment (39%),

causing an unfavorable outcome in 19 episodes (68%). Neurosurgical evacuation of the empy-

ema was performed in 5 patients, all with considerable midline shift.

Conclusions: 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 pneumoniaeis the predominant causative organism and neurosurgical intervention should be

regarded as first-choice therapy in patients with empyema causing midline shift and focal neu-

rologic 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 forBacterial Meningitis.

Bacterial meningitis is a life-threatening disease that requires immediate medical attention. The pre-

dominant causative pathogens are Streptococcus pneumoniae and Neisseria meningitidis in adults,

causing 80%85% of all cases, with mortality rates varying from 19% to 37% forS pneumoniae

and 3%13% forN 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 Sub-

dural 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 2 6 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

2012 American Academy of Neurology. Unauthorized reproduction of this article is prohibited.


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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 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 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 comparedwith use of the x2 test. Pearson correlation test was used to identify

correlations between continuous variables. All tests were 2-tailed

and ap 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.

RESULTSFrom March 2006 to November 2011, we

included 1,034 patients with bacterial meningitis. A

total of 678 (66%) episodes were caused byS pneumo-

niae, 107 (10%) byN meningitidis, and 165 (16%) by

other bacteria. A total of 79 patients had negative CSFcultures 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 238 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 38C 22/28 (79)

Score on Glasgow Coma Scale (GCS) 10 (812)

GCS score


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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 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 pneumoniaeas 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 1.6129 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 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 withsubduralempyema (n 5 28)

Episodes withoutsubduralempyema (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 onadmission

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 neurologicabnormalities

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

aData are number/number evaluated (%).

Neurology 79 November 20, 2012 2135



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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 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 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



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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)weightedMRI of a subdural empyema over theleft

convexity (arrows).




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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 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 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 thedisorder 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 differentiatebetween 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, ataxiaand aphasia both occurred in 1 patient.

2138 Neurology 79 November 20, 2012



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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 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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Empiema Subdural Meningitis 2012