Predictors of outcome of subdural empyema in children

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OBJECTIVE

The aim of this study was to report the etiology, clinical features, microbiology, surgical outcome, and predictors of outcome of spontaneous subdural empyema (SDE).

METHODS

The authors conducted a retrospective study in a tertiary hospital. Children up to 18 years of age, with a diagnosis of SDE with infective etiology, were included in the present cohort. Patients with posttraumatic, postsurgery, and tubercular origin of SDE were excluded from the study. The Glasgow Outcome Scale was used for outcome assessment at the end of 3 months. For analysis purposes, the demographic data, clinical features, radiological data, microbiology, type of surgery, and complication data were categorized, and univariate and multivariable logistic regression analyses were performed to identify the factors associated with outcome.

RESULTS

Ninety-eight children were included in the study and the mean age was 10.9 years. Otogenic origin (34.7%) was the most common source of infection, followed by meningitis (14.3%). The mean duration of symptoms was 12 days. Seventy-six children presented with Glasgow Coma Scale (GCS) score > 8 and the supratentorial location was the most common location. Almost 75% of the children underwent craniotomy or craniectomy and the rest had burr-hole evacuation. Beta-hemolytic Streptococcus (10%) was the most common organism isolated. Cerebral venous thrombosis (CVT; 10.2%) was the most frequent complication in this cohort. The other complications were infarction (6.1%), new-onset seizure (4.1%), and bone flap osteomyelitis (4.1%). Thirteen cases had a recurrence of pus collection, which was more common in the craniotomy group than in the burr-hole group. Age (p = 0.02), GCS score ≤ 8 (OR 8.15, p = 0.001), CVT (OR 15.17, p = 0.001), and presence of infarction (OR 7, p = 0.05) were strongly associated with unfavorable outcome. In multivariable logistic regression analysis, only GCS score ≤ 8 (p = 0.01), CVT (p = 0.02), and presence of infarction (p = 0.04) had a significant impact on unfavorable outcome.

CONCLUSIONS

Prompt diagnosis and immediate intervention is the goal of management of SDE, especially in children as a delay in diagnosis can result in unconsciousness and secondary complications such as CVT and infarction, which adversely affect outcome.

ABBREVIATIONS CVT = cerebral venous thrombosis; GCS = Glasgow Coma Scale; GOS = Glasgow Outcome Scale; IQR = interquartile range; SDE = subdural empyema.

OBJECTIVE

The aim of this study was to report the etiology, clinical features, microbiology, surgical outcome, and predictors of outcome of spontaneous subdural empyema (SDE).

METHODS

The authors conducted a retrospective study in a tertiary hospital. Children up to 18 years of age, with a diagnosis of SDE with infective etiology, were included in the present cohort. Patients with posttraumatic, postsurgery, and tubercular origin of SDE were excluded from the study. The Glasgow Outcome Scale was used for outcome assessment at the end of 3 months. For analysis purposes, the demographic data, clinical features, radiological data, microbiology, type of surgery, and complication data were categorized, and univariate and multivariable logistic regression analyses were performed to identify the factors associated with outcome.

RESULTS

Ninety-eight children were included in the study and the mean age was 10.9 years. Otogenic origin (34.7%) was the most common source of infection, followed by meningitis (14.3%). The mean duration of symptoms was 12 days. Seventy-six children presented with Glasgow Coma Scale (GCS) score > 8 and the supratentorial location was the most common location. Almost 75% of the children underwent craniotomy or craniectomy and the rest had burr-hole evacuation. Beta-hemolytic Streptococcus (10%) was the most common organism isolated. Cerebral venous thrombosis (CVT; 10.2%) was the most frequent complication in this cohort. The other complications were infarction (6.1%), new-onset seizure (4.1%), and bone flap osteomyelitis (4.1%). Thirteen cases had a recurrence of pus collection, which was more common in the craniotomy group than in the burr-hole group. Age (p = 0.02), GCS score ≤ 8 (OR 8.15, p = 0.001), CVT (OR 15.17, p = 0.001), and presence of infarction (OR 7, p = 0.05) were strongly associated with unfavorable outcome. In multivariable logistic regression analysis, only GCS score ≤ 8 (p = 0.01), CVT (p = 0.02), and presence of infarction (p = 0.04) had a significant impact on unfavorable outcome.

CONCLUSIONS

Prompt diagnosis and immediate intervention is the goal of management of SDE, especially in children as a delay in diagnosis can result in unconsciousness and secondary complications such as CVT and infarction, which adversely affect outcome.

Subdural empyema (SDE) is an acute neurological condition, especially in children. The etiopathogenesis of spontaneous SDE is spread from either local or systemic infection. The etiology also varies based on different age groups.8 The incidence of SDE in infants is approximately 1%–2%, and is mainly due to pyogenic bacterial meningitis.13 In older children, the source is either paranasal sinus involvement5,15,16 or the mastoid.21 The pus is noted more often in the supratentorial than in the infratentorial compartment. The empyema may be over the convexity or in the interhemispheric space. Few case series2,7,8,10,12,17,19,23–25 or case reports1,3,6,14,18,22 of SDE have been published in the literature but prognostic factors for outcome have not been analyzed. In the present study we analyzed the prognostic factors for outcome in children with SDE.

Methods

This is a retrospective study conducted at a high-volume neurosurgical center in a developing country (India). The study duration was from January 2005 to December 2017. The study was conducted within the norms of local institutional ethics policies. Children up to 18 years of age with a diagnosis of pyogenic SDE were included in the present cohort. Patients with posttraumatic, postsurgical, and tubercular etiology of SDE were excluded from the study. Clinical data were collected from medical records, and radiological data from direct observation of images or from the medical records. The Glasgow Outcome Scale (GOS) was used at the end of 3 months from surgery to record the outcome. Outcome was dichotomized into favorable outcome, i.e., GOS score of 5 or 4 (good recovery and moderate disability), and unfavorable outcome, i.e., GOS score 1–3 (death, vegetative state, and severe disability).

Prognostic Factors

For comprehensive analyses, we considered demographic data, clinical features, radiological data, microbiology, type of surgery, and complications as prognostic factors for outcome. Age, sex (male and female), duration of symptoms (≤ 7 days and > 7 days), location (supratentorial and infratentorial), site (right and left), compartment (convexity, interhemispheric, and both), Glasgow Coma Scale (GCS) score (≤ 8 and > 8), preoperative seizure (present or absent), etiology related (otogenic and nonotogenic), microbiology (gram-positive and gram-negative), type of surgery (craniotomy and burr holes), and presence of cerebral venous thrombosis (CVT), infarct, cerebral abscess, and recurrence.

The Statistical Package for the Social Sciences software (version 20, IBM Corp.) was utilized for statistical analysis. To identify the association between predictive factors with the outcome, chi-square and Fisher’s exact tests were performed. Both tests were utilized for categorical variables. For continuous variables, the Mann-Whitney U-test was applied. Univariate analysis (post hoc) was performed for other variables. Statistically significant variables (p < 0.25) were further considered for multivariable logistic regression analysis to identify the impact of individual risk factors. Statistical significance was defined at p < 0.05.

Results

A total of 98 children (81 males, 82.6%) were included in the present cohort. The mean age was 10.9 years (range 6 months–18 years). Nine children were younger than 1 year of age (Table 1).

TABLE 1.

Clinical features of the study cohort (n = 98)

ParameterValue (%)
Mean age ± SD, yrs10.9 ± 5.8
Males81 (82.6)
Causes
 Otogenic34 (34.7)
 Paranasal sinusitis11 (11.2)
 Meningitis14 (14.3)
 Lung infection2 (2.0)
 Cardiac1 (1.0)
 Others8 (8.2)
 Unknown28 (28.6)
Clinical features
 Headache64 (65.3)
 Fever89 (90.8)
 Seizures35 (35.7)
 Altered sensorium47 (48)
 GCS score >876 (77.6)
 Cranial nerve deficits11 (11.2)
 Monoparesis6 (6.1)
 Hemiparesis32 (32.7)
 Cerebellar sign3 (3.1)

Etiology, Clinical Features, and Microbiology

The middle ear (34.7%) was the most common source of infection, followed by meningitis (14.3%) and paranasal sinus (11.2%). Twenty-eight children did not have a known source of infection. The mean duration of symptoms was 12 days and 50% of children presented within 7 days of infection. The most common symptom was fever (90.8%) followed by headache (65.3%) and altered sensorium (48%). The other clinical features were seizure (35.7%), hemiparesis (32.7%), monoparesis (6.1%), and cranial nerve deficits (11.2%). Seventy-six children presented with a GCS score > 8. The most common location was supratentorial (84.7%) over cerebral convexity (73.5%) collections (Fig. 1, Table 2). Ten children had associated brain abscess and 11 children had hydrocephalus. Thirty-five children had pus collection over the right hemisphere, 26 children over the left hemisphere, and 9 in the interhemispheric region. Beta-hemolytic Streptococcus (10%) was the most common organism isolated, followed by alpha-hemolytic Streptococcus (8%) and Proteus mirabilis (7%). Thirty-seven children had sterile culture and 2 children had multiple organisms (Table 2).

FIG. 1.
FIG. 1.

A: Axial T1-weighted MR image with contrast enhancement showing a left-sided, frontoparietal, subdural, hypointense collection with peripheral enhancement, suggestive of pus collection. B: Coronal T1-weighted MR image with contrast enhancement showing an interhemispheric pus collection in continuation with the convexity. C: Axial CT image with contrast enhancement showing good evacuation of the pus collection and evidence of craniotomy.

TABLE 2.

Radiology and microbiology

ParameterValue (%)
Radiology
 Supratentorial83 (84.7)
  Convexity61 (73.5)
  Convexity & interhemispheric13 (15.7)
  Interhemispheric9 (10.8)
 Infratentorial15 (15.3)
 Associated abscess10 (10.2)
 Hydrocephalus11 (11.2)
Microbiology
S. aureus4 (4.1)
S. epidermidis5 (5.1)
 Alpha-hemolytic Streptococcus8 (8.2)
 Beta-hemolytic Streptococcus10 (10.2)
Acinetobacter baumannii1 (1.0)
 NFGNB2 (2.0)
Enterobacter1 (1.0)
Escherichia coli7 (7.1)
Pseudomonas spp.6 (6.1)
Proteus spp.7 (7.1)
Klebsiella2 (2.0)
Peptostreptococcus3 (3.1)
Providentia1 (1.0)
 Anaerobic bacteria2 (2.0)
 Multiple organisms2 (2.0)
 Sterile37 (37.8)

NFGNB = nonfermenting gram-negative bacilli.

Surgical Procedures, Complications, and Outcomes

The most common surgical procedure performed was craniotomy evacuation of pus and excision of the outer membrane (73.5% cases; Fig. 2, Table 3). Twenty-six children underwent burr-hole evacuation of the pus collection. After the surgical evacuation of pus, all children received 2 weeks of intravenous antibiotics followed by 2–4 weeks of oral antibiotics based on the culture sensitivity report. Children with initial sterile pus received cefotaxime, amikacin, and metronidazole based on our institute’s antibiotic policy. All children with sinusitis or otitis were referred to an ear, nose, and throat surgeon for further management.

FIG. 2.
FIG. 2.

A: Axial CT image with contrast showing a left-sided, frontal, hypodense collection. B: Intraoperative photograph showing the yellowish pus collection underneath the dura. C: Axial CT image with contrast showing good evacuation of pus.

TABLE 3.

Surgery, complications, and outcomes

ParameterValue (%)
Surgical procedure
 Burr hole26 (26.5)
 Craniotomy/craniectomy72 (73.5)
 Shunt for persisting hydrocephalus2 (2.0)
Complication
 CVT10 (10.2)
 New-onset seizures4 (4.1)
 Infarction6 (6.1)
 Subgaleal pus collection1 (1.0)
 Wound CSF leak2 (2.0)
 Venous sinus injury2 (2.0)
 Bone flap osteomyelitis4 (4.1)
Outcome
 Recurrence13 (13.3)
  Burr-hole group2/26 (7.7)
  Craniotomy group11/72 (15.3)
 Death8 (10.7)
 Favorable outcome63/76 (82.9)
 Unfavorable outcome (including death)13/76 (17.1)

The most frequent complication of SDE was CVT (10.2%) in our cohort. The other complications were cerebral infarction (6.1%), new-onset seizure (4.1%), bone flap osteomyelitis (4.1%), wound CSF leak (2 cases), venous sinus injury (2 cases), and subgaleal collection of pus (1 case). Thirteen children had a recurrence of pus collection, which was more common in the craniotomy group (11 cases) versus the burr-hole group (2 cases; Table 3).

Eight children died due to septicemia in the perioperative period. One child with congenital heart disease suffered cardiac arrest after surgery, and could not be revived. Follow-up was available for 68 children, with a median follow-up duration of 14.5 months (range 3–132 months). Two children developed hydrocephalus at follow-up and underwent ventriculoperitoneal shunt insertion. At 3 months after surgery, 63 children (82.9%) had a favorable outcome and 13 (17.1%) had an unfavorable outcome, including the 8 perioperative deaths.

Prognostic Factors for Unfavorable Outcome

Univariate and multivariable logistic regression analyses were used to identify factors associated with unfavorable outcome (Tables 4 and 5). The median age (interquartile range [IQR]) of the children with favorable outcome was 13 years (IQR 8–16 years) and for unfavorable outcome was 5 years (IQR 2.5–13 years). Age (p = 0.02), GCS score ≤ 8 (OR 8.15, p = 0.001), CVT (OR 15.17, p = 0.001), and presence of infarction (OR 7, p = 0.05) were strongly associated with unfavorable outcome. On multivariable logistic regression analysis, only GCS score ≤ 8 (p = 0.01), CVT (p = 0.02), and presence of infarction (p = 0.04) had a significant impact on unfavorable outcome (Table 5).

TABLE 4.

Univariate analysis for unfavorable outcome

VariableOR (95% CI) for Unfavorable Outcomep Value
Age241*0.02
Sex: male vs female1.29 (0.27–9.55)0.80
Duration: <7 vs >7 days1.98 (0.57–7.3)0.28
Location: supratentorial vs infratentorial1.98 (0.28–47.69)0.59
Side: rt vs lt2.09 (0.50–10.85)0.32
Supratentorial: convexity vs interhemispheric1.13 (0.11–11.18)0.98
GCS score: ≤8 vs >88.15 (2.20–32.81)0.001
Source: otogenic vs nonotogenic1.71 (0.31–10.13)0.53
Microbiology: sterile vs organism isolated2.31 (0.60–11.3)0.23
Surgery: burr hole vs craniotomy1.70 (0.45–6.44)0.63
Symptoms: seizure vs no seizure3.36 (0.80–14.12)0.16
Complication: CVT vs no CVT15.17 (3.05–75.3)0.001
Complication: infarct vs no infarct7.0 (0.92–67.92)0.05
Association lesion: abscess vs no abscess2.08 (0.25–12.09)0.34
Recurrence vs no recurrence1.04 (0.10–10.18)0.91
Hydrocephalus vs no hydrocephalus1.87 (0.24–47.02)0.63

Boldface type indicates statistical significance.

U value.

TABLE 5.

Regression analysis of predictive factors for unfavorable outcome

PredictorsExp (B)95% CIp Value
Age0.8230.67–1.010.06
GCS score ≤8 vs >828.592.21–370.080.01
No CVT vs CVT0.060.006–0.690.02
No infarct vs infarct0.030.001–0.910.04
Seizure vs no seizure0.780.08–7.370.83
Sterile vs organism isolated0.470.04–5.260.54

Exp (B) = exponentiation of the B coefficient.

The correct classification rate of the above fitted model is 87.3%. Boldface type indicates statistical significance.

Discussion

The current study is one of the largest series of SDE in children across all age groups and etiologies. The predictors of unfavorable outcome were also studied. The results of our study were compared with other series (Table 6).2,8–10,17,24,25 In our cohort, the mean age was 10.9 years (range 6 months–18 years), which was consistent with the reported literature (Table 6). Male children were more affected than female children in our study, which is also consistent with the published literature.13 In our cohort, 34.7% of cases were due to otogenic origin and 14.3% were due to sequelae of meningitis. All infants (9 cases) had meningitis prior to development of SDE. The source of infection for SDE varies according to patient age.8 In an infant, the common source was secondary infection of a subdural collection following bacterial meningitis.9 The otogenic source was the predominant origin in both the supratentorial and infratentorial compartment, although the paranasal sinus was the second most common source in the supratentorial compartment,13 especially in older children. These findings are also similar to those in previous studies.

TABLE 6.

Literature review of published series of SDE in children

Authors & YearStudy DetailsPredictorsOutcome
Madhugiri et al., 201127 pts, only infratentorial location, mean age 9.8 yrs, sterile culture 25.9%GCS motor score <M6, presence of hydrocephalus on primary scan, burr hole as 1st op = unfavorable outcomeFavorable 92.5%, death 3.7%
Liu et al., 201033 pts, only infants, etiology = post meningitis, Hemophilus influenzae most common (32.3%)Early detection & evacuation of pus = favorable outcomeFavorable 73%, death 3%
Legrand et al., 200933 pts, median age 10.5 yrs, gram-positive cocci most common organismNeurological deficit on admission, cerebral thrombophlebitis, cerebral herniation, age >1 yr = unfavorable outcomeFavorable 82%, death 4%
Banerjee et al., 200965 pts, only supratentorial location, mean age 9.5 yrs, sterile 35.4%Postop CVT = unfavorable outcomeFavorable 87%, death 10.8%
Wu et al., 200831 pts, infants 87.1%, etiology = head trauma or op 19.4%, S. pneumonia most common organismNot reportedGood recovery (w/o neurological sequelae) 38.7%, death 9.7%
Yilmaz et al., 200628 pts, average age 10 mos, etiology = bacterial meningitis, S. aureus most common organismCraniotomy had better outcome compared to burr holeNo deaths
Pattisapu & Parent, 19878 pts, mean age 5.7 yrsNot reportedGood recovery 62%, no deaths
Present study98 pts, mean age 10.9 yrs, most common etiology = otogenic, beta-hemolytic Streptococcus most common organismGCS score <8, presence of CVT & infarct = unfavorable outcomeFavorable 82.9%, death 10.7%

Pts = patients.

The SDE presents with either systemic manifestation such as fever or symptoms related to the source of infection, or neurological symptoms such as seizures, altered sensorium, and focal neurological deficits.4 In developing countries it is not uncommon for children to present in altered sensorium to a neurosurgeon. In older series, 57%–74.1% of children presented in altered sensorium.2,10,25 In our study, the median GCS score at presentation was 13 and 22.4% presented with GCS scores ≤ 8. The lower incidence of altered sensorium in our series was due to ease of access to CT scans in the last decade in our city, leading to early diagnosis.

In the present antibiotic area, the number of sterile culture reports is rising. In the previous series the sterile culture was reported in 14%–35.4%.2,10,25 In our cohort, the incidence of sterile culture was 37.8%. The organisms isolated depend on the source and age of the child. In a series of infants, or predominantly infants, the organisms isolated were Haemophilus influenza, S. aureus, and Streptococcus.9,24,25 In the present series the most common organism isolated was Streptococcus, and the most common source was otogenic.

Surgical Management and Complications

Commonly craniotomy or craniectomy is the procedure of choice for SDE,11 but if the child is severely ill or not fit for craniotomy, then burr-hole evacuation is an option. In our institute as well, craniotomy is the preferred treatment for SDE. In our study, 73.5% of children underwent craniotomy/craniectomy and 26.5% burr-hole evacuation. The recurrence rate was greater in the burr-hole group compared with the craniotomy group.7 Liu et al.9 reported no difference in either group. In our study, we found that the recurrence rate was greater in the craniotomy group (11 cases) than in the burr-hole group (2 cases). The reasons for greater recurrence in the craniotomy/craniectomy group in our cohort were sterile culture resulting in administration of nonspecific antibiotics, a larger number of interhemispheric collections, delay in treatment of the primary source (otogenic source), and thicker collection of pus. In contrast, children who underwent burr-hole evacuation were more often infants, had less-thick collections, and the etiology was more often postmeningitis. The morbidities of SDE are hemiparesis (15%–35%) and persistent seizures (12%–37.5%), and the reported mortality rate is 3%–10.8% (Table 6).

The complications encountered in our series were CVT (10.2%), venous sinus injury (2.0%), arterial infarction (6.1%), and bone flap osteomyelitis (4.1%). The mortality rate in our cohort was 10.7%. The higher mortality rate in our series was due to a significant proportion of children presenting in a coma.

Predictors of Outcome

We studied a number of predictors of outcome using regression analyses. The predictors of outcome have not been widely reported. We found that younger age, presentation in coma (GCS score ≤ 8), and complications (CVT and infarction) were significantly associated with unfavorable outcome (death, severe disability, vegetative state) at follow-up. The correct classification rate of the fitted model was 87.3%. The commonly perceived predictors of poor outcome such as infratentorial location, duration of symptoms, presence of abscess, associated hydrocephalus, type of surgery, organisms isolated, and recurrence were not found to be significant in our study.

Other studies have reported a few predictors of outcome. Legrand et al. found that age > 1 year was associated with poor outcome.8 The infants had SDE as a sequelae of meningitis, which responds well to antibiotics. They also found that neurological deficit at the time of admission was one of the significant predictors of outcome.8 In a literature review,13 the occurrence of aerobic streptococci was found to be a good prognostication factor and the presence of sterile culture was the poor factor for outcome. However, in our study, outcome was not related to the isolated organisms in the culture. A few studies14,20 have shown inferior outcome in infratentorial SDE as compared to supratentorial SDE due to rapid progression of disease. However, outcome was not related to location of SDE in our series. Complications of SDE such as CVT and hydrocephalus may influence outcome. Legrand et al. reported CVT to be a strong independent predictor of inferior outcome.8 Similarly, in our cohort, occurrence of CVT was associated with unfavorable outcome. In addition, CVT arterial infarction was strongly correlated with unfavorable outcome in our series. The presence of hydrocephalus is a poor prognostication factor according to the literature,10 but in our study it did not influence the outcome.

Study Limitations

Although the present series reports one of the highest numbers of pediatric cases of SDE, it is not devoid of the pitfalls of a retrospective study. We have not included the immune status of the children, the general health of children, management of complications, and socioeconomic status of the family in our analysis. We have combined all the cases across various age groups and etiologies. The number of infants was low in our series, thus we could not perform a subgroup analysis.

Conclusions

Younger age, poor GCS score at presentation, occurrence of CVT, and arterial infarction were poor prognostic factors for outcome of spontaneous SDE. Early surgical intervention and evacuation of pus with proper antibiotic coverage should be the goal of management.

Disclosures

The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

Author Contributions

Conception and design: Konar, Sadashiva. Acquisition of data: Konar, Gohil. Analysis and interpretation of data: Shukla, Konar. Drafting the article: Konar. Critically revising the article: Shukla, Konar. Reviewed submitted version of manuscript: Shukla, Konar. Approved the final version of the manuscript on behalf of all authors: Shukla. Statistical analysis: Shukla, Konar. Administrative/technical/material support: Sadashiva, Uppar, Bhat, Srinivas, Arimappamagan, Devi. Study supervision: Devi.

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Article Information

Correspondence Dhaval Shukla: NIMHANS, Bangalore, India. neurodhaval@rediffmail.com.

INCLUDE WHEN CITING DOI: 10.3171/2019.5.FOCUS19268.

Disclosures The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

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Figures

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    A: Axial T1-weighted MR image with contrast enhancement showing a left-sided, frontoparietal, subdural, hypointense collection with peripheral enhancement, suggestive of pus collection. B: Coronal T1-weighted MR image with contrast enhancement showing an interhemispheric pus collection in continuation with the convexity. C: Axial CT image with contrast enhancement showing good evacuation of the pus collection and evidence of craniotomy.

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    A: Axial CT image with contrast showing a left-sided, frontal, hypodense collection. B: Intraoperative photograph showing the yellowish pus collection underneath the dura. C: Axial CT image with contrast showing good evacuation of pus.

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