Abstract

Little is known regarding typical neuropsychological outcomes of intracranial empyema, a rare complication of sinusitis marked by accumulation of purulent material adjacent to the brain. A 15-year-old, right-handed male presented with a 3-day history of congestion, lethargy, fever, headache, dizziness, unequal pupil dilation, and right-sided facial droop. Computed tomography revealed right-sided subdural empyema causing subfalcine, central, foraminal uncal, and tonsillar herniation. Postoperative inpatient neuropsychological consultation was requested 17 days postsurgery due to language deficits. Through comparison of neuropsychological and radiological findings, this case of subdural empyema demonstrates the anatomical and functional impact of mass effect on the brainstem and the vasculature of the contralateral hemisphere. Deficits were observed in expressive language, processing speed, and fine motor functioning, all of which lingered 6 months postacute. This case study reviews the pathophysiology of subdural empyema and illustrates its potential neuropsychological impact to inform clinicians encountering this rare condition.

Subdural empyema, an accumulation of purulent material between the dura and arachoid mater, can be a rare complication of sinusitis, mastoiditis, meningitis, dental abscess, influenza, or a number of other infections (Kombogiorgas, Seth, Athwal, Modha, & Singh, 2007; Wu, Chiu, & Huang, 2008). As a complication of sinusitis, pus may erode the bony walls of the sinuses directly invading the leptomeninges, or bacteria may infect the bridging veins that run through the bony calvarium and leptomeninges, carrying bacteria along the veins into the leptomeninges. Empyemas form in sequestered potential spaces and may rapidly grow to a large size with significant mass effect on surrounding structures, as large collections of purulent material trigger a cascade of severe inflammatory reaction within the surrounding tissues. The subdural space may be opened up diffusely around a cerebral hemisphere, creating a large cavity for pus to accumulate around the brain, particularly over the cerebral convexities (Bowen & Donovan-Post, 1991). As pus accumulates in the subdural space around the brain, a space-occupying mass is formed and there is a significant, rapid increase in intracranial pressure and mechanical mass effect on the adjacent cerebral hemisphere. The result is midline or downward herniation of the brain.

However, empyema is also a collection of bacterial purulent material that inflames the adjacent brain tissue (cerebritis) and thromboses the cortical veins that traverse the leptomeninges. Cerebritis may create significant edema and swelling in the brain. Cortical vein thrombosis results in stasis of arterial cerebral blood flow due to the back pressure from the thrombosed vein with hypoperfusion and ischemia/infarction in the drainage territory of the vein. If a large dural venous sinsus thromboses, the resulting venous hypertension impairs cerebrospinal fluid (CSF) reabsorption and results in hydrocephalus. The severe inflammatory response in the leptomeninges may also cause a vasopspasm of the arteries in the subarachnoid space resulting in direct arterial ischemia of the brain. The synergistic cascade of rapidly accumulating pus surrounding the brain with raised intracranial pressure and mass effect, severe inflammatory edema, hydrocephalus, and infarction results in death if the patient is not diagnosed and treated emergently. Indeed, the seminal characterization of the pathophysiology and clinical course of subdural empyema by Courville (1944) benefitted from autopsies of all 42 cases studied—a 100% mortality rate due to limited knowledge of the condition and lack of viable treatments at the time.

The prevalence of subdural empyema is difficult to determine, with the most recent formal study suggesting an incidence rate of one case per 193,000 people per year (Nathoo, Nadvi, van Dellen, & Gouws, 1999). However, as that study was conducted in a region of South Africa with a very low socioeconomic index, the incidence rate of subdural empyema in a more developed area of the world, such as the United States, is likely even lower (Bartt, 2010). It is estimated that 3% of all patients hospitalized for sinusitis develop subdural empyema (Hicks, Weber, Reid, & Moodley, 2011). Approximately 70% of cases occur in individuals aged 10–30 (Bayonne, Kania, Tran, Huy, & Herman, 2009; Germiller, Monin, Sparano, & Tom, 2006). Numerous studies suggest that subdural empyema is more commonly seen in males (Banerjee, Pandey, Devi, Sampath, & Chandramouli, 2009; Bayonne et al., 2009; Giannoni, Sulek, & Friedman, 1998; Ong & Tan, 2002; Quraishi & Zevallos, 2006; Rosenfeld & Rowley, 1994; Saxton, Boldt, & Shield, 1995; Wu et al., 2008).

The onset of symptoms in cases of subdural empyema is often abrupt (Bleck & Greenlee, 2000), and most patients present at about 7–12 days (Adame et al., 2005; Germiller et al., 2006; Nathoo et al., 1999). Any earlier detection is extremely difficult due to the nonspecific nature of initial symptoms, which typically include fever, focal cranial pain, and headache (Adame, Hedlund, & Byington, 2005; Bartt, 2010; Bayonne et al., 2009; Giannoni et al., 1998; Rosenfeld & Rowley, 1994; Saxton et al., 1995; Wu et al., 2008). Lethargy and altered mental status are commonly observed upon initial presentation for medical evaluation (Adame et al., 2005; Hartman, Helfgott, & Weingarten, 2004; Kombogiorgas et al., 2007; Osman Farah, Kandasamy, May, Buxton, & Mallucci, 2009; Vehnkatesh et al., 2006; Wackym, Canalis, & Feuerman, 1990). Over 70% of cases present with hemiparesis due to mass effect and up to 48% experience seizures prior to undergoing treatment (Hartman et al., 2004). In severe or prolonged cases, brain abscesses may develop (Adame et al., 2005; Giannoni et al., 1998; Rosenfeld & Rowley, 1994), and as the brain herniates, seizures, stupor, hemiparesis, and cranial nerve palsies progress. If untreated, patients will progress to coma and eventual death (Kombogiorgas et al., 2007; Osman et al., 2009). Even with appropriate treatment, mortality rates are reported from 14% to 28% (Agrawal, Timothy, Pandit, Shetty, & Shetty, 2007).

Contrast-enhanced computed tomography (CT) imaging is commonly used and “very reliable” (Bartt, 2010) in diagnosing subdural empyema (Hicks et al., 2011). However, as CT sometimes fails to detect early-stage subdural empyema (Rich, Deasy, & Jarosz, 2000; van de Beek, Campeau, & Wijdicks, 2007), some healthcare professionals prefer the greater sensitivity of magnetic resonance imaging (MRI). MRI is also more sensitive in detecting the complications of subdural empyema, including cerebritis, abscess, and infarction. After diagnosis, standard of care is immediate craniotomy or burr hole surgery to remove purulent material. Although burr hole drainage is more common, craniotomy may be more effective (Banerjee et al., 2009; Klein et al., 2006; Legrand et al., 2009; Mat Nayan, Mohd Haspani, Abd Latiff, Abdullah, & Abdullah, 2009; Nathoo, Nadvi, Gouws, & van Dellen, 2001). There is much debate over which technique is optimal, and the severity of the empyema is often the determining factor. Following surgery, patients are treated with an antibiotic regimen determined by the pathogens identified as the causal source of the empyema (Bartt, 2010; Greenlee, 2003). Due to the rarity of subdural empyema, the duration of antibiotic therapy is not well established, although 4–6 weeks has been suggested (Bartt, 2010). In addition to antibiotics, corticosteroids are occasionally used due to their established role in the treatment of meningitis, although the rationale and success of using corticosteroids to treat subdural empyema has not been well documented (de Gans, van de Beek, & European Dexamethasone in Adulthood Bacterial Meningitis Study Investigators, 2002).

Prior to the development of CT, overall mortality rates for subdural empyema were consistently 25%–40%, whereas current mortality rates typically are in the range of 8%–22% (Hartman et al., 2004). Mortality rates are as high as 57%–80% for patients who are comatose on initial presentation, in contrast to 0%–7% mortality for patients who present while still conscious (Dill, Cobbs, & McDonald, 1995; Singh, van Dellen, Ramjettan, & Maharaj, 1995). Any lasting neurological disability as a result of subdural empyema is rare (Bartt, 2010). However, survivors commonly experience lingering hemiparesis, and epilepsy develops in 17%–42% of survivors (Hartman et al., 2004; Nathoo et al., 1999). Thus, anti-seizure medications and occupational, physical, or speech therapy may be prescribed for survivors.

Due to the rarity of this condition, there is no known neuropsychological profile of patients in either acute or recovery stages of subdural empyema. This case study is presented in order to advance knowledge of the potential neuropsychological impact of subdural empyema and to provide direction for acute and postacute neuropsychological evaluations of this rare condition. Existing literature is limited to a single prior case study, published over two decades ago in this journal (Maertens, Cohen, & Krawiecki, 1987). Briefly, the patient in that prior study was a 13-year-old, right-handed, African-American male with pre-existing learning difficulties who presented with a 1-week history of upper respiratory infection and a 1-day history of headaches, sleepiness, poor appetite, emesis, and nuchal rigidity. Five days after an initial misdiagnosis of cerebritis and the subsequent development of simple partial seizures, elevated fever, right-sided hemiparesis, and altered mental status, further review of the previous CT scans led to the identification of a left parafalcine subdural empyema. After 4 days of treatment with intravenous penicillin, a follow-up CT showed a reduction in the left parafalcine empyema and a novel left temporal–frontal subdural empyema. By Day 40, the only anomaly visualized on CT was residual left parietal diffusion.

In this prior case study, neuropsychological evaluation was conducted at Day 17 of hospitalization and at 6-month follow-up. Findings were compared with an evaluation conducted by a school psychologist 3 years prior to the patient's hospitalization which indicated pre-existing learning difficulties. Those comparisons indicated acute declines in several areas. Although receptive language was far below average at both time points, expressive language functioning declined from below average to far below average. Similar declines were noted in fine motor functioning, auditory memory, and visual memory. At 6 months postillness, verbal functioning had improved to near premorbid levels, but academic performance measures indicated enduring declines in spelling and arithmetic skills.

The authors of this prior case study noted that the results of their evaluation at Day 17 correlated “extremely well” with the discovery of a left temporal subdural empyema on CT imaging (Maertens et al., 1987). Similarly, they asserted that their neuropsychological findings at 6 months postacute correlated with the complete resolution of the subdural empyema as seen on CT imaging at that time. Residual cortical atrophy in the left frontal lobe was not described as having direct neuropsychological correlates per the testing battery that was administered. In conclusion, the authors mentioned that clinical improvement generally preceded radiological improvement for that patient.

An understanding of the pathophysiology of this rare condition, as reviewed above, informs evaluation of its neuropsychological outcomes. The single prior case study provides some context for understanding the current case, although comparison is clouded by the significant pre-existing cognitive difficulties noted in the prior case. While acute evaluation of the present case was dictated by clinical need, timing of the postacute evaluation was designed to match the prior study, which provided limited information regarding postacute functioning due to that patient's premorbid limitations. In addition to addressing clinical needs dictating the referral for evaluation, a goal of the present study was to clarify whether the acute and postacute deficits observed in the prior case would be observed in a case study of a patient with higher premorbid functioning. Examination of a patient with presumably normal baseline neuropsychological functioning likely affords greater clarity to understanding long-term outcomes. In particular, the current study may more accurately capture patterns of recovery in aspects of fine motor functioning, language functions, and memory, which were selected as areas of particular interest based on clinical concern combined with findings from the prior case study. Additionally, the patients in the current and prior case studies probably experienced differences in the pathophysiological course of subdural empyema, as the cases differed in terms of affected hemisphere. The comparison of patients with different clinical courses enables clinicians to better understand whether neuropsychological recovery is generalizable across subdural empyema or unique based on the neuroanatomical structures most impacted by the disease process.

The following case study illustrates potential neurocognitive changes associated with the mass effect and inflammatory process associated with empyema. The case example advances the limited existing knowledge of both acute and postacute neuropsychological sequelae of subdural empyema, thereby providing direction for both clinical evaluations and future research.

Case Report

The patient is a 15-year-old, right-handed male with an unremarkable developmental, medical, and psychiatric history. He had been earning A's and B's in regular classes and had never been referred for cognitive or academic testing or required educational supports. He presented to the Emergency Department (ED) with sinusitis, worsening headache, low-grade fever, dizziness, neck pain, right-sided facial droop, and unequal pupil dilation. His mother noted that the patient had been sick for ∼4 days prior to his hospitalization. He reportedly began experiencing headache 4 days prior to his admission, followed by increasing motor slowing, fatigue, and one episode of emesis. The day he presented to the ED, the patient reportedly had become unable to dress himself or walk without assistance. An intravenous contrast-enhanced CT scan at his admission detected a right-sided pneumonoccal subdural empyema, originating from the right frontal sinus (see Fig. 1), with associated midline shift toward the left and partial occlusion of the distal Sylvian branches of the left middle cerebral artery (MCA) (see Fig. 2). Extensive subfalcine, central, foraminal uncal, and tonsillar herniation were observed (see Fig. 3), indicating an immediate life-threatening neurosurgical emergency. The patient immediately underwent a frontal craniotomy, evacuation of the empyema, and cranialization of the right frontal sinus. There were no complications of encephalitis or meningitis, according to analysis of the CSF. A peripherally inserted central catheter (PICC) line was inserted that same day for administration of ampicillin and was removed on Day 45 upon completion of that antibiotic course.

Fig. 1.

Subdural empyema originating from the right frontal sinus.

Fig. 1.

Subdural empyema originating from the right frontal sinus.

Fig. 2.

Axial contrast-enhanced CT scan of the head at the level of the brainstem and basal cisterns demonstrating severe central herniation of the temporal lobe uncus (thin arrow) and mass effect on the midbrain (wide arrow) with a decreased flow in posterior cerebral arteries. The extensive herniation also resulted in a decreased flow in the left middle cerebral artery (curved arrow).

Fig. 2.

Axial contrast-enhanced CT scan of the head at the level of the brainstem and basal cisterns demonstrating severe central herniation of the temporal lobe uncus (thin arrow) and mass effect on the midbrain (wide arrow) with a decreased flow in posterior cerebral arteries. The extensive herniation also resulted in a decreased flow in the left middle cerebral artery (curved arrow).

Fig. 3.

Right-sided subdural empyema causing extensive, life-threatening herniation.

Fig. 3.

Right-sided subdural empyema causing extensive, life-threatening herniation.

Postsurgery, the patient exhibited left-sided hemiparesis. This symptom, combined with the right-sided facial droop and unequal pupil dilation, formed the classic triad of symptoms suggesting mass effect at the upper level of the brainstem. Specifically, this triad implicated that the bilateral foraminal uncal herniation observed on contrast-enhanced CT may have been worse on the right, causing unequal pupil dilation due to compression of Cranial Nerve (CN) III, which controls ipsilateral pupil dilation, and right-sided facial droop due to compression of CN VII, which innervates ipsilateral facial muscles. Given that CN III and CN VII are located above the pyramidal decussation, the finding of left-sided hemiparesis is not the contradiction it first appeared, as the mass effect likely impacted those pyramidal motor fibers at a point where they still evidence a contralateral connection.

An informal speech-language evaluation on Day 6 noted mild deficits in expressive and receptive language, in addition to moderate cognitive deficits. The patient's external ventricular drain was removed on Day 8. While hospitalized, the patient participated in occupational, physical, and speech therapies and was followed by Child Life and Psychological Services. He also participated in a sleep evaluation on Day 27 that indicated no concerns. He was discharged on Day 37 with no observable symptoms other than residual left-sided weakness.

With regard to other medical history, the patient is characterized as obese but had no history of other medical conditions or hospitalizations prior to this subdural empyema. He experienced sleep difficulties while hospitalized for treatment of the empyema, but he reportedly was sleeping well at the time of the postacute evaluation, which was conducted on an outpatient basis almost exactly 6 months subsequent to the inpatient assessment. His mother indicated that the patient had had an ophthalmological examination in the month following his discharge from the hospital, the results of which were normal per parental report. The patient reportedly was not prescribed any medications at the time of the follow-up evaluation.

Method

On Day 15, the patient was referred for inpatient neuropsychological consultation due to concerns regarding expressive and receptive language, confusion, and depressive symptoms. At that time, separate clinical interviews with the patient and his mother were conducted, and a brief neuropsychological battery was administered. In order to coincide with the timeline of the prior case study, the patient completed a comprehensive outpatient neuropsychological evaluation ∼6 months after that initial neuropsychological evaluation. Table 1 shows a complete listing of measures and results from each evaluation. Test selection was informed first and foremost by practical treatment planning and return-to-school needs but also by the prior existing case study. Measurement in domains similar to the prior case study permitted the examiners to compare recovery and facilitate cautious conclusions regarding typical acute and post-acute effects of subdural empyema.

Table 1.

Neuropsychological test results

Measure Acute Postacute RCI 
Cognitive ability: Overall 
 WASI FSIQ-2 81 — — 
 WISC-IV FSIQ — 85 — 
 WISC-IV GAI — 92 — 
Cognitive ability: Verbal 
 WASI Vocabulary 61 — — 
 WISC-IV VCI — 87 — 
Cognitive ability: Nonverbal 
 WASI Matrix Reasoning 101 — — 
 WISC-IV PRI — 98 — 
Working memory 
 WISC-IV WMI — 97 — 
Receptive Language 
 PPVT-4 Form A — 98 — 
 PPVT-4 Form B 98 — — 
 NEPSY Comprehension of Instructions 85 100 1.20 
Expressive Language 
 WRAT-4 Word Reading 113 — — 
 WJ-III: Picture Vocabulary — 99 — 
 NEPSY Word Generation: Semantic 55 75 0.96 
 NEPSY Word Generation: Initial Letter 65 60 −0.37 
Processing speed 
 SDMT 65 86 2.02a 
 WISC-IV PSI — 70 — 
Verbal memory 
 CMS Word Pairs: Learning 70 90 3.14a 
 CMS Word Pairs: Total Score 70 95 3.54a 
 CMS Word Pairs: Long Delay 90 115 4.42a 
 CMS Word Pairs: Delayed Recognition 100 105 0.47 
 CMS Stories: Immediate — 75 — 
 CMS Stories: Delayed — 80 — 
 CMS Stories: Delayed Recognition — 70 — 
Visual memory 
 CMS Dot Locations: Learning 90 120 1.66a 
 CMS Dot Locations: Total Score 95 115 2.02a 
 CMS Dot Locations: Long Delay 110 110 
 ROCFT Delay — 73 — 
Attention 
 TMT Part A 65 61 −0.41 
 CPT-II — Averageb — 
Executive Functioning 
 TMT Part B <20 92 15.92a 
 DKEFS Tower: Total achievement — 100 — 
 DKEFS Tower: Time-Per-Move — 85 — 
 DKEFS Tower: Move accuracy — 105 — 
 DKEFS Tower: Rule violations — 100 — 
 BRIEF (T-scores)    
  Inhibit — 69 — 
  Shift — 54 — 
  Emotional Control — 58 — 
  Behavioral Regulation Index — 62 — 
  Initiate — 69 — 
  Working Memory — 63 — 
  Plan/Organize — 63 — 
  Organization of Materials — 69 — 
  Monitor — 68 — 
  Metacognition Index — 68 — 
  Global Executive Composite — 68 — 
Visual Perception 
 HVOT Low average Low average — 
 VMI-5 Visual Perception — 106 — 
 ROCFT Copy — 87 — 
Fine Motor coordination/speed 
 Purdue Pegboard: Right hand 39 75 2.14a 
 Purdue Pegboard: Left hand 60 57 −0.18 
 Purdue Pegboard: Both hands — 85 — 
Measure Acute Postacute RCI 
Cognitive ability: Overall 
 WASI FSIQ-2 81 — — 
 WISC-IV FSIQ — 85 — 
 WISC-IV GAI — 92 — 
Cognitive ability: Verbal 
 WASI Vocabulary 61 — — 
 WISC-IV VCI — 87 — 
Cognitive ability: Nonverbal 
 WASI Matrix Reasoning 101 — — 
 WISC-IV PRI — 98 — 
Working memory 
 WISC-IV WMI — 97 — 
Receptive Language 
 PPVT-4 Form A — 98 — 
 PPVT-4 Form B 98 — — 
 NEPSY Comprehension of Instructions 85 100 1.20 
Expressive Language 
 WRAT-4 Word Reading 113 — — 
 WJ-III: Picture Vocabulary — 99 — 
 NEPSY Word Generation: Semantic 55 75 0.96 
 NEPSY Word Generation: Initial Letter 65 60 −0.37 
Processing speed 
 SDMT 65 86 2.02a 
 WISC-IV PSI — 70 — 
Verbal memory 
 CMS Word Pairs: Learning 70 90 3.14a 
 CMS Word Pairs: Total Score 70 95 3.54a 
 CMS Word Pairs: Long Delay 90 115 4.42a 
 CMS Word Pairs: Delayed Recognition 100 105 0.47 
 CMS Stories: Immediate — 75 — 
 CMS Stories: Delayed — 80 — 
 CMS Stories: Delayed Recognition — 70 — 
Visual memory 
 CMS Dot Locations: Learning 90 120 1.66a 
 CMS Dot Locations: Total Score 95 115 2.02a 
 CMS Dot Locations: Long Delay 110 110 
 ROCFT Delay — 73 — 
Attention 
 TMT Part A 65 61 −0.41 
 CPT-II — Averageb — 
Executive Functioning 
 TMT Part B <20 92 15.92a 
 DKEFS Tower: Total achievement — 100 — 
 DKEFS Tower: Time-Per-Move — 85 — 
 DKEFS Tower: Move accuracy — 105 — 
 DKEFS Tower: Rule violations — 100 — 
 BRIEF (T-scores)    
  Inhibit — 69 — 
  Shift — 54 — 
  Emotional Control — 58 — 
  Behavioral Regulation Index — 62 — 
  Initiate — 69 — 
  Working Memory — 63 — 
  Plan/Organize — 63 — 
  Organization of Materials — 69 — 
  Monitor — 68 — 
  Metacognition Index — 68 — 
  Global Executive Composite — 68 — 
Visual Perception 
 HVOT Low average Low average — 
 VMI-5 Visual Perception — 106 — 
 ROCFT Copy — 87 — 
Fine Motor coordination/speed 
 Purdue Pegboard: Right hand 39 75 2.14a 
 Purdue Pegboard: Left hand 60 57 −0.18 
 Purdue Pegboard: Both hands — 85 — 

Note: All scores are presented as standard scores. A dash indicates that a measure was not administered or that an RCI value was not calculated. FSIQ = Full Scale IQ. VCI = Verbal Comprehension Index. PRI = Perceptual Reasoning Index. WMI = Working Memory Index. PSI = Processing Speed Index.

NEPSY (Korkman et al., 2007). WRAT-4 equals; Wide Range Achievement Test, Fourth Edition (Wilkinson & Robertson, 2006). WJ-III equals; Woodcock-Johnson III Tests of Achievement, Third Edition (Woodcock et al., 2001). CMS equals; Children's Memory Scale (Cohen, 1997). CPT-II equals; Conners' Continuous Performance Test, Second Edition (Conners, 1992). TMT equals; Trail-Making Test (Army Individual Test Battery, 1944). DKEFS equals; Delis-Kaplan Executive Function System (Delis et al., 2001). BRIEF equals; Behavior Rating Inventory of Executive Function (Gioia et al., 2000). VMI-5 equals; Beery–Buktenica Developmental Test of Visual Motor Integration, Fifth Edition (Beery & Beery, 2006). HVOT equals; Hooper Visual Orientation Test (Hooper, 1958). ROCFT equals; Rey-Osterrieth Complex Figure Test (Rey, 1941).

aSignificant according to standard RCI cutoff of ±1.645 (Duff, 2012).

bOn the CPT-II, all scores were within the average range, with the exception of the Variability index, which indicated “Good Performance.”

The patient underwent emergent unenhanced CT scanning of the head upon arrival to the ED, utilizing 3 mm unenhanced axial images through the head (Philips Healthcare Andover, MA). Due to concerns about sinusitis and a suspected extra-axial fluid collection around the right cerebral hemisphere, the unenhanced CT was followed immediately by a repeat intravenous contrast enhanced (Isovue 300, Bracco Milan, Italy) 3 mm axial CT scan of the head. The patient was prohibited from having an MRI scan due to his weight, which exceeded the safe table limit of the MRI scanner. Postoperative imaging was performed with 3 mm unenhanced axial CT scanning.

Results

Due to concerns regarding expressive and receptive language, confusion, and depressive symptoms, the patient was referred for an inpatient neuropsychological evaluation, which was conducted on Day 15. At that time, the patient was observed to demonstrate good effort despite significant lethargy. Attention and concentration were adequate given his lethargic state. He was reluctant to guess and demonstrated a slow response style, particularly as tasks increased in difficulty and on items that required a verbal response. The patient endorsed difficulties with processing speed and word finding, and his mother reported that he was much less talkative than usual. The patient typically shrugged in response to conversational prompts. He also demonstrated significant left-sided weakness and was observed to use objects in the room (e.g., his bed, the wall) to balance himself as he ambulated to the restroom.

The patient's acute neuropsychological profile indicated deficits in three main areas: expressive language, processing speed, and fine motor functioning (see Table 1). Deficits in expressive language were most clearly evidenced by the discrepancy between far below average performance on the Vocabulary subtest of the Wechsler Abbreviated Scale of Intelligence (WASI; Wechsler, 1999) and average performance on the Peabody Picture Vocabulary Test, Fourth Edition, Form B (PPVT-4; Dunn & Dunn, 2007). Expressive language deficits also appeared to impact performance on measures of verbal fluency and verbal memory. Processing speed deficits were evident on the Symbol-Digit Modalities Test (SDMT; Smith, 1982), while performance on the Purdue Pegboard Test (Lafayette Instruments, 1999) was impaired bilaterally.

At the 6-month postacute evaluation, the patient was observed to be appropriately alert, demonstrating good attention and effort. He was much less reluctant to verbally guess on items when compared with the inpatient evaluation. Also in sharp contrast to the acute evaluation, the patient demonstrated a preference for verbal responses. For example, he preferred to verbalize the number of his selected response rather than point to the answer on tasks with multiple choice responses such as the PPVT-4. Additionally, he was increasingly responsive to conversational prompts from the examiner. The patient still demonstrated a slow response style, although the speed of response was improved.

The patient's postacute neuropsychological profile indicated lingering deficits in expressive language—relative to presumably normal functioning prior to illness, as suggested by normal academic performance—despite modest improvements from the initial evaluation. Lingering processing speed deficits were also observed, most clearly on the motor-free SDMT but also on the Processing Speed Index (PSI) of the Wechsler Intelligence Scale for Children, Fourth Edition (WISC-IV; Wechsler, 2003). Fine motor dexterity weakness was also noted, although it is difficult to tease out the impact of processing speed weakness on fine motor performance. In addition to these persisting deficits, it is also important to note significant recovery of function observed in performance on tasks of learning of visual and verbal information, cognitive flexibility, and non-motor cognitive speed. These positive changes were confirmed with reliable change index (RCI) analysis using the Jacobson & Truax (1991) model (Table 1). RCI values were calculated utilizing values from relevant test manuals as well as normative data contained in Strauss, Sherman, and Spreen (2006).

Discussion

Informed by existing knowledge of the underlying pathophysiology in concert with imaging findings, the present case illustrates the potential neuropsychological impact of subdural empyema by identifying several areas of pathology that can occur acutely and which may have long-term neuropsychological sequelae. Based on clinical estimators and parental reports of the patient's premorbid functioning as well within normal limits, the patient's neuropsychological profile at the time of the acute evaluation suggested significant compromise, with a triad of deficits in expressive language, processing speed, and fine motor functioning. That profile likely reflects the impact of diffuse brain injury resulting from mass effect due to frontal subdural empyema, although a lack of premorbid testing data precludes a definitive conclusion. Additionally, given the extent of mass effect and herniation this patient experienced, it is difficult to make conclusive statements regarding the connection between neuroanatomical and neuropsychological findings. However, the presence of extensive subfalcine, central, foraminal uncal, and tonsillar herniation (see Fig. 3) likely contributed to the finding of processing speed deficits, as such herniation would have caused diffuse white matter damage. In contrast to this diffuse injury, the observed expressive language deficits may have been more focal in nature, likely related to the partial occlusion of the left MCA observed on contrast-enhanced CT (see Fig. 2). The neuroanatomical basis for the observed impairment in fine motor functioning remains open for speculation, with the two most likely explanations being ischemic cortical damage or the severity of brainstem compression potentially impacting motor functioning. Deficits in fine motor functioning, processing speed, and expressive language lingered at 6 months, but no imaging was available at that time to further inform understanding of neuroanatomical bases.

These findings must be considered in light of several limitations of the study that were beyond the control of the examiners, such as the idiosyncratic nature of data from a single individual limiting the ability to generalize findings—as with any case study. Situational factors inherent to any inpatient evaluation, such as patient fatigue and environmental distractions (e.g., noises from medical equipment), represent potential threats to the reliability and validity of the findings of the acute evaluation in this case. Additionally, there are inherent threats to the reliability and validity of any comparisons made between scores obtained in two drastically different testing settings, as was the case for the acute inpatient and postacute outpatient evaluations of this patient. Although instrumentation was kept as consistent as possible at each time point, the use of different assessments at acute and postacute evaluation may limit the comparability of scores. When data were available, RCI scores were calculated in an attempt to address this limitation, recognizing that protocols for calculating RCI scores for an individual are still being refined (Duff, 2012). In addition to these challenges, the lack of premorbid neuropsychological data limits the ability to track recovery relative to the patient's neurocognitive baseline. The lack of traditional and more focused (e.g., diffusion-weighted, angiographic) MRI data represents another limitation of this study. Specifically, these neuroimaging techniques likely would have clarified vascular findings demonstrating cerebral edema, ischemia, vascular spasm/occlusion, and white matter injury. Additionally, in older, cooperative patients such as the case described here, even basic functional MRI tasks could be performed to correlate neuropsychological deficits with brain injury. Unfortunately, the patient in this case was unable to participate in any MRI procedures due to obesity.

The informational limits of neuroimaging were quite evident in this case, as indications of widespread mass effect and herniation did little to narrow hypotheses for developing the brief testing battery for the acute evaluation. In this case, testing clarified the imaging findings, indicating that the most prominent mechanism of injury was mass effect related to the presence of purulent material in the subdural space and resulting intracranial inflammatory response. A primary mechanism by which such mass effect likely impacted neuropsychological performance in the present case is restriction of contralateral vasculature. However, depending on the temporal duration (and subsequent severity) of the condition prior to identification and treatment, individuals with subdural empyema may present with a wide variety of neuroanatomical abnormalities and functional deficits. At the more severe end of the spectrum, as evidenced in this case, subdural empyema can cause extensive damage—from the frontal lobes to the brainstem—affecting bilateral cerebral hemispheres at both cortical and subcortical levels due to mass effect, and quickly leading to life-threatening herniation. Subdural empyema is typically an aggressive infection that will rapidly progress to this point if untreated. Thus, a detailed history of the course of the preceding illness and symptoms of mass effect will greatly inform any neuropsychological assessment of subdural empyema, particularly with regard to expectations for recovery and longer-term outcome.

In spite of the potential limitations of this study, the findings provide some potentially useful information about neuropsychological recovery from subdural empyema. As the postacute outpatient evaluation was clearly much more conducive to optimal performance, the findings of enduring deficits in the triad of expressive language, processing speed, and fine motor functioning lent credence to their existence at the acute evaluation. In particular, lingering deficits on a motor-free measure of processing speed at the postacute evaluation suggested that acute processing speed deficits were not simply the result of the patient's lethargic state and fine motor slowing at that time.

Given that this is only the second neuropsychological study of subdural empyema ever published, additional research is greatly needed, moving beyond case studies to analyses of neuropsychological findings in larger samples of both adult and pediatric populations. Future studies should attempt to determine whether this condition tends to produce generalized versus localized effects, with consideration given to the lateralization and severity of the subdural empyema. Comparison of the present case study with the prior study (Maertens et al., 1987) suggests that the triad of language, fine motor functioning, and processing speed deficits may be deserving of particular attention in any neuropsychological evaluation of subdural empyema, although two cases do not provide enough evidence to lend any degree of certainty to this suggestion. Premorbid differences between the two cases, with the prior case study demonstrating notable cognitive impairments at baseline testing in contrast to the reported normal premorbid functioning of the present patient, preclude definitive conclusions based on these two cases alone. The fact that both this patient's and the prior patient's deficits persisted 6 months postacutely may indicate some degree of permanent compromise, although longitudinal neuropsychological follow-up would be needed to confirm this. The possibility of permanent compromise raises an important question: what is the typical neuropsychological outcome—not only acute but also long-term—of subdural empyema? Despite the inherent difficulties in comparing the prior and the present case study, the combined knowledge from these two studies clearly demonstrates the potential for subdural empyema to negatively impact neuropsychological functioning via diffuse and focal mechanisms, and a more thorough understanding of that impact is long overdue.

Funding

The authors gratefully acknowledge the generous support of Dr. and Mrs. Lewis Hollweg for the addition of color illustrations to enhance the educational value of this manuscript.

Conflict of Interest

None declared.

Acknowledgements

The authors gratefully acknowledge Pam Curry for her time, effort, and expertise in creating the illustrations. The authors also thank Glenn Katz and John Stavinoha, M.A., for their assistance in postprocessing the CT image.

References

Adame
N.
Hedlund
G.
Byington
C. L.
Sinogenic intracranial empyema in children
Pediatrics
 , 
2005
, vol. 
116
 
3
(pg. 
e461
-
e467
)
Agrawal
A.
Timothy
J.
Pandit
L.
Shetty
L.
Shetty
J. P.
A review of subdural empyema and its management
Infectious Diseases in Clinical Practice
 , 
2007
, vol. 
15
 
3
(pg. 
149
-
153
)
Army Individual Test Battery
Manual of directions and scoring
 , 
1944
Washington, DC
War Department, Adjutant General's Office
Banerjee
A. D.
Pandey
P.
Devi
B. I.
Sampath
S.
Chandramouli
B. A.
Pediatric supratentorial subdural empyemas: A retrospective analysis of 65 cases
Pediatric Neurosurgery
 , 
2009
, vol. 
45
 
1
(pg. 
11
-
18
)
Bartt
R. E.
Cranial epidural abscess and subdural empyema. In M. J. Aminoff, F. Boller, & D. F. Swaab (Series Eds.)
Handbook of Clinical Neurology: Vol. 96. Bacterial infections of the central nervous system
 , 
2010
 
(pp. 75–89)
Bayonne
E.
Kania
R.
Tran
P.
Huy
B.
Herman
P.
Intracranial complications of rhinosinusitis: A review, typical imaging data, and algorithm of management
Rhinology
 , 
2009
, vol. 
47
 
1
(pg. 
59
-
65
)
Beery
K. E.
Beery
N. A.
The Beery–Buktenica Developmental Test of Visual Motor Integration
 , 
2006
(5th ed.)
San Antonio, TX
Pearson
Bleck
T. P.
Greenlee
J. E.
Mandell
G. L.
Bennett
J. E.
Dolin
R.
Epidural abscess
Mandell, Douglas, and Bennett's principles and practice of infectious diseases
 , 
2000
, vol. 
Vol. 1
 
5th ed.
Philadelphia
Churchill Livingstone
(pg. 
1031
-
1034
)
Bowen
B. C.
Donovan-Post
M. J.
Atlas
S. W.
Intracranial infection
Magnetic resonance imaging of the brain and spine
 , 
1991
New York
Rave
pg. 
517
 
Cohen
M.
Children's memory scale
 , 
1997
San Antonio, TX
The Psychological Corporation
Conners
C. K.
Conners’ continuous performance test computer program, version 2.0
 , 
1992
North Tonawanda, NY
Multi-Health Systems, Inc
Courville
C. B.
Subdural empyema secondary to purulent frontal sinusitis: A clinicopathologic study of forty-two cases verified at autopsy
Archives of Otolaryngology - Head & Neck Surgery
 , 
1944
, vol. 
39
 
3
(pg. 
211
-
230
)
de Gans
J.
van de Beek
D.
European Dexamethasone in Adulthood Bacterial Meningitis Study Investigators
Dexamethasone in adults with bacterial meningitis
New England Journal of Medicine
 , 
2002
, vol. 
347
 (pg. 
1549
-
1556
)
Delis
D. C.
Kaplan
E.
Kramer
J. H.
Delis-Kaplan Executive Function System
 , 
2001
San Antonio, TX
The Psychological Corporation
Dill
S. R.
Cobbs
C. G.
McDonald
C. K.
Subdural empyema: Analysis of 32 cases and review
Clinical Infectious Diseases
 , 
1995
, vol. 
20
 (pg. 
372
-
386
)
Duff
K.
Evidence-based indicators of neuropsychological change in the individual patient: Relevant concepts and methods
Archives of Clinical Neuropsychology
 , 
2012
, vol. 
27
 (pg. 
248
-
261
)
Dunn
L. M.
Dunn
D. M.
Peabody Picture Vocabulary Test
 , 
2007
(4th Ed.)
San Antonio, TX
Pearson
Germiller
J. A.
Monin
D. L.
Sparano
A. M.
Tom
L. W.
Intracranial complications of sinusitis in children and adolescents and their outcomes
Archives of Otolaryngology – Head and Neck Surgery
 , 
2006
, vol. 
132
 
9
(pg. 
969
-
976
)
Giannoni
C.
Sulek
M.
Friedman
E. M.
Intracranial complications of sinusitis: A pediatric series
American Journal of Rhinology
 , 
1998
, vol. 
12
 (pg. 
173
-
178
)
Gioia
G.A.
Isquith
P.K.
Guy
S. C.
Kenworthy
L.
Behavior rating inventory of executive function: Professional manual
 , 
2000
Lutz, FL
Psychological Assessment
Greenlee
J. E.
Subdural empyema
Current Treatment Options in Neurology
 , 
2003
, vol. 
5
 
1
(pg. 
13
-
22
)
Hartman
B. J.
Helfgott
D. C.
Weingarten
K.
Scheld
W. M.
Whitley
R. J.
Marra
C. M.
Subdural empyema and suppurative intracranial phlebitis
Infections of the central nervous system
 , 
2004
Philadelphia
Lippincott Williams & Wilkins
(pg. 
523
-
535
)
Hicks
C. W.
Weber
J. G.
Reid
J. R.
Moodley
M.
Identifying and managing intracranial complications of sinusitis in children: A retrospective series
The Pediatric Infectious Disease Journal
 , 
2011
, vol. 
30
 
3
(pg. 
222
-
226
)
Hooper
H. E.
The Hooper Visual Organization Test manual
 , 
1958
Los Angeles
Western Psychological Services
Jacobson
N. S.
Truax
P.
Clinical significance: A statistical approach to defining meaningful change in psychotherapy research
Journal of Consulting and Clinical Psychology
 , 
1991
, vol. 
59
 
1
(pg. 
12
-
19
)
Klein
O.
Freppel
S.
Schuhmacher
H.
Pinelli
C.
Augue
J.
Marchal
J. C.
Subdural empyema in children: Therapeutic strategy. Five cases
Neurochirurgie
 , 
2006
, vol. 
52
 
2–3 Pt 1
(pg. 
111
-
118
)
Kombogiorgas
D.
Seth
R.
Athwal
R.
Modha
J.
Singh
J.
Suppurative intracranial complications of sinusitis in adolescence: Single institute experience and review of literature
British Journal of Neurosurgery
 , 
2007
, vol. 
21
 
6
(pg. 
603
-
609
)
Korkman
M.
Kirk
U.
Kemp
S.
NEPSY
 , 
2007
(2nd Ed.)
San Antonio, TX
Harcourt Assessment
Lafayette Instruments
Quick reference guide for the Purdue Pegboard #32020
 , 
1999
Lafayette, IN
Lafayette Instruments Company
Legrand
M.
Roujeau
T.
Meyer
P.
Carli
P.
Orliaquet
G.
Blanot
S.
Paediatric intracranial empyema: Differences according to age
European Journal of Pediatrics
 , 
2009
, vol. 
168
 
10
(pg. 
1235
-
1241
)
Maertens
P.
Cohen
M.
Krawiecki
N.
The use of neuropsychological evaluation in the medical management of subdural empyema
Archives of Clinical Neuropsychology
 , 
1987
, vol. 
2
 
2
(pg. 
145
-
154
)
Mat Nayan
S. A.
Mohd Haspani
M. S.
Abd Latiff
A. Z.
Abdullah
J. M.
Abdullah
S.
Two surgical methods used in 90 patients with intracranial subdural empyema
Journal of Clinical Neuroscience
 , 
2009
, vol. 
16
 
12
(pg. 
1567
-
1571
)
Nathoo
N.
Nadvi
S. S.
Gouws
E.
van Dellen
J. R.
Craniotomy improves outcomes for cranial subdural empyemas: Computed tomography-era experience with 699 patients
Neurosurgery
 , 
2001
, vol. 
49
 
4
(pg. 
872
-
877
)
Nathoo
N.
Nadvi
S. S.
van Dellen
J. R.
Gouws
E.
Intracranial subdural empyemas in the era of computed tomography: A review of 699 cases
Neurosurgery
 , 
1999
, vol. 
44
 
3
(pg. 
529
-
535
)
Ong
Y. K.
Tan
H. K.
Suppurative intracranial complications of sinusitis in children
International Journal of Pediatric Otorhinolaryngology
 , 
2002
, vol. 
66
 (pg. 
49
-
54
)
Osman Farah
J.
Kandasamy
J.
May
P.
Buxton
N.
Mallucci
C.
Subdural empyema secondary to sinus infection in children
Child's Nervous System
 , 
2009
, vol. 
25
 
2
(pg. 
199
-
205
)
Quraishi
H.
Zevallos
J. P.
Subdural empyema as a complication of sinusitis in the pediatric population
International Journal of Pediatric Otorhinolaryngology
 , 
2006
, vol. 
70
 
9
(pg. 
1581
-
1586
)
Rey
A.
Psychological examination of traumatic encephalopathy
Archives de Psychologie
 , 
1941
, vol. 
28
 (pg. 
286
-
340
sections translated by J. Corwin & F. W. Bylsma, The Clinical Neuropsychologist, 1993, 4–9
Rich
P. M.
Deasy
N. P.
Jarosz
J. M.
Intracranial dural empyema
British Journal of Radiology
 , 
2000
, vol. 
73
 (pg. 
1329
-
1336
)
Rosenfeld
E. A.
Rowley
A. H.
Infectious intracranial complications of sinusitis, other than meningitis, in children: 12-Year review
Clinical Infectious Diseases
 , 
1994
, vol. 
18
 (pg. 
750
-
754
)
Saxton
V. J.
Boldt
D. W.
Shield
L. K.
Sinusitis and intracranial sepsis: The CT imaging and clinical presentation
Pediatric Radiology
 , 
1995
, vol. 
25
 (pg. 
S212
-
S217
)
Singh
B.
van Dellen
J.
Ramjettan
S.
Maharaj
T. J.
Sinogenic intracranial complications
Journal of Laryngology and Otology
 , 
1995
, vol. 
109
 
10
(pg. 
945
-
950
)
Smith
A.
Symbol Digit Modalities Test
 , 
1982
Los Angeles
Western Psychological Services
Strauss
E.
Sherman
E.M.S.
Spreen
O.
A Compendium of Neuropsychological Tests: Administration, norms, and commentary
 , 
2006
New York, NY
Oxford University Press
van de Beek
D.
Campeau
N. G.
Wijdicks
E. M. F.
The clinical challenge of recognizing infratentorial empyema
Neurology
 , 
2007
, vol. 
69
 (pg. 
477
-
481
)
Vehnkatesh
M. S.
Pandey
P.
Devi
B. I.
Khanapure
K.
Satish
S.
Sampath
S.
, et al.  . 
Pediatric infratentorial subdural empyema: Analysis of 14 cases
Journal of Neurosurgery
 , 
2006
, vol. 
105
 
5 Suppl.
(pg. 
370
-
377
)
Wackym
P. A.
Canalis
R. F.
Feuerman
T.
Subdural empyema of otorhinological origin
Journal of Laryngology and Otology
 , 
1990
, vol. 
104
 (pg. 
118
-
122
)
Wechsler
D.
Wechsler Abbreviated Scale of Intelligence
 , 
1999
San Antonio, TX
The Psychological Corporation
Wechsler
D.
Wechsler Intelligence Scale for Children
 , 
2003
(4th Ed)
San Antonio, TX
The Psychological Corporation
Wilkinson
G. S.
Robertson
G. J.
WRAT4 Wide Range Achievement Test Professional Manual
 , 
2006
Lutz, FL
Psychological Assessment Resources
Woodcock
R. W.
McGrew
K. S.
Mather
N.
Examiner's manual: Woodcock-Johnson III Tests of Achievement
 , 
2001
Itasca, IL
Riverside Publishing
Wu
T. J.
Chiu
N. C.
Huang
F. Y.
Subdural empyema in children: 20-Year experience in a medical center
Journal of Microbiology, Immunology, and Infection
 , 
2008
, vol. 
41
 
1
(pg. 
62
-
67
)