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Executive Dysfunction After Fourth-Ventricle Epidermoid Cyst Resection

Veretennikoff, Katie, BPsychSci*; Coyne, Terry, MBBS, FRACS; Biggs, Vivien, MA; Robinson, Gail A., PhD*

Cognitive and Behavioral Neurology: December 2018 - Volume 31 - Issue 4 - p 207–213
doi: 10.1097/WNN.0000000000000175
Case Reports

Intracranial epidermoid cysts are rare, comprising 0.2% to 1.8% of all primary intracranial expanding lesions, of which <5% occur within the fourth ventricle. Epidermoid cysts are frequently congenital, and patients often present in the fourth decade of life. These cysts produce symptoms as a result of mass effect on surrounding structures, most commonly the cerebellum and cranial nerves. Symptoms can include hearing impairment, trigeminal neuralgia (severe facial pain), facial tics, headaches, double vision, and facial palsy. However, no research has focused on the neuropsychological effects on a patient after surgical resection of these cysts. This case report presents the cognitive profile of a woman after resection of an epidermoid cyst in the fourth ventricle. The 49-year-old patient underwent neuropsychological assessment after removal of the cyst, completing a comprehensive set of cognitive tests of estimated premorbid intelligence, attention, memory, social cognition, language, visual perception, and executive functioning. Test results indicated executive dysfunction and reduced visuospatial memory in the acute stage after surgical removal of the epidermoid cyst. These findings suggest that cognitive deficits can occur after resection of space-occupying lesions in brain regions not typically associated with cognition. To our knowledge, this is the first report of the neuropsychological consequences of surgical removal of a congenital epidermoid cyst in the fourth ventricle. An understanding of the neuropsychological sequelae of this rare cerebral cyst will allow patients, families, and health professionals to better anticipate and manage postoperative difficulties.

*Neuropsychology Research Unit, The University of Queensland, Brisbane, Australia

BrizBrain and Spine, The Wesley Hospital, Brisbane, Australia

The authors declare no conflicts of interest.

Correspondence: Gail A. Robinson, PhD, School of Psychology, The University of Queensland, St Lucia, Queensland, Australia 4072 (e-mail: g.robinson@psy.uq.edu.au).

Received February 18, 2018

Accepted July 30, 2018

Intracranial epidermoid cysts are rare, benign lesions, comprising approximately 0.2% to 1.8% of all intracranial expanding lesions (Cambruzzi et al, 2011). The prevalence estimates of these cysts in the fourth ventricle vary but have been reported to range from 5.0% to 31.4% (Kambe et al, 2003), with only 100 reported cases (Sengupta and Singh, 2015). Epidermoid cysts are congenital and are thought to develop from the entrapment of ectodermal squamous epithelial cells (cells typically covering surfaces such as skin, the esophagus, and blood vessel linings) during neural tube closure and separation from the ectoderm during intrauterine development (Nagasawa et al, 2011). Patients with epidermoid cysts typically remain asymptomatic until the third to fifth decade of life (Nagasawa et al, 2011), with the average age of symptom onset being 42.8 years (Chung et al, 2017).

Symptoms of fourth-ventricle epidermoid cysts vary according to the cyst’s size, location, adherence to surrounding structures and nerves, and compression effects (Lunardi et al, 1990). Acute onset of symptoms is rare, with typical symptom duration of 2 to 4 years before presentation (Akar et al, 2003). Initial symptoms of these cysts include headaches, gait disturbance, and vertigo (Nagasawa et al, 2011). Cranial nerve involvement typically occurs at a later stage and can result in diplopia, dysphagia, and voice hoarseness (Kambe et al, 2003 ; Nagasawa et al, 2011). Other reported symptoms include nystagmus, nausea associated with headaches, unilateral progressive reduction in hearing, paresthesia or nerve pain, and visual obscurations (Chung et al, 2017 ; Kambe et al, 2003 ; Parikh et al, 1995 ; Tsai et al, 1999).

Because of mass-related effects, gross total resection of intracranial epidermoid cysts is the recommended treatment (Samii et al, 1996). However, total resection is not always possible. These cysts commonly attach to nerves and blood vessels and can adhere to crucial structures such as the brain stem (Samii et al, 1996). Although subtotal resection can lead to cyst recurrence (Parikh et al, 1995), it is preferred in cases where there is a high risk to surrounding structures (Samii et al, 1996). Even with subtotal resection, patients with fourth-ventricle epidermoid cysts have a good long-term prognosis (Tancredi et al, 2003). For patients whose neurologic functions are intact before surgery, prognosis is improved regardless of cyst size and the extent of resection (Tancredi et al, 2003). Older age and longer duration of symptoms are significant predictors of unfavorable outcomes in patients with fourth-ventricle epidermoid cysts (Chung et al, 2017). Specifically, the risk for poor outcomes is increased by 19% for each additional year of symptom duration before diagnosis (Chung et al, 2017). Consequently, early diagnosis and treatment are imperative for improving patient outcomes.

Rarely, epidermoid cysts can lead to a malignant recurrence, with only nine such cases having been reported (Nakao et al, 2010). The average interval from cyst resection to malignant recurrence is 15.5 years (Nakao et al, 2010), although malignant transformation after a few years has been reported (eg, Abramson et al, 1989 ; Hamlat et al, 2003). In these cases, the malignancy may have already been present at the time of the initial surgery (Hamlat et al, 2003).

To date, there have been no investigations into the neuropsychological profile of patients who underwent surgical resection of an epidermoid cyst of the fourth ventricle. Fu et al (2014) noted that one patient experienced cognitive deficits, including difficulties with short-term memory, attention, and problem-solving, but the authors did not describe the patient’s cognitive functioning in detail.

Here, we present the case of a patient with a fourth-ventricle epidermoid cyst and the neuropsychological sequelae in the acute stage after surgical resection.

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CASE REPORT

History and Presentation

A 49-year-old, right-handed woman completed schooling to year 12 and 1 year of a university degree program in Scotland. She worked for the same employer for 25 years and then moved to Australia, where she was employed in the same line of work. She continued to work for approximately 4.5 years before the cyst resection. She was married with a child and reported no marital discord or family stress at the time of the assessments.

The patient initially presented with chronic occipital and right-sided headaches. Her medical history included involvement in a motor vehicle accident a few years earlier. She reported having episodes of vertigo and diplopia for 9 months before presentation, and a 6-month history of right-sided facial spasms, with increasing frequency. She reported no cognitive concerns.

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Preoperative Imaging

A magnetic resonance imaging brain scan revealed an irregular lobulated epidermoid cyst measuring 5×5×3.5 cm in the fourth ventricle, which extended through the right-side foramen of Luschka and posteriorly through the foramen of Magendie (Figure 1). Imaging indicated the lesion to be T1-weighted hypointense, T2-weighted hyperintense, and heterogeneous on fluid-attenuated inversion recovery image sequences.

FIGURE 1

FIGURE 1

The lesion showed diffusion restriction, with no evidence of hemorrhage within the lesion. The cyst extended to the level of the C1 vertebra on the right side, partially compressing the spinal cord. The cyst was causing mass effect on the adjacent cerebellar hemispheres, particularly on the right side, as well as on the medulla, which was mildly displaced toward the left side. The right cerebellopontine angle structures, adjacent cranial nerves, and right-sided vertebral artery were also affected by compression effects. There was no evidence of vasogenic edema in the cerebellar hemispheres or the brain stem.

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Surgical Procedure

The patient underwent a stereotactically guided suboccipital craniectomy and subtotal resection of the lesion (performed by author T.C.). Standard neurosurgical anesthetic propofol and remifentanil were used. Final histopathologic findings were consistent with an epidermoid cyst.

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Postoperative Imaging

The day after the resection, the patient had a postoperative computed tomographic scan that indicated the presence of expected postoperative pneumocephalus, but no extra-axial or parenchymal hemorrhage and no hydrocephalus. A magnetic resonance imaging 23 days after surgery (Figure 2) revealed a mostly fluid-filled resection cavity in the midline and right paramedian cerebellum, with preservation of the superior vermis. There was some residual epidermoid tissue about the margins of the resection cavity, as indicated by diffusion restriction. A large, presumably cerebrospinal fluid collection (8×2.5×4.7 cm) was observed in the posterior midline neck superficial to the craniotomy site. A mild prominence of the supratentorial ventricles, as compared with the preoperative scan, was noted, although cerebrospinal fluid flow through the aqueduct into the fourth ventricle was normal.

FIGURE 2

FIGURE 2

A magnetic resonance imaging brain scan completed 220 days after surgical resection indicated a stable volume of residual disease and mild prominence of the supratentorial ventricles compared with preoperative imaging. However, this imaging was similar to the 23-day postoperative imaging. Normal cerebrospinal fluid flow through the cerebral aqueduct was again noted, as was a marginal decrease in the volume of fluid in the posterior soft tissues.

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Postoperative Course of Recovery

The patient experienced increased facial pain and continued diplopia in the early acute period after cyst resection. A patch was used to aid the diplopia, and the pain was managed with low-dose pregabalin (75 mg twice daily). The patient was also prescribed oxycodone hydrochloride (40 mg once daily) in the first month after the operation. There was no clinical evidence of postoperative meningitis, aseptic or otherwise, the symptoms of which typically include an acutely unwell appearance, with fever and features of meningeal irritation, namely, neck stiffness, photophobia, and emotional irritability (Soavi et al, 2016). Because the patient did not develop any of these symptoms, we did not perform a lumbar puncture, which is necessary for a definitive diagnosis of meningitis.

At her first neuropsychological testing session (8 days after surgery), the patient reported difficulties with word finding, concentration, and attention, as well as fatigue. Twenty-four days after surgery, the patient was readmitted to the hospital owing to mild confusion, fatigue, anorexia, and nausea, which were attributed to the analgesic medication (oxycodone hydrochloride) that she had been prescribed for her persisting wound pain. The symptoms that sent her back to the hospital remitted promptly after she stopped taking the analgesic.

At her second neuropsychological testing session (29 days after surgery), the patient reported improvements in vision, facial pain, fatigue, concentration, and attention. At the third testing session (50 days after surgery), she reported no facial pain but some ongoing fatigue and mild difficulties with word finding and concentration.

At her 10-month postoperative follow-up, the patient reported being unable to return to her previous employment because of ongoing fatigue, slowed information processing, word-finding difficulties, trouble with multitasking, reduced memory capacity, and problems working with numbers. She also reported anxiety and trauma-related symptoms.

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Neuropsychological Assessment

The patient was recruited for the current study before her surgery by the brain tumor nurse consultant who was involved in her surgical care (author V.B.). The UnitingCare Human Research Ethics Committee and the University of Queensland Ethics Committee approved the study, and the patient provided written consent.

The patient completed a wide range of cognitive assessments over three testing sessions that took place 8 days, 29 days, and 50 days after surgery. The assessments were administered by a registered psychologist. The first session was conducted at her bedside in the hospital, and the second and third sessions were conducted in her home. To determine the patient’s current level of cognitive functioning, we used a battery of standardized, published neuropsychological tests that measure the following cognitive domains:

  • Intellectual functioning
  • Memory (verbal memory, visuospatial memory, word and face memory, topographical memory)
  • Executive functioning (verbal abstract reasoning, verbal fluency, nonverbal fluency, inhibition, cognitive flexibility, verbal initiation and verbal suppression, rule detection)
  • Attention (auditory attention, selective auditory attention, visual attention and visual searching, selective visual attention)
  • Language (spontaneous speech, naming, repetition, word comprehension)
  • Social cognition (theory of mind, social inference, understanding emotions)
  • Visual perception and visuoconstructional ability.
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RESULTS

In our observation of the patient at the three neuropsychological testing sessions, she exhibited appropriate engagement in social interactions; appropriate conversational style and content; appropriate displays of empathy; and no disinhibited behavior, impulsivity, or inappropriate affect.

On cognitive tests, the patient’s estimated premorbid intelligence was within the superior range (Table 1), and on measures of abstract reasoning, her performance was superior for nonverbal reasoning and average for verbal reasoning. She performed at least within the average range on measures of working memory; verbal memory; and memory for words, faces, and topographical scenes. Her performance was relatively weaker on a measure of visuospatial memory, both immediately after stimulus presentation and after a short delay (low average range). The patient passed all measures of visual perception, and her performance was at least average on measures of social cognition (theory of mind, emotion recognition, understanding the impact of social context on meaning). All of the patient’s assessed aspects of attention were intact and at least within the average range. Her language functions were also intact and at least average, including spontaneous speech, naming, repetition, and word comprehension.

TABLE 1

TABLE 1

The patient’s performance on tasks assessing executive functioning varied. Her performance on measures of semantic verbal fluency and fixed-response design fluency (ie, more restrictions on possible designs produced) was intact (superior range). She had no difficulty detecting rules (high average); switching between two tasks, ie, cognitive flexibility (average range); or suppressing verbal responses (average). Her phonemic verbal fluency for both F and S was reduced (low average and borderline, respectively), and she had difficulty on a measure of free-response design fluency (ie, few restrictions on possible designs produced) (low average range). Her performance was also impaired on the verbal initiation trial on the Hayling Sentence Completion Test (Burgess and Shallice, 1997) and on a measure of inhibition of automatic responses, the Stroop test (low average range) (Stroop, 1935).

Overall, although many of the patient’s cognitive functions were intact, she did exhibit reduced performance in visuospatial memory and some executive functions. She had weaknesses in recalling visuospatial stimuli both immediately after presentation and after a short (5-minute) delay. She showed a reduced speed of response initiation, and when she was required to impose her own strategies to search her memory, her ability to generate verbal (phonemic verbal fluency) and nonverbal (design fluency–free) responses was poor. The patient also had difficulty inhibiting automatic responses.

It is important to note that the patient’s premorbid intelligence quotient was in the superior range, and so the areas of cognition that are within the normal range and are interpreted to be “intact” could represent a relative decline from her previously higher levels. Similarly, her visuospatial memory and the affected executive functions may also represent a greater relative decline from prior functioning than we were able to identify with the assessments. The absence of preoperative neuropsychological data is thus a limitation of this study.

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DISCUSSION

Epidermoid cysts occupying the fourth ventricle and their neurologic profile are well documented, yet their cognitive consequences are not. To our knowledge, the neuropsychological profile of fourth-ventricle lesions has not yet been described in the literature. Cognitive changes have broadly been acknowledged as an uncommon presenting symptom, but they have not been described either before or after resection.

In the present case, the patient’s epidermoid cyst compressed the adjacent cerebellar hemispheres, the medulla, the right cerebellopontine angle structures, the adjacent cranial nerves, the right-sided vertebral artery, and the spinal cord adjacent to the C1 vertebra. After resection, the patient had difficulties with executive functioning and visuospatial memory. In particular, she had weaker recall of visuospatial information both immediately after presentation and after a short delay. She also exhibited reduced initiation of responses both in terms of speed and when presented with a letter cue (phonemic verbal fluency) and a nonverbal cue (unstructured design fluency). Further, she presented with poor inhibition of automatic responses.

The executive function difficulties were unexpected in view of the well-known role of the prefrontal cortex in executive functioning and the fact that the patient’s frontal cortex was not compromised by the cyst or therapeutic intervention. Phonemic verbal fluency is particularly sensitive to left frontal cortex lesions (Baldo et al, 2006 ; Robinson et al, 2012), and design fluency may be more sensitive to right frontal region lesions (Robinson et al, 2012). Reduced semantic verbal fluency has been associated not only with prefrontal lobe lesions, but also with left temporal cortex lesions (Baldo et al, 2006 ; Grogan et al, 2009). The prefrontal cortices have also been implicated in supporting verbal initiation (de Zubicaray et al, 2000 ; Nathaniel-James et al, 1997) and the suppression of automatic responses (Perret, 1974 ; Robinson et al, 2015, 2016 ; Vendrell et al, 1995). In addition, the prefrontal cortex, along with the parietal cortex, is associated with visuospatial processing (Norwood and Haaland, 2016). The patient demonstrated reduced visuospatial memory despite the absence of damage to these cortical regions.

This case report suggests a role of the cerebellopontine structures in cognitive functioning. The patient’s prefrontal cortex was not directly affected by the cyst, but compression effects had an impact on the cerebellar hemispheres, the pons, and the medulla. Until relatively recently, the cerebellum was thought to be involved predominantly in planning and executing motor movements (Strick et al, 2009). Mounting evidence over the past 2 decades has revealed a role of the cerebellum in cognitive functions (Buckner, 2013).

In a seminal study, Schmahmann and Sherman (1998) described cerebellar cognitive affective syndrome, a condition arising from cerebellum damage. As the term implies, damage to the cerebellar hemispheres can result in changes in behavior, affect, and cognitive function. According to Schmahmann and Sherman (1998), cerebellar cognitive affective syndrome is characterized by disturbed executive functioning, including difficulties with planning, working memory, verbal fluency, abstract reasoning, and set-shifting; impairments in spatial cognition, ie, visuospatial organization and memory; personality changes such as flat or blunt affect and disinhibited behavior; and disturbances in language, including mild naming difficulties (anomia), impaired ability to speak with normal intonation patterns (dysprosody), and difficulties in constructing a grammatically correct sentence and using incorrect words (agrammatism).

Although our patient did not present with linguistic difficulties or affective or personality changes, she did demonstrate disturbed executive function, including reduced verbal fluency, response inhibition, and visuospatial memory. Although the patient did not fully meet the criteria for cerebellar cognitive affective syndrome, her case provides further support to the growing body of evidence related to the role of the cerebellum in higher-order cognition.

The role of the cerebellum in executive function is more indirect than that of the frontal lobes. The cerebellum connects to the contralateral cerebral cortex via projections, thus allowing the cerebellum to both receive information from and send information to nonmotor regions of the cortex, including the prefrontal regions (Buckner, 2013). The cerebellum facilitates higher-order cognition via these projections (Buckner, 2013). Lesion studies involving the cerebellum have provided support for the role of the cerebellum in cognitive functions. Particularly relevant to the current case, patients with lesions to the cerebellum have deficits in verbal fluency, response inhibition, and visuospatial skills, as well as deficits in verbal learning and memory, attention, and psychomotor speed (Bolceková et al, 2017).

Similarly, evidence supporting the role of the brain stem in executive functions via neural projections has emerged (D’aes and Mariën, 2015 ; Salgado et al, 2007). The brain stem is primarily responsible for regulating many automatic functions, such as sleep, arousal, heart rate, temperature, and breathing rate (Breedlove et al, 2007). Vertigo, dizziness, and balance difficulties are common neurologic consequences of lesions or compression of the brain stem and are a common first presentation for a fourth-ventricle cyst (Nagasawa et al, 2011). However, evidence has demonstrated that higher-order cognitive dysfunction can also occur as a result of a brain stem lesion. In particular, patients with brain stem damage can experience difficulties with inhibitory control, cognitive flexibility, and self-monitoring (Salgado et al, 2007). These deficits have been attributed to a disruption of the monoaminergic brain stem systems responsible for modulating the prefrontal cortex (Salgado et al, 2007).

In summary, the present case report provides the first detailed description of executive dysfunction after fourth-ventricle epidermoid cyst resection. This case also contributes to the growing body of evidence concerning the role of the cerebellum and brain stem in cognition, including executive functioning. It is important to note that other factors may have contributed to the patient’s cognitive profile, such as the amount and effects of the surgical anesthetic and postsurgical medications, as well as her being assessed in the acute phase after surgery. However, postoperative cognitive dysfunction as a result of anesthetic is uncommon in patients younger than 60 years old, particularly in the absence of any prior underlying brain susceptibility, such as dementia (Wang et al, 2014). The surgical anesthetic, therefore, is an unlikely contributor to our patient’s cognitive dysfunction. Similarly, although pregabalin and oxycodone can affect cognition, the patient’s low dose of pregabalin make this an unlikely explanation, as only mild negative cognitive effects occur when the maximum recommended dose (600 mg/day) is used (Salinsky et al, 2010). Further, although opioid medications can negatively influence an individual’s cognition, these effects are typically most significant in the initial few days of use before tolerance develops, and cognition may actually be improved when pain is relieved (Fitzgibbon, 2007). The patient’s cognition was likely affected during the 24 days after surgery when she experienced the negative side effects of the oxycodone. These side effects remitted quickly after the oxycodone was stopped, and her neuropsychological functions were not tested during this period (testing resumed at postoperative day 29). Although she could have been experiencing effects at testing on postoperative day 8, she did not report such side effects.

Even though frontal and other cortical regions are unaffected by a fourth-ventricle epidermoid cyst and its treatment, the cyst can still disrupt executive functions and visuospatial processing and memory—and potentially other cognitive skills. Although it is apparent that surgical resection of the cyst resulted in disruptions to cognitive functioning, deficits may not be as apparent in a patient with a high level of premorbid functioning. That is, the present case may understate the impact that this type of cyst and its location have on an individual’s cognitive skills, as her high premorbid functioning may have masked a relative decline in these skills from a higher level of functioning. A cognitive assessment completed before symptom onset, and potentially preoperatively, would have helped to clarify the extent of her postoperative cognitive changes in the context of her premorbid abilities.

Further research regarding the impact of fourth-ventricle cysts on cognitive functioning is warranted. An understanding of a patient’s cognitive strengths and weaknesses in the acute stage after treatment can inform future treatment planning and may facilitate discharge planning and reduce the frequency of readmission (Bishop et al, 2003).

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                                        Keywords:

                                        epidermoid cyst; executive dysfunction; neuropsychological sequelae

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