Neurologic Deterioration Due to Brain Sag After Bilateral Craniotomy for Subdural Hematoma Evacuation

Accepted Manuscript Neurological Deterioration Due to Brain Sag Following Bilateral Craniotomy for Subdural Hematoma Evacuation James K.C. Liu, MD PII:

S1878-8750(18)30426-1

DOI:

10.1016/j.wneu.2018.02.153

Reference:

WNEU 7568

To appear in:

World Neurosurgery

Received Date: 9 November 2017 Revised Date:

23 February 2018

Accepted Date: 26 February 2018

Please cite this article as: Liu JKC, Neurological Deterioration Due to Brain Sag Following Bilateral Craniotomy for Subdural Hematoma Evacuation, World Neurosurgery (2018), doi: 10.1016/ j.wneu.2018.02.153. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

ACCEPTED MANUSCRIPT Liu 1 1 2 3 Neurological Deterioration Due to Brain Sag Following Bilateral Craniotomy for Subdural

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Hematoma Evacuation

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James K. C. Liu, MD

9 Department of Neuro-Oncology

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Moffitt Cancer Center

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13 14 Corresponding Author:

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James K. C. Liu, M.D.

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Department of Neuro-Oncology

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Moffitt Cancer Center

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MCB 2nd Floor 12531

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Tampa, FL 33612

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[email protected]

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Keywords: bifrontal craniotomy; intracranial hypotension; brain sag; CSF hypovolemia;

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subdural hematoma

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Abbreviations: SIH spontaneous intracranial hypotension, CSF cerebrospinal fluid, CT

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computed tomography, MRI magnetic resonance imaging

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Running Title: Brain sag following bilateral craniotomies

ACCEPTED MANUSCRIPT Liu 2 ABSTRACT

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Background: Intracranial hypotension from cerebrospinal fluid hypovolemia resulting in

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cerebral herniation is a rare but known complication that can occur following neurosurgical

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procedures, usually encountered in correlation with perioperative placement of a lumbar

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subarachnoid drain. Decrease in CSF volume resulting in loss of buoyancy results in downward

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herniation of the brain without contributing mass effect, causing a phenomenon known as ‘brain

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sag.’ Unreported previously is brain sag occurring without concomitant occult CSF leak or

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lumbar drainage.

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Case Description: This case report describes a patient who underwent bilateral craniotomies

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for subacute on chronic subdural hematomas with successful decompression, but suffered from

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an acute neurological deterioration secondary to brain sag. Despite an initial improvement in

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neurological exam, he subsequently exhibited a progressive neurologic deterioration with

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evidence of cerebral herniation on neuroimaging, without evidence of continued mass effect on

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the brain parenchyma. After a diagnosis of ‘brain sag’ was determined based on imaging

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criteria, the patient was placed in a flat position which resulted in a rapid improvement in

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neurological exam without any further intervention.

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Conclusions: This case is unique from previous reports of intracranial hypotension following

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craniotomy in that the symptoms were completely reversed with positioning alone, without any

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evidence of active or occult CSF drainage. This report emphasizes that the diagnosis of brain

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sag should be taken into consideration when there is an unknown reason for neurologic decline

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after craniotomy, particularly bilateral craniotomies, if the imaging indicates herniation with

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imaging findings consistent with intracranial hypotension, without evidence of overlying mass

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effect.

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ACCEPTED MANUSCRIPT Liu 3 61 Intracranial hypotension is the result of abnormally low intracranial pressure that most

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commonly manifests as positional headaches[1]. The most common form is spontaneous

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intracranial hypotension (SIH), a relatively rare but known pathology that results in brain

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herniation or sagging due to CSF hypovolemia[2-5]. SIH can commonly be misdiagnosed,

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having the pathology attributed to a chiari malformation, compression from a subdural

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hematoma, or possible malignancy leading to leptomeningeal enhancement[6]. It is now known

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that SIH is often secondary to cerebrospinal fluid (CSF) hypovolemia that is often the result of

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an occult spinal CSF leak[7]. Symptoms are typically mild positional headaches, which are

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relieved with bed rest or epidural blood patching[8]. A few reports have noted incidences of

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intracranial hypotension following craniotomies, particularly for treatment of aneurysms[2, 9-11].

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Unlike SIH, neurological decline is often rapid and much more severe in these cases. The

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authors in these reports have noted that lumbar drainage was placed during these procedures

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to assist in intraoperative brain relaxation, and patients developed unexplained neurological

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decline with imaging evidence of brain herniation. Neurological examination was improved with

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subsequent stopping of lumbar drainage and with Trendelenburg positioning, resulting in a

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reversal of ‘brain sag.’[12] This case involves brain sag secondary following a bilateral

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craniotomy without occult CSF drainage or lumbar drain.

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79 CASE REPORT

A 65-year-old male presented to the emergency department for a history of headaches

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and unsteady gait. CT imaging showed bilateral frontal parietal subacute on chronic subdural

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hematomas(cSDH) (Figure 1). Neurological examination on presentation was intact except for

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mild lethargy and confusion. The patient was taken to the operating room for bilateral

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craniotomies for evacuation of subdural hematomas with placement of bilateral subdural drains.

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Immediately after the procedure, he was at his neurological baseline, with improvement of

ACCEPTED MANUSCRIPT Liu 4 headaches. The patient was kept in a recumbant supine position to help with drainage of

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residual fluid. Approximately 12 hours after procedure, the patient became progressively

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lethargic. Subsequent imaging revealed mild re-accumulation of subdural fluid with a large

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amount of pneumocephalus, without significant brain expansion. Approximately 36 hours after

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the initial procedure, while still in a recumbent position, the patient acutely declined requiring

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intubation. He was taken to the operating room for re-exploration of his bilateral craniotomies

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and re-exploration of recurrent subdural fluid/hematomas. There was no evidence of significant

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mass effect from re-accumulated fluid or tension pneumocephalus. Subdural drains were not

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placed after the second procedure for concern of air trapping within the subdural space.

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Immediately following the procedure, the patient improved neurologically, was awake and

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following commands. In the days following the second procedure, the patient demonstrated a

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waxing and waning mental status, with an overall slow progressive neurological decline. He

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stopped following commands and his pupils became minimallyreactive. CT imaging noted

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persistent pneumocephalus without evidence of subdural mass effect and lack of brain re-

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expansion. Magnetic resonance imaging (MRI) performed five days after the second

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decompression demonstrated uncal herniation along with brain stem sagging without any

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evidence of supratentorial mass effect causing the herniation (Figure 2). Given the imaging

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evidence consistent with brain sag, the patient was placed with his head of bed flat. Within 24

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hours, the patient started to improve neurologically. The patient’s pupils started to react briskly,

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followed by spontaneous eye opening, followed by command following within several days and

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verbal communication. The patient was kept flat for 4 days and then gradually progressed to an

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upright position, with continued improvement in his neurological function. At his 6-week follow-

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up, the patient was neurologically intact with imaging showing almost complete parenchymal

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expansion and resolution of subdural fluid collections.

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DISCUSSION

ACCEPTED MANUSCRIPT Liu 5 Intracranial hypotension describes a pathology that results in brain herniation resulting in

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neurological symptoms and potential deficits. Clinically, the syndrome manifests initially as

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orthostatic headaches that improves with flat positioning, but may progress to further

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neurological deterioration[13]. Several key imaging findings are pathognomonic. On MRI there

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is often noted to be leptomeningeal enhancement secondary to venous engorgement, as well as

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downward displacement of the cerebellar tonsils, sagging of the midbrain, effacement of the

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pre-pontine cisterns, enlargement of the pituitary gland, and chiasmatic drooping[4, 14, 15]. As

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a manifestation of the loss of buoyancy from the CSF on the brain and resultant downward

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displacement, subdural hematomas may develop. Once commonly misdiagnosed, it is now

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better understood to be most commonly secondary to CSF hypovolemia, defined as SIH,

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resulting in loss of buoyancy and downward displacement of the brain, tethering neurologic

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elements. The course is typically mild and reversed through application of an epidural blood

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patch.

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Intracranial hypotension from CSF hypovolemia following craniotomy has been much

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less noted in the literature, with only a few reports[11, 12, 16, 17]. Unlike spontaneous

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intracranial hypotension, a rapid herniation of brain contents can occur leading to a progressive

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neurological deterioration. All but two cases previously reported in the literature are related to

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lumbar CSF drainage placed during the operative procedure, primarily in aneurysm surgery for

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intraoperative brain relaxation[10-12]. These cases have a similar etiology to SIH but presenting

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with a more rapid course due to the loss of CSF from the craniotomy in addition to continued

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lumbar drainage. The idea of CSF hypovolemia is further supported by the fact that authors

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have noted in the past that replacement of intrathecal fluid through the lumbar drain has

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reversed the process[14, 18]. What those studies failed to mention was placing the patient in a

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flat or Trendelenburg position to utilize gravity to reverse the brain herniation effect.

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The post craniotomy ‘brain sag’ was noted by Komotar et al., who developed a

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radiographical criteria for brain sag on MRI and noted it to occur in eleven patients having

ACCEPTED MANUSCRIPT Liu 6 undergone surgery for aneurysm clipping, all with intraoperative spinal drainage[12]. The

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patients demonstrated rapid neurological decline with pupillary changes indicative of uncal

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herniation, and all symptoms were reversed by placing the patient in a Trendelenburg (-15 to -

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30 degree) position. There are only two reports of brain sag following craniotomy without active

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lumbar CSF drainage. Kelley and Johnson noted a patient having undergone a bilateral

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craniotomy for evacuation of bilateral subdural hematomas[16]. Post operatively there was

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noted to be pneumocephalus on imaging, and the patient suffered a progressive decline in

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neurological exam. The patient recovered quickly after placement in the Trendelenburg position.

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Subsequently, a CSF leak was found in the thoracic spine and an epidural blood patch was

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placed. Schievink et al. reported a case of brain sag resulting in coma after aneurysm clipping

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that was due to CSF hypovolemia from thoracic spinal CSF leak[17].

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The case reported here is the only case of brain sag following a craniotomy without

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associated spinal drainage of CSF. During initial workup upon presentation, a magnetic

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resonance imaging (MRI) of the spine was not performed to look for occult CSF leak since the

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subdural fluid density was more consistent with hematoma than hygroma, and there was not a

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reported history of positional headaches. After the initial symptomatic improvement following the

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first procedure, the patient suffered a progressive decline in his neurological status. Typically

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following decompression for subdural hematoma, pneumocephalus is common but there is

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usually some expansion of the brain parenchyma, which was not seen in this case. Concern for

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tension pneumocephalus was considered, although the diagnosis was unclear as to how much

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pressure was being placed as there was not the typical ‘Mount Fuji’ sign[19]. After the second

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decompression, in which there was not found to be evidence of tension pneumocephalus or

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mass effect from re-accumulated fluid, there was again an initial improvement with subsequent

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progressive significant neurological decline. Without a clear etiology for the neurological decline,

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the patient was kept flat for 48 hours following drainage of a chronic SDH, and then the head of

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the bed was gradually elevated. Without evidence of overlying mass effect causing the brain

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ACCEPTED MANUSCRIPT Liu 7 165

herniation seen on MRI, a diagnosis of brain sag was considered and the patient was placed in

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a flat position which resulted in a brisk recovery of his neurological function. CSF hypovolemia in the setting of an occult CSF leak or active spinal drainage is well

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known at this point. Unique to this case was the lack of spinal CSF leak, and an acute resolution

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of symptoms purely through positioning the patient flat. The reason for this occurrence is

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unclear. Several hypothesis may indicate why this occurs. One is patients of slightly greater age

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may have less compliant brain resulting in sustained subdural space. Brain expansion following

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long term compression from chronic subdural hematoma is likely to be slower in elderly patients

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compared to younger patients. This lack of expansion has been noted in the literature, and

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techniques such as intrathecal saline injection have been described[20, 21]. This lack of

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elasticity may contribute to the lack of buoyancy on the brain. There could also be a relation to

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the patient sustaining a bilateral craniotomy. In the few reports of this occurrence, regardless of

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the presence of CSF leaks or drainage, a large percentage of bifrontal craniotomies have been

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noted [16, 22]. The correlation between bifrontal/bilateral craniotomies may be due to excessive

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CSF loss from a bilateral perspective, but also from bilateral air trapping, albeit not to the extent

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of causing a tension pneumocephalus.

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Patient positioning following surgical evacuation of chronic subdural hematoma remains

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a controversial topic. The traditional approach is to place the patient in a recumbent position

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post-operatively to facilitate brain expansion and decrease risk of hematoma recurrence[21, 23]

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There is concern that this may lead to an increased risk of post-operative morbidity, including

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pneumonia, deep vein thrombosis, and urinary tract infection[24] This is countered by studies

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that have demonstrated an increase rate of hematoma recurrence after immediate

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immobilization, without any benefit in post-operative morbidity[25]. Although there have been no

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definitive studies to support the best positioning of a patient follow cSDH evacuation, the

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concept of intracranial hypotension following surgical evacuation of cSDH has been noted in the

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literature[21, 26]. These occurrences are relatively rare, and those studies have not introduced

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ACCEPTED MANUSCRIPT Liu 8 191

radiographically whether there was imaging findings consistent with brain sag and whether a

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recumbent position may have been helpful. Most important to note from this case is that the natural neurosurgical response to a

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decline in mental status thought to be from brain herniation includes elevation of the head. In

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this case, this was likely contributing to further ‘brain sag’ and neurological decline, as in the

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immediate post-operative period this patient’s head of bed was flat and he was subsequently

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declined. It is important for neurosurgeon’s to be aware of this pathology as this maneuver

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would be contraindicated and the treatment would be to place the patient flat or in the

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Trendelenburg position. Searching for an occult CSF leak if there was not a history of lumbar

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drainage should be considered in the workup.

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ACCEPTED MANUSCRIPT Liu 10 271 272 273 FIGURE LEGENDS

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Figure 1. CT imaging of the brain pre-operatively (A,B) and post-operative day one(C). Note

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the significant amount of pneumocephalus post operatively without significant brain expansion.

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(D) Imaging on post-operative day 2 prior to neurological decline showed minimal re-

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accumulation of subdural fluid with persistent pneumocephalus and lack of brain re-expansion.

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Figure 2. (A) MRI performed on post operative day 5 from the second procedure shows on the

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sagittal imaging chiasmatic drooping (long arrow), effacement of the prepontine cisterns (short

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arrow), decreased mammilopontine distance (arrowhead), and tonsillar ectopia (double arrows).

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(B) Coronal view shows bilateral uncal herniation without overlying convexity mass effect. (C)

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CT imaging 6 weeks post operatively shows re-expansion of the brain parenchyma with a small

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amount of residual subdural fluid.

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Highlights 1. Intracranial hypotension secondary to CSF hypovolemia following craniotomy occurs rarely, and all previous reports have been associated with an active or occult CSF drainage.

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2. This case report is the first report of a patient undergoing a craniotomy procedure that suffered significant neurological deterioration with imaging consistent for intracranial hypotension resulting in brain sag, without evidence of CSF drainage.

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3. The patient was able to recover from only positional changes to reverse brain sag.

4. Intracranial hypotension following craniotomy, particular bilateral or bifrontal craniotomy,

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needs to be considered if there is neurological deterioration and evidence of brain sag on neuroimaging. This is important to note as the treatment is contrary to usual protocol of head

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elevation for cerebral herniation.