Abstract

Background: Several changes in normal pressure dynamics on the brain occur with a decompressive craniectomy and subsequent cranioplasty. Dead space volume is an important factor contributing to intracranial volume postcranioplasty. A decrease in this volume due to negative suction drain along with relative negative pressure on the brain with the loss of external atmospheric pressure may lead to fatal cerebral edema.

Case Description: A 52-year-old gentleman with a 210 mL volume and middle cerebral artery territory infarction underwent an emergency craniectomy and 6 months later a titanium mold cranioplasty. Precranioplasty computed tomography (CT) scan evaluation revealed a sunken skin flap with a 9 mm contralateral midline shift. Immediately following an uneventful surgery, the patient had sudden fall in blood pressure to 60/40 mmHg and over a few min had dilated fixed pupils. CT revealed severe diffuse cerebral edema in bilateral hemispheres with microhemorrhages and expansion of the sunken right gliotic brain along with ipsilateral ventricular dilatation. Despite undergoing a contralateral decompressive craniectomy due to the midline shift toward the right, the outcome was fatal.

Conclusion: Careful preoperative risk assessment in cranioplasty and close monitoring postprocedure is crucial, especially in malnourished, poststroke cases, with a sinking skin flap syndrome, and a long interval between decompressive craniectomy and cranioplasty. Elective preventive measures and a low threshold for CT scanning and removal of the bone flap or titanium mold are recommended.

Keywords: Craniectomy, Complication, Cranioplasty, Edema, Malignant, Monro-Kellie, Trephination

INTRODUCTION

Cranioplasty in literature dates back to the 16^th century where Fallopius makes mention of a gold plate used to reconstruct a skull defect, though there is a scattered evidence of similar procedures being performed since the Incans.[ 18 ] With the advent of asepsis, antibiotics, and various autologous, allogeneic, and artificial graft materials, cranioplasty has evolved into a relatively low risk, straightforward procedure. It is, however, also subject to its share of complications with reported rates of up to 41%.[ 2 ] Table 1 enumerates the common complications that can occur postcranioplasty[ 2 , 4 , 11 , 17 , 29 ] and how they may be avoided.

Table 1:

Common complications and their avoidance in cranioplasty.

Postcranioplasty rebound cerebral edema, initially described as “pseudohypoxic brain swelling” by Van Roost D et al.,[ 25 ] is a known, albeit extremely rare complication. Since being first described, only a handful of case reports and series exist in the literature.

We report a case of malignant cerebral edema with multiple ipsilateral hemorrhagic foci occurring within an hour of a titanium mold cranioplasty procedure. The aim of this manuscript is to bring to attention a rare, often under-rated complication of a seemingly straightforward procedure, elucidate possible pathophysiological mechanisms, and identify patients at a high risk for the same.

CASE REPORT

Initial evaluation and intervention

A 52-year-old gentleman had presented to the emergency room with sudden onset left hemiparesis, with a Glasgow Coma Scale (GCS) of E2M5Vt. He was diagnosed with a 210 mL volume, middle cerebral artery (MCA) territory infarction on magnetic resonance (MR) imaging with mass effect and a 12 mm midline shift. He was also diagnosed with a right brachial artery embolus on routine large vessel and neck MR angiograms. Carotid vasculature was noted to be normal with no narrowing or filling defect. An emergency right fronto-temporo-parietal decompressive with lax duraplasty was performed followed by a right brachial embolectomy by the vascular team. Further evaluation with a cardiac 2D echogram revealed no regional wall motion abnormality with mild concentric left ventricular hypertrophy (LVH), normally functioning valves and no clots or vegetations. Postoperatively, he had an uneventful recovery and over a week GCS improved to E4M6V5. He was discharged on therapeutic doses of low molecular weight heparin for the brachial artery embolus.

Cranioplasty

He presented 6 months later for a cranioplasty. He was conscious alert and oriented with modified Ashworth Grade II hypertonia and Medical Research Council Grade 3 power in the left upper and lower limbs. A computed tomography (CT) scan revealed a sunken skin flap with a 9 mm midline shift to the left along with gliotic changes in the right MCA territory [ Figure 1 ]. The autologous bone preserved in a freezer was found to be unhealthy and he underwent a customized titanium mold cranioplasty. Intraoperatively, the brain was sunken. Urine output was maintained at 80–150 mL/h and vitals were stable with minimal fluctuations. The surgery was completed uneventfully.

Figure 1:

Precranioplasty computed tomography scan shows a sunken skin flap with a contralateral midline shift suggestive of a significant effect of the atmospheric pressure on the brain.

Postoperative period and outcome

The patient did not wake from anesthesia and had sudden fall in blood pressure (BP) to 60/40 mmHg a few minutes after shifting, on ventilator, to the intensive care unit. The hypotension lasted for less than a minute and he was stabilized with inotropes and noradrenaline boluses and later a drip infusion, with close titration owing to a very labile BP highly sensitive to minor adjustments in the inotropes. Blood gases, electrolytes, and postoperative hematocrit were within normal limits. A screening echocardiogram at the time showed an ejection fraction of 55% with freely moving valves and no clots or vegetations, ruling out a cardiac cause for the hypotension. During and immediately following stabilization, his pupils began dilating bilaterally from 2 mm to 8 mm over 30 min.

A CT scan showed diffuse severe cerebral edema in bilateral hemispheres with effaced basal cisterns, microhemorrhages, and expansion of the sunken right gliotic brain along with ipsilateral ventricular dilatation. There was poor grey-white matter differentiation in the contralateral (left) side with a midline shift of 5 mm toward the right (cranioplasty) side [ Figure 2 ]. GCS remained E1M1Vt (No eye response or motor response, intubated on ventilator support) and pupils was now dilated fixed (8 mm bilaterally). Due to left-sided edema and risk of aggravation of midline shift by the right-sided titanium mold removal, a left-sided decompressive craniectomy and lax duraplasty were deemed suitable and performed.

Figure 2:

(a-c) Axial, sagittal, and coronal computed tomography scan images immediately after the procedure showing malignant bihemispheric cerebral edema with microhemorrhages. (d-f) Axial brain window, axial bone window, and a scout image showing the custom titanium mold in situ.

A magnetic resonance imaging was performed the subsequent day that showed bilateral posterior cerebral artery territory and brainstem infarcts [ Figure 3 ].

Figure 3:

Post procedure magnetic resonance imaging revealed bilateral posterior circulation hemorrhagic infarcts and severe edema. Diffusion-weighted imaging showing diffusion restricting acute infarcts (a and b), decreased apparent diffusion coefficient (c), and blooming on gradient echo sequence (d).

Despite all possible efforts and interventions, the patient did not improve, had absent brainstem signs with dilated fixed pupils and a GCS of E1M1Vt, and eventually a fatal outcome.

Possible etiologies

In this case, other possibilities of malignant cerebral edema include fresh emboli from the heart causing fresh infarcts. Although fresh infarcts developing severe edema rapidly within an hour is rare, a screening cardiac 2D echogram was done at the time which showed normal findings apart from mild concentric LVH, and an ejection fraction of 55%, matching the evaluation done at the time of the initial infarct.

Hypoxia during surgery could theoretically cause bihemispheric edema; however, no such hypoxia or desaturation occurred intraoperatively or immediately postoperatively.

Hypotension due to an unrelated cause and subsequent hypoxic brain injury leading to malignant edema may be considered. However, no other systemic causes of hypotension could be identified. There was minimal blood loss during surgery and an 80–150 mL/h urine output throughout ruling out hypovolemia. Cardiac causes had been ruled out (as mentioned earlier) and there was no cause for septic shock immediate postoperatively. It was hence concluded that the hypotension was a consequence of severe brain edema and loss of autonomic control, further supported by the lability of the BP and extreme sensitivity to inotropic agents.

After excluding the above, the sequence of events suggests postcranioplasty malignant edema due to a change in pressure dynamics, as the most likely cause of the deterioration.

DISCUSSION

Postcranioplasty cerebral edema is, fortunately, an exceedingly rare complication, with twenty odd cases reported throughout world literature till date,[ 5 , 7 - 10 , 12 , 14 , 15 , 19 , 22 , 25 ] with a 90% of mortality rate.

Pathophysiology

Table 2 summarizes the various pathophysiological mechanisms proposed.[ 6 , 8 , 13 , 22 ]

Table 2:

Postulated mechanisms of rebound edema postcranioplasty.

When a decompressive craniectomy is performed, the Monro-Kellie doctrine[ 16 ] no longer applies and over time, a new homeostasis is achieved with the cerebral compliance and intracerebral pressure reaching an equilibrium with the external atmospheric pressure. Cranioplasty re-establishes a closed intracranial compartment. We posit that an extended Monro-Kellie doctrine comes into play where:

k (constant) = Brain parenchymal volume + Cerebral blood volume + Cerebrospinal fluid volume + Dead space volume

This dead space has a natural relative negative pressure[ 25 ] over the brain parenchyma due to the now absent positive atmospheric pressure, which is further accentuated by a negative suction subgaleal drain.[ 20 ] Therefore, the dead space has a natural tendency to reduce in volume and collapse on itself.

In a gliotic brain, the parenchymal volume is already considerably reduced, and with cerebrospinal fluid (CSF) volume being relatively constant in a hyperacute setting, cerebral blood volume increases with decreasing dead space volume. An already dysfunctional cerebral microcirculation (due to trauma/infarction etc.) gives way to increased cerebral blood flow, leading to malignant edema and hemorrhages.

This is supported by the largest reported case series by Sviri[ 22 ] in 2015, who reported four patients with cerebral edema after cranioplasty, all of whom had a significantly sunken craniotomy site preoperatively and a large craniectomy defect, thereby potentially leading to a considerable relative negative pressure in the dead space and postcranioplasty. This creates a controversy in the management of sinking skin flap syndrome where cranioplasty has been accepted as the definitive management.[ 3 , 23 ] We agree with this line of management, with emphasis on early identification of patients in whom acute decompression of the atmospheric pressure over the brain may lead to malignant edema, elaborated further in the manuscript.

Sviri also noted all patients had a closed suction drainage.[ 22 ] A case reported by Shen et al. also involved a 300 mL collection in the drain,[ 20 ] further supporting the negative pressure theory. Table 3 collates the risk factors in various case reports in current literature [Table3].[ 21 , 24 , 26 - 28 , 30 ]

Table 3:

Current case reports in literature of postcranioplasty malignant edema.

Risk factors and predictors

This complication occurred over all age groups and no particular age group could be identified as being at a high risk. Based on the reported cases in the literature till date, the following high-risk factors have been identified – Sinking skin flap syndrome, the time since craniectomy, and the primary pathology [ Figure 4 ]. The risk factors are based on underlying pathophysiological mechanisms of (1) increase in relative negative pressure with increased effects of precranioplasty atmospheric pressure, (2) increased cerebral compliance with time and time-sensitive microcirculatory changes to adapt to the external atmospheric pressure, and (3) observed frequency of primary pathologies in reported cases of postcranioplasty cerebral edema [ Table 4 ]. A patient with more than one high-risk factor, we postulate, warrants extra caution, and postoperative monitoring in an intensive care unit for the first 48-h postprocedure. Nonrecovery from anesthesia, inadequate spontaneous breathing, generalized seizures,[ 20 ] and a low/drop in GCS postoperatively are all red flags that must prompt an immediate CT scan.

Figure 4:

(a-c) Frequency of various risk factors in literature.

Table 4:

Postcranioplasty cerebral edema risk assessment.

The above factors need validation and testing in large numbers of cranioplasty patients and must be suitably extended/modified and condensed into a risk scoring system, before being conclusively used to identify patients at a high risk of developing cerebral edema postcranioplasty.

Possible prevention in high-risk patients postoperatively

As per the extended Monro-Kellie doctrine described above, we believe that minimization of either the dead space or the negative pressure in it[ 25 ] is crucial to prevent increased cerebral blood flow and parenchymal shear, and thereby avoid edema/hemorrhage formation in patients at high risk for the same. The authors would like to emphasize that the following are pathophysiology-based suggestions and need to be clinically evaluated with randomized controlled trials before being incorporated into institutional protocols.

Generous hydration preoperatively to promote CSF formation and decrease shear on the brain parenchyma in accordance with the extended Monro-Kellie doctrine

CONCLUSION

Decompressive craniectomy changes the intracranial milieu and adds external atmospheric pressure to the myriad of forces at play on the brain. The modified Monro-Kellie doctrine as described emphasizes the role of dead space volume after cranioplasty, which we believe plays a critical role in malignant cerebral edema after cranioplasty. It is crucial to assess the risk of this fatal complication preprocedure and take steps to prevent it in the high-risk subgroup. Trephination syndrome, an etiology of traumatic brain injury and cranioplasty within 3 months after craniectomy, is high-risk factors. In these patients, close monitoring and measures to prevent cerebral edema are recommended.

Declaration of patient consent

Patient’s consent not required as patient’s identity is not disclosed or compromised.

Financial support and sponsorship

Publication of this article was made possible by the James I. and Carolyn R. Ausman Educational Foundation.

Conflicts of interest

There are no conflicts of interest.

Disclaimer

The views and opinions expressed in this article are those of the authors and do not necessarily reflect the official policy or position of the Journal or its management. The information contained in this article should not be considered to be medical advice; patients should consult their own physicians for advice as to their specific medical needs.

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