Introduction

Decompressive craniectomy (DCR) is a potentially lifesaving procedure used in neurosurgery for the relief of medically intractable intracranial hypertension in patients with severe head injuries, large-vessel infarcts, intraoperative brain swelling and severe brain edema after intracranial procedures.8)10)11)16)17)19) Once patients undergo a DCR, those who survive are obligated to undergo a second procedure, cranioplasty, for surgical cranial reconstruction. Cranioplasty following a DCR is associated with a high complication rate. Perioperative and postoperative complications are wound infection, hematoma, bone resorption, sunken bone plate, hydrocephalus, intraoperative hemodynamic instability and status epilepticus.10)

Bilateral hemorrhagic infarction following cranioplasty is an extremely rare complication; only one case of bilateral hemorrhage has been reported to date. Here, the occurrence of bilateral diffuse intracerebral hemorrhagic infarction following routine cranioplasty in a 68-year-old woman who underwent a DCR 3 months previously due to a right middle cerebral artery (MCA) territory infarction is reported and the possible pathogenesis is discussed.

Case Report

A 68-year-old woman was transferred to the neurosurgical department from a local hospital after the sudden onset of left hemiparesis followed by progressive neurological deterioration with a GCS score of 11. The medical history was significant for atrial fibrillation; however, the patient was not taking any medication. Neurological examination revealed a slightly drowsy mental state and left hemiplegia. The initial brain computed tomography (CT) scan showed a slightly low density lesion in the frontal lobe and the CT angiogram revealed total occlusion of the right internal carotid artery (ICA). The patient arrived at our hospital 3 hours after the onset of symptoms. The patient underwent intra-venous thrombolysis with urokinase (20,000 units). Subsequent magnetic resonance (MR) diffusion images and MR angiography showed a right MCA territory infarction and revealed total occlusion of the right ICA (Figs. 1A and 1B). The level of consciousness deteriorated to a stupor. A follow-up brain CT scan showed a large right fronto-parietal infarction compressing and dislocating the midline structures (Fig. 1C). Subsequently, the patient underwent a right fronto-temporo-parietal DCR with duraplasty. The general condition stabilized postoperatively. The patient was bedridden but communicated with family members. The neurological symptoms included loss of concentration, depression and memory impairment. The skin at the surgical site was markedly depressed due to large bone defects. The patient had repeat CT scans of the brain 3 months after the initial surgery that revealed a post infarct encephalomalacia in the region of the right MCA with marked depression of the brain (Fig. 2). A diagnosis of sinking skin flap syndrome (SSSF) was considered. The patient then underwent elective cranioplasty using an autologous bone graft. The cranioplasty was performed in the usual manner and hemodynamic/metabolic factors remained within normal limits during and after the operation. However, 5 hours postoperatively, the patient had not recovered from the anesthesia, and her level of consciousness deteriorated to a GCS score of 5 (E3, VT, M2). A cranial CT scan revealed increasingly diffuse brain swelling and multifocal hemorrhagic infarctions in both cerebral hemispheres (Fig. 3). On the following day, a cerebral angiography was performed. It revealed right distal ICA occlusion, which had no interval changes compared to the initial MRA; there was no arterial/venous occlusion, deep venous occlusion or congestion (Fig. 4 A, B, C, D). The level of consciousness gradually improved. Currently, the patient can open her eyes spontaneously but cannot communicate with others.

Discussion

After a large DCR, a series of neurological symptoms associated with the depression of the skin at the site of the cranial defect can develop that include neurological symptoms such as dizziness, undue fatigue, headache, memory impairment, irritability, convulsions, mental depression and vague discomfort, with worsening of symptoms during postural changes. This is known as SSFS.20) The mechanism associated with the SSFS has been considered to be as follows. The cranial defect produced by the craniotomy is directly affected by atmospheric pressure. As cerebral swelling improves, the skin at the cranial defect site gradually sinks due to atmospheric pressure and deforms the cerebral tissue, resulting in a local cerebral circulation disorder and cerebral dysfunction.15)18) SSFS is characterized by rapid improvement of neurological symptoms after cranioplasty. More recent reports have suggested that cranioplasty may help optimize neurological recovery, both physiologically and/or clinically.2)3)5)6)12)

In the present case, it was unclear what had caused the bilateral diffuse hemorrhagic infarctions in this patient with the SSFS following cranioplasty. To date, only two cases with a similar complication following cranioplasty have been reported. Cecchi et al.4) described a case of ipsilateral large hemorrhagic infarction following cranioplasty in a 77-year-old woman with SSFS following a DCR. Kang et al.7) described a case of bilateral multiple hemorrhagic infarctions after autologous cranioplasty in a 63-year-old man following a DCR for right MCA territory infarction. They proposed that the hemorrhagic infarction was a reperfusion complication related to a sudden increase in CBF after cranioplasty. It is very difficult to determine the possible mechanisms underlying this extremely rare complication. Isago et al.12) reported a change in the cerebral blood flow in patients with the SSFS after cranioplasty, as measured using xenon CT imaging. The increased blood flow observed in that case might have been associated with the mechanism underlying the development of this problem. In fact, bilateral hemorrhagic infarction could be related to a sudden increase in the CBF in the cerebral hemisphere where the cranioplasty was performed, which was already weakened from a prior stroke.

On return of the cerebral blood flow, there is a resumption of the principal functions of tissue perfusion: oxygen delivery, provision of substrates for metabolism, and clearance of metabolic wastes. However, return of blood flow to the post ischemic lesion also plays a potential negative role. Interactions between blood and the damaged tissue can lead to further tissue injury, which is referred to as reperfusion injury.13) To date, reperfusion injuries have been observed in the brain, heart, and other organs. Primary hemodynamic alterations in patients with cerebral ischemia decrease cerebral perfusion pressure and blood flow in the damaged brain as a result of diffuse damage to the large and small intracranial vessels. The common underlying mechanism appears to be chronic cerebral hypoperfusion caused by regional arterial hypotension and venous hypertension.14) Restoration of cerebral perfusion and blood flow after cranioplasty may result in the hyperemia phenomena and can be regarded as a type of reperfusion.12) In lesions caused by cerebral ischemia, the findings are similar to the pathology of acute cerebral ischemia/ reperfusion injury.

The patient reported here underwent a DCR for a large cerebral infarction, and these events might have diffusely damaged the large and small intracranial vessels, and decreased the CBF because of the SSFS. When collaterals are insufficient, cranioplasty can cause a rapid increase in the bilateral CBF and volume in a chronically dysfunctional brain, resulting in the hyperemia phenomena and subsequent extensive acute cerebral reperfusion injury.

In addition, numerous possible mechanisms related to this complication have been postulated and include: 1) coagulopathy and bleeding tendency, 2) hemodynamic events during and /or after an operation, 3) surgical position, 4) disturbance of venous flow from compression of the jugular vein, 5) massive CSF leakage during surgery, and 6) mechanical shifting of the brain. In this case, there were no abnormal laboratory results, especially coagulation parameters. Moreover, the patient discontinued anti-platelet medication for cerebral infarction 7 days before the cranioplasty. There was no massive bleeding or cerebrospinal fluid leakage during the operation. The patient had stable vital signs and the surgical procedures were performed in the usual manner without any remarkable events during and after the operation. There are a few possibilities that cannot be excluded. Firstly, atrial fibrillation; although echocardiography performed just before the cranioplasty revealed normal systolic function, atrial fibrillation may be a causative factor, because the patient had a history of asymptomatic intermittent atrial fibrillation. Thus, atrial fibrillation could in fact induce a prothrombotic or hypercoagulable state. The second possibility is positional stenosis. Although cerebral angiography after cranioplasty presently revealed no abnormal lesion of vessels (except right ICA occlusion), disturbance of venous flow from the compression of the jugular vein (rotation and flexion of the neck during lengthy surgery result in venous outflow obstruction on the other side) could be another possible causative factor.1)

Various abnormal changes related to a chronically dysfunctional brain with impaired cerebral autoregulation, atrial fibrillation and positional stenosis could result in synergistic effects maintaining blood stasis and result in bilateral multiple hemorrhagic infarctions.

Conclusion

Bilateral diffuse hemorrhagic infarctions following cranioplasty is an extremely rare complication. This is the second reported case of bilateral diffuse hemorrhagic infarctions following cranioplasty. Although the pathogenesis underlying the deleterious cascade of events following cranioplasty remains unclear, an intracerebral hemorrhage might be a re-perfusion complication of cranioplasty. Further research is warranted to clarify and avoid this rare complication.

References

11)    Agarwal D, Rezak K, Hines GL: Positional symptomatic occlusion of the internal carotid artery: evaluation and surgical management. Ann Vasc Surg 22:293-296, 2008

12)    Agner C, Dujovny M, Gaviria M: Neurocognitive assessment before and after cranioplasty. Acta Neurochir (Wien) 144:1033-1040, 2002

13)    Bijlenga P, Zumofen D, Yilmaz H, Creisson E, de Tribolet N: Orthostatic mesodiencephalic dysfunction after decompressive craniectomy. J Neurol Neurosurg Psychiatry 78:430-433, 2007

14)    Cecchi PC, Rizzo P, Campello M, Schwarz A: Haemorrhagic infarction after autologous cranioplasty in a patient with sinking flap syndrome. Acta Neurochir (Wien). 150(4):409-410, 2008

15)    Dujovny M, Agner C, Aviles A: Syndrome of the trephined: theory and facts. Crit Rev Neurosurg 9:271-278, 1999

16)    Dujovny M, Fernandez P, Alperin N, Betz W, Misra M, Mafee M:Post-cranioplasty cerebrospinal fluid hydrodynamic changes: magnetic resonance imaging quantitative analysis. Neurol Res 19:311-316, 1997

17)    Eom KS, Kim DW, Kang SD: Bilateral diffuse intracerebral hemorrhagic infarction after cranoplasty with autologous bone graft. Clin Neurol Neurosurg. 112(4):336-340, 2010

18)    Gaab MR, Rittierodt M, Lorenz M, et al: Traumatic brain swelling and operative decompression: a prospective investigation. Acta Neurochir Suppl 51:326-328, 1990

19)    Gooch MR, Gin GE, Kenning TJ, German JW: Complications of cranioplasty following decompressive craniectomy: analysis of 62 cases. Neurosurg focus 26(6):E9, 2009

10)    Hatashita S, Hoff JT: The effect of craniectomy on the biomechanics of normal brain. J Neurosurg 67:573-578, 1987

11)    Hutchinson P, Timofeev I, Kirkpatrick P: Surgery for brain edema. Neurosurg Focus 22(5):E14, 2007

12)    Isago T, Nozaki M, Kikuchi Y, Honda T, Nakazawa H: Sinking skin flap syndrome: a case of improved cerebral blood flow after cranioplasty. Ann Plast Surg 53:288-292, 2004

13)    J.M Hallenbeck, A.J Dutka, Background review and current concepts of reperfusion injury, Arch. Neurol. 47:1245-1254, 1990

14)    L.H.S Sekhon, M.K Morgan, I Spence, N.C Weber: Chronic cerebral hypoperfusion: pathological and behavioral consequences. Neurosurgery 40:548-556, 1997

15)    Nakamura T, Takashima T, Isobe K, Yamaura A: Rapid neurological alteration associated with concave deformity of the skin flap in a craniectomized patient: case report. Neurol Med. 20:89-93, 1980

16)    Polin RS, Shaffrey ME, Bogaev CA, Tisdale N, Germanson T, Bocchicchio B, et al: Decompressive bifrontal craniectomy in the treatment of severe refractory posttraumatic cerebral edema. Neurosurgery 41:84-94, 1997

17)    Schirmer CM, Ackil AA, Malek AM: Decompressive craniectomy. Neurocrit Care 8:456-470, 2008

18)    Stula D: The problem of the ?inking skin-flap syndrome?in cranioplasty. J Maxillofac Surg. 10:142-145, 1982

19)    Vahedi K, Vicaut E, Mateo J, Kurtz A, Orabi M, Guichard P, et al: Sequential-design, multicenter, randomized, controlled trial of early decompressive craniectomy in malignant middle cerebral artery infarction (DECIMAL Trial). Stroke 38:2506-2517, 2007

20)    Yamaura A, Makino H: Neurological deficits in the presence of the sinking skin flap following decompressive craniectomy. Neurol Med. 17:43-53, 1977