Cerebellar hemorrhage as a complication of temporal lobectomy for refractory medial temporal epilepsy: report of three cases

Hemorragia cerebelar como complicação de lobectomia temporal para epilepsia do lobo temporal medial: relato de três casos

Luciano de Paola André R. Troiano Francisco M.B. Germiniani Patrícia Coral Marcus V. Della Coletta Carlos E.S. Silvado Marlus Moro João Cândido de Araújo Maria Joana Mäder Lineu C. Werneck About the authors

Abstracts

Cerebellar hemorrhage is listed among the potential complications following neurosurgical pro ce dures. In this scenario it is usually reported as a rare condition. However, it seems that epilepsy surgery pa tients are somewhat more prone to this kind of complication, compared to other surgical groups. Head po si tioning, excessive cerebral spinal fluid draining and the excision of non-expanding encephalic tissue (or combinations among the three) are likely to be cause underlying remote cerebellar hemorrhage. Out of the 118 ATL/AH performed at our institution, between 1996 and 2002, we identified 3 (2.5%) patients pre sen ting with cerebellar hemorrhage. We report on such cases and review the literature on the topic.

cerebellar hemorrhage; epilepsy surgery; neurosurgical complications


A hemorragia cerebelar faz parte das potenciais complicações dos procedimentos neurocirúrgicos. De forma geral, é considerada uma condição rara. Entretanto, há aparente propensão dos pacientes sub metidos ao tratamento cirúrgico de epilepsia em apresentar este tipo de complicação, quando compara dos com outros grupos cirúrgicos. O posicionamento da cabeça, excessiva drenagem de líquido cefalorraquidiano e a excisão de tecido cerebral não expansível (ou talvez combinações entre os três) constituem as po ten ciais causas da hemorragia cerebelar remota. Entre os 118 pacientes em nossa série de LTA ¼ AH, identifi camos 3(2.5%) casos de hemorragia cerebelar. Relatamos os três casos desta natureza, com revisão da lite ratura pertinente a esta complicação.

hemorragia cerebelar; cirurgia de epilepsia; complicações neurocirúrgicas


Cerebellar hemorrhage as a complication of temporal lobectomy for refractory medial temporal epilepsy: report of three cases

Hemorragia cerebelar como complicação de lobectomia temporal para epilepsia do lobo temporal medial: relato de três casos

Luciano de PaolaI, II; André R.TroianoIII; Francisco M.B. GerminianiI; Patrícia CoralI, II; Marcus V. Della ColettaI; Carlos E.S. SilvadoI, II, IV; Marlus MoroV; João Cândido de AraújoV; Maria Joana MäderVI; Lineu C. WerneckI, VI

Programa de Cirurgia de Epilepsia, Serviço de Neurologia, Hospital de Clínicas da Universidade Federal do Paraná, Curitíba PR, Brasil (UFPR)

IMédico Neurologista

IINeurofisiologista Clínico

IIIMédico Residente em Neurologia

IVProfessor Adjunto de Neurologia

VProfessor Adjunto de Neurocirurgia

VIPsicóloga

VIIProfessor Titular de Neurologia

ABSTRACT

Cerebellar hemorrhage is listed among the potential complications following neurosurgical pro ce dures. In this scenario it is usually reported as a rare condition. However, it seems that epilepsy surgery pa tients are somewhat more prone to this kind of complication, compared to other surgical groups. Head po si tioning, excessive cerebral spinal fluid draining and the excision of non-expanding encephalic tissue (or combinations among the three) are likely to be cause underlying remote cerebellar hemorrhage. Out of the 118 ATL/AH performed at our institution, between 1996 and 2002, we identified 3 (2.5%) patients pre sen ting with cerebellar hemorrhage. We report on such cases and review the literature on the topic.

Key words: cerebellar hemorrhage, epilepsy surgery, neurosurgical complications.

RESUMO

A hemorragia cerebelar faz parte das potenciais complicações dos procedimentos neurocirúrgicos. De forma geral, é considerada uma condição rara. Entretanto, há aparente propensão dos pacientes sub metidos ao tratamento cirúrgico de epilepsia em apresentar este tipo de complicação, quando compara dos com outros grupos cirúrgicos. O posicionamento da cabeça, excessiva drenagem de líquido cefalorraquidiano e a excisão de tecido cerebral não expansível (ou talvez combinações entre os três) constituem as po ten ciais causas da hemorragia cerebelar remota. Entre os 118 pacientes em nossa série de LTA ¼ AH, identifi camos 3(2.5%) casos de hemorragia cerebelar. Relatamos os três casos desta natureza, com revisão da lite ratura pertinente a esta complicação.

Palavras-chave: hemorragia cerebelar, cirurgia de epilepsia, complicações neurocirúrgicas.

Anterior temporal lobectomy (ATL) and amygdalohippocampectomy (AH) are effective treatment alternatives in patients with temporal lobe e pi le psy refractory to medical treatment. Neu ropsy chological disturbances (language and memory) are the most common post-operatory derangements. Nevertheless, surgical complications are rarely ex pec ted, both locally and at remote sites. Recent pa pers have shed some light on the relative high fre quency of cerebellar hemorrhage in patients submitted to anterior temporal lobectomy, when compared to other surgical groups. It seems that ATL/AH pa ti ents are particularly prone to this kind of complication. At our institution ATL / AH are always performed using the same surgical technique (that is, a trans-temporal approach). Out of the 118 ATL / AH performed at our institution we were able to iden tify 3(2.5%) patients presenting with cerebellar hemorrhage. Their cases are reported.

CASES

Patient 1. A 31 year-old male patient, presenting with a seizure disorder starting at the age of 9 y/o, cha ra cterized by an aura (epigastric sensation), shortly followed by a complex partial seizure and on occasion a ge ne ralized tonic-clonic seizure. He was tried on pheno barbital and carbamazepine, with unsatisfactory seizure con trol. A combination of valproic acid, phenytoin and clo ba zam ultimately led to control of the secondarily ge ne ra lized seizures. The complex partial seizures still oc cur red many times per week. Physical and neurological exa minations were normal. An electroencephalogram (EEG) showed left temporal interictal spikes and a brain mag netic resonance image (MRI) disclosed left hippocam pal atrophy, consistent with the diagnosis of mesiotempo ral sclerosis (MTS). During videoeletroencephalographic (VEEG) monitoring, 3 complex partial and 1 secondari ly generalized seizures were recorded from the left me si o temporal lobe.

He was then admitted to undergo left ATL. There we re neither metabolic nor coagulation disorders, as veri fied by normal platelets count and PT / aPTT values. While supine with his head turned to the right, the pa ti ent underwent a craniotomy for a left 3 cm ATL and 3.5 cm AH. At the end of the surgery, a subgaleal suctor drain was placed. Pathology was confirmatory of hippo campal sclerosis.

In the immediate post-operatory (PO) period, he was observed in the Intensive Care Unit (ICU) with an i ni tial Glasgow Coma Scale (GCS) of 10. On the second day at the ICU he was still judged as "unusually drowsy and dysarthric". On the 3rd PO day a brain computed to mo graphy (CT) scan disclosed multiple foci of cerebellar hemorrhage, predominantly on the right cerebellar he mis phere, but no surgical drainage was necessary (Fig 1). A cerebral angiographic study was normal.


In the 9th PO day the patient developed a liquoric fistula and fever. A cerebrospinal fluid (CSF) study showed 21 red cells/mm3, 7680 leucocytes/mm3, 80% neutrophils, glu cose 1mg/dL and proteins 404mg/dL. He was put on ce fe pime for 14 days, after which CSF showed 58 red cells/mm3, 19 leucocytes/mm3, 87% lymphocytes, gluco se 39 mg/dL and proteins 124 mg/dL. He was discharged on the 24th PO day, without significant coordination im pairment and later returned in the out-patient clinic for re evaluation of his seizures. He remained seizure-free on antiepileptic drugs (AEDs) for approximately twelve mon ths, after which he experienced seizure recurrence. Drug adjustments were unsuccessful. A follow-up CT scan performed on the 28th PO day showed resolution of the hemorrhage on both cerebellar hemispheres.

Patient 2. A 37 year-old female patient with a seizure disorder starting at the age of 13 y/o, consisting of complex partial seizures with frequent secondary generaliza tion. Her best AED combination was sodium valproate and carbamazepine, when she presented with complex par tial seizures 2 to 3 times per week and infrequent secondarily generalized seizures. Other combinations or a regime including higher doses invariably lead to intolerable side effects. Past and familial history were unremarkable. EEG disclosed right temporal interictal epileptiform discharges. Brain MRI showed right hippocampal atrophy consistent with MTS. She was submitted to VEEG and two of her typical complex partial seizures were re cor ded from the right temporal lobe.

She then underwent right ATL. Pre-operative metabolic and coagulation studies were normal. While supine with her head turned to the left, a right craniotomy was per formed for right ATL and AH, using the vein of Labbé as the posterior margin for the resection, that is, approximately a 6cm resection from the temporal tip . At the end of the surgery, a subgaleal suctor drain was placed.

After surgery, consciousness recovery was normal and she presented with no deficits. In the 2nd PO day, the patient presented with headache, nausea and vomiting. Fundoscopy was normal, as well as, motor and coordination tests. Brain CT scan showed laminar right hemisphere cerebellar hemorrhage (Fig 2). A neurosurgery consult was requested and the option was for clinical treat ment. The patient received analgesic and antiemetic treatment and was discharged four days later. At discharge she was asymptomatic with a normal physical and ne uro logical exam. A control CT scan performed on the 4th PO day showed partial resolution of the hemorrhage.


Patient 3. This is a 38 year-old male patient, presenting with a seizure disorder starting at the age of 7 y/o, cha rac terized by an aura ("light-headedness" sensation), shortly followed by a complex partial seizure with se condarily generalization. He was tried on phenytoin, val proic acid, lamotrigine, clobazam and clonazepam, with unsatisfactory seizure control. A combination of carbamazepine and phenobarbital led to a better control of the generalized seizures, whereas complex partial seizures still occurred monthly, usually in clusters of up to four seizures a day. Physical and neurological examinations were normal. An EEG showed left temporal in terictal spikes and a brain MRI disclosed left hippocampal atrophy, consistent with the diagnosis of MTS. During VEEG monitoring, 6 complex partial seizures were recorded from the left mesiotemporal lobe.

He was then admitted to undergo left ATL. There were neither metabolic nor coagulation disorders. While su pine with his head turned to the right, the patient un de rwent a craniotomy for a left 3 cm ATL and 3.5 cm AH. A subgaleal suctor drain was placed.

At the ICU, in the immediate PO, he presented with a GCS of 8, aphasic and had a generalized tonic-clinic sei zure. Diazepam 5 mg was administered intravenously, as well as, a bolus of manitol, with improvement of cons ciousness. A skull CT scan disclosed laminar cerebellar hemorrhage, more prominent on the left cerebellar hemisphere (Fig 3). Once again, no surgical drainage was ne ces sary. On the 7th PO day he was discharged, with no further cerebellar signs. He later returned in the out-pa tient clinic for reevaluation of his seizures and he has re mained seizure-free on AEDs for seven months. A follow-up CT scan was obtained on the 30th PO day, showing good resolution of the cerebellar hemorrhage.


DISCUSSION

Although infrequent, cerebellar hemorrhage may be a potential complication following neurosurgical interventions. Nevertheless, its development at a distant site from the operative incision is de finitively a rare situation to which attention has be en drawn only in the past few years. In a retrospective survey of 4992 intracranial procedures, Kal fas and Little1 found 40 patients (0.8%) to present hemorrhages, 33 of them at the operative site (intracerebral, epidural, subdural or intrasellar) and 7 at a distant location. The most common etiology that led to surgical treatment was brain tu mor in 56%, with meningioma as the leading pa tho lo gical type.

A group analysis of 37 cases of remote intracerebral hemorrhage conducted by Brisman et al.2 (5 patients from their own series and 32 reviewed from the literature) included supratentorial hemor rhages in infratentorial craniotomies and the re verse. Seventy-eight percent of patients had symptoms suggestive of acute intracranial hypertensi on in the first few hours after surgery. In the setting of infratentorial hemorrhage, 81% of the pa tients underwent access through the deep sylvian fis sure and paraclinoid regions. The cerebellar vermis was the focus in 67%. Such derangements we re not related to hypertension, coagulopathies or the volume of cerebrospinal fluid drainage. Four teen percent of patients from this heterogenic sam ple were disabled, and 32% died.

The specific concern of cerebellar hemorrhage after epilepsy surgery is illustrated by the reports of Toczek et al. and Yacubian et al. The former presented four patients treated with ATL and/or AH who presented uni or bilateral cerebellar hemorrha ge 1 to 4 days after surgery3. Blood pressure, plate lets count and coagulation were normal in all pati ents except for one, promptly treated with anti-hy per tensive drugs. Varying amounts of cerebros pinal fluid drained in the PO period (215 to 525mL) was reported as the only potentially implicated factor. One patient had a ventricle drain placed to compensate hydrocephalus, the others needed nothing but conservative measures. All of them had normal neurological examinations at one month follow-up. A series of three patients submitted to ATL/AH found similar results both on patient profi le and clinical outcome. One patient did not have his lateral ventricles opened or a suctor drain in the post-operative period4.

Doubt about the timing of cerebellar hemorrhage, whether intra or post-operatory, was fed by dis cordant data on patients who did not recover cons ciousness after surgery and those who, after awaking from anesthesia, re-entered coma state or developed cerebellar signs. This issue was addres sed by Honegger et al. with data from a neurosurgical institution in which all patients are routinely CT scanned in the first hour after surgery5. Of 1650 patients who undergone supratentorial craniotomy over a three-year period, 10 had cerebellar hemorrhage. Seven of these had been submitted to ATL/AH. In addition, out of the original ten, seven patients had an initial normal CT scan, an indicator that posterior fossa bleeding appeared over the next few hours following surgery (mean time for diagnosis: 7 hours and 35 minutes).

Systemic hypertension, the top-ranking etiologic factor of spontaneous cerebellar hemorrhage, is not related to this entity. Apparently, the sa me applies to coagulation disorders and anticoagulant treatment. Sodium valproate was once bla med as a cause to peri-operatory excessive ble eding, but even this remote cause has been recently questioned in the literature6.

Positioning of the patient during surgery might play a secondary role in increasing venous pressure over the posterior fossa. Seoane and Rhoton7, in an elegant microsurgical anatomical study in adult cada veric specimens, showed unilateral jugular com pression, to the point of occlusion, by transver se process of C1 when the head is turned contrala teraly. That perhaps would be sufficient explanation if remote cerebellar hemorrhage was secondary to virtually any surgical access based on head til ting, which certainly does not hold true on neurosurgical routine. Nevertheless, we still lack a better hypothesis, since evidence shows that most su pra tentorial approaches other than epilepsy surgery do not present with cerebellar bleeding. Plus, ac cording to Kalfas and Little, the recumbent position does not seem safer than the sitting position in preventing posterior fossa bleeding1.

The most accepted theory to date underlying re mote cerebellar hemorrhage is an association bet ween liquor overdraining and the excision of non-expanding encephalic tissue. ATL/AH is commonly carried out with opening of lateral ventricles and sub sequent CSF flow. Intracranial drains and suctors are part of the post-operative protocol in various institutions. Moreover, removal of a brain tu mor would cause supratentorial pressure to return to near normal values, but lobectomy is an adjunct fac tor to create a gradient between supra and infratentorial compartments. Such pressure gradient may act as a suction mechanism over the cappilary veins of cerebellum, which are then traumatized, leading to intraparenquimatous bleeding4,5. The association of fluid overdraining and removal of non-tumorous tissue is specially prone to happen in epilepsy surgery, and this might be the reason why such complication is infrequently seen involving other neurosurgical approaches.

In conclusion, cerebellar hemorrhage in post-o pe rative supratentorial craniotomy for epilepsy sur gery constitutes a rare complication and its phy siopathology is yet to be entirely understood. So me patients may not even present with clear symptomatology, and hyperdense signals on posterior fos sa may be an occasional finding in follow-up CT stu dies. Treatment of such complication is similar to that of nontraumatic cerebellar hematomas and must be individualized. Most cases are associated with an excellent outcome.

Received 6 October 2003, received in final form 9 January 2004. Accepted 9 February 2004.

Dr. Luciano De Paola - Programa de Cirurgia de Epilepsia/Serviço de Neurologia - Hospital de Clínicas UFPR - Rua General Carneiro 181/3º andar - 80060-900 Curitiba PR - Brasil.

  • 1. Kalfas IH, Little JR. Postoperative hemorrhage: a survey of 4992 intracranial procedures. Neurosurgery 1988;23:343-347.
  • 2. Brisman MH, Bederson JB, Sen CN, Germano IM, Moore F, Post KD. Intracerebral hemorrhage occurring remote from the craniotomy site. Neurosurgery 1996;39:1114-1121.
  • 3. Toczek MT, Morrell MJ, Silverberg GA, Lowe GM. Cerebellar hemorrhage complicating temporal lobectomy: report of four cases. J Neurosurg 1996;85:718-722.
  • 4. Yacubian EM, Andrade MM, Jorge CL, Valério RM. Cerebellar hemorrhage after supratentorial surgery for treatment of epilepsy: report of three cases. Neurosurgery 1999;45:159-161.
  • 5. Honegger J, Zentner J, Spreer J, Carmona H, Schulze-Bonhage A. Cerebellar hemorrhage arising postoperatively as a complication of supratentorial surgery: a retrospective study. J Neurosurg 2002;96:248-254.
  • 6. Ward MM, Barbaro NM, Laxer KD, Rampil IJ. Preoperative valproate administration does not increase blood loss during temporal lobectomy. Epilepsia 1996;37:98-101.
  • 7. Seoane E, Rhoton AL. Compression of the internal jugular vein by the transverse process of the atlas as the cause of cerebellar hemorrhage after supratentorial craniotomy. Surg Neurol 1999;51:500-505.

Publication Dates

  • Publication in this collection
    20 July 2004
  • Date of issue
    June 2004

History

  • Accepted
    09 Feb 2004
  • Reviewed
    09 Jan 2004
  • Received
    06 Oct 2003
Academia Brasileira de Neurologia - ABNEURO R. Vergueiro, 1353 sl.1404 - Ed. Top Towers Offices Torre Norte, 04101-000 São Paulo SP Brazil, Tel.: +55 11 5084-9463 | +55 11 5083-3876 - São Paulo - SP - Brazil
E-mail: revista.arquivos@abneuro.org
Accessibility / Report Error