CHAPTER 66 Hemispheric Disconnection Procedures

Definition

Hemispheric disconnection procedures are a group of surgical interventions for chronic epilepsy that are used as alternatives to anatomic hemispherectomy. The common denominator of these procedures is disconnection of the cortical layer of one hemisphere from the contralateral hemisphere and from the deeper structures of the basal ganglia. The term hemispherotomy is frequently used as an alternative expression for the same group of operations. Although the terms hemispheric deafferentation and hemispherotomy imply that the hemispheric tissue is not removed, other techniques such as hemicorticectomy or hemidecortication also disconnect the cortex from the deeper structures but do so by removing the cortex. Preferably, hemispheric deafferentation should be reserved for techniques in which no or very little resection of cortical brain tissue is included.

Development

The first anatomic hemispherectomy was done for glioma surgery by Dandy in 1928,¹ and Krynauw performed the first resection for drug-resistant epilepsy in 1950.² A change from anatomic hemispherectomy, frequently used in the 1950s and 1960s and in which one whole hemisphere was removed (with or without the basal ganglia block), to the less invasive disconnection techniques has taken place since the early 1990s. An important step in the evolution from large resection to large disconnection occurred with development of the technique of functional hemispherectomy, introduced by Rasmussen.³ It included removal of two larger brain segments (temporal lobe and central suprasylvian tissue block), combined with callosotomy and disconnection of the frontal, parietal, and occipital lobes. Although the hemisphere as such is no longer totally removed, the effect of this surgery is functionally equivalent to total hemispherectomy. For the aims of epilepsy surgery, it is not important whether parts of the hemisphere are removed or just disconnected because to achieve a seizure-free outcome, it is sufficient to disconnect the ictogenic cortical part of the hemisphere from its connections to the other hemisphere and the long tracts to the basal ganglia. It makes sense to limit use of the term functional hemispherectomy to Rasmussen’s and Mathern’s techniques.⁴ The latter consists of a large central peri-insular resection, including the basal ganglia block and the temporal lobe, combined with disconnection of the frontal, parietal, and occipital lobes.

After a period of increased use of anatomic hemispherectomy in the 1960s and 1970s, a high rate of late complications was described, such as superficial cerebral hemosiderosis (SCH), occlusion of the foramen of Monro and aqueduct, development of hydrocephalus and its complications,⁵^–⁸ and even fatal outcomes.^3,^9,¹⁰ In 27 anatomic hemispherectomies performed in Montreal between 1952 and 1968 with long-term follow-up, hydrocephalus developed in 52% of patients, 33% from SCH and 19% from other causes. Three of nine patients with SCH died of hydrocephalus.¹¹ SCH is thought to be caused by recurrent minor intracranial bleeding in the large cavity as a result of the resection surgery. Such bleeding may occur after minor head trauma or intermittent rises in intracranial pressure from physiologic events such as sneezing.

Less Resection—More Disconnection

Because of the considerable mortality from these complications, the use of anatomic hemispherectomy decreased until the 1970s, when Rasmussen described an alternative technique based on the observation that in patients with multilobectomies, these complications did not occur. Because the frontal lobe and the parieto-occipital lobe are left in situ, a lower incidence of hydrocephalus and hemosiderosis was expected and later confirmed. Rasmussen demonstrated in his patient series that seizure-free outcome rates after anatomic and functional hemispherectomies were very similar, 83% and 85%, respectively, but the rate of complications from increased intracranial pressure was reduced from 35% to 7%. A lower rate of SCH has been reported for functional hemispherectomy techniques after a follow-up of 20 years.^3,^10,¹² Another approach to avoid these complications was the technique by Adams, who occluded the foramen of Monro, excised the choroidal plexus, and obliterated the subdural space by folding down the dura toward the midline and over the residual basal ganglia.¹³ The hemidecortication and hemicorticectomy techniques¹⁴^–¹⁶ approached the problem of these complications by preserving nearly all of the ventricular system and leaving the cerebrospinal fluid (CSF) space uncontaminated.

It also makes sense to consider hemidecortication and hemicorticectomy separately from disconnection procedures (e.g., transsylvian/transventricular keyhole procedure,¹⁷ Delalande’s vertical parasagittal hemispherotomy, and perisylvian window techniques¹⁸^,¹⁹), which usually include very little brain resection. Differentiation between mostly disconnective procedures and functional hemispherectomies³^,⁴ or decortications, including larger resections, is useful because the latter procedures appear to have a different set of characteristics and disadvantages.

The modern transition to nearly exclusively disconnective techniques started in 1992 after a brief description of two quite different approaches developed independently by Schramm, Delalande, and their colleagues.²⁰^,²¹ This was followed in the mid-1990s by the first patient series treated via perisylvian techniques.¹⁷^,¹⁹ Closely related to Villemure’s technique is a variation of a perisylvian resective approach by Shimizu and Maehara.¹⁸ Among the disconnective procedures, the technique by Delalande and associates (vertical parasagittal hemispherotomy)²² and the transsylvian transventricular keyhole procedures²³ include minimal tissue removal and mostly consist of disconnections. The change to less resective procedures during the past 15 years is being made in many centers, and a number of reports have confirmed the initial results indicating that disconnection procedures are associated with shorter operative time, less blood loss, fewer intraoperative complications, and possibly a lower rate of hydrocephalus.

Indications, Patient Selection, and Timing

Because anatomic hemispherectomy, functional hemispherectomy, hemispherotomy, and hemispheric deafferentation are similarly effective, all are established and very successful methods used to treat drug-resistant epilepsy resulting from diffuse damage to one hemisphere. Such damage is usually associated with hemiparesis, hemianopia, and frequently, delayed cognitive development. The indications, selection of patients, and timing are similar for all variants of these procedures.

Causes

The diagnoses typical in these patients may be grouped into inborn, perinatal, or acquired conditions (Table 66-1) and include Sturge-Weber syndrome (SWS), developmental defects (multilobar cortical dysplasia, polymicrogyria, lissencephaly, hemimegalencephaly [HME]), cystic defects from intrauterine or perinatal infarction or hemorrhage, and hemiplegia-hemiconvulsion-epilepsy syndrome (HHE) (Fig. 66-1). Rasmussen’s encephalitis leads to hemiatrophy, which may also be posttraumatic, postencephalitic, or of unknown origin. The epilepsy syndromes associated with these lesions may include several seizure types occurring with different frequencies. Patients can have up to hundreds of seizures per day or suffer from focal status epilepticus (i.e., epilepsia partialis continua, typical of Rasmussen’s encephalitis).

TABLE 66-1 Etiology of Seizures

Infarct, ischemia, porencephaly	54
Cortical dysplasia, migration disorders	10
Hemimegalencephaly	12
Sturge-Weber syndrome	6
Rasmussen’s encephalitis	15
Hemiatrophy, unclear etiology	7
Postencephalitic, HHE, or other	6
Total	110

HHE, hemiplegia-hemiconvulsion-epilepsy syndrome.

FIGURE 66-1 Magnetic resonance images and computed tomography scans from three typical causes. Upper row, Sturge-Weber syndrome. Middle row, Hemimegalencephaly. Bottom row, Perinatal porencephalic cyst, most likely of ischemic origin. (Copyright J. Schramm, with permission.)

Hemimegalencephaly

Patients with HME usually have an enlarged hemisphere displaying different features of abnormal architecture. Parts of the ventricle may be enlarged, whereas others may be compressed by abnormal brain tissue. There may be pachygyria, polymicrogyria, grossly enlarged gyri, and areas of ectopic gray matter around the ventricle in the white matter (Fig. 66-E1).

FIGURE 66-E1 Magnetic resonance images of hemimegalencephaly in a 17-month-old girl. Note the combination of a thickened brain mantle and an enlarged ventricle. Transsylvian hemispheric deafferentation with a small opercular window resulted in a class I seizure outcome at 36 months.

(Copyright J. Schramm, with permission.)

The cause is commonly a neuronal migration disorder. HME is often associated with seizures that are frequent and intractable. The hemiparesis can be mild or pronounced, and a marked degree of mental retardation is usually present.

Sturge-Weber Syndrome

SWS is a rare congenital disorder with a variable natural history. Its characteristic feature is leptomeningeal angiomatosis, and in a proportion of cases it may be associated with a facial nevus, the latter variant occasionally described as encephalotrigeminal angiomatosis. The clinical syndrome is characterized by a progressive neurological disorder consisting of epilepsy, cortical calcifications, cerebral atrophy, and if the epilepsy is untreatable, frequently the development of mental retardation. Seizures usually develop by the end of the first year, may respond to medical treatment initially, but often become resistant to drugs. The cerebral manifestations generally involve the occipital or parietal cortex, or both, but the entire cortex or large parts of it may be involved; however, the pathologic changes remain restricted to one hemisphere. Epilepsy surgery should be considered for patients with refractory seizures, but one has to differentiate between the need for hemispheric deafferentation and a multilobar or more restricted resection. Hemianopia may be present from the beginning or may develop together with hemiparesis during progression of the epileptic encephalopathy, which is associated with cognitive decline and mental retardation. Children with widespread hemispheric involvement are classic candidates for hemispheric deafferentation. The results from three multicenter series have been reported.²⁴^–²⁶ Seizure-free rates after hemispherotomy were reported to be 100% in 8, 6, and 5 patients.^24,^25,²⁷ In three larger series, rates of 80% to 82% were reported in 12, 28, and 70 patients.^22,^26,²⁸

Rasmussen’s Encephalitis

The origin of Rasmussen’s encephalitis is unknown. The clinical syndrome is characterized by intractable epilepsy and progressive hemiparesis inexorably resulting in hemiplegia, mental decline, and hemispheric atrophy. The median age at onset in a multicenter study of 16 patients was 4.2 years with a range of 2 to 11 years.²⁸ Most of the brain damage occurs during the first 8 to 12 months.²⁹ Progression to hemiplegia or aphasia (or to both) and finally cognitive decline occur invariably. The seizure disorder may begin with generalized seizures, but focal seizures are most frequent and epilepsia partialis continua develops in a large proportion of patients. A characteristic histologic finding is a perivascular infiltrate of T lymphocytes, which is associated with destruction of neurons.³⁰ Seventy-seven percent of 83 patients in that study were seizure free after hemispheric surgery. Once the diagnosis is suspected, the atrophic process may be staged by serial magnetic resonance imaging (MRI).³¹ A difficult decision on when to operate will arise. These patients are classic candidates for hemispheric deafferentation.

Indications

The decision to perform hemispherotomy is straightforward for unihemispheric lesions that are either inborn or occurred around the time of birth and became manifested during infancy or early childhood as frequent and intractable seizures. Hemispherotomy is also indicated for small infants with so-called catastrophic epilepsy, or very severe epilepsy manifested early after birth, usually from severe hemispheric damage or an inborn malformation in which lengthy drug treatment is known to be unsuccessful. The procedure is less frequently performed in adults, generally after long-standing drug-resistant epilepsy.

Why is it possible to have a useful life after such a procedure? The disconnection is performed on a mostly nonfunctional or partly destroyed hemisphere, where language and motor function either have been or will be transferred to the other hemisphere, as is the rule if the damage occurred intrauterinely or perinatally. These patients already have spastic hemiparesis, and although the procedure always results in loss of fine motor control of the hand and occasionally deterioration of gait, the majority of patients are able to walk and even use their arm and hand to a certain degree. Hemispherotomy is associated with a 70% to 80% probability of being seizure free in most series and up to 90% with some causes. Frequently, improvement in cognition and behavioral problems is seen.

Timing

Children with holohemispheric malformations or HME with unilateral severe and continuous seizures may be operated on very early (in our group at 4 months), even without demonstrating classic hemiparesis because it may be difficult to detect early in life and would surely become evident later. If hemiparesis is well established or severe, little motor function will be lost. The timing of surgery in children with a progressive disease such as Rasmussen’s encephalitis is more difficult to determine. Progressive worsening of epilepsy with deteriorating cognitive deficits and increasing hemiparesis may also be found in patients with SWS or HME or after encephalitis. Particularly problematic is the timing of surgery in children older than 7 or 8 years if the language-dominant hemisphere is affected by progressive disease. Some language function may still develop after surgery, even in children between 4 and 7 years of age. Nonetheless, it should not be forgotten that Rasmussen’s encephalitis invariably leads to severe atrophy of the affected hemisphere together with complete hemiplegia and loss of language function. It is not infrequent in many institutions to elect to proceed to surgery at a time when the relentless series of severe epileptic seizures has not caused irreversible damage to the unaffected hemisphere. This outcome may be minimized by accepting earlier surgery and earlier motor loss from surgery and not waiting until the disease process has destroyed the hemisphere. Performing surgery earlier for children with Rasmussen’s encephalitis also increases the chance that the healthy hemisphere may compensate better for the loss of motor (or speech) function from the affected hemisphere.

Another argument in support of hemispheric disconnection is the deleterious effects of frequent seizures on cognition and behavior, as well as other neurological functions. These seizures may be clinically apparent or subclinical. This complex of frequent seizures and neurological decline is sometimes called epileptic encephalopathy, and abolishing it constitutes a legitimate aim for this extensive type of epilepsy surgery. Instead of giving the epileptic encephalopathy a chance to further impair the developmental and cognitive potential of the infant, this approach is particularly applicable when the cause of the epilepsy has been recognized as being untreatable early in the clinical course (such as hemispheric cortical malformations) and when repeated trials of antiepileptic drugs appear useless.

Contraindications

Hemispheric deafferentation is contraindicated if the presurgical evaluation cannot demonstrate that all typical ictal activity originates from the affected hemisphere. A relative contraindication may be seen in patients with independently arising seizures from the so-called healthy hemisphere. Occasional isolated contralateral seizure episodes may be acceptable because they do not automatically result from an independent seizure focus. Bilateral epileptogenic activity may be seen on the electroencephalogram in as many as 75% of patients, but it may be secondary and originate from the diseased hemisphere. Because bilateral involvement may represent an independent seizure focus and not just activity conducted from the diseased hemisphere, it is associated with a somewhat reduced probability of a seizure-free outcome after surgery. Nonetheless, high rates of freedom from seizures ³² can still be achieved,³³ as demonstrated in a large series in which 77% of patients with suspected bilateral disease were found to either be seizure free or have only “minor events.”³⁴

Occasionally, the presence of incomplete hemianopia may be considered a contraindication, especially in older children. However, it has been our experience that patients who have grown up with hemianopia adjust well to this deficit. Mental retardation is no longer considered a contraindication in our institution and others.³⁵

Presurgical Evaluation

The mainstays of the presurgical evaluation are high-quality MRI and video electroencephalographic monitoring of seizures. In most patients, this plus the clinical history is sufficient to establish the indications for surgery. If possible, neuropsychological testing is also performed to be able to quantify any changes that occur after surgery. An intracarotid amobarbital test (Wada test) will frequently be necessary to demonstrate which hemisphere is language dominant and to exclude the presence of dissociated sensory and motor speech areas. With late-onset disease or other progressive disease types in which there are doubts about the hemispheric transfer of language functions, this test will be particularly important. In patients with contralateral ictogenic activity, the Wada test may be helpful for differentiating between ictal activity conducted from the diseased hemisphere and ictal activity arising from an autonomous focus in the “healthy” hemisphere. If the contralateral ictal activity disappears when amobarbital is injected into the affected hemisphere, it is safe to assume that the contralateral activity is a conducted phenomen on and will not adversely affect the prognosis. If Rasmussen’s encephalitis is suspected, it may be necessary to perform a brain biopsy to confirm the diagnosis. The use of implanted electrodes is rarely necessary to establish the indication for surgery. Intradural recordings may occasionally be used to identify the few patients in whom the hemispheric damage seems to be confined to several but not all lobes of the brain for the purpose of identifying those in whom multilobectomy would be sufficient rather than complete hemispheric deafferentation.

Goals of Surgery

Hemispheric deafferentation has three goals: (1) cessation of seizures, (2) relief of the epileptic encephalopathy and neurologic deterioration, and (3) better cognitive development and improvement of behavioral disturbances. Achievement of these goals will lead to better psychosocial development and improved quality of life. Although the second and third goals are very ambitious and cannot be attained in all cases, in some situations this objective is realized when the seizures are eliminated. Elimination of seizures is achieved by completely disconnecting the epileptogenic area, which in these cases refers to all cortex of the affected hemisphere. Disconnecting the cortex is functionally equivalent to anatomic removal. When total cortical disconnection is performed, the results are comparable to those obtained with anatomic hemispherectomy.

Side Effects and Complications

Distinction must be made between expected side effects and unexpected complications. Patients or parents need to be informed about the unavoidable side effects of hemispheric deafferentation: complete hemianopia and loss of some motor function, such as fine pincer movement of the thumb and index finger. The impact of postoperative loss of motor function is influenced by the patient’s preoperative condition. Adverse effects are more severe when the disease develops late and the hemiparesis is mild. In the case of incomplete transfer from the affected dominant hemisphere, severe aphasia may be unavoidable after surgery. Typical risks that patients or parents need to be informed about include lack of success with regard to seizures, need for shunting of CSF, need for transfusions, superficial wound infection or meningitis, or both, and rarely, death.

Surgical Techniques

The various forms of hemispheric deafferentation surgery currently in use all evolved from Rasmussen’s functional hemispherectomy technique. The principle behind this surgery is to forgo anatomic removal of brain tissue by instead disconnecting brain regions. One of the early variations of Rasmussen’s method was developed by Mathern’s group in Los Angeles.⁴ This procedure involved performing a large resection of the operculum, insula, underlying basal ganglia, and temporal lobe to achieve a functional hemispherectomy. An intermediate step short of a pure deafferentation procedure involves perisylvian techniques in which only restricted parts of the opercula (Fig. 66-E2D), corona radiata, or temporal lobe are resected. This is usually combined with disconnection of the frontal and parieto-occipital lobes and callosotomy, which is performed from within the ventricular system.^17,^18,³⁶ The latest versions of these evolving procedures are two disconnection operations that involve little or no brain removal and extensive disconnections: transsylvian keyhole hemispheric deafferentation^21,²³ and central vertical hemispherotomy (Fig. 66-2).^20,²²

FIGURE 66-2 Schematic coronal views of the perisylvian and disconnection techniques. A, Step 1 of the transsylvian/transsulcal keyhole approach to the ventricle.²³ B, Step 2 of the transsylvian/transventricular keyhole approach: facultative temporomesial resection, removal of the insular cortex, and paramedian callosotomy. C, Peri-insular window technique.³⁶ D, Japanese variant of the peri-insular window technique.¹⁸ E, Vertical parasagittal hemispherotomy.²²