Temporal-lobe seizures with additional loci treated by resection J o a n M. VAN BUREN, M.D., PH.D., COSIMO AJMONE MARSAN,M.D., AND NAOMI MUTSUGA, M.D.

Surgical Neurology Branch and Electroencephalography and Clinical Neurophysiology Branch, National Institute of Neurological and Communicative Disorders and Stroke, National Institutes of Health, Bethesda, Maryland The authors describe the use of temporal lobectomy following careful and repeated electroencephalogram (EEG) evaluation (with implanted electrodes in otherwise unresolvable cases) in the epileptic group characterized by automatisms (psychomotor seizures) with temporal epileptiform activity complicated by EEG loci in the opposite temporal lobe or by extratemporal activity. They found that this can render a significant number of patients (between 25% and 50%) either seizure-free or with significant and useful reduction in their seizure frequency. The cure and improvement rates of cases followed up after temporal resection with or without prior study with implanted electrodes were approximately equal. However, the implanted electrodes permitted surgical treatment of certain cases which would have been rejected on the basis of evidence derived from the scalp recordings alone. Of 28 of these 34 patients with persisting EEG epileptiform activity in the postoperative period, only one had such activity in a different location in a follow-up period of 6 years. No evidence of spreading epileptic activity or appearance of"mirror foci" was seen during a follow-up period averaging 8.2 years. Seizure remission up to 15 years with eventual recurrence of the original seizure type may occur following surgical therapy. Follow-up studies of surgical epileptic treatment of less than 3 to 5 years are of doubtful value. KEY WORDS 9 epilepsy 9 mirror foci 9 t e m p o r a l - l o b e epilepsy depth e l e c t r o d e s 9 surgical t r e a t m e n t o f e p i l e p s y

EMPORAL-LOBE epilepsy is often considered a well-defined entity which is characterized by epileptic automatisms following a visceral or psychical aura with an epileptic focus localized in one temporal lobe on the electroencephalogram (EEG). Since the automatisms provide a serious socioeconomic handicap and often are resistant to medication, 12a~ surgical therapy should be considered. In these otherwise untreatable patients, temporal lobectomy in properly

T

596

9

selected cases is followed by a substantial number o f instances o f cure or improvement with a low rate of complications. In practice, the matter of surgical selection may not be easy since the "temporal-lobe s y n d r o m e " frequently shows wide variation in individual cases and the prognostic significance of these variations remains uncertain. Particularly troublesome is the finding of epileptiform activity on the E E G not only in one but in both temporal lobes a n d / o r

J. Neurosurg. / Volume 43 / November, 1975

Resection for temporal-lobe seizures TABLE 1 Factors of possible etiological significance in 34 cases of temporal lobe seizures*

Factor positive familyhistory labor complications cyanosis severe head deformity infantile hemiplegia delayed development febrile fits (l-10 yrs) closed head injury unconscious (rain) unconscious (hrs) CNS infections encephalitis suppurative

Implant (Case Nos.)

Non-implant (Case Nos.)

59

59, 40, 52, 105

--

11, 43

29 32 15, 32, 146

52 52 55 19, 21, 30, 43, 49, 132

15, 57, 266 197

52

---

49 37

Total 4 3 2 2 9 5 2

* Implant=cases in which implanted electrodes were employed in addition to scalp and nasopharngeal EEG recording prior to operation. Non-implant=cases studied with EEG recording alone. CNS=central nervous system.

combinations of temporal epileptiform activity accompanied by similar activity from extratemporal sites. In practice one tends to proceed with resection if a preponderance of activity arises from one temporal lobe and the remaining features of the case provide adequate indication. In a number of medically untreatable and seriously handicapped individuals, bitemporal and/or temporal-extratemporal EEG evidence appears without a definite preponderance. In these instances we have employed depth electrodes for further study. When a region of maximal activity has appeared from these studies, we have proceeded with the resection. This report presents the late follow-up results of 34 patients who were selected on the basis of the presence of independent bitemporal and/or extratemporal epileptiform activity and underwent temporal craniotomy. In 17 cases implanted electrodes were required to establish the definite preponderance of epileptiform discharges in one temporal region required for surgical exploration.

patients who were considered to have only a minimal handicap, only three achieved a work level of a skilled or lower white-collar worker. Perhaps contributing to these employment difficulties, various psychiatric symptoms were encountered in 12 patients (six poor emotional control, two destructive or assaultive, three depression, one hypochondriasis), Etiological factors of possible significance are shown in Table 1. Medication

In the preoperative period medication was not uniform, but was commonly centered on combinations of Dilantin and phenobarbital in generally accepted dosages. With the exception of two patients (Cases 13 and 109) who respectively received phenobarbital and Mysoline, all other patients received combinations of medication (Table 2). Since the patients were operated on between 1956 and 1968, reliable information regarding the blood levels of antiepileptic drugs was not available. Clinical Material and Methods As has been noted by others, medication was successful in suppressing generalized Patient Selection seizures for periods of years in six cases. In Patients were referred for surgical con- only one instance, however, was it possible by sideration after they had proved refractory to medication to suppress the automatism of a long trial of medication. All 34 patients temporal lobe epilepsy for a period of over a suffered socioeconomic difficulties. Of the five year. J. Neurosurg. / Volume 43 / November, 1975

597

J. M. Van Buren, C. Ajmone Marsan and N. Mutsuga TABLE 2 Preoperative medication in 34 cases of temporal lobe seizures

Implant (Case Nos.)

Medication* phenobarbital Mysoline D,-'lantin -~ phenobarbital Mysoline q- phenobarbital Dilantin q- Mysoline Dilantin q- Mysoline q- phenobarbital other medication total

Non -implant (Case Nos.)

Total

109 1 13 1 15, 32, 51,146, 148,250, 259 11, 17, 24, 43, 49, 52 13 197 132 2 29, 11l, 202 3 57, 230, 253 14, 21, 30, 37, 55 8 59, 266

19, 40, 105, 133

6 34

* Dosages =phenobarbital 100 mgq- ; Mysoline= 750 mgq- ; Dilantin= 300 mgq-. Other medication includes dosages of these drugs in various combinations below the given levels with or without other medication. Preoperative Seizure Evaluation

84 multiple-contact depth electrodes) has been rather reassuring. No serious infection The patients' workup consisted of neurohas been encountered. After nearly 20 years' logical examination, along with plain x-ray experience with implanted diagnostic elecfilms of the skull, carotid arteriography, and trodes without hemorrhagic complication, a p n e u m o e n c e p h a l o g r a p h y with particular recent subdural hematoma with residual attempts to visualize adequately the tempbrain-stem damage forcibly reminds us that oral horns. The electroencephalographic exthe decision to use diagnostic electrodes can amination, with the standard 10-20 system 11 never be taken lightly. including basal leads in all cases, consisted of repeated records during wakefulness and Electrodes for Chronic Implantation sleep, on medication, after withdrawal of The type of electrode sets used is shown in medication, and, in certain instances, of Fig. 1. A needle-and-flap electrode used in observation of spontaneous or Metrazolinduced seizures. The use of Metrazol has earlier studies, consisting of a 4-cm rigid neegradually diminished over the last 5 years in dle with four recording ports starting at the our clinic and now it is rarely employed. Par- tip and continuing at l-cm intervals, was an ticular attention, however, was paid to spon- integral part of the seven-contact electrode taneous seizures and the cases in which set. The needle was inserted with a longseizures were observed electrographically are shafted instrument with a small clamp on the end. The long handle assisted in aligning the indicated by asterisks in the tables. electrode. The electrode position was controlled by a small pneumoencephalogram. Depth Electrode Studies The flap electrode was slipped into the Depth electrodes have been used in our epidural space with a probe inserted into a clinic only as a last resort when the medical pocket (like the toe of a slipper) on the back treatment appeared to be a failure, the of the electrode to guide it under the socioeconomic situation was most pressing, calvarium. Subdural insertions are rarely and routine EEG recording from the scalp used (except along the midline or undersurshowed either prominent bitemporal indepen- face of the brain, where an epidural position dent involvement a n d / o r temporal plus ex- cannot be used) due to the hyperemia and t r a t e m p o r a l activity without a definite reaction of the cortex to the foreign body, preponderance of side a n d / o r lobe. In princi- with the consequent possibility of producing a ple, the electrodes were not left in place for further potentially epileptogenic scar. long periods (never over 2 weeks). Current practice is to insert a nine-contact Concerning possible risks, our general ex- recording electrode stereotaxically, ~2 then perience in a total of 67 patients with im- place one or more of the flap electrodes (four planted electrodes (141 epidural and 24 sub- contacts at l-cm intervals) in the epidural dural multiple-contact surface electrodes, and space. The electrode contacts are platinum598

J. Neurosurg. / Volume 43 / November, 1975

Resection for temporal-lobe seizures iridium and consist of 7-mil Teflon-insulated wire* wound about a central 9-mil wire with a terminal ring to permit attachment of the electrode to the stereotaxically-guided probe during insertion. The flap is of segmented polyurethane (Lycra), with platinum-iridium contacts. Initial experience with stainless steel electrodes was unsatisfactory, due to the appearance of spurious potentials which appeared after sterilization, and especially with cleaning and reuse of the electrodes.

Electrode Implantation The selection of a target for implantation was determined largely by the electroencephalographic evidence. Thus, if approximately equal epileptiform activity appeared in both temporal lobes, epiduralflap electrodes were placed on the temporal convexity and a depth-recording electrode directed toward the amygdala on both sides except as mentioned below. Prior to the use of stereotaxic methods, freehand placements showed the expected variations when evaluated by x-ray study after placing air in the tips of the temporal horns. The variations, however, clustered about the amygdala to include this structure, the anterior pes hippocampi, uncus, and temporal tip a few millimeters anterior to the amygdala. The depth of insertion from the temporal surface was adjusted (4.0 to 4.5 cm) so that the terminal electrodes were in or straddled the mesial temporal cortex. Eleven patients were studied with epidural flap electrodes on the temporal convexity and depth electrodes that were directed toward the amygdala due to the approximately symmetrical bilateral temporal epileptiform activity (Cases 15, 29, 51, 59, 111, 148, 197, 202, 230, 259, 266). Three were studied with unilateral placement of an electrode in the amygdala and epidural flap electrodes in the frontal and temporal regions on the same side (Cases 13, 32, 253). Two had epidural flaps placed in the temporal and frontal regions on one side (Cases 110, 250), and one (Case 146) had bilateral depth placements in the pes hippocampi and epidural temporal-flap electrodes. *Insulated wire obtained from Med Wire Corporation, 121 South Columbus Avenue, Mount Vernon, New York.

J. Neurosurg. / Volume 43 / November, 1975

FI~. 1. Upper: Nine-contact platinum iridium electrode, Teflon-insulated, with wrapped contacts at 5-mm intervals and the needle-and-flap combined electrode for temporal lobe surface and depth recording. The needle has four contacts at lcm intervals on the shaft and three contacts on the Lycra flap. Center: The flap is reversed to show the pocket at the tip in which a probe can be inserted to facilitate placement. A four-contact flap without the needle side arm is also used. Lower: The leads are held by a small nylon clamp secured about the electrode by a screw on either side and sutured to the scalp by a fine stainless steel suture.

Surgical Technique In general, surgery was carried out under local anesthesia according to Penfield's technique. 18-18 Electrocorticography (ECoG) 1 was performed routinely. In the initial cases operated by the late M. Baldwin resections were often limited to the areas of ECoG paroxysmal abnormalities.

Pathology No report was currently available in six cases and no obvious pathology was found in 599

J. M. Van Buren, C. A j m o n e Marsan and N. M u t s u g a one case. Gliosis was the most common pathological diagnosis in 20 of the remaining 27 cases. This was most commonly manifested by fibrous transformation of the astrocytes in the cortical layers II-IV, which was apparent on the gold chloride sublimate and the phosphotungstic acid stains. Fat stains (oil red O) in some instances showed lipid material. Tlais usually lay in the perivascular spaces but occasionally small flecks of material staining as lipid were seen

within the cortical neurons. Occasional samples showed small perivascular accumulations of mononuclear cells similar to the findings reported by Rasmussen and McCann 2~ in their epileptic patients. In our study there was little clinical evidence that this was related to a previous symptomatic encephalitic process. Tissue sampling was limited, in general, to the lateral and inferior aspects of the temporal lobe since the mesial structures (uncus, amygdala, and hippocam-

TABLE 3

Patients operated on on the basis of EEG localization* Yrs. of Pre-op Seizures

Seizure Type[

Positive Pre-op EEG's

11 14

A A

11./14 12/12

49 46 36 132 32 27 Cases with l + y r seizure rem~sion 14 35 24 37 29 17

G A

105

25

109 133

14 25

Case No.

Age at Operation

Seizure-free cases 21 15 24 54

EEG Focusw Maximal

Also Active

Temporal Resection Size Side (cm) Medial It rt

5 5

+ +

7/9 14/41

Ts, Pg2** F7, T3, T6,** P4, O5 T4, T6, Pg2 T~, Ts, Pgl Fs, T4, Pg~ F;, T3, F4, C4

rt rt

4 8

+ +

A A

10/'20 20/20

1"4 FT, Pg]

18

A

19/23

10 3

A A

Cases without seizure remission 11 17 10

FT, Ta, Pgl Fs, 3"4

rt It

4

FT, T~, Pgl

FT, Ts** F~, Ta, T4.** ag~ T4**

It

14/14 16/16

Ta, T6 Fs, T4

F8, T3 FT, T~

rt rt

4 (partial) 6 3 (partial)

4

ll/ll

FT, Ta

2"4, Ts**

It

4

--

12/'12

FT, T3, F3, C.~ Fs, T4, T6

F8, T4, F4**

It

Fpl, Fp~,** F~, F4 T3 FT, T4, T.~** No max T~, T4, Ts, T6, 02 Fs, T4, Pg~ FT, Tu, C4 Fs, T4, Pg2 FT, T3 Fs, T4, Pg~ FT, T3, Pgl

rt

3 (partial) 6

It It

4

17

14

4

G head It G

19

15

9

G It A

19/19

30 40

27 23

13 10

A A

29/29 12/14

43 52 55

23 29 36

20 16 32

A A G A

23/24 16,/16 9/9

rt rt rt

5

6

5 8 5 (partial)

+

o ? + +

? o

* In the column headings "Seizure type" refers to the predominant type of seizure. "Positive" EEG's indicate the presence of epileptiform activity. "Final seizure reduction" is given as the percent of preoperative seizure frequency. "Remission" indicates lack of attacks with loss of consciousness or motor activity. The temporal resection was quantitated in terms of the cm of resection measured from the anterior tip of the temporal fossa. A "total" resection indicates removal of the first, second, and third temporal gyri, fusiform, and hippocampal gyri, while a "partial" resection spares one or more of these structures. "Medial" indicates the removal ( + ) or lack of it (--) of the amygdala, uncus, and hippocampus. f A = A u t o m a t i s m ; G = Generalized seizure. ~t Discharges at new localization and lateralization. w Electrode nomenclature from Standard International 10-20 System. ** Seizure (s) recorded.

600

J. Neurosurg. / Volume 43 / November, 1975

Resection for temporal-lobe seizures pus) were c a r e f u l l y r e m o v e d f r o m the m e s i a l p i a b y suction to a v o i d p o s s i b l e d a m a g e to the o c u l o m o t o r n e r v e which lies i m m e d i a t e l y below. Thus, c o m m e n t c a n n o t be m a d e reg a r d i n g h i p p o c a m p a l a b n o r m a l i t i e s such as "mesial temporal sclerosis." F i v e cases w e r e classified as h a m a r t o m a s . T h e s e lesions c o n s i s t e d o f d i s r u p t i o n o f the n o r m a l c o r t i c a l a r c h i t e c t u r e , i n v a s i o n o f glial cells, a n d in s o m e c a s e s calcification. T h e single instance of a tumor (ependymo-

a s t r o c y t o m a ) m a y well h a v e b e e n m i s d i a g nosed a n d m a y a c t u a l l y h a v e fallen in t h e h a m a r t o m a g r o u p . This p a r t i c u l a r c a s e h a s been f o l l o w e d for 8 y e a r s w i t h o u t c l i n i c a l evidence o f an e x p a n d i n g p r o c e s s a n d p r i o r to o p e r a t i o n , n o n e h a d been s u s p e c t e d f r o m t h e clinical findings o r t h e c o n t r a s t studies. T h e r e was also one c a s e o f v a s c u l a r t u m o r w h i c h consisted o f a c a p i l l a r y a n g i o m a w i t h c o n s i d e r a b l e glial a n d f i b r o b l a s t i c i n f i l t r a t i o n a n d s o m e calcified a c c u m u l a t i o n s .

TABLE 3 (Continued)

Follow-up (yrs)

Duration of Remission (yrs)

Post-op Medication

Positive Post-op EEG's

Final Seizure Reduction

5 9

5 9

0 0

0/6 2/7

100 ~o 1007o

2/4 1/9

100~o 100~o

3

3

Temporal-lobe seizures with additional foci treated by resection.

The authors describe the use of temporal lobectomy following careful and repeated electroencephalogram (EEG) evaluation (with implanted electrodes in ...
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