E p i / q m , 40(7):X45-XSS, I999 Lippincott Williams & Wilkins, Inc., Philadelphia D International League Against Epilepsy

Clinica1 Research

Localized Pain Associated with Seizures Originating in the Parietal Lobe *Adrian M. Siegel, *Peter D. Williamson, ?David W. Roberts, *Vijay M. Thadani, and *Terrance M. Darcey Dartmouth-Hitchcock Medical Center, Section of *Neurology and ?Neurosurgery, Lebanon, New Hampshire, U.S.A.

Summary: Purpose: Ictal pain is a rare symptom of seizures. Epileptic pain may be experienced unilaterally (lateral/ peripheral), cephalically, or in the abdomen. Painful seizures have been associated with seizure origin in both the parietal and the temporal lobes. We report on the different types of epileptic pain and discuss its etiology and possible localizing value. Methods: We reviewed the records of patients referred to our epilepsy program over the last 6 years. Eight (1.4%) of 573 patients had pain as an early prominent symptom of their seizures. Results: Pain was predominantly unilateral in three patients, cephalic in two, and abdominal in three patients. Seizure onset

was in or involving the parietal lobe in all patients, and when the painful symptoms were lateralized, they were contralateral to the side of seizure origin. Parietal lobe seizure origin was determined by both intracranial EEG recording and neuroimaging [magnetic resonance imaging (MRI), ictal single photon emission computed tomography (SPECT)] in five patients, and by both scalp EEG and neuroimaging in three patients. Conclusions: We conclude that ictal pain is a rare symptom of parietal lobe seizure origin with lateralizing potential. Key Words: Epilepsy-Parietal lobe epilepsy-Somatosensory seizures-Painful epileptic seizures-Epilepsy surgery.

Ictal pain is one of several types of somatic sensations felt during partial seizures, other sensations being tingling paresthesias, thermal sensations, and sexual sensations. Ideomotor apraxia and disturbances in body image can also be observed (1). In a general series of patients with epilepsy ictal pain is a rare phenomenon (2,3). Among patients with somatosensory seizures, however, it is one of the more common sensations (2,3). Epileptic pain can be experienced anywhere in the body and, based on the principal location, is divided into three categories: lateralized peripheral, cephalic, and abdominal (2,3). Most patients report unilateral sensations, but bilateral pain also has been described (43). Epileptic pain is commonly caused by epileptic discharges in the parietal lobe, but temporal lobe seizure origin also has been postulated ( J ,3). Although epileptic pain is usually associated with other seizure symptoms, it can sometimes be the only manifestation of epilepsy (6). In such cases, seizures are often misdiagnosed, and patients go through unnecessary diagnostic procedures before the correct diagnosis is made (7-9).

We present eight patients in whom pain was a prominent initial or early ictal symptom. Emphasis is on the different types of epileptic pain and its localizing value. A representative patient from each of the epileptic pain categories is described.

METHODS AND MATERIALS Between January 1, 1992, and December 31, 1997, long-term videolEEG monitoring sessions were performed in 573 patients. Eight (1.4%) patients had obvious distressing pain as part of their seizures. Of these eight patients, five underwent further evaluation of their seizures with intracranial electrodes. When appropriate, functional mapping by using electrical stimulation and somatosensory evoked potentials was also done in the patients with intracranial monitoring. Patients were grouped under unilateral, cephalic, or abdominal, according to their predominant pain location. Patients with postictal pain, such as headache, were not included in this study.

RESULTS

Accepted December 29, 1998. Address correspondence and reprint requests to Dr. P. D. Williamson at Section of Neurology, Dartmouth-Hitchcock Medical Center. One Medical Center Drive, Lebanon, NH 03756, U.S.A.

Table 1 summarizes demographic and clinical data for the eight patients. Age at seizure onset varied between I

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846

TABLE 1. Summary of data ,from patients with painful epileptic seizure.,

Pat./ sex

Age at on\et (yr)

Seizure onset Etiology

LateraliLed, unilateral pain IIM 42 Head lrauma

21M

31M

37

28

Cephalic pain 4/M 314

SIM

30

Seizure Seizure characteristics duration

MRI

SPECT

lctal scalp EEG

lctal intracranial EEG

Operation (histology)

Outcome" (follow-up in mo)

Cold and throbbing sensation head L R; burning pain L shoulder + L arm/hand and L leg; confused; rarely sec.gen. Burning pain R hand + arm; parctic R arm: aphasia Vertigo; aching pain L hand + arm + L body side; deja vu; followed by confurion

Few sec to 2 min

Encephalomaiacia R sup. I m p . gyrua and par operculum

-

R heniiR pa, spheric operculuin rhythmic activity

Resection of R par. encephalomalacia (severe gliosis)

I (23)

5-9 min

Nonenhancing lesion L par. convexity

-

L front:

[II (35)

1-3 min

Wedge-jhaped watershed infarct R par.

-

Partial resection of L par. lesion (neurocytoma) N o surgery

Migration disorder

Severe headache; with or without pain R facehand; stifteniiig R limbs

1-5 min

Tumor

Bilateral squeezing facial sensation and headache; burning pain R body; R arm chic

3-5 min

Atrophic L hemisphere; dilation ventricle L post. Lesion L front.-par.

Severe, knife-like pain R lower abdominal quadrant; writhing, groaning: occasionally sec. gen. Nausea; alien hand; severe cramping pain L lower abdominal quadrant; pain and numbness L arm; occasionally sec. gen. Cramping periumbilical pain; grating teeth occasionally sec.gen.

1-2 min

Tumor

Infarct

Ahdominal pain 6/M 7 Unknown (anoxia'!)

7/M

30

Encephdlomalacia after tumor resection

8lF

I

Unknown

Bipar. atrophy

5 3 0 min Postop. changes with encephaloinalacia R occ.-par.

Few sec

Normal

par. R par

No clear 1ctal changes

Interictal: L front.-par. hyperperfusion

-

L medial par. lobe

L front.. par.

Resection L occ. and par. lobe (migration dirorder) Tumor biopsy (astrocytoma 11)

[ctal 1: hyper- No ictal perfusion L changes par. and L front.; ictal 2: hyperperfuyion R par. and R SMA Ictal: hyperR par. perfurion R par. occ.

Ictal I and 2: R par. hyperperfusion

L par. operculum

R par.

Inconsistent onset L par midline convexity

No surgery

R par.

Resection (gliotic ?car)

-

-

Lost to follow-up

Died after malignant change of astrocytoma

No surgery

~

Pat., patient; M, male; F, female; L, left; R, right; sup,, superior; post., posterior; temp., temporal; par., parietal; front., frontal; occ., occipital; sec.gen., secondarily generalized; min, minutes; sec, seconds. " Epileptological outcome was classified according to Engel into class 1, seizure free; class 11, rare seizures; class 111. worthwhile improvement; class IV, no worthwhile improvement.

and 42 years (mean, 22.0 years). Mean age at evaluation was 35.6 years (range, 23-56 years). Seven patients were right-handed, and one was left-handed. Pain was predominantly unilateral in three patients (patients 1, 2, and 3). Cephalic pain was the major early ictal symptom in two patients (patients 4 and 5) who also had lateralized pain. In three patients (patients 6 , 7, and 8), the seizures consisted of abdominal pain. One of the patients with ictal abdominal pain (patient 7) also had lateralized peripheral pain. Epikpsiu, Vol. 40, No. 7, 1999

ILLUSTRATIVE CASES (ONE OF EACH TYPE) Patient 1 This 44-year-old, right-handed man enjoyed excellent health until age 42, when he was accidentally shot in the right parietotemporal area with an arrow while deer hunting. The arrow tip penetrated the skull and required surgical removal. Three months after the injury, he developed his habitual seizures. These began with a consistent description of cold sensation in his left ear, followed by

PAINFUL EPILEPTIC SEIZURES

a throbbing sensation behind the ear that would migrate to the right side of his head, and then down the left side of his neck. He would then experience a severe burning sensation in his left shoulder that would march down his arm into his hand and eventually involve his leg on the same side. During more prolonged episodes, he would become confused. Seizures occurred up to twice a day despite trials of various antiepileptic drug (AED) regimens. Between seizures, he developed unpleasant leftsided dysesthesias that were exacerbated by hot showers. His neurologic examination was normal. Magnetic resonance imaging (MRI) showed a region of encephalomalacia involving most of the right superior temporal gyrus and extending posteriorly and superiorly into the parietal operculum (Fig. 1). Numerous episodes were recorded during video and scalp EEG monitoring. Unequivocal rhythmic EEG changes were recorded over the right hemisphere during a prolonged episode. No interictal EEG abnormalities were recorded. A subdural grid was placed over the right frontotemporoparietal junction to define more accurately the region of seizure

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origin (Fig. 1). After 2 weeks of continuous recording, he had a single habitual seizure that progressed to a secondarily generalized tonic-clonic convulsion. It began in the right inferior parietal lobe in the region of injury (Fig. 2). He underwent a parietal resection that included the region of encephalomalacia. Pathology revealed severe gliosis. The patient became seizure free postoperatively. Immediately after surgery, the unpleasant left-sided dysesthesias, which had been present before, became more severe and assumed a burning and painful quality similar to his presurgical seizures. This has gradually improved, but he still has persistent burning sensations in his left hand.

Patient 4 This 23-year-old, left-handed man developed infantile spasms at the age of 9 months. An EEG at that time revealed hypsarrhythmia. Intramuscular adrenocorticotropic hormone (ACTH) controlled the seizures for 6 months, after which he was maintained on phenytoin

FIG. 1. MRI of patient 1. Top right shows placement of 8 x 8 subdural grid and region of seizure onset (black circles). Top left and bottom, encephalomalacia in the right superior temporal gyrus extending posteriorly and superiorly into the parietal lobe.

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FIG. 2. EEG from patient 1 reveals seizure onset in the parietal area (G 19, 28 top panel). Successive segments demonstrate slow progressive spread over 9 min. Clinical onset has a delay of 6 min after electrical onset (see Fig. 1 for electrode orientation; G 19, 28 are black circles). Eptiupsia. Vol. 40, No. 7, 1999

PAINFUL EPILEPTIC SEIZURES

(PHT). At the time of seizure onset, a mild right hemiparesis was observed. He was considered significantly developmentally delayed, but over the next 2 years, he improved cognitively and developmentally to the degree that he was able to attend regular school with some special educational assistance. Infrequent seizures persisted, occurring every 6-12 months. At age 14, seizures increased in frequency to six per week. Seizures began with a severe midline headache, with or without sharp pains in the right face and hand, followed by tonic stiffening of the right arm and leg. Seizures lasted from 1 to 5 min. Rarely seizures would last up to an hour, but consciousness was never impaired. On examination, he had a spastic right hemiparesis with the leg more impaired than the hand and arm. Cortical sensation was impaired, and there was a dense right homonymous hemianopsia. MRI of the head revealed an atrophic left hemisphere with maximal atrophy in the parietal and occipital regions, and dilation of the posterior portion of the left ventricle (Fig. 3). During initial video and scalp EEG monitoring, recorded seizures consisted of tonic posturing of the right hand and arm. During a more prolonged seizure, tonic posturing spread to involve the right leg, and it terminated with some superimposed clonic activity. All recorded seizures were preceded by midline sharp head pain and a vibratory feeling of energy buildup on the right side, but no lateralized pain. With the exception of bilateral seizure activity during more prolonged seizures, the ictal and interictal scalp EEG recordings were generally uninformative, containing considerable artifact and no clear epileptiform seizure activity. Subdural electrodes were placed to sample the left

FIG. 3. MRI of patient 4 shows atrophy of the left hemisphere and a porencephalic dilatation of the occipital horn.

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parietooccipital convexity and the left medial parietal and frontal supplementary motor area (SMA) surfaces. Although a precise region of seizure origin could not be demonstrated, there was no evidence of SMA or other, more anterior seizure onset or spread. Some seizures appeared to begin diffusely in the parietal lobe behind the postcentral gyrus, but most often originated in the medial parietal region (retrosplenial). In the case of the former, occipital lobe origin could not be ruled out, but the painful part of the seizure was associated with parietal lobe seizure involvement. The patient underwent a resection of the occipital lobe and the parietal lobe region behind the postcentral gyrus. Pathology revealed severe architectural disorganization and disorders of neural migration. After a stormy first postoperative year including development of hydrocephalus, infection, and occasional focal motor seizures, he was seizure free for a year. He was then lost to follow-up.

Patient 6 This 26-year-old, right-handed man had a 5-min period of respiratory arrest due to a blocked trachea when 9 months old. Seizures began at the age of 7 years. His initial seizure consisted of stomach pain followed by a generalized convulsive seizure. Seizures persisted with severe “knife-like’’ right lower quadrant pain accompanied by writhing and groaning. The seizures occurred almost exclusively at night, often in clusters lasting for hours, during which he was partially responsive. This pattern has persisted to the present, despite trials of a variety of AED regimens. Extensive evaluations at several other institutions found no EEG abnormalities between or during typical episodes, and the diagnosis of epilepsy was questioned. Each time this happened, AEDs were discontinued. Subsequently, a typical attack would evolve into a secondarily generalized tonicxlonic convulsion. At the time of the patient’s referral to the Dartmouth Epilepsy Program, he was having three to five seizures per night, but could have seizure-free periods for up to 2 weeks. MRI revealed probable mild, biparietal atrophy, but was otherwise normal. During video and scalp EEG monitoring, there were no interictal or ictal electrographic abnormalities, except when he had secondarily generalized convulsions. Most seizures occurred out of sleep, starting with him crying out or groaning in pain, clutching his right groin, and rocking back and forth or writhing in the bed. Two ictal single photon emission computed tomography (SPECT) scans were done. The first injection took place between 15 and 20 s after he complained of right lower quadrant abdominal pain. This scan showed hyperperfusion both in the high left parietal convexity and the left frontal lobe. The videotape of this event showed him clutching his right groin. The second ictal scan was done as an outpatient without video moniQ?ilepJiu. Vol. 40, N o . 7, 1999

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toring. The injection was reportedly during the seizure, but the exact timing was not recorded. This second scan showed hyperperfusion in the right parietal lobe and right SMA. An intracranial electrode study using a combination of subdural grids and strips was designed to cover both SMAs and the right parietal convexity. Additional subdural strips were placed over both frontal lobes and the left parietal convexity (Fig. 4). Seizures recorded consistently began in the most distal contact of the left parietal subdural strip (Fig. 5 ) with spread to the right parietal convexity and to the posterior regions of the SMA. Because seizures appeared to originate high in the left parietal convexity, a brain region that had minimal intracranial electrode sampling, a second study was designed to cover more thoroughly the left parietal convexity and parietal interhemispheric region. Because of technical limitations, this second study was not able to confirm the findings of the first study. Epilepsy surgery was therefore not recommended.

DISCUSSION Although painful epileptic seizures have been recognized since the nineteenth century (lo), it was Gowers in

FIG. 4.

1901 (2) who first elaborated on ictal pain. Many subsequent reports were anecdotal single cases (1 1-16). In a larger series of auras (17), and in a series of posttraumatic motor and sensory epilepsy (18), painful sensations were found in 3.0 and 4.7% of the patients, respectively. In 1983, Young and Blume (3) reviewed a series of 858 patients with epilepsy followed in their clinics and reported that 24 (2.8%) had pain as a part of their seizures. Among somatosensory seizures, Mauguiere and Courjon (6) found pain in 23.6% of the seizures, forming the second most frequent type of seizure. In several recent reports of parietal lobe epilepsy (l9-21), pain is described in only one patient each. However, in a surgical series of 82 patients with nontumoral parietal lobe epilepsy, 13 (1 5.9%) patients experienced painful auras (22,23). Our eight patients represent only 1.4% of patients evaluated at our Epilepsy Program over the last .6 years. Painful seizures may occur in all age groups. Age at seizure onset did not differ between patients with unilateral ictal pain and patients with cephalic ictal pain. Seizure onset for both of these ictal pain groups is most common in the first two decades (3,5,8,9,24); however,

Position of grids and strips in patient 6: interhemispheric 3 x 8 grid with electrodes on both sides. Two right (G, H) and one left

(C)1 x 8 frontoparietal subdural strips placed as illustrated. Not shown are five left and right frontal convexity eight-contact subdural strips. Epilrpsia. Vol. 40, N o . 7, 1999

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late onset has been described (4,25). Abdominal pain occurs mainly in pediatric patients (26-28), but several studies have reported this also in adults (29-3 1). The spectrum of epileptic pain properties is vast. A precise description is often difficult to obtain and may depend on cultural and emotional influences (32). Penfield and Jasper (33) reported ictal pain to be usually mild, and questioned whether the term “pain” is not a misnomer. Other authors and many patients have, however, reported very severe pain. Painful unilateral sensations of the extremities are most commonly experienced as burning, dull, throbbing, cramp- or electric-like. Abdominal pain is a more severe, sharp (“like a knife”) feeling (3), but can also be oppressive (24). Cephalic pain can be nonspecific, or throbbing and migraine-like (3). Ictal pain may be felt anywhere in the body, but the most common locations are a part or the whole of one side, the head (cephalic), and the abdomen (2,3,34). Unilateral or cephalic pain is found in the majority of painful seizures and occurred in one series in 41.7 and 45.8% of patients, respectively (3). Among several large series of patients with epileptic pain, the incidence of abdominal pain varied widely between 12.5 and 38.6% (2,3). Bilateral pain involving all limbs and paroxysmal rectal or genital pain are exceptional among somatosensory seizures (4,5,35,36). Unilateral pain is more often a well-localized than a diffuse sensation (2,3,7). At the time of seizure onset, it usually involves one arm, especially the hand and fingers, and then spreads to the face and leg and then the shoulder (3,8,9). Spread of the pain usually follows the sensory homunculus, but the trunk may sometimes be spared (as in our patient 1). For this there are two possible explanations. First, spread from upper to lower limb (or vice versa) may be so rapid that the involvement of the trunk is not registered. Second, the lack of sensation may be caused by the limited representation of the trunk in the sensory cortex ( 1 ) . Cephalic epileptic pain may be diffuse or well localized. In their 11 patients with cephalic ictal pain, Young and Blume (3) found three patients with diffuse and eight patients with localized headache, with the latter showing no predominant location. Epileptic cephalic pain could either secondarily involve the whole head or spread to one side of the body (3). This was seen in patients 4 and 5 of our series. Abdominal pain is most often periumbilical(29), but it can also involve the whole or a quadrant of the abdomen as in patients 6 and 7 of this series (24). Painful abdominal sensations rarely spread across the homunculus to involve other parts of the body (patient 7). Seizures associated solely with pain are rare, and only a few patients have been reported in the literature (7,13Epilepiu, Vol. 40. N o . 7, 1999

15). In their examination of 30 patients with ictal pain, Mauguiere and Courjon (6) found only two cases in which pain is the only seizure manifestation. In a large series of somatosensory seizures, almost 40% of the patients had multiple sensory symptoms (6). When unilateral pain is associated with other features, the most common are paresthesias and thermal sensations (as in our patients 1 and 3), disturbances in body image, and less frequent motor signs (3,6,12,13,15,32). Abdominal pain is often associated with nausea and diarrhea (29,3 1). The occurrence and type of coexisting symptoms depends on location and spread of the epileptic discharge in the brain. Whereas ictal discharge in the anterior parietal lobe can be associated with seizures beginning with sensorimotor symptoms, posterior seizure origin has been associated with more complex phenomenon (20,2 I). This complex phenomenon can include elementary visual symptoms (19,20), and others experience complex partial seizures as “psychoparetic” (21), consisting of a psychic aura such as fear or d6jh vu (as our patient 3), followed by motor arrest and loss of consciousness. Five of the eight patients presented here experienced at least one secondarily generalized seizure: two had unilateral pain (patients 1 and 3), two had cephalic or abdominal pain (patients 4 and 6), and the remaining patient (patient 7) had abdominal and unilateral pain. These findings were similar to those of Young and Blume (3), who found secondary generalization in five of 10 patients with unilateral ictal pain, Data regarding the duration of painful seizures are limited in the literature. In a series of unilateral episodes, pain lasted between 20 and 120 s (6). Other authors reported the duration of unilateral ictal pain between a few seconds (9) and several minutes (7,8,20,37). Abdominal pain, however, may last for several hours (26,29). There was no evidence in our series and in previously reported ones that seizures consisting of pain and additional symptoms (most likely due to involvement of a larger brain area in the ictal discharge) last longer than seizures with pure pain. One patient in our series developed chronic pain syndrome resembling his ictal pain. Based on clinical-pathological observations, the link between unilateral epileptic pain and the contralateral parietal lobe was already known at the beginning of this century (2,l I). Subsequently, Penfield and Gage (14) elicited a painful response in two patients with epilepsy from area 5a in the parasagittal region. However, because pain rarely occurred in response to electrical stimulation of the parietal lobe (38), Penfield and Jasper (33) questioned whether pain is really a cortical sensation. Subsequent stimulation studies, however, supported the role of the primary sensory area (S I, Brodman’s area 3, 2, and 1) in pain perception. In more recent human studies, the controversy regarding the role of S I in pain

PAINFUL EPILEPTIC SEIZURES perception was again revived. Measurements of regional cerebral blood flow (rCBF) in S I in response to experimental pain, as a surrogate marker of its involvement in pain perception, give conflicting results. Some authors found an increase of rCBF (39,40); in other studies rCBF in S I did not change (41);and in others there was a decrease in rCBF (42)during painful stimuli. Another structure thought to be involved in pain perception is the secondary sensory area (S II), which lies along the upper portion of the sylvian fissure. Both sides of the body, with a contralateral predominance, are represented here (4,37,43,44). Recent animal studies (4446) demonstrated regions containing sparse nocicresponsive neurons (i.e.,