Interictal behavioral syndrome in non-dominant temporal lobe epilepsy

Interictal behavioral syndrome in non-dominant temporal lobe epilepsy

Paulo Cesar Trevisol-Bittencourt
André Ribeiro Troiano

Abstract

Summary – The syndrome of interictal personality in non-dominant temporal lobe epilepsy consists of hypossexuality, hyperreligiosity, humorlessness and hypergraphia. Its notification, in 1974, was followed by an extensive search for these traits in broad epileptic populations. Nevertheless, these statistical studies failed to match this syndrome in general temporal lobe epileptics, and its existence became then target of doubt. We report the case of a 35 year-old man presenting partial complex epilepsy, whose singularity lies in his sophisticated drawing abilities. The large amount of buildings and houses he paints expresses his hypergraphia. He also presents hypossexuality and hyperreligiosity. MRI shows right mesial temporal sclerosis. Temporal hyperconnection, caused by a basal temporal irritative focus, is the most probable physiopathological mechanism. Epileptic fits can be controlled in the majority of cases. However, behavioral symptoms usually do not respond to pharmacological approach or psychotherapy.

key-words: temporal lobe epilepsy, interictal personality.

Introduction

In general, humankind has always presented a mistaken approach to epileptic phenomena. For centuries, epileptic patients were considered invalid individuals, were rejected by other people, and even considered dangerous to society. As a result, epileptic patients were feared and ridiculed by people in general and by doctors. While being characterized as presenting a mental and spiritual disability, epileptic patients were submitted to severe and debilitating social restrictions. The social isolation imposed upon epileptic patients was, consequently, the cause of behavior changes that contributed to aggravate the mistaken understanding of the conditions of these patients, thus increasing the already significant difficulties faced by epileptic patients. In earlier times, therefore, medical science established a strong relationship between epilepsy and psychiatric distress, corroborating, thus, to the misguided understanding of epilepsy.

In this sense, Joaquim Maria Machado de Assis, one of the most important writers in Brazilian literature, had epilepsy. The disorder, however, did not prevent Machado de Assis from offering a lasting contribution to our national literature while addressing the ever unstable social relationships. Also in this sense, it is possible that his book, the Alienist, may be considered as a groundbreaking statement, in Brazil, against the orthodox psychiatry that understood epilepsy as a symptom of a mental disorder. The referred work of literature may represent the rebellious statement of an epileptic individual who, in being gifted with a unique ability to use irony and criticize, was living under the difficulties imposed by a pseudo-scientific and highly oppressive psychiatry. The literary figures of Doctor Simão Bacamarte, the alienist, and of the Casa Verde, his asylum, are a representation of the dogmatic tyranny underlying the practice of psychiatry until just a few decades ago.

As if to worsen the misguided approach to epilepsy, the first antiepileptic drugs employed, namely bromides and barbiturates, played a significant role in deteriorating patient cognitive functions and patient behavior. With new antiepileptic drugs, however, the negative aspects of treatment were minimized and epileptic seizures were more controllable, resulting in less influencing upon patient cognitive performance and behavior. Consequently, new perspectives appeared in terms of pursuing both patient freedom from epileptic seizures and from social stigma that came with the disease. In this sense, the first burdening stain to be removed from the misguided understanding of epileptic patients was that of the epileptic personality. Curiously, and absurdly, the described characteristics of the epileptic personality could also be identified in secondary symptomatology of chronic use of barbiturics.

The resulting movement opposing prejudice against epileptic patients, however, also affected, in an inadequately significant and generalizing manner, the behavioral studies related to epilepsy. From the initial statement of William Lennox, one of the pioneers in US epilepsy studies, asserting that the great majority of patients were psychologically considered normal, 1 emerged an interpretation that absolutely denied any relationship between epilepsy and personality disorder. 2

As in any extremist trend, the referred interpretation, in turn, also incurred into significant limiting aspects of stopping or preventing the society at large and doctors from perceiving specific personality traits. Consequently, research funding for any studies related to epilepsy and its patients were systematically denied. Studies in epilepsy were, thus, quantitatively and qualitatively reduced to a point of near nonexistence. 2 Conversely to the trend at the time, the first reports of Norman Geschwind and his colleague, Stephen Waxman, 3, 4 regarding the incidence and the nature of interictal behavior syndrome, were published between 1974 and 1975. As a result, these reports caused a great impact in the realm of neurology. 5 The clinical case reports of non-dominant temporal lobe epilepsy presented by these authors resulted in the designation of the eponym Geschwind, or Geschwind-Waxman, Syndrome. Geschwind and Waxman were the first to describe a specific set of marked personality alterations associated to a specific type of epilepsy. From these initial reports, it was possible to separately group behavioral symptoms by (1) circumstantiality; (2) intensified preocupations related to moral, philosophical, religious, or ethical themes; (3) hypossexuality; and (4) irritability. 3, 4

The description of these symptoms led to a search for these personality traits in numerous patients and to the designing of a score for quantitative analysis of interictal behavior in temporal lobe epilepsy (TLE). The score, designed by Bear and Fedio, 6 was applied in various studies oriented towards different groups of individuals. 7, 8, 9, 10, 11 Most study results, however, were conflicting and, consequently, the existence of the Geschwind syndrome itself started being questioned. 12

With the objective of illustrating the approach presented by Norman Geschwind and Stephen Waxman, we will present a case report of a patient who presented with classical clinical status of interictal behavior syndrome in non-dominant TLE. Next, it is also our objective to review the literature in this aspect.

Table 1. Behavior Traits surveyed in Bear-Fedio scale 6

Emotionality Philosophical interest

Mission Sense of destiny

Manic tendencies Dependence

Passivity Paranoia

Depression Moralism

Ill-humor Guilt

Hyposexuality Obsession

Hostility Circumstantiality

Aggressiveness Stickiness

Religiosity Hypergraphia

Case Report

Male, 35-year old patient; born in Brazil and of Native-Brazilian, Portuguese, and African-Brazilian origin. Patient, heretofore referred to also as JCS, at the moment of the study, was single and retired. He was born in the city of Lages, and living in the city of Palhoça, both in the state of Santa Catarina. Patient level of formal education was elementary, he is also a right-handed man and who has strong religious beliefs. Patient presented with complex partial seizures originated at left temporal lobe and secondary to febrile convulsion during infancy.

At ten years of age, patient presented partial seizure with psychic involvement, sudden fear, followed by complex partial seizure (CPS) with secondary generalization. Patient has continuously presented with these three types of seizures. It was noted that partial seizure occurred with daily frequency, CPS occurred with weekly frequency, and secondary generalizations occurred with monthly frequency.

Patient was born from normal, term delivery without any intercurrences. At 4 months of age, patient presented one episode of complicated febrile convulsion (prolonged seizure). Patient had no family history of epilepsy or neurological diseases. Patient epidemiology presented positive for cysticercosis. Long-term medical follow-up was carried out and seizures remained refractory to therapeutic treatment employed. Subsequently, JCS was submitted to outpatient follow-up at the Clínica Multidisciplinar de Epilepsia, starting March of 1992. Patient was administered diphenyl-hydantoin at 300 mg/day and carbamazepine at 800 mg/day. Patient presented with acne and gingival hyperplasia at physical examination and normal at both neurological examination and laboratory examination upon admission. Electroencephalogram (EEG) indicated a right temporal irritative focus. Nuclear magnetic resonance (NMR) of the cranium indicated right medial temporal sclerosis. Patient was diagnosed with non-dominant TLE and was submitted to monotherapy with carbamazepine. Despite progressive increase in carbamazepine dosage, frequency of patient simple partial seizures and complex seizures remained unaltered; generalized seizures, however, were reduced. One year prior to this report, patient was being administered the maximum dosage of carbamazepine and, consequently, clobazam was included in the treatment. Due to unsuccessful clinical treatment, patient surgical treatment is being considered.

Figure 1. Aerial view of buildings; reduction from a 1×1.6-m original drawing

Aerial view of buildings; reduction from a 1x1.6-m original drawing

In the period between seizures, it is possible to observe that patient presents uncommon personality traits derived from (1) altered behavior, (2) altered sexuality, and (3) circumstantiality.

Patient behavior alteration is observable in intense concern related to matters of religion and concern towards strictly following the dogmas of his church. Hypereligiosity is a marked trait in the personality of the patient since it is underlying, and manifested in, other pathological personality traits, including circumstantiality (excessive verbal output with repetitive mystical and religious terms) and hypossexuality. JCS is a single patient and has never engaged in sexual intercourse. Every few months, patient presents occasional sexual thoughts or impulses that are immediately repressed by his oppressive religious conscience. Patient presents a characteristic of excessive verbal output and of a perceivable increase in the need for verbal communication and for communicating through graphic images. Long interviews were directed solely by the patient in an continuous soliloquy. Patient spoke in an ordered sequence of subjects, which were minutely dissected and illustrated with commonplace ideas, and in sentences or interjections that were extremely formal and constantly repeated, all of which describe his trait of circumstantiality.

Figure 2. Facade of a large, two-story house

Facade of a large, two-story house

The most observable form used by our patient to externalize communicative energy was through hypergraphia, more specifically, in architectural drawings (Figures 1 and 2). During outpatient follow-up appointments, JCS mentioned his drawings, at which point we requested him to, upon his return appointment, bring some of the referred works. One month later, patient returned with a 1.5-meter wide roll of paper that extended to about 10 meters of house, street, and building designs. Patient reported being compelled to draw architectural design since adolescence, including house , building, and facade designs. Identically to the amount of information conveyed verbally, patient presented the characteristic of meticulous expression through architectural designs, which were drawn for hours on end. We observed the concern with precise representation and the strong impulse to draw in many of JCS’s works. Patient presented us with drawings of 31-story buildings carefully designed with verandas and railings systematically decorated according to architectural concepts. Patient drawings also presented a characteristic of observing techniques of perspective. Buildings normally were drawn with a ground perspective and houses with an aerial perspective just so that their roofs could be observed. Patient indicated, however, that the perspective of a drawing can be changed upon request as long as he is given enough time to redraw the house or building. Patient reported being able to project a mental image and walk through his designs. Images are not involuntarily projected nor did we observe diplopia of consciousness.

Discussion

Between 1974 and 1975, Waxman and Geschwind, in two different opportunities, described the clinical status of nine epileptic patients out of which eight presented with a non-dominant temporal lobe irritative focus and one dominant focus. 3, 4 All patients presented with an uncommon tendency towards writing extensively and, typically, in a meticulous fashion. Other traits observed in the patients were of hypossexuality, with rare or nonexistent sexual impulses, irritability and hypereligiosity. It is possible that the metaphysical aptitude observed is part of a larger set of personality traits presented by these patients, which is constituted by a concern with mystical, moral, ethical, and philosophical matters. Despite being the first report of an association of a behavior syndrome with epilepsy, the psychopathology of epilepsy is well-known. Kraeplin, 13 in 1906, observed that the patient “ used to give a long, but coherent description of his own condition” (*), and Glaser, 14 in 1964, observed that “many patients were concerned with the clarity of their exposures, and made significant efforts in order to control, restrtict or restrain emotions and actions in a way to become clear, accurate and realistic”(*). These displays of oral or written communication were mistakenly characterized as pedant, circumstantial, extensively pondered upon, and prolix. After the reports by Waxman and Geschwind, there followed other studies presenting similar cases. 15, 16, 17 Roberts, 18 reported other 6 cases of patients who presented hypergraphia, randomly combined with hyposexuality, hypereligiosity, persecutory delusion, elation, mystical and messianic feelings, déjà vu, auditory hallucinations, interest in philosophical questions, and mania. Roberts reported that most patients presented with non-dominant temporal irritative focus at EEG. Sacks, with his refined literary style, tells the story of Franco Magnani, an artist whose complex partial seizures and eidetic visual memory was converted into exquisite paintings as a result of his compulsion to paint. The author writes that during epileptic seizures, patient reported being able to see, hear, and smell characteristic places, sounds, and odors of his city of birth, in Italy, which he had not visited for 30 years. Naito, 17 briefly describes the case of a 62-year old female patient with posttraumatic epilepsy. The patient presented with interictal behavior of hypergraphia; the author indicates that the written works of the patient described in detail and repeatedly experiences of great mystical pleasure, unity, and completeness. These reported phenomena were diagnosed as TLE with ictal ecstatic state. Other authors have noted that the extraordinary Russian writer, Fyodor Mikhailovitch Dostoievski presented similar traits. 19, 20 The author of “The Brothers Karamazov” presented complex mental states at onset of epileptic seizures. It is reported that the Dostoievski once made a comment in this sense: “You, healthy people, cannot imagine the happiness that we, epileptics, feel in the second just before our seizures begin […] I don’t know if this happiness lasts seconds, hours or months, but, believe me, I would not exchange it for all the happiness that life can offer”19 (*). Evidently, the ictal ecstatic state is not associated with all epileptic syndromes, as the comment of the author may lead to interpret. Nonetheless, Dostoievski’s unknowingness of epileptology is irrelevant when faced with the effect of his works in the behavior of the Western society. Kumagusu Minakata (1867-1941), a Japanese genius devoted to Natural History and folklore, was known for his eidetic memory and extensive literary production (almost 1,500 different papers). In his works, in addition to dealing with biological matters, Minakata also presented a concern with ecology, theology, and sexology. A recent study has demonstrated that Minakata, who had TLE, presented signs of right hippocampal atrophy and characteristic traits of interseizure behavior syndrome. 21

Stimulated by the findings of Geschwind, Bear and Fedio reviewed medical literature from 1877 to 1977 in a search of reports of psychiatric and behavior alterations associated to epilepsy. Next, the authors selected the 18 most representative traits among those surveyed and classified them in three categories (Table 1). The authors designed a standard stimulus letter that sought, throughout its 100 questions, for clues related to any of the eighteen traits of personality listed. Positive answers were computed with a psychopathology score. The letter was applied to 27 patients with TLE and 21 control patients. Results indicated higher scores for patients with TLE. 6, 22

Bear and Fedio’s study was in agreement with that of Geschwind and widely quoted in subsequent articles due to its designing of a new psychological test and to its solid foundation on data. The results by Bear and Fedio, however, presented a reduced applicability in clinical practice and the conclusions presented difficulties in being validated. 7, 8, 9, 10, 11, 12, 23 There are diverse clinical and pathological factors among the etiologic and epileptic agents of temporal lobe seizures. Among these factors, we can identify infections (cysticercosis, encephalitis, and meningitis), head and cranium trauma, familial epilepsy seizures, temporal lobe atrophy, and mesial temporal sclerosis. Independently from etiology, a significant parameter that should be quantified is time from evolution and frequency of epileptic seizures. Frequent seizures are associated with early behavior alterations. In this sense, mesial temporal sclerosis is significantly important. This neuropathological factor, which was observed in our patient, is frequently associated with complciated febrile convulsions during childhood, 24 with early onset of seizures (during the first or second decade of life) and untractable partial epilepsy.

The neurophysiological mechanism of Geschwind-Waxman’s syndrome is still not well-understood. Interesting hypotheses, however, have been presented, such as heightening of emotional responses in the presence of preserved intellectual function, of personal psychological and environment factors, and of congenital or developmental abnormalities. An anatomical mechanism, which can be correlated to congenital or developmental abnormalities, is the basis of one of the currently most accepted hypotheses. In order to understand the phenomenon, it is important to note that the dominant cerebral hemisphere (usually the left-side) is responsible for language understanding and communication. The non-dominant cerebral hemisphere possibly modulates the emotional content of language. In this sense, any disorder of the non-dominant hemisphere leads, through a process of contralateral delivery (probably by means of the callous body), to a change in the function of the dominant hemisphere and to an alteration of the volume of speech and writing. Consequently, the usual response to electrical stimuli in the areas of language of the left hemisphere is an interruption of speech. If the referred site is an epileptic focus, it is possible to observe temporary aphasia. Right hemisphere activity disorders, especially of the cortical / temporal basal / medial areas could allow activity in the left hemisphere, thus leading to a clinical status opposite to those that induce aphasia and to pathological disorder of the level of language production. 25

David Bear classified the interictal behavior syndrome of Geschwind-Waxman as a temporal hyperconnection syndrome by establishing a clear and diametrically opposite difference with the Kluver-Bucy syndrome. While the earlier is caused by a temporal irritative focus (increase in activity) usually located in the anterior pole, the latter is caused by bilateral ablation of the amygdala. The typical clinical status of a Kluver-Bucy animal model is that of a fearless animal that presents extreme curiosity, that forgets very easily, that has a great tendency towards oral recognition of objects (as in inserting everything in its mouth), and that has a highly increased sexual impulse. In addition, the animal model presents hypermetamorphosis, cognitive decay, and placidity. In temporal hyperconnection, in turn, patients have presented hyposexuality and deepened cognitive and emotional responses (Table 2). Among the hypotheses presented, the above indicated theory seems to better transcend the boundaries of speculation of possible interictal syndrome mechanisms. 2

Table 2. Differences between Geschwind-Waxman and Kluver-Bucy syndromes (temporal hyper- and hypoconnection) 2

Geschwind-Waxman Kluver-Bucy

Hyposexuality Hypersexuality

Stickiness Hypermetamorphosis

Deepened cognitive response Cognitive decay

Deepened emotional response Placidity

Epileptic focus of temporal lobe Structural damage of temporal lobe

Even though a significant amount of patients with interictal behavior syndrome present with gradual onset of their clinical status, with increasing interest in human and metaphysical matters and increasing compulsion to transcribe these matters into paper, other patients with interictal behavior syndrome present with abrupt onset of clinical status, including no previous history of epilepsy. Magnani, as discussed by Sacks, suffered of a “ decision, hope and fear fit, but also of a high fever, loss of weight, delusions, maybe convulsions; it was suggested that it could be tuberculosis, or psychosis, or any neurologic state. […] In the peak of the disease […], Franco started to dream, every night, incredibly sharp dreams. He dreamed every night with Pontito […], the streets, the houses, the buildings, the stones – dreams with the most microscopical and truthful. […] In the hospital, with these onirical images imposing themselves over his own consciousness and will, he was taken by a novel feeling – the feeling that he was being ‘called’ “.5 (*)

Hypergraphia is one of the most evident traits in interictal syndrome and that is difficult to define, since there are no criteria, such as in word count or type of graphical design, that determine precise limits with what would be normal behavior. Hypergraphia can be observed in psychiatric disorders, such as mania, and associated occasionally with religious matters. 25 In a study by Sachdev and Waxman, the authors sent stimulus letters to patients with varied epileptic syndromes surveying neurological condition in the form of open, written answers. Seventeen patients answered the survey, out of which 9 had TLE. Out of the 33 patients who did not answer the survey, only 7 had TLE and 71% who responded with extensive written answers (hypergraphia) presented TLE. 26 Others have corroborated these results. 27, 28 Roberts reported the occurrence of hypergraphia in the almost absolute form of non-dominant TLE, in a study regarding the lateralizing significance of hypergraphia in TLE. The author reported that hypergraphia was more frequently associated with basal temporal focus than with medial focus. 18 Our patient represents an important case that is worth reporting since he presents a compulsion to write in a peculiar manner. Though there have been reported cases of patients who draw, 2 this is the first report of a patient who expresses himself graphically exclusively through technical design; some of which recognizably followed a sophisticated conception.

The treatment for the Geschwind-Waxman includes two aspects, that of treatment of seizures and that of attending patient behavior. Drug treatment for the Geschwind-Waxman syndrome follows current principles in antiepilepsy treatments. The therapy of support, however, is crucial for patients diagnosed with this syndrome. These patients present circumstantial and stickiness characteristics and, thus, are considered tiresome, or boring, people. People who have Geschwind-Waxman syndrome are usually bothersome to relatives, friends, and even to doctors. The approach with therapy, however, is not very effective, since these patients are refractory and inaccessible to psychotherapeutic insight and are not aware of the psychopathological seriousness of their condition. 2

At last, it is our objective to emphasize that the alterations perceived in these patients are usually not harmful and do not necessarily result in maladjustment. Even though some cases may represent social difficulties, which certainly affect the patients, these individuals can convey the creative side of their syndrome to other people. Instead of treating it as a deficit, it can be considered an improvement; instead of a incapability and stagnation, the transcending of production. 29 This is a side to the disease that only Neurology and Psychiatry have had the privilege to study. The potential in these patients should not be overlooked, considering an underlying individual, social, artistic, and economical picture. It is evident that the abilities presented by our patient are a case-specific variation of the syndrome. Nonetheless, the talent in patients such as ours may never be perceived if his or her healthcare professional’s main concern is with examinations and prescribing drugs. We would like to end this case report quoting William Osler: “Ask not what disease the person has, but what person has the disease”.

Acknowledgments

The realization of this paper would have never been possible if it were not for the most valuable assistance of Sérgio Samuel Soares and for the cooperation of our patient, JCS.

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