Which Type Of Epileptic Psychosis Should Be Compared With Which Primary Psychotic Disorder

With regard to the wide-ranging clinical manifestations of epileptic psychoses and primary psychotic disorders, it is important, first of all, to determine which should be compared. Table 8.1 demonstrates the incidence of subcategories of psychosis occurring in patients with epilepsy who visited the Kansai Regional Epilepsy Center from 1983 to 1999 (Kanemoto et al, 2001), definitions of which are listed in Table 8.2. Chronic epileptic psychosis (CP), acute interictal psychosis (AIP), and postictal psychosis (PIP) together constituted 95% of all patients who had

TABLE 8.1 Subcategories of epileptic psychoses (n — 200)

Postictal psychosis AIP as well

26.5% (53/200) 2.0% (4/200) 1.0% (2/200) 52.0% (104/200) 11.5% (23/200) 29.5% (59/200) 5.0% (10/200)

evolving into CP

Acute interictal psychosis evolving into CP Chronic psychosis Others

Source: Data recalculated from Kanemoto et al. (2001). AIP: Acute interictal psychosis; CP: Chronic psychosis.

TABLE 8.2 Definitions of subcategories of epileptic psychoses

■ Postictal psychosis: Psychosis that follows immediately after 1 or generally multiple seizures (mostly complex partial or secondarily generalized), occurring within 1 week of the last seizure.

■ Acute interictal psychosis: Psychosis that develops when seizures have ceased or reduced significantly in frequency (alternative psychosis) or when seizures are unrelated to any recent increase in seizure activity.

■ Chronic epileptic psychosis: Any psychotic state lasting for more than 6 months in patients with epilepsy.

experienced psychotic episodes at any time in their history. The others include psychotic episodes newly occurring postoperatively, psychotic episodes corresponding to diffuse spike and wave discharges in EEG findings, and other miscellaneous psychotic episodes of an obscure nature. In agreement with the current data, previous studies have shown that an overwhelming majority of epileptic psychosis can be explained by the first three major subcategories. For example, CP occupied 33.3% (n = 102) in the series ofAdachi et al. (personal communication) and CP plus AIP 75.4% (n = 58) in the series of Matsuura et al. (2004) which agree well with the figures shown in Table 8.2 .

As for primary psychotic disorders, one of the most widely used criteria of psychiatric diagnosis, DSM-IV (American Psychiatric Association, 1994) subdivides primary psychotic disorders mainly into five subcategories: nuclear schizophrenia, schizophreniform disorder (SFD), brief psychotic disorder (BPD), delusional disorder, and schizoaffective disorder. In DSM-IV, the pivotal reference point on which the first three psychotic disorders are divided is time criteria. On the other hand, the determinant features of the last two categories are the contents of the psychotic experience. Figure 8.1 is a rough sketch of the interrelationships between subcategories of primary psychotic disorders in DSM-IV and corresponding epileptic psychoses. Since the duration of psychotic episodes might be a potent determinant of the contents of psychotic episodes at the same time,

Affective

Non-affective

Affective

Non-affective

days 1 month

6 months years days 1 month

6 months years

Duration of psychosis

Epileptic psychoses Q Primary psychotic disorders

FIGURE 8.1 Duration of illness of primary psychotic disorders and corresponding epileptic psychoses.

comparisons would be more unbiased if the durations matched, at least roughly. Along that line, good matches to AIP and CP ideally would be SFD and schizophrenia, respectively. If the same rule is applied, PIP should be preferentially compared with BPDs, because most episodes of PIP remit within 1 month (Adachi et al.; Levin, 1952 ; Logsdail and Toone 1988; So et al., 1990; Savard et al., 1991; Devinsky et al.; 1995 ; Umbricht et al.; 1995 ; Kanemoto 1996, 2002; Kanner et al.; 1996 ; Lancman 1999). While transient psychotic episodes are more often encountered than chronic ones in consecutive series of patients with epilepsy, as shown above, this trend seems to be reversed in populations with primary psychotic disorders (Perala et al.; 2007; . Although this could be more apparent than real as a result of a failure to recruit some patients with transient psychotic episodes into the group with primary psychotic disorders, nevertheless, a simple comparison between functional and epileptic psychosis without further specification would reveal only a difference between subacute and chronic courses of psychotic illnesses, instead of an aimed comparison. Actually, such matching based on time criteria between subcategories of primary psychotic disorders and epileptic psychoses can only be done with difficulty at present, because psychopathological observations devoted to SFD and BPD are mostly skipped in the recent literature. Under the rubric of acute and transient psychotic disorders (ATPD) of ICD-10 (Pull et al.; 1984; World Health Organization, 1992), a comparatively greater number of psychopathological descriptions are found (Marneros et al.; 2005). However, as already noted, a dichotomy of transient psychosis with illness duration of 1 and 6 months in the DSM criteria conforms better to the well-recognized division of transient epileptic psychoses into PIP and AIP. Thus, reference to a mixture of literature based on DSM and ICD is preferable especially for this review of transient psychotic episodes.

TABLE 8.3 Clinical features of CP in comparison with other organic psychoses

■ Predominance of Schneiderian first-rank symptoms

■ Less frequent visual hallucinations

■ Less frequent rapidly changing higher cognitive function except for epileptic seizures

Note: Diffuse Lewy body disease (DLBD) and Systemic lupus erythematosus (SLE) psychoses as model organic psychoses. CP: Chronic psychosis.

TABLE 8.4 CP with and without preceding AIP episodes

CP without preceding AIP episodes (n = 36)

AIP evolving into CP (n = 24)

TLEa

41.7% (n = 15)

82.6% (n = 19)

Others

II 4)

Source: Data recalculated from Kanemoto et al. (2001).

aTLE was diagnosed here only if complex focal seizures except for those of apparent frontal origin were registered, or if typical auras with limbic characteristics such as déjà vu and ictal fear preceded seizures with impaired consciousness, including secondarily generalized seizures. CP: Chronic psychosis; AIP: Acute interictal psychosis; TLE: Temporal lobe epilepsy.

Source: Data recalculated from Kanemoto et al. (2001).

aTLE was diagnosed here only if complex focal seizures except for those of apparent frontal origin were registered, or if typical auras with limbic characteristics such as déjà vu and ictal fear preceded seizures with impaired consciousness, including secondarily generalized seizures. CP: Chronic psychosis; AIP: Acute interictal psychosis; TLE: Temporal lobe epilepsy.

Chronic epileptic psychosis vs. schizophrenia

Superficially, the comments of previous authors on the psychopathologi-cal similarities that appear to exist between CP and functional schizophrenia are conflicting (Gibbs, 1951; Hill, 1953 ; Pond, 1957 ; Flor-Henry, 1969 ; Taylor, 1972; Stantage and Fenton, 1975 ; Jensen and Larsen, 1979 ; Perez and Trimble, 1980; Toone et al, 1980; Parnas et al, 1982; Sherwin et al.; 1982; Edeh and Toone, 1987 ; Stevens, 1988; Roberts et al.; 1990; Trimble, 1991; Mace, 1993 ; Bruton et al.; 1994; Kanemoto et al.; 2001; Matsuura et al, 2004). However, this diversity of opinions seems to be more apparent than real in some aspects. First, the problem of control subjects should be mentioned. When looking at other representative organic psychoses such as those occurring in diffuse Lewy body disease (Del Ser et al.; 2000; Ballard et al, 2001) and SLE psychosis (World Health Organization, 1992; Iverson, 1993 ; Velakoulis et al, 2006; Wekking, 1993; Yu et al, 2006), the similarities between CP and schizophrenia supervenes (Table 8.3). On the other hand, dissimilarities are obvious when CP is directly compared with schizophrenia (Table 8.4) (Slater and Beard 1963; Perez and Trimble 1980; Toone et al.; 1980; Tadokoro et al, 2007). For example, visual hallucinations are often assumed to be more frequently encountered in patients with CP when schizophrenia is adopted as a control, while the reverse is true when compared with other organic psychoses. Further, the important question that should be asked is whether the psychopathological difference, if any, between CP and schizophrenia is really qualitative. In other words, some authors suspect that the apparent psychopathological characteristics of CP are nothing more than artifacts resulting from a less severe course of illness. Matsuura et al. (2004) were the first to ask this question seriously. Thereafter, after recruiting all consenting patients with interic-tal psychosis and schizophrenia during the same study period, we also confirmed significantly lower scores in the group with epileptic psychosis using assessments with PANSS (Positive and Negative Syndrome Scale). Matsuura et al. concluded that the differences in symptom profiles in both groups were quantitative rather than qualitative, and that a psychopathological distinction between both groups could not be maintained. However, their conclusion requires further amplification, because epileptic psychosis was treated as a unified entity in their analysis (so was CP and AIP in ours), which inevitably biases epileptic psychoses toward lower scores.

The heterogeneity of CP, especially in association with TLE, should also be addressed, because the reported proportion of TLE varies greatly among published studies (Slater and Beard, 1963 ; Bruens, 1971; Shukla et al.. 1979 ; Perez and Trimble 1980; Parnas et al.. 1982; Adachi et al.. 2000; Kanemoto et al.. 2001; Adachi et al.; 2002). In Table 8.5, patients who had CP without preceding AIP episodes (18%) and those who had AIP episodes evolving into CP (11%) in our series are compared. Strikingly, the correlation between each group with TLE showed a statistically significant difference. While the second group was mainly associated with TLE, accompanied epilepsy types varied considerably in the first group. In our series, CP without preceding AIP episodes showed a more insidious onset and took a clinical course scarcely distinguishable from functional schizophrenia in a substantial number of patients. Such an observation regarding the first CP group leads to another fundamental question of whether a personal history of epilepsy increases the susceptibility to nuclear schizophrenia. This question dates back to the former "psychodynamic hypothesis ; ' proposed by Pond (1957), which is echoed later in the holistic concepts of Schmidt and Wolf (1989) and Wolf (1991). A recent study by Qin et al. (2005), one of the largest population-based studies to date to investigate schizophrenia-like psychosis in epilepsy, seems to answer this question in the affirmative, though a number of limitations such as preclusion of ambulatory patients from the study, lack of direct contact with the patients, and the non-critical acceptance of epilepsy types diagnosed by physicians with presumably extremely diverse backgrounds, diminish the validity of their results in regard to other subsidiary questions. In addition, the obscure nature of the allegedly generalized type of epilepsy, which remained unanswered whether it included secondarily

TABLE 8.5 Clinical features of CP in comparison with schizophrenia

■ Better pre-morbid personality

■ Well-retained affect (less negative symptoms)

■ Deteriorates finally to organic type of impairment rather than a typically schizophrenic defect state

■ Paranoid features predominate generalized seizures or not and whether this concept should be understood in the frame of epileptic seizures or epileptic syndromes, makes their results, especially those concerning epilepsy types, unreliable. However, such shortcomings are shared by all previous population-based studies on this topic (Krohn 1961; Helgason 1964; Gudmundsson 1966; Zielinski 1974; Jalava and Sillanpaa 1996 ; Bredkjaer et al.; 1998; Qin et al., 2005). Nevertheless, even with these limitations, their answer to the main question remains valid and is supported by several other studies as well (Jalava and Sillanpaa, 1996; Bredkjaer et al.; 1998). Separated from epilepsy, a variety of types of insults to brain tissue, such as head trauma (Zhang and Sachdev, 2003; David and Prince, 2005) and intrauterine infection (Kendell and Kemp, 1989) , irrespective of localization, are known to increase the risk of later development of schizophrenia. It is plausible that epilepsy could be such a non-specific contributor to developing schizophrenia. If that is the case, some proportion of CP, presumably the first group in our series, should be regarded as genuine schizophrenia that only becomes manifested with epilepsy as a precipitating factor.

In contrast, when discussing the second CP group, CP following repeated AIP episodes, true epileptic psychosis may be in question. In this situation, seizures may somehow modify the brain over the long term, which results in some structural change that leads to the genesis of psychosis. Indeed, it remains unsettled whether seizures themselves cause permanent changes to brain tissue, however, there is some evidence of plastic regenerative changes in response to repeated occurrences of seizures (Sutula, 2004) and brief psychotic episodes (Umbricht et al.; 1995; , with a proportion of patients developing CP on follow-up. It is important to repeat here that, in our series, this development from AIP into CP was rather specific to patients with TLE. In a review of data from depth EEG studies of patients who underwent lobectomy procedures, Mace (1993) suggested a unique electrophysiological interrelationship between limbic epilepsy and schizophrenia. As illustrated in Figure 8.2, both schizophrenia and CP are reported to exhibit spike discharges alongside the whole limbic circuit, including the septal and amygdalo-hippocampal regions. However, spiking is most marked in the sep-tal area in schizophrenia and in the amygdalo-hippocampal region in TLE without psychosis. Mace postulated that CP mimics the distribution of spiking seen in schizophrenia, though it remains to be distinguished from that of schizophrenia. It follows that both schizophrenia and TLE are disorders of the limbic circuit, with only different components that are preferentially disturbed. Thus, CP represents a shifted pattern of disturbance within the limbic circuit toward schizophrenia.

Acute interictal psychosis vs. schizophreniform disorder

A literature search revealed no previous studies that directly compared AIP either with SFD (DSM-IV) or ATPD (ICD-10), however, most of the features listed in Table 8.5 as characteristics of epileptic psychoses, in contrast to those of schizophrenia, are shared in common with SFD as well as ATPD. Based on the present

Schizophrenia

Limbic epilepsy with psychosis

Limbic epilepsy

Schizophrenia

Limbic epilepsy with psychosis

Limbic epilepsy

Spiking; S Septal area; AH Amygdalo-Hippocampal area

FIGURE 8.2 Hypothesis of unique electrophysiological interrelationships between limbic epilepsy and schizophrenia (Mace, 1993). Source: Data from Kendrich and Gibbs (1957) and Heath (1986) are schematized.

TABLE 8.6 Delusion/hallucination ratios in patients with epileptic psychosis and schizophrenia

Schizophrenia

Interictal psychosis

(n = 13)

(n = 46)

0.37 (SD = 0.17)

0.49 (SD = 0.11)

Note: F = 7.37, p = 0.009; t = 2.32, p = 0.035.The delusion/hallucination ratios presented here were calculated using PANSS scores. Scores of hallucinatory behavior are the numerators, while those of delusion plus suspiciousness are the denominators.

Source: Recalculated from personal data in a prospective study in the process of submission by Tadokoro et al. (2007)

Note: F = 7.37, p = 0.009; t = 2.32, p = 0.035.The delusion/hallucination ratios presented here were calculated using PANSS scores. Scores of hallucinatory behavior are the numerators, while those of delusion plus suspiciousness are the denominators.

Source: Recalculated from personal data in a prospective study in the process of submission by Tadokoro et al. (2007)

knowledge, no phenomenological differences between AIP and SFD for both symptomatology and course of illness appear to exist, except for the relative predominance of paranoid complaints. In Table 8.6, personal data in this respect are presented. However, as mentioned above, this could also be an artifact merely as a result of the difference in duration of psychosis.

In Table 8.7, AIP with and without complete remission at the time of examination were demonstrated as a function of linking with TLE. Paradoxically, AIP with complete remission exhibited a less related link with TLE, just like CP without preceding AIP episodes. This is in sharp contrast to the high proportion of TLE in patients with AIP that eventually evolves into CP. Even if a massive inclusion of extra-temporal and generalized epilepsies in CP without preceding AIP episodes can be understood under the rubric of the "epilepsy as a non-specific risk factor

TABLE 8.7 AIP with and without complete remission

AIP with complete remission (n = 81)

AIP evolving into CP (n = 23)

TLEa

49.4% (n = 40)

82.6% (n = 19)

Others

50.6% (n = 41)

17.4% (n = 4)

Source: Recalculated data from Kanemoto et al. (2001).

aTLE was diagnosed here only if complex focal seizures except for those of apparent frontal origin were registered, or if typical auras with limbic characteristics such as déjà vu and ictal fear preceded seizures with impaired consciousness, including secondarily generalized seizures. CP: Chronic psychosis; AIP: Acute interictal psychosis; TLE: Temporal lobe epilepsy.

Source: Recalculated data from Kanemoto et al. (2001).

aTLE was diagnosed here only if complex focal seizures except for those of apparent frontal origin were registered, or if typical auras with limbic characteristics such as déjà vu and ictal fear preceded seizures with impaired consciousness, including secondarily generalized seizures. CP: Chronic psychosis; AIP: Acute interictal psychosis; TLE: Temporal lobe epilepsy.

TABLE 8.8 Incidence of drug-induced and alternative psychosis

Schizophrenia (n = 54)

Psychotic disorders (n = 78)

Non-schizophrenic

Drug-induced

7 (13.0%)

31 (39.7%)

Alternative

8 (14.8°%)

33 (42.3%)

Note:A statistically significant difference was seen between the groups (p < 0.01). Source: Cited from Kanemoto et al. (2001) ;

Note:A statistically significant difference was seen between the groups (p < 0.01). Source: Cited from Kanemoto et al. (2001) ;

for schizophrenia" hypothesis, this cannot be applied easily to AIP with complete remission, because the resulting clinical picture including the transient nature differs decisively from schizophrenia. Most episodes in so-called drug-induced epileptic psychosis as well as the controversial alternative psychosis fall into this category. While alternative and drug-induced psychosis tend to be regarded as very rare entities in epilepsy centers mainly dedicated to epilepsy surgery (Mace, 1993), they stand out in tertiary epilepsy centers, where exhaustive pharmacotherapy is routinely attempted for intractable epilepsy for an extended period of time by physicians (Wolf, 1991; Adachi et al., 2000; Kanemoto et al., 2001) . As shown in Table 8.8, more than one third of the group of patients with non-schizophrenic epileptic psychosis in our previous series, mostly those with AIP, were composed of the alternative or drug-induced type (Kanemoto ;t al., 2001; . It should also be noted that drug-induced psychosis and alternative psychosis are closely interrelated. Indeed, two thirds of drug-induced psychotic episodes (30 of 45 episodes) became manifest in the form of alternative psychosis.

Usually, drug-induced or alternative psychosis appears not within days, but rather within weeks and lasts for more than 1 month and less than half a year, which agrees well with the concept of SFD. Since alternative psychosis has an intrinsic relationship to seizure activity, though the specific involvement of relevant antiepileptics such as ethosuximide (Wolf, 1991; Schmitz and Trimble, 1998), viga-batrin (Sander et al., 1991; , and zonisamide (Kanemoto et al., 2001; may modify the clinical picture, it seems to be a good candidate as a genuine epileptic psychosis.

Postictal psychosis vs. brief psychotic disorder (or bouffée délirante)

Bouffée délirante is a traditional term used in French psychiatry for primary psychotic disorder of short duration (Ferrey and Zebdi, 1999 ; Pichot, 1986; Pillmann et al.; 2003; Pull et al.; 1984) . The clinical features listed by Pichot (Pichot, 1986) , such as sudden onset, "bolt from the blue", delusions characterized by numerous, diverse, and protean delusional themes without recognizable structure and cohesive-ness, sometimes accompanied by hallucinations, clouding of consciousness associated with emotional instability, and a rapid return to the premorbid level of functioning, all show strong phenotypic similarities to PIP. However, bouffée délirante, which fulfills these strict criteria, is reported to represent only 2.4% of all patients with non-organic psychotic disorders (Pull ;t al., 1984; , in contrast to the continuing popularity of that diagnosis among French clinicians (Ferrey and Zebdi, 1999).

As mentioned in the introduction section, based on the duration of psychosis, BPD is in good accordance with PIP just like bouffée délirante. However, little has been reported about the precise psychopathological nature of this DSM-IV category. Thus, more definite conclusions await precise case control studies between these groups in the future, though some speculation can be made based on previous reports of PIP, BPD, ATPD, and bouffée délirante as well as our own data. Episodes in the nuclear group of PIP show a very stereotyped course of illness (Logsdail and Toone 1988; Savard et al., 1991; Devinsky et al., 1995 ; Umbricht et al., 1995 ; Kanemoto ;t al., 1996; Kanner ;t al., 1996 ; Oshima ;t al., 2006; . Following clustered complex partial seizures or secondarily generalized seizures, mental function returns to the premorbid level of functioning, except for a subtle feeling of derealization in some patients. Following this intervening lucid interval, which lasts for 1—3 days on average (Adachi et al, 2007), a rapidly increasing emotional lability with a mostly hypomanic nature comes to the fore, culminating into polymorphous psychosis without a recognizable structure or cohesiveness within a few days. The most notable difference between nuclear PIP and BPD/ bouffée délirante lies in how the symptoms develop, rather than what kind of symptoms are presented. A delicate inquiry during the lucid interval often reveals a unique feeling of detachment from the surrounding environment with perfectly preserved cognitive function. In contrast to bouffée délirante or BPD, the initial hypomanic state is strikingly short (usually from 12 to 36 hours) and tends to remain purely affective, uncontaminated by various psychotic complaints such as protean delusional themes and visual hallucinations. It should be noted, however, that the "bouffée délirante-type" clinical picture soon predominates during the ensuing stage shortly after the initial hypomanic stage. In the nuclear group of PIP, initial detached and ensuing affective stages, mainly with elevated moods, are so characteristic and regularly repeating that pertinent intervention during the affective stage could often prevent PIP from developing fully into frank psychosis (Lancman, 1999).

In our recent study (Oshima et al.; 2006; , we focused on a variant of PIP that showed a different clinical picture from nuclear PIP. Typically, episodes of this variant of PIP widely outnumber those of the nuclear type and often occur without an intervening lucid interval. A noted similarity between the contents of illusory experiences during PIP and those during aura was also suggested. In this variant, complex partial seizures can occur even in the midst of PIP. This variant of PIP often overlaps with peri-ictal psychosis (Hermann et al.; 1982; Wieser et al.; 1985 ; Kanemoto, 1997 ; Takeda et al.; 2001), in which psychotic symptoms develop gradually and parallel to increases in seizure frequency (Trimble and Schmitz, 1997). Wiesers hypothesis, which assumes circumscribed limbic status epilepticus limited within the limbic circuit as an underlying pathogenesis, may explain this variant of PIP very well. A strikingly close association of PIP with TLE also supports this, which has been confirmed in previous series (Logsdail and Toone, 1988; Devinsky et al.; 1995 ; Umbricht et al.; 1995; , as well as in our series: 41 (77.4%) out of 53 patients with PIP also had TLE (Kanemoto, 2002).

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