Peri-ictal behavioural change in people with an intellectual disability

Epileptology ∎ (∎∎∎∎) ∎∎∎–∎∎∎

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Peri-ictal behavioural change in people with an intellectual disability Jessica York a,n, Mike Kerr b a b

BCUHB, Ysbyty Bryn Y Neuadd, Llanfairfechan, Conwy LL33 0HH, UK Institute of Psychiatric Medicine & Clinical Neurosciences, 2nd Floor, Haydn Ellis Building, Maindy Road, Cardiff CF24 4HQ, UK

art ic l e i nf o

a b s t r a c t

Article history: Received 13 February 2014 Accepted 24 July 2014

The purpose of this article is twofold. Firstly we review the knowledge on peri-ictal behaviour change and its importance in people with an intellectual disability. Secondly we explore methods of identifying peri-ictal behaviour change in people with an intellectual disability through data from a pilot project. The literature search identified a clear association between seizure activity and behaviour change in people with epilepsy and no intellectual disability; but for people with intellectual disability research is scarce and conflicting. The pilot project provided data on three individuals. This showed behavioural inconsistencies from one month to the next independent of seizure activity. There is a sparsity of research on peri-ictal behaviour change pertaining to individuals with intellectual disabilities and epilepsy. Further research into this area is needed to clearly ascertain the presence (or not) of an association between epilepsy and behavioural changes in people with intellectual disabilities. Novel methodology specific to people with an intellectual disability should be considered. One such methodology would be an extended period of descriptive analysis in the form of a prospective single case design. & 2014 Elsevier GmbH. All rights reserved.

Keywords: Intellectual disabilities Peri-ictal Behavioural

1. Introduction Behavioural changes, both real and imagined, have been recognised in association with epilepsy since antiquity (Masia and Devinsky, 2000). The pervasive negative portrayal of behavioural changes in people with epilepsy (PWE) has caused stigmatisation and led many to hide their disorder (Masia and Devinsky, 2000). Recent research has shown an association between the presence of active epilepsy and behavioural change (Kanner, 2001; Silberman et al., 1994). Peri-ictal behavioural and cognitive changes cause disability and distress in PWE; despite this they are poorly investigated and recognised (Boylan, 2002; Mula and Monaco, 2011). Epilepsy is common and severe in people with intellectual disabilities (PWID) (Espie et al., 2012). Peri-ictal changes are of increasing interest in terms of behavioural change yet are poorly understood in PWID (Boylan, 2002).

2. The phases of peri-ictal change The peri-ictal period refers to a period of days before and after a seizure (Boylan, 2002). It consists of pre-ictal, ictal and post-ictal periods (Boylan, 2002). Research has demonstrated major and prolonged changes in motor cortex excitability in the pre and the n

Corresponding author.

postictal period (Badawy et al., 2009). This is in keeping with the growing body of evidence that supports that seizures begin and end after we initially thought (Boylan, 2002). 2.1. Pre-ictal period The pre-ictal period consists of two distinct entities epileptic auras and prodromes. Epileptic auras are ictal events manifesting as alterations in subjective perception and mostly occur several seconds up to a few minutes before seizure onset (Maiwald et al., 2010). They include formed images, humming, buzzing, irritability, jamais vu, time distortion, affective changes (Silberman et al., 1994); also insomnia, fearfulness, headaches, elation, emotional distress, epigastric sensations and some patients call out a warning of an imminent seizure (Boylan, 2002). Prodromes are sensations preceding a seizure by a period of hours to days (Maiwald et al., 2010). They are often associated with detectable surface EEG change (Mula et al., 2010). They may present as increased irritability, apprehension, mood lability, depression, psychosis, and directed aggression any of which may last several minutes, hours or days before a seizure (Marsh and Rao, 2002). Pre-ictal symptoms may wax and wane, but generally escalate up to the time of the seizure (Marsh and Rao, 2002). Up to 29% of PWE report prodromal sensations more than 30 min prior to seizures; despite this the significance of prodromes is poorly understood (Maiwald et al., 2010; Marsh and Rao, 2002). Research has repeatedly identified BOLD (blood oxygen level

http://dx.doi.org/10.1016/j.epilep.2014.07.002 2212-8220/& 2014 Elsevier GmbH. All rights reserved.

Please cite this article as: York J, Kerr M. Peri-ictal behavioural change in people with an intellectual disability. Epileptology (2014), http://dx.doi.org/10.1016/j.epilep.2014.07.002i

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dependent) fMRI changes occurring several minutes before seizure onset (Baumgartner and Aull-Watschinger, 2005). The process of ictogenesis therefore probably evolves over minutes or hours and involves a spatially distributed neuronal network with a complex interplay of excitatory and inhibitory processes (Baumgartner and Aull-Watschinger, 2005). 2.2. Ictal period Behavioural changes and psychopathology may be seen during the ictal period (during an ictal EEG discharge) especially in association with simple and complex partial seizures (Lancman, 1999). Ictal psychiatric disturbances include – anxiety, intense feelings of fear or horror, panic attacks, depressed mood, tearfulness, sexual excitement, paranoia, hallucinations, illusions, laughter, forced thoughts, obsessions, déjà vu and other memory experiences, confusion, aggression/violence (Marsh and Rao, 2002). They are more commonly associated with seizures originating from the frontal and temporal lobes (Adachi et al., 2000; Swinkels et al., 2005). 2.3. Postictal period The term postictal describes changes in behaviour, motor function and neuropsychological performance that may arise immediately after a seizure, or be delayed in onset, and last seconds to days (Boylan, 2002; Remi and Noachtar, 2010). The postictal period leaves a trail of altered brain function (So and Blume, 2010). It is likely that the emergence of postictal behavioural change is related to the brain's homoeostatic response to seizure and continued non-convulsive epileptic discharges (Boylan, 2002; Elliott et al., 2009). There are many types of behavioural change in the post ictal period, some of which are noted below. Post ictal aggression may be acute in onset (occurring several minutes after a tonic clonic seizure when the patient is confused) or sub acute (occurring hours to days after a seizure) (Gerard et al., 1998; Yankovsky et al., 2005). Sub acute post ictal aggression is rare (Gerard et al., 1998; Yankovsky et al., 2005). PIP (Post Ictal Psychosis) is characterised by an episode of psychosis occurring within one week, after a seizure (Morrow et al., 2006). The concept of PIP was introduced in the 19th century but it was not established as a clinical entity until the 1990s (Oshima et al., 2006). Lishman believed PIP to be an extension of the post-ictal confusional state with clouding of consciousness or at least amnesia for the episode as a key characteristic (Prendergast et al., 1999). More recently it has become accepted that patients frequently have no evidence of clouded consciousness, as supported by Logsdail and Toone's definition (Joshi et al., 2006; Prendergast et al., 1999). PIP is common, accounting for approximately 25% of psychoses in epilepsy and may be associated with profound morbidity (Morrow et al., 2006; Prendergast et al., 1999; Trimble et al., 2010). It generally follows an exacerbation in seizure frequency or intensity and emerges after a lucid interval (Akanuma et al., 2005). In certain populations, e.g. PWID, PIP can cause very difficult management problems; recognition of the condition is important (Trimble et al., 2010). The duration of PIP ranges from 1 to 90 days and is likely to be longer in PWID (Trimble et al., 2010). Postictal headaches are prevalent, moderate to severe in intensity, last many hours and frequently have characteristics of migraine; they impinge on patient quality of life (Ekstein and Schachter, 2010). Depressive postictal symptomatology is relatively common in patients with treatment resistant epilepsy; it arises in approximately 50% of patients and has a median duration of 24 h, but can last up to two weeks (Kanner et al., 2010; LaFrance et al., 2008).

Postictal depression describes a period of depressive symptomatology that typically occurs within 5 days of a seizure and lasts more than 24 h (Kanner et al., 2010). It may arise immediately after a seizure but more typically occurs after a latent symptom free period and rarely meets the criteria of DSM IV (Kanner et al., 2010). Postictal anxiety occurs in 45% of patients with a median duration of symptoms of 6–24 h (Mula et al., 2010). Postictal manic symptoms arise in approximately 22% of PWE, some authors have made close associations between post ictal mania and PIP (Kanner et al., 2010; Mula and Monaco, 2011; Mula et al., 2010). Typically post ictal mania presents with racing thoughts and excessive energy lasting on average 2 h (Kanner et al., 2010).

3. Peri-ictal behaviour change in PWID The importance of being aware of functional and behavioural consequences of epilepsy in PWID is cited in the literature and acknowledged by Psychiatrists working in the field (Espie et al., 2012). Turky et al. (2008) concluded that children with cognitive impairment and severe epilepsy were at higher risk of developing behavioural and emotional problems. It is also recognised that post-ictal psychosis can be difficult to manage and of longer duration in PWID (Trimble et al., 2010). Publications in this area concentrate on a specific phenomena occurring either pre or post-ictally (e.g. post or pre-ictal affective changes (Kanner et al., 2010; Marsh and Rao, 2002)). There is little literature relating to the study of behavioural changes in the periictal period for PWID. Bonaventura et al. (2006) reported peri-ictal neuroimaging findings of a patient with Fragile X Syndrome in status epilepticus. Clinical practice recognises the importance of ictal behavioural change, especially fluctuation in conscious level associated with Non-Convulsive Status Epilepticus. Research has concentrated on establishing if PWID and epilepsy, on average present with greater behavioural disturbances than PWID and no epilepsy. Little distinction has been made between inter-ictal and peri-ictal periods in previous research relating to PWID and epilepsy.

4. Behaviour change in people with intellectual disabilities (PWID) and epilepsy Behavioural problems in PWID have long been considered a major impediment to successful and sustained community placements and general adjustment (Grizenko et al., 1991). A widely accepted definition is provided by Emerson (2001) “Culturally abnormal behaviour(s) of such an intensity, frequency or duration that the physical safety of the person or others is likely to be placed in serious jeopardy, or behaviour which is likely to seriously limit use of, or result in the person being denied access to, ordinary community facilities.” The causation of behavioural change is complex including communication problems, the nature of the cognitive impairment and the presence of psychiatric pathology. Independent of the presence of epilepsy, PWID are more likely to develop a psychiatric disorder than those without (Smith and Matson, 2010). It is postulated that underlying neurological damage, causing ID, may affect behaviour and emotional responses (Grizenko et al., 1991). Associated brain damage may also cause changes and abnormalities in perception, discrimination and the ability to abstract, leading to concrete coping mechanisms (Ghaziuddin, 1988). Additionally environmental factors may pose challenges and threats that exceed the patient's comprehension and ability to adapt, all which contribute to the presentation of behavioural challenges (Grizenko et al., 1991). PWID can also differ from the rest of the

Please cite this article as: York J, Kerr M. Peri-ictal behavioural change in people with an intellectual disability. Epileptology (2014), http://dx.doi.org/10.1016/j.epilep.2014.07.002i

J. York, M. Kerr / Epileptology ∎ (∎∎∎∎) ∎∎∎–∎∎∎

population in their response to life events; apparently commonplace life events may acquire immense psychological meaning (Ghaziuddin, 1988), this is further compounded under emotional stress as it causes a tendency to become disorganised; a process described as cognitive disintegration (Ghaziuddin, 1988). Psychiatric and medical diagnoses are generally more difficult to establish in PWID with lower functional levels, secondary to limited social skills, limited verbal communication, potential presence of behavioural problems and environmental factors (Deb and Hunter, 1991; Roberts et al., 2005; Smith and Matson, 2010). Traditional methods of assessing psychiatric disorders rely on self-reporting, interviews and behavioural observations (Smith and Matson, 2010). In PWID, these methods are more challenging with a greater reliance of third party reports and objective measures. Clinical features of psychiatric disorders are often atypical and co-morbidity is common. 5. The use of rating scales to measure behaviour There are a range rating scales for psychopathology and aberrant behaviour designed for use in PWID. We describe two widely used and practical measures here. The PAS-ADD (Psychiatric Assessment Schedule for Adults with Developmental Disabilities) Checklist is a screening instrument specifically designed to help staff recognise mental health problems in PWID and help them decide if it is appropriate to refer the individual onto secondary care (Moss et al., 1998). It is a validated tool that can be used by untrained people to identify PWID at risk of developing psychiatric illness (Sturmey et al., 2005). The PAS-ADD checklist is quick and easy to use, but not recommended as a sole method of identify psychiatric disorders amongst PWID (Sturmey et al., 2005; Taylor et al., 2004). The PAS-ADD checklist uses ICD 10 criteria and generates three threshold scores that reliably identify possible psychiatric disorder (Espie et al., 2003). It consists of a life events checklist and 29 symptom items scored on a four point Likert scale (Moss et al., 1998). The Aberrant Behaviour Checklist has been extensively validated as a tool for behaviour abnormality; and it has been recommended for PWID and epilepsy (Capone et al., 2005; Espie et al., 2003; Moss et al., 1998). Statistical analyses of the questionnaire have shown high internal consistency, good test–retest reliability, inter-rater reliability and good concurrent validity with Part II of the ABC and direct observation of behaviours (Aman et al., 1985; Newton and Sturmey, 1988). The ABC has five subscales that are scored across 58 items each on a four point Likert scale (Moss et al., 1998). Ferdinand assessed psychopathology in children and adolescents using categorical and dimensional measures and compared the predictive value of the measures for outcome, approximately 3 years later (Dunn et al., 2009). They discovered that, the two

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different approaches were useful, neither was superior, and each gave important but different information for predicting outcomes (Dunn et al., 2009). Therefore interpreting information gleaned from behavioural studies needs to be carefully analysed as different tools study different aspects of behaviour; making results from studies using only one tool unlikely to be able to make generalised conclusions. 6. Measurement of peri-ictal change in PWID – an exploratory study In the context of the relative dearth of information on peri-ictal change in people with an intellectual disability we performed an exploratory study on a small sample to examine whether behavioural change was measurable. Ethical and Research and Development approval was obtained and consent/assent was obtained for each participant. Patients were selected from a specialist tertiary epilepsy clinic for PWID in South Wales (UK). Validated measures of behaviour and psychopathology were applied, namely the ABC and PAS-ADD Checklist as discussed above. Three individuals with an intellectual disability participated in the study. Average pre-ictal, inter-ictal and post-ictal behaviours each month were calculated; two months of data was collected. Carers and family members completed the questionnaires. Questionnaires were completed and returned on three patients. Tables 1 and 2 highlight changes seen in the study period for the three participants. The findings of this small study demonstrate a fluctuation in the data obtained from one month to the next for the same questionnaire and also for each month between questionnaires. Furthermore data collection proved complicated for carers and the utility of such an approach is in doubt. 7. Novel approaches – an extended period of descriptive analysis Single subject research designs have a place in medical research, for example Nof1 trials enable a single participant to undergo periods of comparative treatment (Cepeda et al., 2008; Guyatt et al., 1990). They empower the patient, improve doctor patient communication and increase clinician confidence in treatment options (Guyatt et al., 1990; Nickles et al., 2005). It is recognised within the field of behavioural analysis that indirect methods of measuring behaivour (e.g. rating scales) are a less valid (Cooper et al., 2007). Such Nof1 studies allow for direct measurement of behaviour and the benefits of this may outweigh the drawback of the limited statistical power of a single case design (Guyatt et al., 1990). If a number of individuals are simultaneously analysed then the primary limitation, of single subject research designs, can partly be overcome (Ridenour et al.,

Table 1 ABC total scores pertaining to the postictal, pre-ictal and inter-ictal periods of months 1 and 2 of data collection. Patient

Seizure number month 1

Postictal month 1 ABC

Preictal month 1 ABC

Interictal month 1 ABC

1 2 3

1 7C 4

10 5 22

3 7 9

20 2 7

Patient

Seizure number month 2

Postictal month 2 ABC

Preictal month 2 ABC

Interictal month 2 ABC

1 2 3

1 9C 3P

5 5 13

4 15 17

14 2 20

High ABC scores are associated with greater behavioural anomalies. C – denotes the presence of a seizure cluster at some point that month. P – denotes the presence of a prolonged seizure at some point that month.

Please cite this article as: York J, Kerr M. Peri-ictal behavioural change in people with an intellectual disability. Epileptology (2014), http://dx.doi.org/10.1016/j.epilep.2014.07.002i

J. York, M. Kerr / Epileptology ∎ (∎∎∎∎) ∎∎∎–∎∎∎

4

Table 2 PAS ADD total scores pertaining to the postictal, pre-ictal and inter ictal periods of months 1 and 2 of data collection. Patient

Seizure number month 1

Postictal month 1 PAS-ADD

Preictal month 1 PAS-ADD

Interictal month 1 PAS-ADD

1 2 3

1 7C 4

15 21 7

7 18 14

2 21 3

Patient

Seizure number month 2

Postictal month 2 PAS-ADD

Preictal month 2 PAS-ADD

Interictal month 2 PAS-ADD

1 2 3

1 9C 3P

9 5 11

9 9 9

0 1 10

PAS-ADD scores are associated with greater levels of psychopathology. None of the patients had any recent and significant life events as defined by the PAS-ADD. C – denotes the presence of a seizure cluster at some point that month. P – denotes the presence of a prolonged seizure at some point that month.

2009). It could be argued that the detail lost on the individual level, in large group designs, far outweighs concerns regarding statistical importance (Cooper et al., 2007). Descriptive assessments involve direct observation of behaviour and events in the individual's natural environment (Anderson and Long, 2002; Sloman et al., 2005). It's a structured approach to exploring environment–behaviour relations (McComas et al., 2009; Thompson and Iwata, 2007). Observers record the frequency or duration of specific events and the behaviour of the participant and their carers and it can take the form of unscripted descriptive observations (Camp et al., 2009; Sloman et al., 2005; Woods et al., 2010). Descriptive analyses have many uses in the field of ABA e.g. they may be used to help operationally define appropriate or inappropriate behaviours, give additional information relating to baseline rate, latency, duration or intensity of target behaviour (Samaha et al., 2009), describe response sequences or the temporal organisation of behaviour (Borrero and Borrero, 2008). Descriptive assessments are useful when it is difficult or impossible to conduct analogue/ experimental functional analyses or when their results are inconclusive (Anderson and Long, 2002; Borrero and Borrero, 2008). In this instance the independent variable (seizure activity) is unpredictable and the dependent variable (peri-ictal behavioural change) is currently unknown; therefore an experimental functional analysis would not be possible. The ABC method of descriptive analysis involves recording antecedent and consequent environmental events that are associated with each instance of problem behaviour (Pence et al., 2009). Taking the above points into consideration, the following methodology could be an alternative approach to measuring peri-ictal behavioural change in PWID. The emphasis would be on an in-depth study of the individual. Duration – 3 months of observation and 3 months of measurement. Patient selection would include individuals with ID and seizures occurring on average more than once a month. Initial background information would have to be gathered regarding communication methods, medication and comorbid conditions. Appropriate ethical and R&D approval would be sort and consent/assent established. Daily telephone conversations would occur between the researcher and the carers. These would be unscripted and concentrate on changes in behaviour and the occurrence of any concerning behaviour. The ABC method would be implement;ed to explore these areas further. Additional data relating to the occurrence of seizure activity and other potential environmental confounders would also be sort. The descriptive analysis would identify the presence, or not, of a specific dependent variable (behavioural change) related to the independent variable (seizure activity). If a dependent variable is identified then it should be carefully defined and measured over time.

The experimental approach would have to be flexible to the needs of the experiment and the individual.

8. Conclusion Peri ictal behavioural change is likely to have significant impact on PWID and their carers. Our focus should be on the identification of such changes, as without this treatment strategies cannot be implemented. Novel methodologies may be needed to aid identification.

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Please cite this article as: York J, Kerr M. Peri-ictal behavioural change in people with an intellectual disability. Epileptology (2014), http://dx.doi.org/10.1016/j.epilep.2014.07.002i