| | Characterising de novo depression after epilepsy surgeryReceived 21 January 2008; received in revised form 26 September 2008; accepted 28 September 2008. Summary De novo depression is a common psychiatric sequelae of epilepsy surgery. To date, no studies have described possible clinical correlates of de novo depression in this population. This qualitative study presents a detailed analysis of five cases of de novo depression. Data were collected from patients’ medical files and routine in-depth psychosocial and psychiatric interviews (the Austin CEP Interview). All patients who developed de novo depression underwent anterior temporal lobectomy (ATL). Four out of five cases occurred within the first 3 months following surgery, and all were preceded by significant post-operative irritability reported by the patient's family. All experienced post-operative marital/relationship conflict that appeared to be a catalyst for deteriorating mood. Post-operative seizures were not temporally linked to the onset of depressive symptoms. This series provides an initial account of factors associated with de novo depression following anterior temporal lobectomy and may be of use in guiding larger scale studies. Introduction  Surgical excision of epileptogenic tissue via anterior temporal lobectomy (ATL) is a well-established method of controlling intractable complex partial seizures. Although ATL often results in excellent seizure control, it has been clearly documented that patients are at risk of post-operative psychiatric complications, including depression (Devinsky et al., 2005, Wrench et al., 2004). Approximately a third of patients undergoing epilepsy surgery have a history of major depression with prevalence figures ranging from 10% to 40% (Stub Naylor et al., 1994, Altshuler et al., 1999, Derry et al., 2000, Glosser et al., 2000, Ionue and Mihara, 2001, Malmgren et al., 2002, Quigg et al., 2003, Reuber et al., 2004, Wrench et al., 2004, Cankurtaran et al., 2005, Devinsky et al., 2005). Although relief from intractable seizures is accompanied by improved psychiatric and psychological well-being for many patients (Dalby, 1969, Derry et al., 2000, Spencer et al., 2003, Reuber et al., 2004, Devinsky et al., 2005), there are some who experience a significant deterioration in mood (Ring et al., 1998, Ionue and Mihara, 2001, Malmgren et al., 2002, Racine et al., 2002, Quigg et al., 2003, Cankurtaran et al., 2005). Estimates of de novo, or new onset, depression in the months or years following ATL have been reported at approximately 10% (Ring et al., 1998, Altshuler et al., 1999, Anhoury et al., 2000, Derry et al., 2000, Wrench et al., 2004, Cankurtaran et al., 2005, Devinsky et al., 2005). New onset post-operative depression has been linked to poorer quality of life, increased hospital admissions and suicide rates (Barraclough, 1981, Bladin, 1992, Nees et al., 2001, Quigg et al., 2003, Cramer et al., 2005). These deleterious effects make recognizing and treating depression a clinical imperative. To this end, studies have attempted to identify predictors of post-operative mood disturbance. Possibly the most commonly reported correlates are a pre-operative personal or family history of psychiatric disturbance (Anhoury et al., 2000, Derry et al., 2000, Quigg et al., 2003) and poor pre-operative psychosocial adjustment (Rose et al., 1995, Derry et al., 2000). The post-operative period can entail significant psychosocial adjustment challenges, including difficulties discarding the sick role and losing the consideration extended to the chronically ill. These difficulties form part of the “burden of normality” (Bladin, 1992, Babb and Brown, 1993, Wilson et al., 2001a, Wilson et al., 2004), and may contribute to a decrease in post-operative mood (Wrench et al., 2004). Epileptological factors may also be associated with depression following epilepsy surgery, with recurrent seizures linked to depression in some (Blumer et al., 1998, Reuber et al., 2004, Devinsky et al., 2005), but not all studies (Glosser et al., 2000, Suchy and Chelune, 2001, Spencer et al., 2003). Importantly, whilst all of the above variables have been linked with depression after surgery, no studies have specifically explored whether these factors predict the occurrence of de novo depression. Thus far, the only known factor linked to de novo depression is surgery to the temporal lobes compared to extra-temporal resection (Wrench et al., 2004). This suggests that disruption to key limbic system structures involved in the regulation of mood may contribute to de novo depression following ATL. To date, there has been no detailed characterization of the occurrence of de novo depression after epilepsy surgery, or the factors associated with its development. The current study began to address this gap in the literature using descriptive, detailed case analyses. Method Materials and procedure The Seizure Surgery Follow-up and Rehabilitation Program at the Austin Hospital provides intensive pre- and post-operative assessment and support of patients. As part of this Program, all patients routinely complete The Austin CEP Interview with a clinical neuropsychologist pre-operatively and at 1, 3, 6, 12 and 24 months post-operatively (Wilson et al., 1998a, Wilson et al., 1998b, Wilson et al., 1999). This standardised, in-depth, semi-structured clinical interview was originally developed by Bladin (1992) and forms the primary method of gathering clinical and research data in the Seizure Surgery Follow-up and Rehabilitation Program. It incorporates a detailed examination of patients’ psychosocial and psychiatric status and has been used to evaluate mood outcome following surgery (Wrench et al., 2004, Wilson et al., 2001b). The responses are coded on the basis of a coding manual, and previous research has shown that the overall agreement of coding for the interview averaged at 79% for nine response protocols with a range of 75–89% for individual protocols (Wilson et al., 2001b). This interview was used to glean information for each case report and also to classify patients depression status pre- and post-operatively. The interview includes coding of depression each time point using the criteria of the Diagnostic and Statistical Manual of Mental Disorders (DSM-IV) (American Psychiatric Association, 1994). The most salient psychosocial information as reported by the patients and family members were included in each case report. In addition pre-operatively, a detailed history was taken by a psychiatrist, including corroborative evidence from significant family members. This information was used to confirm the psychiatric history gathered from the CEP interview. Patients who had no record of a previous history of depression, but developed a diagnosable depression at some point in the first 2 years post-operatively were identified as de novo cases and included in the case series. All cases of de novo depression were confirmed clinically by a treating psychiatrist. Suicidal ideation and risk was assessed at each review. Risk was ascertained based on whether patients had thoughts of suicidality, active plans, access to means and reports of a previous suicide attempt. All patients described in this case series were prospectively recruited into the longitudinal study, which involved completing a range of measures to assess psychological functioning. Data on seizure and clinical variables was sought from medical records. This included a detailed neurological and seizure history, and the results of pre-operative structural and functional imaging, video EEG monitoring, and formal neuropsychological assessment. Results The prevalence rate of de novo depression after ATL in this series was 15%. The key findings for these patients are summarized in Table 1. Patient 1 – SM Medical and seizure history SM suffered measles encephalitis at 30 months with febrile convulsions. At the time of surgery she experienced approximately two seizures per week, with secondarily generalization a few times per month. On video EEG monitoring left temporal interictal spikes and independent seizures from both temporal lobes were recorded. Bilateral hippocampal sclerosis with greater atrophy on the left was seen on MRI. FDG-PET showed left temporal hypometabolism. She underwent a left ATL at the age of 31. Psychosocial history SM was educated to the second year of high school and had been employed as a shop assistant prior to surgery. She reported stigma and embarrassment about her epilepsy, with discrimination at school and in previous employment. She was in a long-term de facto relationship with a significantly older male and had a 6-year-old child. She described her partner as overprotective and controlling. SM reported that surgery offered her the opportunity to change her life. She hoped to increase her independence and leave her partner if the relationship dynamics did not improve. Although not aware of this “hidden agenda”, her partner expressed concern that surgery might make her “less dependent on him”. Post-operative follow-up SM was slow to recover from surgery and experienced significant anxiety. In the months following surgery, SM attempted to assert her independence and noted that she was a different person. Her partner struggled to cope with this change. They were offered marital counselling but refused. Nine months after surgery SM reported a change in sexual orientation from heterosexuality to homosexuality. She remained seizure-free over the 2-year follow-up period. Emergence of de novo depression The first feature of mood disturbance to emerge post-operatively was increased irritability reported by both the patient and her family 1 month after surgery. She was also experiencing panic attacks at this time. Three months after surgery she developed clinical depression. Features of her depression included decreased mood, teariness, sleep disturbance, difficulties concentrating, irritability, and appetite change with a weight gain of 13 kg in 3 months. She commenced anti-depressant treatment 9 months after surgery, but ceased this soon after due to side effects. By 1 year post-operatively she was expressing suicidal ideation in the context of continued marital conflict. Patient 2 – TM Medical and seizure history TM had late onset epilepsy at the age of 35 with approximately two complex partial seizures per month. MRI revealed post-traumatic scarring of the left temporal lobe and inferior frontal lobe that was most likely caused by a head injury at age 20 years. Ictal scalp EEG recordings showed left posterior quadrant onset. Interictal SPECT showed left anterior temporal hypoperfusion and ictal SPECT found bilateral temporal hyperperfusion that was greater on the left than the right side. He underwent a left ATL at age 46 years. Psychosocial history TM was working as a government employee prior to his surgery and had not divulged his epilepsy to his work colleagues. At the time of surgery he was married with a 1-year-old child. His wife displayed a managerial approach towards him and his epilepsy. She down played the impact of his surgery and the recovery process, contrasting with TM's clear anxiety about the procedure. He impressed as being very dependent on his wife in his day-to-day decision-making. The remaining members of TM's family were unaware of his impending surgery. Post-operative follow-up TM returned to work only 6 weeks after surgery. At this time, he reignited a long-standing dispute with his neighbour, causing significant stress to both TM and his wife. His wife felt his activity levels were excessive, and reported significant marital tension. He remained seizure-free until 9 months post-surgery, when he began to experience approximately one complex partial seizure per month. Emergence of de novo depression At his 1-month post-operative review, TM's mood was noted to be elevated. He reported feeling cured and ‘on top of the world’. By 3 months post-surgery, his mood had declined and he was experiencing bouts of teariness. TM's wife noted that he had become highly irritable both with family and friends. He denied lowered mood and was resistant to psychiatric or psychological intervention. A major depressive episode was diagnosed at his 12-month review and he was commenced on anti-depressant therapy. Features of his depression included episodes of teariness, anhedonia, decreased concentration, anergia and sleep disturbance. His depression resolved with the commencement of anti-depressant therapy and counselling. Patient 3 – WT Medical and seizure history WT began experiencing complex partial seizures at age 10. He was seizure-free from age 15 until seizures returned at age 31. MRI showed no definitive lesion. A left temporal ictal rhythm was found on EEG scalp recordings. Cerebral FDG-PET showed hypometabolism involving the left temporal lobe. He underwent a left ATL at the age of 35 years. Psychosocial history WT had completed tertiary education and was employed as a school teacher. He was married with three children and his wife was pregnant with their fourth child at the time of surgery. A history of marital difficulties predated surgery for which a brief period of marital counselling was undertaken. He had no contact with his extended family due to long-standing conflict and they were unaware of his surgery. He displayed limited insight into the demands of post-operative recovery. Post-operative follow-up Prior to being discharged from hospital, WT attempted unsuccessfully to resolve his long-standing family conflict. On his return home, he engaged in excessive activity, and expressed frustration about the limitations imposed by the recovery period. He began driving against medical instruction 4 months post-operatively. Significant marital conflict re-developed and his wife described him as a “different person”. He had allegedly become irritable, intolerant, more egocentric, quick-tempered, verbally abusive, and aggressive. He had threatened to harm both himself and his wife but never acted upon these threats. Throughout this period, he remained seizure-free. Emergence of de novo depression Following WT's discharge from hospital his wife noted his appetite was reduced, his sleep disturbed, he was expressing morbid thoughts, had withdrawn from family activities, and appeared unable to cope with any level of stress or pressure in the home setting. Despite this, WT steadfastly denied any alteration to his mood in the early post-operative period. He lost 7kg within the first 3 months of surgery and was experiencing recurring, distressing dreams. He was diagnosed with depression 3 months post-surgery. Ongoing mood fluctuations continued for the next year. He declined anti-depressant therapy. Patient 4 – NP Medical and seizure history NP experienced febrile convulsions at the age of three with complex partial seizures beginning at age 12. At the time of surgery he was experiencing approximately two seizures per month with secondarily generalization a couple of times per year. A pre-operative MRI scan showed right hippocampal sclerosis. Video-EEG monitoring found right ictal rhythm in the temporal region. Cerebral FDG-PET showed right temporal hypometabolism and an ictal SPECT found right temporal hyperperfusion. He underwent a right ATL at the age of 45 years. Psychosocial history NP had completed an apprenticeship and was employed as a building supervisor prior to his surgery. His employer was unaware of his epilepsy and he continued to drive despite medical advice. He was married with two young children. Pre-operatively, he down played the significance of his epilepsy and the impact it was having on his life. He nonetheless experienced persistent anxiety associated with risks at work and fears of losing his job. Post-operative follow-up Significant marital tension developed post-operatively in the context of adjustment difficulties. In particular, he was slow to recover from the acute effects of surgery, citing persistent headaches and his family's expectation to be “normal” quickly. He also acknowledged some long-standing communication problems with his wife, which became accentuated following surgery. The marital relationship slowly improved overtime on his return to work. He experienced two brief tonic-clonic seizures at 6 and 11 months post-surgery. Both seizures arose from sleep and were associated with extreme stress at home or work. Emergence of de novo depression At the 1-month review, NP's mood was noted to be flat. His wife described him as uncommunicative, withdrawn, pedantic, argumentative, and irritable. Whilst NP denied feeling depressed at this time, he subsequently admitted to lowered mood with increased irritability, significantly lowered libido, disturbed sleep, and diminished appetite (associated with a 12kg weight loss). He experienced ongoing concerns about the possibility of post-operative seizures and how he might cope with these. At 3 months post-surgery, he was diagnosed with an adjustment disorder with depressed mood although pharmacotherapy was not felt to be warranted by the treating psychiatrist. His depressed mood persisted until approximately 1 year post-surgery. Patient 5 – DQ Medical and seizure history DQ's seizures began at age 45 years. At the time of surgery he was experiencing approximately 15 complex partial seizures per month. A pre-operative MRI scan found no definite lesion. Ictal scalp EEG found an ictal rhythm in the right anterior temporal region. Cerebral FDG-PET was within normal limits. Ictal SPECT showed mild relative right temporal hyperperfusion. DQ underwent a right ATL at the age of 56 years. Psychosocial history DQ was educated to Year 8. He was on extended sick leave from his employment in the public service at the time of surgery. He had been married for 35 years with two adult children. His wife was highly anxious and coped poorly with her husband's seizures. DQ's reasons for seeking surgery included reducing the burden on his wife and in so doing, decreasing her levels of anxiety, as well as returning to paid employment. Post-operative follow-up DQ's post-operative recovery was complicated by a chronic subdural haematoma that became symptomatic 3 months post-surgery and required surgery. During this period DQ's wife became extremely anxious and overprotective of him, leading to considerable martial conflict. She refused to leave DQ alone, restricted his activities, and over-interpreted any medical complaints. Her level of anxiety limited any attempts by DQ to assert his independence. Whilst remaining seizure-free, he made few psychosocial gains in the first year following surgery. Emergence of de novo depression Mild emotional lability was evident in the acute recovery period. During this time, DQ's wife also noted he was more irritable and was generally slow to recover. Significant periods of lowered mood accompanied the subdural collection and its subsequent treatment. These periods were characterized by tearfulness, irritability, poor motivation, and social withdrawal. He lost 12kg in weight in the 6 months following surgery and his sleep remained poor. His mood remained variable at 1 year post-surgery. DQ refused pharmacotherapy for his depression. Discussion This study has described five cases of de novo depression that occurred within the first 2 years following ATL. Whilst previous studies have reported a similar prevalence of de novo depression (approximately 10%) (Ring et al., 1998, Altshuler et al., 1999, Anhoury et al., 2000, Derry et al., 2000, Wrench et al., 2004, Cankurtaran et al., 2005, Devinsky et al., 2005) none have attempted to characterize commonalities amongst these cases. The patients in this case series presented with common patterns of mood symptoms and these features allow possible early markers of mood deterioration to be identified. All patients underwent ATL and experienced significant relationship conflict post-operatively. Depression was heralded by irritability and a prominent change in weight occurred in four of the five cases. These commonalities may assist with the early identification and treatment of patients at risk of developing de novo depression. The emergence and nature of de novo depression Four out of the five patients developed depression in the first 3 months after surgery. This is in keeping with previous research highlighting that depression commonly presents within the first few months of seizure surgery (Blumer et al., 1998, Glosser et al., 2000, Gaitatzis and Sander, 2004). Nonetheless, one of our de novo cases occurred 12 months post-operatively. As such, whilst the immediate post-operative period presents the greatest risk, follow-up of patients and monitoring of mood should extend beyond this time frame. Accurate recognition of depression may assist in staving off many of its deleterious effects, including raised mortality via suicide. Crucially, the presence of co-morbid depression in epilepsy is frequently overlooked, and it remains under-reported and under-treated (Kanner, 2003). The importance of recognition and treatment is highlighted in this series, with four patients expressing suicidal ideation, although none were considered active suicide risks. We note that the Austin CEP includes long-term psychiatric and psychosocial follow-up of all patients. This ensured all the patients in the current series were closely monitored for suicidal ideation, and appropriate psychiatric and psychosocial support was provided. The high rate of suicidal ideation in the current series highlights the value of intensive follow-up programs that assist patients with post-operative adjustment and closely observe their mood state. Common correlates of de novo depression: stress-vulnerability This case series highlights that no single factor can predict de novo depression. The correlates identified in this series fit broadly into two categories: (1) neurobiological factors related to the site of surgical resection, and (2) psychosocial factors including the ‘burden of normality’. These two factors have previously been related to post-operative depression by our group (Wrench et al., 2004). Importantly, the individual contribution of these factors is not known, and it is likely that they interact to contribute to the development of de novo depression. All patients in the current series who developed de novo depression underwent standard ATL. It has been previously suggested that removal or deafferentation of limbic system structures key to mood via ATL may place patients at risk of exacerbating a previously existing mood disturbance, or may even cause de novo depression (Wrench et al., 2004). As such, it is possible that ATL sets up an “environment of vulnerability”, whereby surgical disruption to mesial temporal structures places patients at increased risk of mood disturbance post-operatively. In addition to this possible neurobiological ‘vulnerability’ depression in all cases occurred with in the context of life challenges and relationship conflicts. Indeed, all patients experienced significant psychosocial ‘stress’ that directly preceded their depressive episode. This ‘stress’ should be viewed within the context of pre-operative psychosocial difficulties. Superficially, the five patients in this study appeared resilient – all were previously employed, of normal intellectual ability, were either married or living with a partner, and had no personal or family psychiatric history. Epilepsy, however, had affected multiple facets of their lives, with all cases having experienced significant marital or relationship tension prior to surgery. In addition, in four of the five patients, epilepsy had formed an integral part of their pre-operative relationship dynamics, with carer and patient roles clearly defined. Post-operatively, despite relief from seizures, all five patients experienced an exacerbation of pre-operative psychosocial tension. Most saliently, marital strain was intensified in all cases and preceded the onset of the depressive episode. In particular, family members struggled to cope as patients asserted their independence. In three cases this desire to redress previous imbalances within the relationship was met with resistance from partners. This significant aggravation of marital tension has been previously described as a sociological feature of the ‘burden of normality’ (Bladin et al., 1999, Wilson et al., 2001a). This syndrome characterizes the often difficult process of adjustment following successful epilepsy surgery as patients learn to live without their epilepsy and can occur in up to two thirds of patients (Wilson et al., 2001a, Wilson et al., 2004). In our view, psychosocial stress post-operatively may be seen as a trigger or catalyst for de novo depression in the face of neurobiological risk. The precise contribution of each factor, and their possible interactions, remains unknown and cannot be clearly delineated from this small case series. Larger scale studies exploring the relative contribution of these biological and psychosocial factors may shed further light on this issue. We note that post-operative seizure activity did not coincide with the onset of depression in any case. This finding is in keeping with previous research suggesting that post-operative depression is not always associated with a poor seizure outcome (Glosser et al., 2000, Suchy and Chelune, 2001, Spencer et al., 2003). Interestingly, all patients were treated with lamotrigine, although this was also used pre-operatively. In other words, its commencement was not associated with depressive symptoms. More generally, lamotrigine is considered a mood stabilizer, and may be effective as an augmentation therapy for depression (Barbosa et al., 2003, Ettinger et al., 2006). Other clinical variables such as age of epilepsy onset, neuropsychological outcome, duration of epilepsy, and side of surgery, did not appear to impact the occurrence of de novo depression in this small sample. Conclusion This is the first paper to describe a case series of de novo depression after epilepsy surgery. 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a School of Behavioural Science, University of Melbourne, Melbourne, Victoria 3010, Australia b Department of Clinical Neuropsychology/Comprehensive Epilepsy Program, Austin Health, Melbourne, Australia c Southern Clinical School, Monash University, Melbourne, Australia  Corresponding author. Tel.: +61 3 8344 8036; fax: +61 3 9347 6618.
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