Elsevier

Epilepsy Research

Volume 108, Issue 7, September 2014, Pages 1228-1237
Epilepsy Research

Long-term memory performance after surgical treatment of unilateral temporal lobe epilepsy (TLE)

https://doi.org/10.1016/j.eplepsyres.2014.05.002Get rights and content

Highlights

  • Long-term memory performance after TLE surgery was evaluated.

  • Verbal learning and memory declined in both left and right TLE groups.

  • Individual postoperative long-term memory performance was variable.

  • Risk factors for decline in verbal memory were left side of surgery, better baseline performance and older age at surgery.

Summary

Long-term cognitive and memory performance after surgical treatment of unilateral temporal lobe epilepsy (TLE) was investigated in a series of 98 patients. Neuropsychological evaluation was performed preoperatively and after one and three years postoperatively. Fifty-eight patients (59%) became seizure-free (Engel's class I). Verbal learning and memory declined in long-term follow-up in both left and right TLE groups. Visual memory remained stable. Ongoing postoperative seizures were related to decline in the immediate recall of logical prose, and postoperative seizure-freedom to improvement in verbal fluency in patients with left TLE. There was significant variability in the individual postoperative long-term memory performance. Left side of surgery, better baseline performance and older age at surgery were identified as risk factors for individual decline in delayed verbal memory. Selected patients undergoing surgery for drug-resistant TLE are at risk for significant postoperative memory decline especially after left temporal lobe surgery. Preoperative counseling and long-term follow-up of cognitive performance in individual patients is recommended. Additionally, more accurate predictors of individual postoperative memory performance would be needed.

Introduction

Surgery is an effective treatment for drug resistant temporal lobe epilepsy (TLE) in adults (Wiebe et al., 2001, Spencer et al., 2005) and currently 66% of patients become postoperatively seizure-free in the long-term (Tellez-Zenteno et al., 2005). When defining the surgical success, the improved seizure control must be weighed against possible risks of surgery. Depending on the classification the overall rate of complications after TLE surgery is 9−14% (Behrens et al., 1997, Rydenhag and Silander, 2001, Tanriverdi et al., 2009), but often long-term neuropsychological or psychiatric outcomes have not been included.

The knowledge of the cognitive sequelae of TLE surgery is still somewhat concentrated to those occurring during the first postoperative year. Although many short-term follow-up studies have addressed the postoperative cognitive performance both at the group level and based on the analyses of individual change scores, the maximum duration of follow-up in these studies has usually extended only up to one year. At group level, the most consistent finding has been the decline in verbal memory performance after dominant temporal lobe resection (Lee et al., 2002); whereas the pattern of visual memory change after non-dominant temporal lobe resection has been more variable (Vaz, 2004). However, the impact of surgery on cognitive functions is multifaceted and between 10 and 20% of patients may experience a postoperative improvement in their cognitive function (Baxendale et al., 2008).

If one evaluates the short-term follow up studies, then it seems that the most important risk factors for postoperative cognitive decline are dominant temporal lobe surgery (Lee et al., 2002) and factors indicating structural or functional status of the ipsilateral temporal lobe. These factors include better baseline performance (Hermann et al., 1995, Helmstaedter and Elger, 1996, Stroup et al., 2003, Gleissner et al., 2004, Baxendale et al., 2006), relatively intact hippocampal structures in the preoperative magnetic resonance imaging (MRI) (Trenerry et al., 1993, Stroup et al., 2003), absence of or mild hippocampal sclerosis in the pathological analyses (Sass et al., 1994, Martin and Grote, 2002) and better Wada memory performance after a contralateral injection (Kneebone et al., 1995, Stroup et al., 2003). In some studies older age at the time of surgery (Hermann et al., 1995, Helmstaedter and Elger, 1996, Baxendale et al., 2006), later age at onset of epilepsy (Wolf et al., 1993, Hermann et al., 1995), male gender (Trenerry et al., 1995, White et al., 2002), extent of resection (Helmstaedter and Elger, 1996, Joo et al., 2005), and seizure outcome (Novelly et al., 1984, Sanyal et al., 2005) have also been identified as potential risk factors for the postoperative memory decline. On the other hand, a shorter duration of epilepsy and a better cognitive capacity to allow the development of compensatory strategies were identified as predictive factors for postoperative memory improvement following TLE surgery (Baxendale et al., 2008).

A growing number of studies have evaluated the long-term postoperative cognitive outcome of TLE surgery (Engman et al., 2001, Engman et al., 2004, Engman et al., 2006, Helmstaedter et al., 2003, Rausch et al., 2003, Alpherts et al., 2004, Alpherts et al., 2006, Bjørnaes et al., 2005, Grammaldo et al., 2009, Andersson-Roswall et al., 2010, Andersson-Roswall et al., 2012, Baxendale et al., 2012). However, the number of patients in these studies has ranged between 25 and 147, with a mean follow-up between 2 and 13 years. Although some of these studies indicate cognitive stability (Engman et al., 2001, Engman et al., 2006, Alpherts et al., 2004, Grammaldo et al., 2009, Andersson-Roswall et al., 2012, Baxendale et al., 2012), a decline in verbal memory during long-term follow-up has been reported, particularly after left or dominant anterior temporal lobe resection (Helmstaedter et al., 2003, Rausch et al., 2003, Engman et al., 2004, Bjørnaes et al., 2005, Alpherts et al., 2006, Andersson-Roswall et al., 2010). Analyses of risk factors for postoperative memory change also indicate that patients with left or dominant side of surgery may be at greater risk for postoperative verbal memory decline (Helmstaedter et al., 2003, Rausch et al., 2003, Alpherts et al., 2006), when compared to patients with right TLE. Better baseline performance can be associated with better postoperative memory performance (Helmstaedter et al., 2003, Alpherts et al., 2006), but also with greater decrease in postoperative memory (Rausch et al., 2003). In two studies the poor postoperative seizure control has been identified as a risk factor for postoperative decline in memory function (Helmstaedter et al., 2003, Baxendale et al., 2012). However, in another study becoming and remaining seizure-free after surgery did not result in a better memory performance in the long-term (Alpherts et al., 2006). Finally, younger age at surgery (Alpherts et al., 2006, Grammaldo et al., 2009), tailored resection (Helmstaedter et al., 2003) as well as male gender (Grammaldo et al., 2009) have been associated with better or improved postoperative memory performance.

The aim of this study was (1) to assess memory and cognitive performance after surgical treatment of unilateral TLE during three-year follow-up, and (2) to identify possible predictive factors for postoperative decline in memory performance, with special emphasis on the impact of postoperative seizure outcome on the long-term memory outcome.

Section snippets

Patients

The patients were retrieved from a series of 172 consecutive adult patients, who were operated on at Kuopio Epilepsy Center, Kuopio University Hospital between December 1988 and November 2002 because of drug resistant TLE (Fig. 1). Among these 128 patients with unilateral TLE were identified. The other 44 patients operated for TLE had documented or probable bitemporal epilepsy or multifocal epilepsy, or the epileptic focus could not otherwise be completely removed. Also three patients with

Clinical characteristics and preoperative cognitive performance

The clinical characteristics of the patients are displayed in Table 1. The left and right TLE groups were comparable in terms of age at onset of epilepsy, duration of epilepsy, etiology of epilepsy, seizure frequency, age at surgery and postoperative seizure outcome. There were more female patients in the right TLE group (65%) than in the left TLE group (39%) (p < 0.05). Fifty-eight patients (59%) achieved Engel's class I (free of disabling seizures) outcome during the three-year follow-up.

Discussion

We analyzed memory and cognitive performance after surgical treatment of unilateral TLE during three-year follow-up in a series of adult patients. In our study verbal learning and memory declined in the long-term follow-up both in the left and the right TLE groups. Visual memory performance remained stable. In previous studies the verbal memory decline in the group analyses has been restricted to patients with left temporal lobe surgery (Engman et al., 2004, Bjørnaes et al., 2005, Alpherts et

Conflicts of interest

L.J. has received travel honoraria from UCB Pharma and Eisai. R. K. has served on scientific advisory boards for UCB Pharma, Eisai, Lundbeck, GlaxoSmithKline and Fennomedical, and has received funding for travel and speaker honoraria from UCB Pharma, Eisai, GlaxoSmithKline, Medtronic, Pfizer, Orion and Fennomedical. The remaining authors have no conflicts of interest.

Acknowledgements

We warmly thank the late Heleena Hurskainen (MSc) for performing all the neuropsychological tests in the current study and for her dedicated work in the field of neuropsychology in the Kuopio University Hospital Epilepsy Surgery Program. We also thank the late professor of neurosurgery Matti Vapalahti (MD, PhD) for operating many patients in this study and especially for his pioneering work in the field of neurosurgery in the Kuopio University Hospital. Your knowledge and friendship will be

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