Resective surgery for focal cortical dysplasia in children

2 downloads 0 Views 517KB Size Report
Abstract. Purpose Seizure freedom following resection of focal cortical dysplasia (FCD) correlates with complete resection of the dys- plastic cortical tissue.
Childs Nerv Syst DOI 10.1007/s00381-016-3070-x

ORIGINAL PAPER

Resective surgery for focal cortical dysplasia in children: a comparative analysis of the utility of intraoperative magnetic resonance imaging (iMRI) Matthew F. Sacino 1 & Cheng-Ying Ho 2 & Matthew T. Whitehead 3 & Tesfaye Zelleke 4 & Suresh N. Magge 1 & John Myseros 1 & Robert F. Keating 1 & William D. Gaillard 4 & Chima O. Oluigbo 1

Received: 22 November 2015 / Accepted: 21 March 2016 # Springer-Verlag Berlin Heidelberg 2016

Abstract Purpose Seizure freedom following resection of focal cortical dysplasia (FCD) correlates with complete resection of the dysplastic cortical tissue. However, difficulty with intraoperative identification of the lesion may limit the ability to achieve the surgical objective of complete extirpation of these lesions. Intraoperative magnetic resonance imaging (iMRI) may aid in FCD resections. The objective of this study is to compare rates of postoperative seizure freedom, completeness of resection, and need for reoperation in patients undergoing iMRIassisted FCD resection versus conventional surgical techniques. Methods We retrospectively reviewed the medical records of pediatric subjects who underwent surgical resection of FCD at Children’s National Medical Center between March 2005 and April 2015. Results At the time of the last postoperative follow-up, 11 of the 12 patients (92 %) in the iMRI resection group were seizure free (Engel Class I), compared to 14 of the 42 patients (33 %) in the control resection group (p = 0.0005). All 12 of the iMRI patients (100 %) achieved complete resection, compared to 24 of 42 patients (57 %) in the control group * Chima O. Oluigbo [email protected]

1

Department of Neurosurgery, Children’s National Medical Center, 111 Michigan Avenue NW, Washington, DC 20010, USA

2

Department of Neuropathology, Children’s National Medical Center, Washington, DC 20010, USA

3

Department of Neuroradiology, Children’s National Medical Center, Washington, DC 20010, USA

4

Department of Neurology, Children’s National Medical Center, Washington, DC 20010, USA

(p = 0.01). One (8 %) patient from the iMRI-assisted resection group has required reoperation, compared to 17 (40 %) patients in the control resection group. Conclusion Our results suggest that the utilization of iMRI during surgery for resection of FCD results in improved postoperative seizure freedom, completeness of lesion resection, and reduction in the need for reoperation.

Keywords Intraoperative MRI . Focal Cortical Dysplasia . Epilepsy surgery . Pediatric . Utility

Introduction Focal cortical dysplasia (FCD) is a common cause of intractable epilepsy in children, constituting about 40 % of pediatric epilepsy surgical cases [10, 13]. Seizure freedom following surgical resection of the epileptogenic lesion is between 46 and 67 % [1, 3, 6, 7, 12, 20, 27]. The most significant predictor of postoperative seizure freedom is a complete resection of the cortical dysplastic tissue [3, 5, 7, 12, 13, 19, 23, 24]. However, difficulty with intraoperative identification of the FCD lesion may limit the ability to achieve this surgical objective of complete extirpation of these lesions. The incorporation of intraoperative magnetic resonance (iMRI) into existing epilepsy surgical protocols has previously been shown to enhance intraoperative decision making and aid in achieving greater postoperative outcomes [22, 29]. The use of iMRI may, therefore, preclude the need for repeat craniotomies, which reduces patient morbidity and could be economically beneficial [26]. In this study, we aim to assess the utility of iMRI-incorporated resection on completeness of resection and postoperative seizure outcomes in comparison

Childs Nerv Syst

to conventional operative technique and protocol in pediatric patients undergoing respective epilepsy surgery for FCD.

neuroradiologist and discussed jointly. Upon evidence of residual dysplasia, the patient was returned to surgery for further evaluation of the resection cavity.

Methods

Duration of operative event

Following approval by the Institutional Review Board (IRB), we retrospectively reviewed the medical records and epilepsy protocol brain magnetic resonance imaging (MRI) scans of 55 pediatric subjects undergoing resection for intractable epilepsy secondary to FCD at Children’s National Medical Center between March 2005 and April 2015. Surgical resections from March 2005 to June 2013 were performed using standard microsurgical techniques incorporating neuronavigation (Stealth Station navigation system, Medtronic-Sofamor Danek, USA Patients) and electrocortigraphy (ECoG). The standard microsurgical technique used in the resection of FCDs in our institution has been previously well described [19]. From January 2014, we modified our surgical practice and began to use intraoperative magnetic resonance imaging to ensure complete resection of the cortical dysplasia. We analyzed and compared patients undergoing standard protocol resection (n = 43) with patients undergoing iMRIguided resection (n = 12). Factors assessed include demographics, length of surgery, completeness of resection, postoperative seizure outcome, postoperative neurological morbidity, and need for reoperation. Postsurgical seizure outcome was assessed utilizing the Engel Epilepsy Surgery Outcome Scale and comparatively analyzed at the last postoperative follow-up visit.

Duration of the operative event (OE) was recorded as the time of entry into the OR suite until exit from the OR suite. Hence, in addition to surgical time, this encompassed time for anesthesia, placement of line, prepping of the patient, acquisition of all MRI scans, and anesthesia recovery. On average these extrasurgical activities took up to 2–3 h. We felt it was relevant to include these other (extraoperative) components because they are a reflection of the complexity of coordination of care and therefore indirect costs in undertaking this type of procedure. Statistical analysis Demographic and clinical statistics were recorded as medians or mean ± standard error of mean (SEM), and follow-up was recorded as median values. Statistical analysis between groups was performed via Student t test for continuous variables and Fischer exact test for categorical variables. Kaplan–Meier method was used to estimate time to seizure recurrence for the two groups. Log rank test was used to compare time to seizure recurrence for the two groups. All tests performed were two tailed, and a p < .05 was considered significant. Data analysis was performed using R statistical software (version 3.1.2; R Founding for Statistical Computing, Vienna Austria).

iMRI surgical setup Neuronavigation was utilized in all cases for initial localization of the FCD lesion, and the lesion was further confirmed by intraoperative ECoG using subdural strips, grids or depth electrodes in 9 of 12 patients (ECoG was not used in cases where it posed risk to critical vasculature). Surgical resection was undertaken utilizing standard microsurgical techniques until the surgeon felt a complete resection had been achieved. At this time, the patient was prepped using standard MR safety considerations and transferred to the adjoining 1.5 T iMRI system (Greenline Achieva Nova Dual, Philips Medical System, Best, The Netherlands). The intraoperative sequences taken in the iMRI cohort included a T1-weighted 3D Fast Field Echo (TE 3.2 ms, TR 6.7 ms, matrix 240 × 240, FOV 300 mm, slice thickness 1.6 mm, slab 34 cm) reformatted into orthogonal planes, T2-weighted Turbo spin-echo (TE 100 ms, TR 4019 ms, matrix 296 × 225, FOV 280 mm, slice thickness 3 mm), and diffusion-weighted imaging (DWI) sequence (TE 103 ms, TR 5096 ms, matrix 152 × 106, FOV 230 mm, slice thickness 4 mm). The images were then reviewed independently by the attending pediatric neurosurgeon and pediatric

Results Patient demographics Between March 2005 and June 2013, 43 consecutive pediatric patients (28 males and 15 females) underwent conventional (non-iMRI) resections of FCD. One patient was lost to followup. Between January 2014 and April 2015, 12 consecutive pediatric patients (four males and eight females) underwent iMRI-assisted resection of FCD. Patient demographics are summarized in Table 1. There was no significant difference between the two groups for mean age at surgery (p = 0.33), mean age of seizure onset (p = 0.85), mean duration of seizures (p = 0.95), and postoperative length of stay (p = 0.28). Postoperative follow-up for the iMRI cohort ranged from postoperative day 14 to 12.91 months (median, 7.11 months) and from postoperative day 12 to 8.8 years (median, 24.21 months) for the conventional resection cohort. Histopathology and localization of the seizure foci are summarized in Table 2. FCD was localized in tissue adjacent to

Childs Nerv Syst Table 1 Patient demographics and surgical data

iMRI-incorporated resection group Male/female ratio

4/8

Mean age at surgery (year) Mean age at seizure onset (year) Mean duration of seizures (month) Mean duration of operative event (min) Post-operative length ofstay (day)

Conventional epilepsy protocol resection group

P value

28/14

0.05

8.83 ± 1.6

7.10 ± 0.8

0.33

2.75 ± 1.0 56.25 ± 13.8

2.53 ± 0.5 55.19 ± 8.0

0.85 0.95

373 ± 22.9 3.50 ± 0.3

286 ± 9.0 4.05 ± 0.3

0.0001 0.28

Mean represented with ±SEM

eloquent cortex in 7 of the 12 (58.3 %) patients undergoing iMRI-assisted resection and 18 of the 42 (43 %) patients undergoing conventional resection.

Surgical data Mean duration of operative event was different between the two groups (p = 0.0001). IMRI-assisted resections ranged from 261 to 508 min (mean, 373 ± 22.9 min) and conventional resections ranged from 199 min to 431 min (mean, 286 ± 9.0 min). A total of 41 intraoperative MR images [three-dimensional (3D)-SPGR, T2-weigthed turbo spin echo, and DWI] were acquired (mean per case, 3.4 image ± 0.5 images) in the iMRI resection cohort, with total scanning acquisition time ranging 7 to 39 min (mean, 18.9 ± 3.0 min). Scanning acquisition, in addition to intraoperative preparation, transfer to the MRI suite, and return to surgery accounted for approximately 60 min.

Table 2

Descriptive characteristics iMRI-assisted resection cohort

Pathology type Type 1 FCD Type 2A FCD Type 2B FCD Undetermined FCD Lesion location Frontal Parietal Temporal Occipital Insular Multilobar Eloquent cortex

2 (17 5 (42 2 (17 3 (25

Conventional resection cohort

%) %) %) %)

19 (45 %) 6 (14 %) 15 (36 %) 2 (5 %)

2 (17 %) 5 (42 %) 1 (8 %) NA 3 (25 %) 1 (8 %) 7/12 (58 %)

14 (33 %) 7 (17 %) 10 (24 %) 4 (10 %) 2 (5 %) 5 (12 %) 18/42 (43 %)

Postoperative completeness of resection and seizure outcome Postoperative 1.5 T or 3.0 T MRI confirmed incomplete gross total resection (residual dysplasia) in 18 of the 42 (43 %) patients in the conventional resection group. Each of these 18 patients experienced recurring seizures postoperatively (median duration to seizure recurrence was 2.18 months, ranging from postoperative day 1 to 7.7 years). Moreover, 13 of these 18 patients (72 %) returned to surgery at a later date for re-resection of the residual dysplastic tissue. In the iMRI group intraoperative indication of residual FCD and further resection was carried out in 4 of the 12 patients (33.3 %). Overall, 1.5 T iMRI or 3 T postoperative MRI confirmed that all 12 patients in iMRI group achieved gross total resection. This was a statistically significant increase in rate of completeness of resection compared to conventional surgery (p = 0.01). Ten patients in the conventional resection cohort continued to experience seizures postoperatively despite postoperative MR indication of a complete resection. Moreover, four of these patients returned to surgery at a later date for reresection with extraoperative brain mapping through grids that had been placed intraoperatively. Additionally, one patient from the iMRI cohort experienced seizures postoperatively despite no clear indication of residual dysplasia on 1.5 T iMRI and 3.0 T postoperative MRI. The patient later returned to surgery at a later date for re-resection with extraoperative brain mapping through grids that had been placed intraoperatively. Overall, there was a reduction in the rate of reoperations that neared statistical significance between the iMRI cohort and the conventional cohort, (1/12 versus 17/42; p = 0.08). At the time of the last postoperative follow-up (median duration of 7.11 months for the iMRI cohort and 24.21 months for the conventional resection cohort), complete seizure freedom (Engel Class I) was achieved in 11 of the 12 (92 %) patients in the iMRI-assisted cohort (Fig. 1a) compared to 14 of the 42 (33 %) in the conventional resection cohort (Fig. 1b) (p = 0.0005). The median duration to seizure recurrence in patients from the conventional resection group (n = 28) was postoperative 2.59 months (ranging from

Childs Nerv Syst Fig. 1 a Pie chart illustrating iMRI-assisted resection cohort seizure freedom at last postoperative follow-up. b Pie chart illustrating conventional resection cohort seizure freedom at last postoperative follow-up

postoperative day 1 to 7.7 years). One patient in the iMRI cohort experienced recurrence of seizures within the first month following surgery. Log rank test showed no difference in time to seizure recurrence between the two cohorts (p = 0.13). Kaplan–Meier analysis (Fig. 2) showed that the probability of no-recurrence at 5 months was 0.558 (95 % CI, 0.42 to 0.74) for the conventional FCD resection group and 0.857 (95 % CI, 0.63 to 1.0) for the iMRI-assisted group.

Postoperative neurological morbidity Neurological morbidity was noted in only patients with FCD lesions within or adjacent to eloquent cortex. However, these expected morbidity tended to be more transient in the patients who had undergone iMRI-guided resective surgery. In the iMRI cohort, postsurgical neurological complications included transient (resolved by first postoperative follow-up) hemiparesis in four patients (FCD located adjacent to motor cortex). Additionally, one of those four patients experienced expected transient alteration of sensation in the lower extremity (FCD located adjacent to sensory cortex). In the conventional resection cohort, 3 patients developed transient deficits, while 12 patients developed permanent (unresolved by last postoperative follow-up) deficits.

Fig. 2 Kaplan–Meier curve of seizure recurrence in patients undergoing standard epilepsy protocol FCD resection (n = 28)

Case illustrations Case 1 A 4-year old girl presented with intractable epilepsy secondary to right frontal cortical dysplasia (Fig. 3a). She underwent right frontal craniotomy for excision of this FCD guided by neuronavigation using conventional microsurgical techniques. At surgery, it was felt that complete resection of the lesion had been achieved based on visual and tactile assessment as well as corresponding improvement in post resection electrocorticography (ECoG) findings. However, postoperative brain MRI scan showed residual cortical dysplasia tissue (Fig. 3b), and the patient had recurrence of seizures within 1 month postoperatively. The patient subsequently underwent a second resection to remove the residual dysplasia at the margins of the previous surgery. Case 2 A 9-year old girl presented with intractable epilepsy secondary to a focal cortical dysplasia located in the right posterior insula and the posterior aspect of the right Sylvian fissure (Fig. 4a). Using neuronavigation and 3DGM derived from preoperative scans the lesion was identified in the right posterior sylvian fissure. Resection was carried out utilizing standard microsurgical technique until the surgeon felt a complete extirpation of the lesion had been achieved. At this point, the patient was prepped and transferred to the adjoining 1.5 T iMRI suite. 3D T1WI and FSE T2WI MRI scans were obtained, and residual dysplasia was identified anterior to the resection cavity (Fig. 4b). An update to neuronavigation was performed, the patient was returned surgery, and further resection of the iMRI directed residual dysplasia was carried out. Once the surgeon felt complete resection of the residual dysplasia had been achieved, the patient was prepped and transferred to the iMRI scanner for a second set of 3D T1WI and FSE T2WI images. This indicated a complete resection had been achieved (Fig. 4c). The patient is seizure free postoperatively.

Childs Nerv Syst Fig. 3 a Preoperative T2W brain MRI scan showing area of blurring of gray-white matter margin suggestive of a focal cortical dysplasia within right frontal lobe. b Postoperative T2W brain MRI showing residual cortical dysplasia

Discussion In comparison to conventional neurosurgical resection of FCD, surgery guided by iMRI is associated with increased rates of postsurgical seizure freedom (Engel Class I) (p = 0.0005). We found that the utilization of iMRI resulted Fig. 4 a Preoperative T1W brain MRI scan showing area of blurring of gray-white matter margin suggestive of a focal cortical dysplasia deep within the right posterior Sylvian fissure. b Sagittal reconstruction of 3D T1W MR image acquired intraoperatively showing residual cortical dysplasia tissue just anterior to the resection cavity in the right posterior insula. c Intraoperative T1W brain MRI scan confirming complete resection of the area of focal cortical dysplasia

in significantly increased rates of gross complete resection (p = 0.01) and reduced the need for further reoperations (p = 0.08). The only potential disadvantage to iMRI utilization we note is that iMRI-guided surgeries were 30 % longer on average compared to non-iMRI resections (p = 0.0001).

Childs Nerv Syst

We previously reported that completeness of resection of the radiological dysplastic lesion is the most significant predictor of seizure freedom [19]. In the conventional resection group, nearly half of the surgeries were recorded as incomplete resections upon postoperative MRI analysis. Over a median duration of 2.2 months after surgery, all of these patients went on to have recurring seizures and in many cases this necessitated reoperation. Intraoperative MR imaging, on the other hand, provides near real-time detection of the lesions during the surgery, allowing the surgeon to re-evaluate the surgical site and if necessary extend surgical extirpation of dysplastic tissue leading to a complete resection. With the incorporation of iMRI into our epilepsy surgery protocol, we were able to increase our rate of complete resections by over 40 % and achieve gross complete resections in all 12 patients. Importantly, this has reduced the need for repeat surgeries by one-third over the conventional resection cohort. While reoperation for intractable epilepsy has been shown to result in favorable seizure freedom in 19–57 %, there have been few studies looking specifically at surgical outcomes following reoperation for pediatric patients with FCD [2, 4, 8, 11, 25, 28]. Two recent studies have reported achieving seizure freedom in 61 and 50 % upon further surgeries in pediatric and mixed aged patients with intractable epilepsy secondary to FCD; however, it is difficult to correlate such findings as each cohort is small and heterogeneous [13, 21]. Moreover, further reoperations lead to greater chance of post-surgical neurological complications and surgical site infections (SSIs) [2, 16]. We found IMRI to provide a powerful improvement in postsurgical outcomes over conventional; however, we report limitations in its utility. Importantly, we note that 10 patients in the conventional resection cohort and 1 patient in the iMRI resection group experienced recurrence of seizures without any definitive findings of residual dysplasia on postoperative MRI. While the underlying cause in each case is undetermined, FCD is one of the most common pathologies of MRI-negative intractable epilepsy [30]. Detection of dysplastic lesions on imaging is often complicated by the subtle, diffuse nature of the lesion and difficulty of identifying the margins [14, 15, 31, 32]. For this reason, it is possible that these patients may still have residual microscopic dysplasia at the margins of the resection or even other microscopic foci which are not visible on MRI. Hence, a major possible limitation to iMRI utility is the presence of MRI-negative nonlesional dysplasia. Furthermore, surgical trauma, swelling, and blood products have the ability to distort intraoperative imaging, making it hard to discern areas of residual dysplastic tissue. In our current study, our center utilized a 1.5 T MRI scanner for intraoperative images which has been shown to have inferior resolution and quality to that of a 3 T scanner [18]. The case illustrations demonstrate the capacity of iMRI to aid in achieving high rates of complete extirpation of FCD,

and hence achieving seizure freedom and precluding the need for reoperation. Additionally, iMRI utilization is safe, with no reported surgical hazards in this cohort. In fact, in patients who had FCD lesions located within or adjacent to the motor or sensory cortex, expected neurological morbidity in the form of hemiparesis or hemianesthesia was transient in all patients who underwent iMRI-assisted surgery. We found no difference in postoperative length of stay stays between our two cohorts. In addition to patient safety and surgical outcome advantages, iMRI may have important health economic benefits as well. Shah et al. previously reported that the primary economic benefit of iMRI utilization during resective surgery is the ability to prevent immediate re-operations; in such instances saving approximately $24,000 per case over conventional epilepsy surgery [26]. Given that 17 of the 42 patients in our conventional resection cohort have undergone further resections, and reoperation has been precluded in 4 of the 12 cases in our iMRI cohort by intraoperative intervention, this illustrates the great potential iMRI has in reducing healthcare costs. Importantly, a complete economic valuation of iMRI should include necessary capital costs associated with purchasing a dedicated iMRI scanner and yearly investments on maintenance and upgrades [9, 17, 26]. A possible limitation of this study is the unmatched duration of the last postoperative follow-up between the cohorts. However, while the iMRI cohort median duration of follow up is short at 7.1 months; it should be noted that of the 28 patients in the conventional resection cohort who continued to have seizures the median duration of postoperative recurrence was 2.6 months. Another possible confounding variable is that different surgeons performed the conventional resection surgeries and iMRI surgeries which may have introduced operator dependency bias. Finally, differences in field strength (1.5 versus 3 T) and other neuroassistive technologies across cases may have skewed our results. To illustrate the full surgical and health economic potential of iMRI utilization for FCD resection, a randomized prospective study of a larger cohort with a longer postoperative follow-up duration may be needed.

Conclusion Our results suggest that the utilization of iMRI during surgery for resection of FCD results in improved postoperative seizure freedom, completeness of lesion resection and reduction in the need for reoperation. Additionally, iMRI utilization is a safe and may be an economically beneficial addition to standard epilepsy surgery protocols. Acknowledgments We wish to acknowledge Ling Cai, Ph.D., and Chaojie Yang, B.S., for their assistance with statistical analysis.

Childs Nerv Syst Compliance with ethical standards Conflict of interest None of the authors have a conflict of interest.

References 1.

2.

3.

4.

5.

6.

7.

8.

9.

10.

11.

12.

13.

14.

15.

Alexandre V Jr, Walz R, Bianchin MM, Velasco TR, TerraBustamante VC, Wichert-Ana L, et al. (2006) Seizure outcome after surgery for epilepsy due to focal cortical dysplastic lesions. Seizure 15(6):420–427 Bower RS, Wirrell EC, Eckel LJ, Wong-Kisiel LC, Nickels KC, Wetjen NM (2015) Repeat resective surgery in complex pediatric refractory epilepsy: lessons learned. J Neurosurg Pediatr 16(1):94– 100 Cohen-Gadol AA, Ozduman K, Bronen RA, Kim JH, Spencer DD (2004) Long-term outcome after epilepsy surgery for focal cortical dysplasia. J Neurosurg 101(1):55–65 Cruz VB, Prayson RA (2012) Neuropathology in patients with multiple surgeries for medically intractable epilepsy. Ann Diag Pathol 16(6):447–453 Fauser S, Bast T, Altenmuller DM, Schulte-Monting J, Strobl K, Steinhoff BJ, et al. (2008) factors influencing surgical outcome in patients with focal cortical dysplasia. J Neurol Neurosurg Psychiatry 79(1):103–105 Fauser S, Essang C, Altenmuller DM, Staack AM, Steinhoff BJ, Strobl K, et al. (2015) Long-term seizure outcome in 211 patients with focal cortical dysplasia. Epilepsia 56(1):66–76 Fountas KN, King DW, Meador KJ, Lee GP, Smith JR (2004) Epilepsy in cortical dysplasia: factors affecting surgical outcome. Stereotact Funct Neurosurg 82(1):26–30 Gonzalez-Martinez JA, Srikijvilaikul T, Nair D, Bingaman WE (2007) Long-term seizure outcome in reoperation after failure of epilepsy surgery. Neurosurgery 60(5):873–880 discussion 873-80 Hall WA, Kowalik K, Liu H, Truwit CL, Kucharezyk J (2003) Costs and benefits of intraoperative MR-guided brain tumor resection. Acta Neurochirurgica Suppl 85:137–142 Harvey AS, Cross JH, Shinnar S, Mathern GW (2008) & ILAE pediatric epilepsy surgery survey Taskforce. Defining the spectrum of international practice in pediatric epilepsy surgery patients. Epilepsia 49(1):146–155 Holmes MD, Wilensky AJ, Ojemann LM, Ojemann GA (1999) Predicting outcome following reoperation for medically intractable epilepsy. Seizure 8(2):103–106 Kim DW, Lee SK, Chu K, Park KI, Lee SY, Lee CH, et al. (2009) Predictors of surgical outcome and pathologic considerations in focal cortical dysplasia. Neurology 72(3):211–216 Krsek P, Maton B, Jayakar P, Dean P, Korman B, Rey G, et al. (2009) Incomplete resection of focal cortical dysplasia is the main predictor of poor postsurgical outcome. Neurology 72(3):217–223 Krsek P, Maton B, Korman B, Pacheco-Jacome E, Jayakar P, Dunoyer C, et al. (2008) Different features of histopathological subtypes of pediatric focal cortical dysplasia. Ann Neurol 63(6): 758–769 Krsek P, Pieper T, Karlmeier A, Hildebrandt M, Kolodziejczyk D, Winkler P, et al. (2009) Different presurgical characteristics and seizure outcomes in children with focal cortical dysplasia type I or II. Epilepsia 50(1):125–137

16.

Lietard C, Thebaud V, Besson G, Lejeune B (2008) Risk factors for neurosurgical site infections: an 18-month prospective survey. J Neurosurg 109(4):729–734 17. Makary M, Chiocca EA, Erminy N, Antor M, Bergese SD, AbdelRasoul M, et al. (2011) Clinical and economic outcomes of lowfield intraoperative MRI-guided tumor resection neurosurgery. J Magn Reson Imaging: JMRI 34(5):1022–1030 18. Mellerio C, Labeyrie MA, Chassoux F, Roca P, Alami O, Plat M, et al. (2014) 3 T MRI improves the detection of transmantle sign in type 2 focal cortical dysplasia. Epilepsia 55(1):117–122 19. Oluigbo CO, Wang J, Whitehead MT, Magge S, Myseros JS, Yaun A, et al. (2015) The influence of lesion volume, perilesion resection volume, and completeness of resection on seizure outcome after resective epilepsy surgery for cortical dysplasia in children. J Neurosurg Pediatr 15(6):644–650 20. Park CK, Kim SK, Wang KC, Hwang YS, Kim KJ, Chae JH, et al. (2006) Surgical outcome and prognostic factors of pediatric epilepsy caused by cortical dysplasia. Child’s Nervous System: ChNS: Off J Int Soc Pediatr Neurosurg 22(6):586–592 21. Ramantani G, Strobl K, Stathi A, Brandt A, Schubert-Bast S, Wiegand G, et al. (2013) Reoperation for refractory epilepsy in childhood: a second chance for selected patients. Neurosurgery 73(4):695–704 discussion 704 22. Roessler K, Sommer B, Grummich P, Coras R, Kasper BS, Hamer HM, et al. (2014) Improved resection in lesional temporal lobe epilepsy surgery using neuronavigation and intraoperative MR imaging: favourable long term surgical and seizure outcome in 88 consecutive cases. Seizure 23(3):201–207 23. Rowland NC, Englot DJ, Cage TA, Sughrue ME, Barbaro NM, Chang EF (2012) A meta-analysis of predictors of seizure freedom in the surgical management of focal cortical dysplasia. J Neurosurg 116(5):1035–1041 24. Sarkis RA, Jehi LE, Bingaman WE, Najm IM (2010) Surgical outcome following resection of rolandic focal cortical dysplasia. Epilepsy Res 90(3):240–247 25. Schwartz TH, Spencer DD (2001) Strategies for reoperation after comprehensive epilepsy surgery. J Neurosurg 95(4):615–623 26. Shah MN, Leonard JR, Inder G, Gao F, Geske M, Haydon DH, et al. (2012) Intraoperative magnetic resonance imaging to reduce the rate of early reoperation for lesion resection in pediatric neurosurgery. J Neurosurg Pediatr 9(3):259–264 27. Siegel AM, Cascino GD, Meyer FB, Marsh WR, Scheithauer BW, Sharbrough FW (2006) surgical outcome and predictive factors in adult patients with intractable epilepsy and focal cortical dysplasia 2006. Acta Neurol Scand 113(2):65–71 28. Siegel AM, Cascino GD, Meyer FB, McClelland RL, So EL, Marsh WR, et al. (2004) Resective reoperation for failed epilepsy surgery: seizure outcome in 64 patients. Neurology 63(12):2298–2302 29. Sommer B, Grummich P, Coras R, Kasper BS, Blumcke I, Hamer HM, et al. (2013) Integration of functional neuronavigation and intraoperative MRI in surgery for drug-resistant extratemporal epilepsy close to eloquent brain areas. Neurosurg Focus 34(4):E4 30. Wang ZI, Alexopoulos AV, Jones SE, Jaisani Z, Najm IM, Prayson RA (2013) The pathology of magnetic-resonance-imaging-negative epilepsy. Modern Pathology Off J United States Canadian Acad Pathol Inc 26(8):1051–1058 31. Widdess-Walsh P, Diehl B, Najm I (2006) Neuroimaging of focal cortical dysplasia. J Neuroimaging Off J Am Soc Neuroimaging 16(3):185–196 32. Widdess-Walsh P, Kellinghaus C, Jeha L, Kotagal P, Prayson R, Bingaman W, et al. (2005) Electro-clinical and imaging characteristics of focal cortical dysplasia: Correlation with pathological subtypes. Epilepsy Res 67(1–2):25–33