Temporal lobe epilepsy in patients with nonlesional MRI and normal memory: an SEEG study

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OBJECT

Temporal lobe epilepsy (TLE) in the absence of MRI abnormalities and memory deficits is often presumed to have an extramesial or even extratemporal source. In this paper the authors report the results of a comprehensive stereoelectroencephalography (SEEG) analysis in patients with TLE with normal MRI images and memory scores.

METHODS

Eighteen patients with medically refractory epilepsy who also had unremarkable MR images and normal verbal and visual memory scores on neuropsychological testing were included in the study. All patients had seizure semiology and video electroencephalography (EEG) findings suggestive of TLE. A standardized SEEG investigation was performed for each patient with electrodes implanted into the mesial and lateral temporal lobe, temporal tip, posterior temporal neocortex, orbitomesiobasal frontal lobe, posterior cingulate gyrus, and insula. This information was used to plan subsequent surgical management.

RESULTS

Interictal SEEG abnormalities were observed in the mesial temporal structures in 17 patients (94%) and in the temporal tip in 6 (33%). Seizure onset was exclusively from mesial structures in 13 (72%), exclusively from lateral temporal cortex and/or temporal tip structures in 2 (11%), and independently from mesial and neocortical foci in 3 (17%). No seizure activity was observed arising from any extratemporal location. All patients underwent surgical intervention targeting the temporal lobe and tailored to the SEEG findings, and all experienced significant improvement in seizure frequency with a postoperative follow-up observation period of at least 1 year.

CONCLUSIONS

This study demonstrates 3 important findings: 1) normal memory does not preclude mesial temporal seizure onset; 2) onset of seizures exclusively from mesial temporal structures without early neocortical involvement is common, even in the absence of memory deficits; and 3) extratemporal seizure onset is rare when video EEG and semiology are consistent with focal TLE.

ABBREVIATIONSEEG = electroencephalography; SEEG = stereoelectroencephalography; TLE = temporal lobe epilepsy.

Abstract

OBJECT

Temporal lobe epilepsy (TLE) in the absence of MRI abnormalities and memory deficits is often presumed to have an extramesial or even extratemporal source. In this paper the authors report the results of a comprehensive stereoelectroencephalography (SEEG) analysis in patients with TLE with normal MRI images and memory scores.

METHODS

Eighteen patients with medically refractory epilepsy who also had unremarkable MR images and normal verbal and visual memory scores on neuropsychological testing were included in the study. All patients had seizure semiology and video electroencephalography (EEG) findings suggestive of TLE. A standardized SEEG investigation was performed for each patient with electrodes implanted into the mesial and lateral temporal lobe, temporal tip, posterior temporal neocortex, orbitomesiobasal frontal lobe, posterior cingulate gyrus, and insula. This information was used to plan subsequent surgical management.

RESULTS

Interictal SEEG abnormalities were observed in the mesial temporal structures in 17 patients (94%) and in the temporal tip in 6 (33%). Seizure onset was exclusively from mesial structures in 13 (72%), exclusively from lateral temporal cortex and/or temporal tip structures in 2 (11%), and independently from mesial and neocortical foci in 3 (17%). No seizure activity was observed arising from any extratemporal location. All patients underwent surgical intervention targeting the temporal lobe and tailored to the SEEG findings, and all experienced significant improvement in seizure frequency with a postoperative follow-up observation period of at least 1 year.

CONCLUSIONS

This study demonstrates 3 important findings: 1) normal memory does not preclude mesial temporal seizure onset; 2) onset of seizures exclusively from mesial temporal structures without early neocortical involvement is common, even in the absence of memory deficits; and 3) extratemporal seizure onset is rare when video EEG and semiology are consistent with focal TLE.

Temporal lobe epilepsy (TLE) is the most common form of focal epilepsy, accounting for the vast majority of partial seizures.30,32 Most patients with TLE will improve after a temporal lobectomy, and 58% will be free of disabling seizures postoperatively.31,37 However, even after complete removal of the anterior temporal lobe and mesial structures, a significant number of patients will experience seizures again,6,17,31,32,37 which raises the possibility that in some cases of TLE the epileptogenic zone may be distributed across a wider region than the temporal lobe or may lie outside the temporal lobe altogether. A number of anatomically deep and semiologically silent areas can produce seizures clinically and electrophysiologically indistinguishable from mesial TLE, including the temporal pole,10 orbitofrontal cortex,19,34 insula,17,19 posterior cingulate gyrus,2,12 and temporoparietooccipital area.29 The distinction is important because resection of only the mesial temporal structures in these patients will not control the epileptic seizures.

Most cases of TLE are associated with evidence of mesial temporal sclerosis on MRI, and epilepsy surgery for TLE in the absence of MRI abnormalities has been shown to be associated with a significantly lower rate of seizure freedom.6–8,11,15,21,23,32,35 In addition, memory loss is often present in TLE, and material-specific memory deficits are highly specific to indicate laterality of TLE.4,9 Therefore, it might be expected that the absence of MRI abnormalities and memory deficits would suggest an extramesial or extratemporal source of the seizures, even when the ictal semiology and the video electroencephalography (EEG) results are typical of TLE. The purpose of this study is to examine stereoelectroencephalography (SEEG) localization of ictal activity and surgical outcome after temporal lobe surgery among a homogeneous group of patients with normal MRI, normal memory and semiology, and EEG typical for TLE.

Methods

Patient Population

Consecutive patients undergoing implantation of SEEG electrodes into the temporal lobe for evaluation of medically intractable epilepsy were identified from a prospectively maintained clinical database. Each patient had undergone extensive preoperative testing, including video EEG and comprehensive neuropsychological testing, and was discussed at a multidisciplinary conference of epileptologists, neurosurgeons, and neuropsychologists. Patients with seizure semiology or video EEG findings inconsistent with TLE were excluded.

Neuropsychological Testing

All patients underwent comprehensive neuropsychological testing prior to implantation of depth electrodes. Verbal memory and visual-spatial memory were assessed using the Wechsler Memory Scale-Third Edition,36 Auditory Delayed Memory Index (verbal memory), and Visual Delayed Memory Index (visual-spatial memory). Patients were excluded if scores on either test were greater than 1 standard deviation lower than the mean.

Imaging Protocol

MRI studies were obtained using a 3-T MRI machine (Siemens) and included 3D T1-weighted postgadolinium (number of slices 160, flip angle 9°, slice thickness 1 mm, pixel size 0.67 × 0.67, TR 1600 msec, and TE 3.05 msec) and 3D T2-weighted FLAIR (number of slices 160, flip angle 120°, slice thickness 1 mm, pixel size 0.5 × 0.5, TR 6000 msec, and TE 356 msec). All images were reviewed by a neuroradiologist who was blinded to the expected location of epilepsy onset. Patients were excluded if there was any evidence of mesial temporal sclerosis or other pathological findings within the mesial temporal lobe.

Surgical Technique

Depth electrodes (Integra Life Sciences) were implanted stereotactically using a Leksell frame and a volumetric CT scan fused to preoperative MRI. Each electrode consisted of 12 platinum-iridium cylinders measuring 1.1 mm in diameter and 2.3 mm in length, evenly spaced at 5-mm intervals. Trajectories were planned using the iPlan workstation (BrainLAB, Inc.). All patients underwent electrode implantation into the following structures via a lateral or parasagittal approach: 1) amygdala, 2) head of hippocampus, 3) body of hippocampus, 4) orbitofrontal cortex, 5) posterior temporal lobe, 6) anterior insula, 7) posterior insula, and 8) posterior cingulated cortex (retrosplenial area; Fig. 1). Electrodes were implanted under general anesthesia using stab incisions and a 2.1-mm twist drill to make a small bur hole. Intraoperative fluoroscopy was used to verify accuracy of electrode placement, and a volumetric CT scan was subsequently obtained to verify electrode location by coregistration with presurgical volumetric MRI.

FIG. 1.
FIG. 1.

Montage of electrodes implanted into the mesial and lateral temporal lobe, temporal tip, posterior temporal neocortex, orbitomesiobasal frontal lobe, posterior cingulate gyrus, and insula.

SEEG Analysis, Surgery, and Outcome

All SEEG channels were recorded for offline analysis. Signals were amplified, filtered (0.1–1000 Hz), and recorded digitally with a sampling frequency of 1 kHz. Results of the SEEG study were analyzed offline by an experienced epileptologist (H.L.) and correlated with video evidence of seizures to determine ictal and interictal activity. Monitoring occurred in the epilepsy monitoring unit for 7 to 14 days to establish the precise location of seizure onset, and decisions about subsequent surgical treatment were made based on the data. All patients were closely followed for at least 12 months postoperatively. The study was reviewed and approved by the Institutional Review Board of University Hospitals Case Medical Center.

Results

Demographic Characteristics

Eighteen patients with MRI-negative nonlesional TLE and normal memory function who underwent depth electrode implantation were included in the study (Table 1). Ten patients were male and 8 were female, ranging in age from 23 to 56 years old (mean age 37.0 years) at the time of surgery. The average age of seizure onset was 19.4 years (range 0–45 years) and the average duration of epilepsy was 17.6 years (range 3–34 years). The average score on delayed verbal memory was 101.9 (range 92–117) and on delayed visual memory was 105.7 (range 85–132). Seizure frequency while on antiepileptic medications at the time of surgical evaluation ranged from 0.5 to 30 seizures per month (mean 5.4 seizures per month).

TABLE 1.

Patient demographics, results of preoperative video EEG evaluation, and results of memory testing

Case No.HandednessAge of Onset (yrs)Age at Surgery (yrs)Side of Epilepsy on Video EEGDelayed Verbal Memory Score*Delayed Visual Memory Score*
1Rt2631Lt105111
2Rt4556Lt102115
3Rt1423Lt108103
4Rt2124Lt117132
5Rt842Rt92106
6Rt1344Rt114112
7Rt2128Rt9994
8Lt1746Lt99115
9Rt1944Lt94109
10Rt3054Rt9497
11Rt1532Lt102106
12Rt026Lt9489
13Rt2023Lt102112
14Lt941Lt11188
15Rt3036Lt108112
16Rt226Lt9797
17Rt2535Rt104120
18Rt3455Lt9285
Mean ± SD19.4 ± 2.737.0 ± 2.6101.9 ±1.8105.7 ± 2.9

Memory scores are normalized to average = 100, standard deviation = 15.

Seizure Semiology and EEG

All patients had semiology typical of TLE. Four patients had no aura prior to their ictal event, 9 patients had psychic auras, and 4 had abdominal auras. Fourteen patients (78%) had dialeptic seizures, and 13 (72%) had automotor seizures (oral and/or hand automatisms; Table 2). All patients had evidence of unilateral interictal and ictal abnormalities arising from the temporal lobe, 11 from the dominant side, and 7 from the nondominant side. Thirteen patients underwent implantation of sphenoidal electrodes, which confirmed likely TLE.

TABLE 2.

Seizure semiology

Case No.Seizure Frequency (per month)Aura: PsychicAura: AbdominalAura: OtherDialepsisOral AutomatismsOther*
14YesNoWarm tingling all over the bodyYesYesStirring motion of the rt hand
22NoYesNauseaYesNoCrying, trembling, sialorrhea
31YesNoNumbness of whole bodyYesYesStuttering, rt hand fiddling followed by dystonic posturing, rt version, occasional incontinence
41YesYesRapid thoughtsNoNoHypnopompic, ictal scream, rt version, waving movement of rt hand, anomic aphasia postictally
52NoNoAbnormal sensation in head, gustatory auraYesYesFumbling of both hands, lt version
60.5NoNoNoneNoYesHypnopompic, high amplitude arm flailing, paradoxical rt clinic/sign-of-4 (lt arm extension), nonsensical words
70.5YesNoLightheadedness, facial flushingYesYesLt version, sign-of-4 (rt arm extension)
81YesNoHeadacheYesYesMouth clenching, rt version, clonic movements of upper & lower extremities, sialorrhea
910NoYesYesYesFiddling movements of hands
1030YesYesYesNoRubbing of fingers on lt hand, slurred speech, lt version
111YesNoSounds “echo”YesNoGrunting, occasional urinary incontinence & tongue biting
122NoNoHeadacheYesYes
1310YesNo“Out of body” experienceYesYesRt version, rt facial clonus
141NoNoSensation of movement, diaphoresis, feeling of heatYesYesRhythmical movement of feet, postictal aphasia
150.5NoNoNoneNoNoHypnopompic, body convulsions, occasional tongue biting
161NoNoNoneNoYesSialorrhea, lt version, proximal asymmetric clonus
174YesNoNausea, olfactory, & gustatory auraYesYes
186NoNoNoneYesYesRt M2e sign, right figure of 4, rt arm clonic seizure, paradoxical lt clonic seizure

Right/left version = side of head turning.

SEEG Findings and Surgical Outcome

All but 1 patient (Case 13; 94%) had mesial temporal seizure onset during ictal events on SEEG (Table 3). Four patients (Cases 4, 8, 9, and 14; 22%) had concurrent mesial and neocortical (temporopolar) ictal activity, 3 of whom also had mesial and neocortical interictal activity, while 1 had only mesial interictal activity. Thirteen patients (Cases 1–3, 5–7, 10, 12, 13, and 15–18; 72%) had exclusively mesial ictal activity, 4 of whom (Cases 1–3, 6) also had exclusively mesial interictal spikes, 8 (Cases 5, 7, 10, 12, 15–18) had both mesial and neocortical interictal spikes, and 1 (Case 13) had only neocortical interictal spikes. One patient (Case 11; 6%) had exclusively neocortical ictal activity but had both mesial and neocortical interictal spikes. None of the patients had extratemporal ictal or interictal abnormalities.

TABLE 3.

Results of SEEG evaluation, operation performed, and 12-month postsurgical outcome

Case No.Interictal SpikingIctal SpikingOperation PerformedMesial Pathological FindingsNeocortical Pathological FindingsPostop Outcome (Engle Class)
MesialTemporopolarMesialTemporopolar
1YesNoYesNoMHTNANAIIIA
2YesNoYesNoMHTNANAIC
3YesNoYesNoMHT+NANo abnormalityIA
4YesYesYesYesCortical resection*NAType IA CDIB
5YesYesYesNoATLNo abnormalityType IA CDIA
6YesNoYesNoATLNo abnormalityType IA CDIA
7YesYesYesNoMHTNANAIIA
8YesYesYesYesMHT+NANo abnormalityIIIA
9YesYesYesYesMHT+NAType IA CDIA
10YesYesYesNoATLNo abnormalityType IA CDIIA
11YesYesNoYesCortical resectionNAType IA CDID
12YesYesYesNoMHT+NAType IA CDIB
13NoYesYesNoMHT+NAType IIA CDIA
14YesNoYesYesCortical resection*NANo abnormalityIA
15YesYesYesNoNo surgeryNANANA
16YesYesYesNoMHT+NANo abnormalityIA
17YesYesYesNoMHT+NANo abnormalityIA
18YesYesYesNoCortical resection*NAType IA CDIA

CD = cortical dysplasia; MHT = multiple hippocampal transaction with preservation of amygdala and neocortex; MHT+ = multiple hippocampal transection with resection of the amygdala and neocortex; NA = not applicable.

Three patients were noted to have complete cessation of hippocampal spikes after resection of the temporal neocortex and amygdala, so the hippocampus was left intact.

Seventeen (94%) of the 18 patients underwent subsequent surgery to treat their temporal lobe seizures, either anterior temporal lobectomy or multiple hippocampal transections with or without resection of the lateral temporal cortex. The decision about whether to resect the lateral temporal cortex was dictated by the SEEG findings, and the decision as to whether to resect or transect the hippocampus was made based on whether the epileptogenic zone was on the dominant or nondominant side. All patients experienced improvement in seizure frequency at 12 months postoperatively, with 13 patients (76%) in Engel Class I, 2 patients (12%) in Engel Class II, and 2 patients (12%) in Engel Class III. During the hippocampal transection operation, 3 patients were observed to have complete cessation of hippocampal spikes following resection of the temporal neocortex and amygdala, so the hippocampus was left intact. All 3 of these patients were Engel Class I.

Discussion

The central finding of our study is that extension of the epileptogenic zone outside the temporal lobe is very infrequent in patients whose presurgical evaluation (EEG and semiology) is typical for TLE and who have normal memory and MRI findings. In this study, we examined a homogeneous population with normal MR images and memory scores. We also performed a consistent SEEG montage with electrode implantation into a set of targets that in previous reports has been shown to produce epilepsy that may falsely be localized to the temporal lobe.2,10,12,17,19,29,34 While early spread of epileptic activity into distant areas often occurs, we found that interictal and early ictal activity is rarely noted outside of the mesial temporal structures and adjacent temporal tip. These findings reinforce the concept that semiology and EEG are highly relevant for identification of the epileptogenic zone. In addition, our results provide evidence that normally functioning tissue (in this case, tissue in patients with normal memory scores and no visible hippocampal lesion on MRI) is frequently capable of producing epilepsy.

Accurate localization of the epileptogenic zone is essential for good surgical outcome because a temporal lobectomy is not helpful if the epileptogenic zone is extensive or extratemporal.1,17,29 Localization of epilepsy in TLE may have important implications for prognosis as well, because certain types of “temporal plus” epilepsy (e.g., insular epilepsy) may be associated with a higher incidence of major complications such as sudden death in epilepsy.28,29 The etiology of temporal plus epilepsy may be related to progressive recruitment of tissue within the functional network associated with the epileptic tissue, with seizure activity within the mesial structures acting either as cause or effect in a more diffuse epilepsy syndrome.3,13,24,26

Noninvasive localization of the epileptogenic zone can usually be accomplished by examining semiology, EEG, imaging, and the chronic effect of seizures on eloquent areas.27 However, when semiology, MRI, EEG, and neuropsychological tests are contradictory, intracranial recordings are often indicated to determine the epileptogenic zone. There are isolated reports in the literature of epilepsy arising from outside the mesial temporal lobe even in the presence of obvious mesial temporal sclerosis.10,13,14,25

A number of studies have analyzed clinical characteristics and seizure outcome after temporal lobectomy in patients with MRI-negative TLE, although most of these have included patients with heterogeneous semiology, EEG, and memory scores.6–8,11,15,21,23,32,35 In general, these investigations have documented inferior results after temporal lobectomy compared with mesial temporal sclerosis. Studies using intracranial recordings have demonstrated that the epileptogenic zone can lie exclusively within the mesial temporal lobe even when MRI results are completely normal.9,20,21 However, neocortical temporal epilepsy, usually associated with highly epileptogenic foci of cortical dysplasia, is somewhat more common in this population than in patients with mesial temporal sclerosis.13,14,16,21,22 Extratemporal onset in MRI-negative TLE is rare but has been documented.12,17 In either case, there are a relatively small number of anatomical structures that have been identified as commonly associated with TLE, and these are the targets we chose for SEEG.

The value of memory tests on neuropsychological evaluation for localization of seizure onset is controversial. Because the mesial temporal structures are involved in memory processes, memory deficits are often observed in TLE, and the degree of memory loss tends to be proportional to the severity of the mesial temporal sclerosis.5 Memory is often tested prior to temporal lobectomy to determine the risk of surgery,33 but the localizing or lateralizing value of memory loss is less clear, particularly for nonverbal memory.4,18 Material-specific deficits are infrequently encountered in TLE but, when they are noted, they tend to be specific for lateralization.9 However, about half of patients with TLE will have intact memory on neuropsychological testing, equally distributed between dominant and nondominant TLE.9 We have confirmed that normal memory does not rule out temporal onset in MRI-negative TLE. On the contrary, mesial temporal seizure onset was documented in the vast majority of these patients. Mesial temporal onset of seizures with normal memory and onset from mesial temporal sources without extratemporal onset have both been described before, but to our knowledge this is the first study to examine a population with normal memory and imaging results using a stereotypical montage of electrodes implanted into temporal and extratemporal structures that might be involved in the epileptogenic zone.

Our study has important limitations. We investigated only 18 patients, which is a relatively small number compared with other studies of TLE; a larger cohort might have identified more cases of extratemporal onset. Although the patient population was highly homogeneous upon presentation and the SEEG evaluation was identical across all patients, patients were treated differently based on SEEG results. Although seizure outcome was good in all cases, there are too few patients in this study to draw any conclusions regarding how the decision about which operation to perform might have affected clinical outcome. Also, although we do not have detailed postoperative neuropsychological outcome data on this population, postoperative memory loss is a major concern after a surgical approach to normal hippocampi with normal memory, which is why we decided to perform multiple hippocampal transections rather than resection when operating on the dominant side. Finally, we cannot rule out the possibility that extratemporal epilepsy might have arisen from an area outside of the region where our electrodes were placed, although it is unlikely considering that all patients did improve when only the temporal lobe was addressed, which is not generally observed in temporal plus epilepsy syndromes.29

Conclusions

Seizures usually arise from the mesial temporal lobe when seizure semiology and EEG suggest TLE and there are no MRI or memory abnormalities. In this context, extension of the epileptogenic zone or triggering of temporal lobe seizures from outside the temporal lobe is rare. In addition, normal memory does not preclude seizure onset exclusively within the mesial temporal structures with no contribution from extratemporal sources.

Author Contributions

Conception and design: Miller, Suresh, Sweet. Acquisition of data: all authors. Analysis and interpretation of data: all authors. Drafting the article: Miller, Suresh, Sweet. Critically revising the article: Miller, Sweet. Reviewed submitted version of manuscript: Miller, Suresh. Approved the final version of the manuscript on behalf of all authors: Miller. Statistical analysis: Miller, Suresh, Sweet, Fastenau, Lüders. Administrative/technical/material support: Miller, Suresh.

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Article Information

Correspondence Jonathan P. Miller, Department of Neurological Surgery, Case Western Reserve University, 10900 Euclid Ave., Cleveland, OH 44106. email: jonathan.miller@uhhospitals.org.

INCLUDE WHEN CITING Published online July 24, 2015; DOI: 10.3171/2015.1.JNS141811.

DISCLOSURE The authors report no conflict of interest concerning the materials or methods used in this study or the findings specified in this paper.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Montage of electrodes implanted into the mesial and lateral temporal lobe, temporal tip, posterior temporal neocortex, orbitomesiobasal frontal lobe, posterior cingulate gyrus, and insula.

References

1

Aghakhani YRosati ADubeau FOlivier AAndermann F: Patients with temporoparietal ictal symptoms and inferomesial EEG do not benefit from anterior temporal resection. Epilepsia 45:2302362004

2

Alkawadri RSo NKVan Ness PCAlexopoulos AV: Cingulate epilepsy: report of 3 electroclinical subtypes with surgical outcomes. JAMA Neurol 70:99510022013

3

Bartolomei FCosandier-Rimele DMcGonigal AAubert SRégis JGavaret M: From mesial temporal lobe to temporoperisylvian seizures: a quantified study of temporal lobe seizure networks. Epilepsia 51:214721582010

4

Baxendale SThompson P: Beyond localization: the role of traditional neuropsychological tests in an age of imaging. Epilepsia 51:222522302010

5

Bell BLin JJSeidenberg MHermann B: The neurobiology of cognitive disorders in temporal lobe epilepsy. Nat Rev Neurol 7:1541642011

6

Bell MLRao SSo ELTrenerry MKazemi NStead SM: Epilepsy surgery outcomes in temporal lobe epilepsy with a normal MRI. Epilepsia 50:205320602009

7

Berkovic SFMcIntosh AMKalnins RMJackson GDFabinyi GCBrazenor GA: Preoperative MRI predicts outcome of temporal lobectomy: an actuarial analysis. Neurology 45:135813631995

8

Carne RPO’Brien TJKilpatrick CJMacGregor LRHicks RJMurphy MA: MRI-negative PET-positive temporal lobe epilepsy: a distinct surgically remediable syndrome. Brain 127:227622852004

9

Castro LHSilva LCAdda CCBanaskiwitz NHXavier ABJorge CL: Low prevalence but high specificity of material-specific memory impairment in epilepsy associated with hippocampal sclerosis. Epilepsia 54:173517422013

10

Chabardès SKahane PMinotti LTassi LGrand SHoffmann D: The temporopolar cortex plays a pivotal role in temporal lobe seizures. Brain 128:181818312005

11

Chapman KWyllie ENajm IRuggieri PBingaman WLüders J: Seizure outcome after epilepsy surgery in patients with normal preoperative MRI. J Neurol Neurosurg Psychiatry 76:7107132005

12

Enatsu RBulacio JNair DRBingaman WNajm IGonzalez-Martinez J: Posterior cingulate epilepsy: clinical and neurophysiological analysis. J Neurol Neurosurg Psychiatry 85:44502014

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