Diagnosis of mesial temporal sclerosis: sensitivity,specificity and predictive values of the quantitative analysis of magnetic resonance imaging

Abstract

In the diagnosis of mesial temporal sclerosis (MTS), sensitivity, specificity and predictive values of qualitative assessment using conventional magnetic resonance imaging are low, mainly in mild or bilateral atrophy. Quantitative analysis may improve this performance. We evaluated the sensitivity, specificity, positive predictive value (PPV) and negative predictive value (NPV) of quantitative analysis using the hippocampal volumetric index (HVI) and hippocampal asymmetry index (HAI) compared with qualitative assessment in the MTS diagnosis. Twenty-five patients diagnosed with MTS, and 25 healthy subjects underwent conventional magnetic resonance imaging. Hippocampal volumes were obtained using an automated software (FreeSurfer); HVI and HAI were calculated. Receiver operating characteristic curve analysis was performed to obtain the optimal threshold values. Sensitivity, specificity and predictive values were calculated. Sensitivity, specificity, PPV and NPV for qualitative analysis were 44.00%, 96.00%, 91.67% and 63.16%, respectively. In the quantitative analysis, a threshold value of K = 0.22 for HVI provided a sensitivity value of 76.00%, specificity value of 96.00%, PPV of 95.00% and NPV of 80.00%. A threshold value of K = 0.06 for HAI provided the minimum C1 and C2 errors, with a sensitivity value of 88.00%, specificity value of 100%, PPV of 100% and NPV of 89.30%. A statistically significant difference was observed for HAI (P < 0.0001), and ipsilateral HVI (left MTS, P = 0.0152; right MTS, P < 0.0001), between MTS and healthy groups. The HVI and HAI, both individually and in conjunction, improved the sensitivity, specificity and predictive values of magnetic resonance imaging in the diagnosis of MTS compared to the qualitative analysis and other quantitative techniques. The HAI is highly accurate in the diagnosis of unilateral MTS, whereas the HVI may be better for bilateral MTS cases.

Keywords

Epilepsy mesial temporal sclerosis hippocampal sclerosis voxel-based morphometry brain volumetry

Get full access to this article

View all access options for this article.

References

Burneo

Tellez-Zenteno

Wiebe

. Understanding the burden of epilepsy in Latin America: a systematic review of its prevalence and incidence. Epilepsy Res 2005; 66: 63–74.

Granados

Orejuela

Rodriguez-Takeuchi

. Neuroimaging evaluation in refractory epilepsy. Neuroradiol J 2015; 28: 529–535.

Engel

. Surgery for seizures. N Engl J Med 1996; 334: 647–652.

Jobst

Cascino

. Resective epilepsy surgery for drug-resistant focal epilepsy. JAMA 2015; 313: 285–293.

Margerison

Corsellis

JAN

. Epilepsy and the temporal lobes: a clinical, electroencephalographic and neuropathological study of the brain in epilepsy, with particular reference to the temporal lobes. Brain 1966; 89: 499–530.

Palacios E and Boleaga-Durán B. Imagen diagnóstica en epilepsia. In: Palacios E (ed.) Avances en Diagnóstico por Imágenes: Neuroradiología, 1 ed. Buenos Aires: Ediciones Journal, 2010, pp. 211–231.

Rosenow

. Presurgical evaluation of epilepsy. Brain 2001; 124: 1683–1700.

Sánchez-Álvarez

Serrano-Castro

Cañadillas-Hidalgo

. Epilepsia refractaria del adulto. Rev Neurol 2002; 35: 931–935.

Ramey

Martirosyan

Lieu

et al.

Current management and surgical outcomes of medically intractable epilepsy. Clin Neurol Neurosurg 2013; 115: 2411–2418.

10.

Jette

Wiebe

. Update on the surgical treatment of epilepsy. Curr Opin Neurol 2013; 26: 201–207.

11.

Gil-Nagel

. El síndrome de esclerosis mesial temporal en la epilepsia. Neurologia 1998; 13: 132–144.

12.

Mackay

Webb

Eldridge

et al.

Quantitative magnetic resonance imaging in consecutive patients evaluated for surgical treatment of temporal lobe epilepsy. Magn Reson Imag 2000; 18: 1187–1199.

13.

Sánchez-Álvarez

Pastor-Pons

García-Gómez

et al.

El diagnóstico de la esclerosis temporal mesial mediante imagen de resonancia magnética. Rev Neurol 2000; 31: 701–711.

14.

Silva

Martins

Moreira da Silva

et al.

Automated volumetry of hippocampus is useful to confirm unilateral mesial temporal sclerosis in patients with radiologically positive findings. Neuroradiol J 2017; 30: 318–323.

15.

Cascino GD. Magnetic resonance imaging in epilepsy: mesial temporal sclerosis. In: Lüders HO, ed. Textbook of Epilepsy Surgery. 1st ed. London, UK: Informa, 2008: pp. 716–721.

16.

Farid

Girard

Kemmotsu

. Temporal lobe epilepsy: quantitative MR volumetry in detection of hippocampal atrophy. Radiology 2012; 264: 542–550.

17.

Fountas

Tsougos

Gotsis

et al.

Temporal pole proton preoperative magnetic resonance spectroscopy in patients undergoing surgery for mesial temporal sclerosis. Neurosurgical Focus 2012; 32: E3.

18.

Park

Chang

Kim

et al.

Lateralizing ability of single-voxel proton MR spectroscopy in hippocampal sclerosis: comparison with MR imaging and positron emission tomography. AJNR Am J Neuroradiol 2001; 22: 625–631.

19.

Guo

Wang

et al.

Asymmetry of cerebral blood flow measured with three-dimensional pseudocontinuous arterial spin-labeling mr imaging in temporal lobe epilepsy with and without mesial temporal sclerosis. J Magn Reson Imag 2015; 42: 1386–1397.

20.

Tae

Kim

Lee

et al.

Validation of hippocampal volumes measured using a manual method and two automated methods (FreeSurfer and IBASPM) in chronic major depressive disorder. Neuroradiology 2008; 50: 569–581.

21.

Wenger

Mårtensson

Noack

et al.

Comparing manual and automatic segmentation of hippocampal volumes: reliability and validity issues in younger and older brains. Human Brain Mapping 2014; 35: 4236–4248.

22.

Dale

Fischl

Sereno

. Cortical surface-based analysis. NeuroImage 1999; 9: 179–194.

23.

Dale

Sereno

. Improved localizadon of cortical activity by combining EEG and MEG with MRI cortical surface reconstruction: a linear approach. J Cogn Neurosci 1993; 5: 162–176.

24.

Fischl

Dale

. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci 2000; 97: 11050–11055.

25.

Fischl

Liu

Dale

. Automated manifold surgery: constructing geometrically accurate and topologically correct models of the human cerebral cortex. IEEE Transact Med Imag 2001; 20: 70–80.

26.

Fischl

Salat

Busa

et al.

Whole brain segmentation. Neuron 2002; 33: 341–355.

27.

Fischl

Salat

Van der Kouwe

et al.

Sequence-independent segmentation of magnetic resonance images. NeuroImage 2004; 23: S69–S84.

28.

Fischl

Sereno

Dale

. Cortical surface-based analysis. II: Inflation, flattening, and a surface-based coordinate system. NeuroImage 1999; 9: 195–207.

29.

Fischl

Sereno

Tootell

et al.

High-resolution intersubject averaging and a coordinate system for the cortical surface. Human Brain Mapping 1999; 8: 272–284.

30.

Fischl

Van der Kouwe

Destrieux

et al.

Automatically parcellating the human cerebral cortex. Cerebral Cortex 2004; 14: 11–22.

31.

Han

Jovicich

Salat

et al.

Reliability of MRI-derived measurements of human cerebral cortical thickness: The effects of field strength, scanner upgrade and manufacturer. NeuroImage 2006; 32: 180–194.

32.

Jovicich

Czanner

Greve

et al.

Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. NeuroImage 2006; 30: 436–443.

33.

Segonne

Dale

Busa

et al.

A hybrid approach to the skull stripping problem in MRI. NeuroImage 2004; 22: 1060–1075.

34.

Reuter

Rosas

Fischl

. Highly accurate inverse consistent registration: a robust approach. NeuroImage 2010; 53: 1181–1196.

35.

Reuter

Schmansky

Rosas

et al.

Within-subject template estimation for unbiased longitudinal image analysis. NeuroImage 2012; 61: 1402–1418.

36.

Ascencio

Ochoa

. Volumen y función hipocampal en epilepsia del lóbulo temporal medial. Rev Colomb Radiol 2013; 24: 3622–3627.

37.

Ashtari

Barr

Schaul

et al.

Three-dimensional fast low-angle shot imaging and computerized volume measurement of the hippocampus in patients with chronic epilepsy of the temporal lobe. AJNR Am J Neuroradiol 1991; 12: 941–947.

38.

Bigler

Blatter

Anderson

et al.

Hippocampal volume in normal aging and traumatic brain injury. AJNR Am J Neuroradiol 1997; 18: 24–28.

39.

Cook

Fish

Shorvon

et al.

Hippocampal volumetric and morphometric study in frontal and temporal lobe epilepsy. Brain 1992; 115(Pt 4): 1001–1115.

40.

Akos-Szabo

Xiong

Lancaster

et al.

Amygdalar and hippocampal volumetry in control participants: differences regarding handedness. AJNR Am J Neuroradiol 2001; 22: 1342–1345.

41.

Jack

Twomey

Zinsmeister

et al.

Anterior temporal lobes and hippocampal formations: normative volumetric measurements from MR images in young adults. Radiology 1989; 172: 549–554.

42.

Camacho

Castillo

. MR imaging of temporal lobe epilepsy. Semin Ultrasound CT MR 2007; 28: 424–436.

43.

Kälviäinen

Salmenperä

Partanen

et al.

Recurrent seizures may cause hippocampal damage in temporal lobe epilepsy. Neurology 1998; 50: 1377–1382.

44.

Tasch

Cendes

et al.

Neuroimaging evidence of progressive neuronal loss and disfunction in temporal lobe epilepsy. Ann Neurol 1999; 45: 568–576.

45.

Chan

Erickson

Yoon

. Limbic system abnormalities associated with mesial temporal sclerosis: a model of chronic cerebral changes due to seizures. Radiographics 1997; 5: 1095–1110.

46.

Ende

Laxer

Knowlton

et al.

Temporal lobe epilepsy: bilateral hippocampal metabolite changes revealed at proton MR spectroscopic imaging. Radiology 1997; 202: 809–817.

47.

Hsu

Chang

et al.

Proton MR spectroscopy in patients with complex partial seizures: single-voxel spectroscopy versus chemical-shift imaging. AJNR Am J Neuroradiol 1999; 20: 643–651.

48.

Theodore

Bhatia

Hatta

et al.

Hippocampal atrophy, epilepsy duration and febrile seizures in patients with partial seizures. Neurology 1999; 52: 132–136.

49.

King

Spencer

McCarthy

et al.

Surface and depth EEG findings in patients with hippocampal atrophy. Neurology 1997; 48: 1363–1367.

50.

Cascino

Trenerry

et al.

Routine EEG and temporal lobe epilepsy: relation to long-term EEG monitoring, quantitative MRI, and operative outcome. Epilepsia 1996; 37: 651–656.

51.

Cendes

Dubeau

Andermann

et al.

Significance of mesial temporal atrophy in relation to intracranial ictal and interictal stereo EEG abnormalities. Brain 1996; 119: 1317–1326.

52.

Gilliam

Bowling

Bilir

et al.

Association of combined MRI, interictal EEG, and ictal EEG results with outcome and pathology after temporal lobectomy. Epilepsia 1997; 38: 1315–1320.

53.

Pataraia

Lurger

Serles

et al.

Ictal scalp EEG in unilateral mesial temporal lobe epilepsy. Epilepsia 1998; 39: 608–614.

54.

Arruda

Cendes

Andermann

et al.

Mesial atrophy and outcome after amygdalohippocampectomyor temporal lobe removal. Ann Neurol 1996; 40: 446–450.

55.

Holmes

Dodril

Ojemann

et al.

Outcome following surgery in patients with bitemporal interictal epileptiform patterns. Neurology 1997; 48: 1037–1040.

56.

Jeong

Lee

Kim

et al.

Prognostic factors in anterior temporal lobe resections for mesial temporal lobe epilepsy: multivariate analysis. Epilepsia 1999; 40: 1735–1739.

57.

Knowlton

Laxer

Ende

et al.

Presurgical multimodality neuroimaging in electroencephalographic lateralized temporal lobe epilepsy. Ann Neurol 1997; 42: 829–837.

58.

Radhakrishnan

Silbert

et al.

Predictors of outcome of anterior temporal lobectomy for intractable epilepsy. A multivariate study. Neurology 1998; 51: 465–471.