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Published in: Acta Neurochirurgica 7/2019

01-07-2019 | Trigeminal Neuralgia | Original Article - Functional Neurosurgery - Pain

Diffusion tensor imaging abnormalities of the trigeminal nerve root in patients with classical trigeminal neuralgia: a pre- and postoperative comparative study 4 years after microvascular decompression

Authors: Paulo Roberto Lacerda Leal, Jean Roch, Marc Hermier, Yves Berthezene, Marc Sindou

Published in: Acta Neurochirurgica | Issue 7/2019

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Abstract

Background

As diffusion tensor imaging (DTI) is able to assess tissue integrity, authors used diffusion to detect abnormalities in trigeminal nerves (TGN) in patients with trigeminal neuralgia (TN) caused by neurovascular compression (NVC) who had undergone microvascular decompression (MVD). The authors also studied anatomical TGN parameters (cross-sectional area [CSA] and volume [V]). The study compared pre- and postoperative findings.

Methods

Using DTI sequencing on a 3-T MRI scanner, we measured the fraction of anisotropy (FA) and apparent diffusion coefficient (ADC) of the TGN in 10 patients who had undergone MVD for TN and in 6 normal subjects. We compared data between affected and unaffected nerves in patients and both nerves in normal subjects (controls). We then correlated these data with CSA and V. Data from the affected side and the unaffected side before and 4 years after MVD were compared.

Results

Before MVD, the FA of the affected side (0.37 ± 0.03) was significantly lower (p < 0.05) compared to the unaffected side in patients (0.48 ± 0.03) and controls (0.52 ± 0.02), and the ADC in the affected side (5.6 ± 0.34 mm2/s) was significantly higher (p < 0.05) compared to the unaffected side in patients (4.26 ± 0.25 mm2/s) and controls (3.84 ± 0.18 mm2/s). Affected nerves had smaller V and CSA compared to unaffected nerves and controls (p < 0.05). After MVD, the FA in the affected side (0.41 ± 0.02) remained significantly lower (p < 0.05) compared to the unaffected side (0.51 ± 0.02), but the ADC in the affected side (4.24 ± 0.34 mm2/s) had become similar (p > 0.05) to the unaffected side (4.01 ± 0.33 mm2/s).

Conclusions

DTI revealed a loss of anisotropy and an increase in diffusivity in affected nerves before surgery. Diffusion alterations correlated with atrophic changes in patients with TN caused by NVC. After removal of the compression, the loss of FA remained, but ADC normalized in the affected nerves, suggesting improvement in the diffusion of the trigeminal root.
Literature
1.
go back to reference Acosta-Cabronero J, Williams GB, Pengas G et al (2010) Absolute diffusivities define the landscape of white matter degeneration in Alzheimer’s disease. Brain 133(Pt 2):529–539CrossRefPubMed Acosta-Cabronero J, Williams GB, Pengas G et al (2010) Absolute diffusivities define the landscape of white matter degeneration in Alzheimer’s disease. Brain 133(Pt 2):529–539CrossRefPubMed
2.
go back to reference Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reason 213:560–570CrossRef Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reason 213:560–570CrossRef
3.
go back to reference Chen DQ, DeSouza DD, Hayes DJ et al (2016) Diffusivity signatures characterize trigeminal neuralgia associated with multiple sclerosis. Mult Scler 22(1):51–63CrossRefPubMed Chen DQ, DeSouza DD, Hayes DJ et al (2016) Diffusivity signatures characterize trigeminal neuralgia associated with multiple sclerosis. Mult Scler 22(1):51–63CrossRefPubMed
4.
go back to reference Chen F, Chen L, Li W et al (2016) Pre-operative declining proportion of fractional anisotropy of trigeminal nerve is correlated with the outcome of micro-vascular decompression surgery. BMC Neurol 16:106CrossRefPubMedPubMedCentral Chen F, Chen L, Li W et al (2016) Pre-operative declining proportion of fractional anisotropy of trigeminal nerve is correlated with the outcome of micro-vascular decompression surgery. BMC Neurol 16:106CrossRefPubMedPubMedCentral
5.
go back to reference Chen ST, Yang JT, Yeh MY et al (2016) Using diffusion tensor imaging to evaluate microstructural changes and outcomes after radiofrequency rhizotomy of trigeminal nerves in patients with trigeminal neuralgia. PLoS One 11(12):e0167584CrossRefPubMedPubMedCentral Chen ST, Yang JT, Yeh MY et al (2016) Using diffusion tensor imaging to evaluate microstructural changes and outcomes after radiofrequency rhizotomy of trigeminal nerves in patients with trigeminal neuralgia. PLoS One 11(12):e0167584CrossRefPubMedPubMedCentral
6.
go back to reference Cottier JP, Barantin L, Destrieux C et al (2005) Cerebral diffusion tensor imaging and brain fiber tracking: principles and current limitations. Feuill Radiol 45(3):191–199CrossRef Cottier JP, Barantin L, Destrieux C et al (2005) Cerebral diffusion tensor imaging and brain fiber tracking: principles and current limitations. Feuill Radiol 45(3):191–199CrossRef
7.
go back to reference Cruccu G, Finnerup NB, Jensen TS et al (2016) Trigeminal neuralgia: new classification and diagnostic grading for practice and research. Neurology 87(2):220–228CrossRefPubMedPubMedCentral Cruccu G, Finnerup NB, Jensen TS et al (2016) Trigeminal neuralgia: new classification and diagnostic grading for practice and research. Neurology 87(2):220–228CrossRefPubMedPubMedCentral
8.
go back to reference DeSouza DD, Hodaie M, Davis KD (2014) Abnormal trigeminal nerve microstructure and brain white matter in idiopathic trigeminal neuralgia. Pain 155:37–44CrossRefPubMed DeSouza DD, Hodaie M, Davis KD (2014) Abnormal trigeminal nerve microstructure and brain white matter in idiopathic trigeminal neuralgia. Pain 155:37–44CrossRefPubMed
9.
go back to reference DeSouza DD, Davis KD, Hodaie M (2015) Reversal of insular and microstructural nerve abnormalities following effective surgical treatment for trigeminal neuralgia. Pain 156(6):1112–1123PubMed DeSouza DD, Davis KD, Hodaie M (2015) Reversal of insular and microstructural nerve abnormalities following effective surgical treatment for trigeminal neuralgia. Pain 156(6):1112–1123PubMed
10.
go back to reference Devor M, Govrin-Lippmann R, Rappaport H (2002) Mechanism of trigeminal neuralgia: an ultrastructural analysis of trigeminal root specimens obtained during microvascular decompression surgery. J Neurosurg 96:532–543CrossRefPubMed Devor M, Govrin-Lippmann R, Rappaport H (2002) Mechanism of trigeminal neuralgia: an ultrastructural analysis of trigeminal root specimens obtained during microvascular decompression surgery. J Neurosurg 96:532–543CrossRefPubMed
11.
go back to reference Erbay SH, Bhadelia RA, O’Callaghan M et al (2006) Nerve atrophy in severe trigeminal neuralgia: non-invasive confirmation at MR imaging – initial experience. Radiology 238:689–692CrossRefPubMed Erbay SH, Bhadelia RA, O’Callaghan M et al (2006) Nerve atrophy in severe trigeminal neuralgia: non-invasive confirmation at MR imaging – initial experience. Radiology 238:689–692CrossRefPubMed
12.
go back to reference Fish CJ, Blakemore WF (1983) A model of chronic spinal cord compression in the cat. Neuropathol Appl Neurobiol 9:109–120CrossRefPubMed Fish CJ, Blakemore WF (1983) A model of chronic spinal cord compression in the cat. Neuropathol Appl Neurobiol 9:109–120CrossRefPubMed
13.
go back to reference Fujiwara S, Sasaki M, Wada T et al (2011) High-resolution diffusion tensor imaging for the detection of diffusion abnormalities in the trigeminal nerves of patients with trigeminal neuralgia caused by neurovascular compression. J Neuroimaging 21:102–108CrossRef Fujiwara S, Sasaki M, Wada T et al (2011) High-resolution diffusion tensor imaging for the detection of diffusion abnormalities in the trigeminal nerves of patients with trigeminal neuralgia caused by neurovascular compression. J Neuroimaging 21:102–108CrossRef
14.
go back to reference Gardner (1962) Concerning the mechanism of trigeminal neuralgia and hemifacial spasm. J Neurosurg 19:947–958CrossRefPubMed Gardner (1962) Concerning the mechanism of trigeminal neuralgia and hemifacial spasm. J Neurosurg 19:947–958CrossRefPubMed
15.
go back to reference Gledhill RF, Harrison BM, McDonald WI (1973) Demyelination and remyelination after acute spinal cord compression. Exp Neurol 38:472–487CrossRefPubMed Gledhill RF, Harrison BM, McDonald WI (1973) Demyelination and remyelination after acute spinal cord compression. Exp Neurol 38:472–487CrossRefPubMed
17.
go back to reference Harrison BM, McDonald WI (1977) Remyelination after transient experimental compression of the spinal cord. Ann Neurol 1:542–551CrossRefPubMed Harrison BM, McDonald WI (1977) Remyelination after transient experimental compression of the spinal cord. Ann Neurol 1:542–551CrossRefPubMed
18.
go back to reference Herweh C, Kress B, Rasche D et al (2007) Loss of anisotropy in trigeminal neuralgia revealed by diffusion tensor imaging. Neurology 68:776–778CrossRefPubMed Herweh C, Kress B, Rasche D et al (2007) Loss of anisotropy in trigeminal neuralgia revealed by diffusion tensor imaging. Neurology 68:776–778CrossRefPubMed
19.
go back to reference Hilton DA, Love S, Gradidge T et al (1994) Pathological findings associated with trigeminal neuralgia caused by vascular compression. Neurosurgery 35:299–303CrossRefPubMed Hilton DA, Love S, Gradidge T et al (1994) Pathological findings associated with trigeminal neuralgia caused by vascular compression. Neurosurgery 35:299–303CrossRefPubMed
20.
go back to reference Hodaie M, Chen DQ, Quan J et al (2012) Tractography delineates microstructural changes in the trigeminal nerve after focal radiosurgery for trigeminal neuralgia. PLoS One 7:e32745CrossRefPubMedPubMedCentral Hodaie M, Chen DQ, Quan J et al (2012) Tractography delineates microstructural changes in the trigeminal nerve after focal radiosurgery for trigeminal neuralgia. PLoS One 7:e32745CrossRefPubMedPubMedCentral
21.
go back to reference Horsfield MA, Jones DK (2002) Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases – a review. NMR Biomed 15:570–577CrossRefPubMed Horsfield MA, Jones DK (2002) Applications of diffusion-weighted and diffusion tensor MRI to white matter diseases – a review. NMR Biomed 15:570–577CrossRefPubMed
22.
go back to reference Johansen-Berg H, Rushworth MF (2009) Using diffusion imaging to study human connectional anatomy. Annu Rev Neurosci 32:75–94CrossRef Johansen-Berg H, Rushworth MF (2009) Using diffusion imaging to study human connectional anatomy. Annu Rev Neurosci 32:75–94CrossRef
23.
go back to reference Kopp N, Adabotti J, Sindou M (1994) Histological study (photon and electron microscopic) of trigeminal rootlet specimen in patients with idiopathic trigeminal neuralgia operated on for vascular decompression (13 cases). Acta Neurochir 109:129 Kopp N, Adabotti J, Sindou M (1994) Histological study (photon and electron microscopic) of trigeminal rootlet specimen in patients with idiopathic trigeminal neuralgia operated on for vascular decompression (13 cases). Acta Neurochir 109:129
24.
go back to reference Kress B, Schindler M, Rasche D et al (2005) MRI volumetry for the preoperative diagnosis of trigeminal neuralgia. Eur Radiol 15:1344–1348CrossRefPubMed Kress B, Schindler M, Rasche D et al (2005) MRI volumetry for the preoperative diagnosis of trigeminal neuralgia. Eur Radiol 15:1344–1348CrossRefPubMed
25.
go back to reference Le Bihan D (1995) Molecular diffusion, tissue microdynamics and microstructure. NMR Biomed 8(7–8):375–386CrossRefPubMed Le Bihan D (1995) Molecular diffusion, tissue microdynamics and microstructure. NMR Biomed 8(7–8):375–386CrossRefPubMed
26.
go back to reference Leal PRL, Hermier M, Froment JC et al (2010) Preoperative demonstration of the neuro-vascular compression characteristics with special emphasis on the degree of compression, using high resolution magnetic resonance imaging. A prospective study, with comparison to surgical findings, in 100 consecutive patients who underwent micro-vascular decompression for trigeminal neuralgia. Acta Neurochir 152(5):817–825CrossRefPubMed Leal PRL, Hermier M, Froment JC et al (2010) Preoperative demonstration of the neuro-vascular compression characteristics with special emphasis on the degree of compression, using high resolution magnetic resonance imaging. A prospective study, with comparison to surgical findings, in 100 consecutive patients who underwent micro-vascular decompression for trigeminal neuralgia. Acta Neurochir 152(5):817–825CrossRefPubMed
27.
go back to reference Leal PR, Roch JA, Hermier M et al (2011) Structural abnormalities of the trigeminal root revealed by diffusion tensor imaging in patients with trigeminal neuralgia caused by neurovascular compression: a prospective, double-blind, controlled study. Pain 152:2357–2364CrossRefPubMed Leal PR, Roch JA, Hermier M et al (2011) Structural abnormalities of the trigeminal root revealed by diffusion tensor imaging in patients with trigeminal neuralgia caused by neurovascular compression: a prospective, double-blind, controlled study. Pain 152:2357–2364CrossRefPubMed
28.
go back to reference Leal PRL, Hermier M, Souza MA et al (2011) Visualization of vascular compression of the trigeminal nerve with high-resolution 3-T MRI: a prospective study comparing pre-operative imaging analysis to surgical findings in 40 consecutive patients who underwent micro-vascular decompression for trigeminal neuralgia. Neurosurgery 69(1):15–26CrossRefPubMed Leal PRL, Hermier M, Souza MA et al (2011) Visualization of vascular compression of the trigeminal nerve with high-resolution 3-T MRI: a prospective study comparing pre-operative imaging analysis to surgical findings in 40 consecutive patients who underwent micro-vascular decompression for trigeminal neuralgia. Neurosurgery 69(1):15–26CrossRefPubMed
29.
go back to reference Leal PR, Barbier C, Hermier M et al (2014) Atrophic changes in the trigeminal nerves of patients with trigeminal neuralgia due to neurovascular compression and their association with the severity of compression and clinical outcomes. J Neurosurg 120:1484–1495CrossRefPubMed Leal PR, Barbier C, Hermier M et al (2014) Atrophic changes in the trigeminal nerves of patients with trigeminal neuralgia due to neurovascular compression and their association with the severity of compression and clinical outcomes. J Neurosurg 120:1484–1495CrossRefPubMed
30.
go back to reference Liu Y, Duan Y, He Y et al (2012) A tract-based diffusion study of cerebral white matter in neuromyelitis optica reveals widespread pathological alterations. Mult Scler 18(7):1013–1021CrossRefPubMed Liu Y, Duan Y, He Y et al (2012) A tract-based diffusion study of cerebral white matter in neuromyelitis optica reveals widespread pathological alterations. Mult Scler 18(7):1013–1021CrossRefPubMed
31.
go back to reference Liu Y, Li J, Butzkueven H et al (2013) Microstructural abnormalities in the trigeminal nerves of patients with trigeminal neuralgia revealed by multiple diffusion metrics. Eur J Radiol 82:783–786CrossRefPubMed Liu Y, Li J, Butzkueven H et al (2013) Microstructural abnormalities in the trigeminal nerves of patients with trigeminal neuralgia revealed by multiple diffusion metrics. Eur J Radiol 82:783–786CrossRefPubMed
32.
go back to reference Love S, Hilton DA, Coakham HB (1998) Central demyelination of the Vth nerve root in trigeminal neuralgia associated with vascular compression. Brain Pathol 8:1–12CrossRefPubMed Love S, Hilton DA, Coakham HB (1998) Central demyelination of the Vth nerve root in trigeminal neuralgia associated with vascular compression. Brain Pathol 8:1–12CrossRefPubMed
33.
go back to reference Lummel N, Mehrkens JH, Linn J et al (2015) Diffusion tensor imaging of the trigeminal nerve in patients with trigeminal neuralgia due to multiple sclerosis. Neuroradiology 57:259–267CrossRefPubMed Lummel N, Mehrkens JH, Linn J et al (2015) Diffusion tensor imaging of the trigeminal nerve in patients with trigeminal neuralgia due to multiple sclerosis. Neuroradiology 57:259–267CrossRefPubMed
34.
go back to reference Lutz J, Linn J, Mehrkens JH et al (2011) Trigeminal neuralgia due neurovascular compression: high-spatial-resolution diffusin-tensor imaging reveals microstructural neural changes. Radiology 258:524–530CrossRefPubMed Lutz J, Linn J, Mehrkens JH et al (2011) Trigeminal neuralgia due neurovascular compression: high-spatial-resolution diffusin-tensor imaging reveals microstructural neural changes. Radiology 258:524–530CrossRefPubMed
35.
go back to reference Lutz J, Thon N, Stahl R et al (2016) Microstructural alterations in trigeminal neuralgia determined by diffusion tensor imaging are independent of symptom duration, severity, and type of neurovascular conflict. J Neurosurg 124(3):823–830CrossRefPubMed Lutz J, Thon N, Stahl R et al (2016) Microstructural alterations in trigeminal neuralgia determined by diffusion tensor imaging are independent of symptom duration, severity, and type of neurovascular conflict. J Neurosurg 124(3):823–830CrossRefPubMed
36.
go back to reference Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893–906CrossRef Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med 36:893–906CrossRef
37.
go back to reference Pierpaoli C, Jezzard P, Basser PJ et al (1996) Diffusion tensor MR imaging of the human brain. Radiology 201(3):637–648CrossRefPubMed Pierpaoli C, Jezzard P, Basser PJ et al (1996) Diffusion tensor MR imaging of the human brain. Radiology 201(3):637–648CrossRefPubMed
38.
go back to reference Sindou M, Howeidy T, Acevedo G (2002) Anatomic observations during microvascular decompression for idiopathic trigeminal neuralgia with correlations between topography of pain and site of the neurovascular conflict: prospective study in a series of 579 patients. Acta Neurochir 144:1–12CrossRefPubMed Sindou M, Howeidy T, Acevedo G (2002) Anatomic observations during microvascular decompression for idiopathic trigeminal neuralgia with correlations between topography of pain and site of the neurovascular conflict: prospective study in a series of 579 patients. Acta Neurochir 144:1–12CrossRefPubMed
39.
go back to reference Sindou M, Leston J, Decullier E et al (2007) Microvascular decompression for trigeminal neuralgia: long-term effectiveness and prognostic factors in a series of 362 consecutive patients with clear-cut neurovascular conflicts who underwent pure decompression. J Neurosurg 107:1144–1153CrossRefPubMed Sindou M, Leston J, Decullier E et al (2007) Microvascular decompression for trigeminal neuralgia: long-term effectiveness and prognostic factors in a series of 362 consecutive patients with clear-cut neurovascular conflicts who underwent pure decompression. J Neurosurg 107:1144–1153CrossRefPubMed
40.
go back to reference Smith KJ, McDonald WI (1980) Spontaneous and mechanically evoked activity due to central demyelinating lesion. Nature 286(5769):154–155CrossRefPubMed Smith KJ, McDonald WI (1980) Spontaneous and mechanically evoked activity due to central demyelinating lesion. Nature 286(5769):154–155CrossRefPubMed
41.
go back to reference Wilcox SL, Gustin SM, Eykman EN et al (2013) Trigeminal nerve anatomy in neuropathic and non-neuropathic orofacial pain patients. J Pain 14(8):865–872CrossRefPubMed Wilcox SL, Gustin SM, Eykman EN et al (2013) Trigeminal nerve anatomy in neuropathic and non-neuropathic orofacial pain patients. J Pain 14(8):865–872CrossRefPubMed
Metadata
Title
Diffusion tensor imaging abnormalities of the trigeminal nerve root in patients with classical trigeminal neuralgia: a pre- and postoperative comparative study 4 years after microvascular decompression
Authors
Paulo Roberto Lacerda Leal
Jean Roch
Marc Hermier
Yves Berthezene
Marc Sindou
Publication date
01-07-2019
Publisher
Springer Vienna
Published in
Acta Neurochirurgica / Issue 7/2019
Print ISSN: 0001-6268
Electronic ISSN: 0942-0940
DOI
https://doi.org/10.1007/s00701-019-03913-5

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