Abstract
Introduction
Neurovascular compression (NVC) is the most common cause of trigeminal neuralgia (TN), leading to microstructural changes in the affected nerve detectable using diffusion tensor imaging (DTI). But TN may also emerge as a symptom of multiple sclerosis (MS). The aim of this study was to evaluate if patients with MS-related TN feature the same DTI characteristics as patients with TN caused by NVC.
Methods
Twelve patients with MS-related TN, 12 age-matched patients with NVC-related TN, and 12 healthy controls were included. Using 3T-DTI, mean fractional anisotropy (FA) and apparent diffusion coefficient (ADC) values were calculated for each affected and contralateral trigeminal nerve in patients with MS and NVC-related TN as well as healthy controls. Furthermore, presence of NVC was evaluated for patients with TN.
Results
There was no significant difference concerning FA or ADC when comparing the affected and the non-affected sides in patients with MS. FA was significantly lower and ADC higher in patients with MS on the TN affected as well as on the non-affected side compared to the non-affected side of patients with idiopathic TN or healthy controls. Likewise, FA was significantly lower on the affected side compared to the non-affected side in patients with idiopathic TN or healthy controls. NVC was evident in 41.7/0 % on the affected/contralateral side in MS patients and 100/8 % in the patients with NVC-related TN.
Conclusion
In patients with MS-related TN, DTI reveals microstructural changes within the trigeminal nerve not only on the affected side but also on the clinically non-affected side.
Similar content being viewed by others
References
Love S, Gradidge T, Coakham HB (2001) Trigeminal neuralgia due to multiple sclerosis: ultrastructural findings in trigeminal rhizotomy specimens. Neuropathol Appl Neurobiol 27(3):238–244
O’Connor AB, Schwid SR, Herrmann DN, Markman JD, Dworkin RH (2008) Pain associated with multiple sclerosis: systematic review and proposed classification. Pain 137(1):96–111. doi:10.1016/j.pain.2007.08.024
Martinelli Boneschi F, Colombo B, Annovazzi P, Martinelli V, Bernasconi L, Solaro C, Comi G (2008) Lifetime and actual prevalence of pain and headache in multiple sclerosis. Mult Scler 14(4):514–521. doi:10.1177/1352458507085551
Solaro C, Brichetto G, Amato MP, Cocco E, Colombo B, D’Aleo G, Gasperini C, Ghezzi A, Martinelli V, Milanese C, Patti F, Trojano M, Verdun E, Mancardi GL (2004) The prevalence of pain in multiple sclerosis: a multicenter cross-sectional study. Neurology 63(5):919–921
Jensen TS, Rasmussen P, Reske-Nielsen E (1982) Association of trigeminal neuralgia with multiple sclerosis: clinical and pathological features. Acta Neurol Scand 65(3):182–189
Cruccu G, Biasiotta A, Di Rezze S, Fiorelli M, Galeotti F, Innocenti P, Mameli S, Millefiorini E, Truini A (2009) Trigeminal neuralgia and pain related to multiple sclerosis. Pain 143(3):186–191. doi:10.1016/j.pain.2008.12.026
Gass A, Kitchen N, MacManus DG, Moseley IF, Hennerici MG, Miller DH (1997) Trigeminal neuralgia in patients with multiple sclerosis: lesion localization with magnetic resonance imaging. Neurology 49(4):1142–1144
Meaney JF, Watt JW, Eldridge PR, Whitehouse GH, Wells JC, Miles JB (1995) Association between trigeminal neuralgia and multiple sclerosis: role of magnetic resonance imaging. J Neurol Neurosurg Psychiatry 59(3):253–259
Mills RJ, Young CA, Smith ET (2010) Central trigeminal involvement in multiple sclerosis using high-resolution MRI at 3T. Br J Radiol 83(990):493–498. doi:10.1259/bjr/65228893
Lutz J, Linn J, Mehrkens JH, Thon N, Stahl R, Seelos K, Bruckmann H, Holtmannspotter M (2011) Trigeminal neuralgia due to neurovascular compression: high-spatial-resolution diffusion-tensor imaging reveals microstructural neural changes. Radiology 258(2):524–530. doi:10.1148/radiol.10100477
DeSouza DD, Hodaie M, Davis KD (2014) Abnormal trigeminal nerve microstructure and brain white matter in idiopathic trigeminal neuralgia. Pain 155(1):37–44. doi:10.1016/j.pain.2013.08.029
Liu Y, Li J, Butzkueven H, Duan Y, Zhang M, Shu N, Li Y, Zhang Y, Li K (2013) Microstructural abnormalities in the trigeminal nerves of patients with trigeminal neuralgia revealed by multiple diffusion metrics. Eur J Radiol 82(5):783–786. doi:10.1016/j.ejrad.2012.11.027
Pierpaoli C, Basser PJ (1996) Toward a quantitative assessment of diffusion anisotropy. Magn Reson Med Off J Soc Magn Reson Med Soc Magn Reson Med 36(6):893–906
Hilton DA, Love S, Gradidge T, Coakham HB (1994) Pathological findings associated with trigeminal neuralgia caused by vascular compression. Neurosurgery 35(2):299–303, discussion 303
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):1–11, discussion 11–12
Devor M, Govrin-Lippmann R, Rappaport ZH (2002) Mechanism of trigeminal neuralgia: an ultrastructural analysis of trigeminal root specimens obtained during microvascular decompression surgery. J Neurosurg 96(3):532–543. doi:10.3171/jns.2002.96.3.0532
Solaro C, Uccelli MM (2011) Management of pain in multiple sclerosis: a pharmacological approach. Nat Rev Neurol 7(9):519–527. doi:10.1038/nrneurol.2011.120
Lassmann H (2010) Axonal and neuronal pathology in multiple sclerosis: what have we learnt from animal models. Exp Neurol 225(1):2–8. doi:10.1016/j.expneurol.2009.10.009
Hooge JP, Redekop WK (1995) Trigeminal neuralgia in multiple sclerosis. Neurology 45(7):1294–1296
De Simone R, Marano E, Brescia Morra V, Ranieri A, Ripa P, Esposito M, Vacca G, Bonavita V (2005) A clinical comparison of trigeminal neuralgic pain in patients with and without underlying multiple sclerosis. Neurol Sci 26(Suppl 2):s150–s151. doi:10.1007/s10072-005-0431-8
Cruccu G, Biasiotta A, Galeotti F, Iannetti GD, Truini A, Gronseth G (2006) Diagnostic accuracy of trigeminal reflex testing in trigeminal neuralgia. Neurology 66(1):139–141. doi:10.1212/01.wnl.0000191388.64530.8f
Lazar ML, Kirkpatrick JB (1979) Trigeminal neuralgia and multiple sclerosis: demonstration of the plaque in an operative case. Neurosurgery 5(6):711–717
Olafson RA, Rushton JG, Sayre GP (1966) Trigeminal neuralgia in a patient with multiple sclerosis. An autopsy report. J Neurosurg 24(4):755–759. doi:10.3171/jns.1966.24.4.0755
Filippi M, Iannucci G, Cercignani M, Assunta Rocca M, Pratesi A, Comi G (2000) A quantitative study of water diffusion in multiple sclerosis lesions and normal-appearing white matter using echo-planar imaging. Arch Neurol 57(7):1017–1021
Love S, Coakham HB (2001) Trigeminal neuralgia: pathology and pathogenesis. Brain 124(Pt 12):2347–2360
Adamczyk M, Bulski T, Sowinska J, Furmanek A, Bekiesinska-Figatowska M (2007) Trigeminal nerve-artery contact in people without trigeminal neuralgia—MR study. Med Sci Monit 13(Suppl 1):38–43
Le Bihan D (1995) Molecular diffusion, tissue microdynamics and microstructure. NMR Biomed 8(7–8):375–386
Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111(3):209–219
Wilcox SL, Gustin SM, Eykman EN, Fowler G, Peck CC, Murray GM, Henderson LA (2013) Trigeminal nerve anatomy in neuropathic and non-neuropathic orofacial pain patients. J Pain 14(8):865–872. doi:10.1016/j.jpain.2013.02.014
Fujiwara S, Sasaki M, Wada T, Kudo K, Hirooka R, Ishigaki D, Nishikawa Y, Ono A, Yamaguchi M, Ogasawara K (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(2):e102–e108. doi:10.1111/j.1552-6569.2010.00508.x
Filippi M, Cercignani M, Inglese M, Horsfield MA, Comi G (2001) Diffusion tensor magnetic resonance imaging in multiple sclerosis. Neurology 56(3):304–311
Lerner A, Mogensen MA, Kim PE, Shiroishi MS, Hwang DH, Law M (2013) Clinical applications of diffusion tensor imaging. World Neurosurg. doi:10.1016/j.wneu.2013.07.083
Ethical standards and patient consent
We declare that this study was approved by our Institutional Review Board and has therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. We declare that all patients gave informed consent prior to inclusion in this study.
Conflict of interest
We declare that we have no conflict of interest.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Lummel, N., Mehrkens, J.H., Linn, J. et al. Diffusion tensor imaging of the trigeminal nerve in patients with trigeminal neuralgia due to multiple sclerosis. Neuroradiology 57, 259–267 (2015). https://doi.org/10.1007/s00234-014-1463-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00234-014-1463-7