Impaired integrity of commissural and association fibers in essential tremor patients: Evidence from a diffusion tensor imaging study

Impaired integrity of commissural and association fibers in essential tremor patients: Evidence from a diffusion tensor imaging study

Background/aim: The evolving understanding of essential tremors (ET) has led to a new definition of neurodegenerative disease, pointing to diffuse brain network involvement with a wide spectrum of associated motor and nonmotor symptoms. Considering the fact that white matter should also be affected by the nature of the disease, our study aimed to evaluate the integrity of white matter and its clinical correlations in ET patients. Materials and methods: Approximately 40 patients diagnosed with ET and 40 age-and sex-matched control subjects (ranging between 18–80 years old) were included in the study. The sociodemographic characteristics and clinical features of the patients were recorded. Tremors were assessed using the Fahn-Tolosa-Marin Tremor Rating Scale (FTM-TRS). Diffusion Tensor Imaging (DTI) was performed to evaluate the integrity of white matter. The selected white matter regions used for DTI assessment were the corpus callosum (CC) (i.e., the largest commissural tract in the human brain), the superior longitudinal fasciculus (SLF), and the inferior longitudinal fasciculus (ILF) (i.e., the largest association fiber bundles). Results: The mean age of the ET patients and control subjects was 44.23 ± 18.91 and 37.45 ± 10.95 years old (P = 0.542). The fractional anisotropy (FA) values of the CC body (P = 0.003), ILF (p = 0.016), average diffusion coefficient (ADC) values of the CC body (p = 0.001), genu (P = 0.049), SLF (V < 0.001), and ILF (P < 0.001) differed between groups. After controlling for age and sex, there was no correlation between tremor severity and DTI parameters, but impaired integrity in the genu of CC FA (P = 0.035, r = 0.442) and the splenium of CC ADC (P = 0.007, r = 0.543) were related with a longer duration of tremor. Finally, positive family history was correlated with the splenium of CC FA and ADC (P = 0.008, r = 0.536; P = 0.027, r = 0.461) and ILF ADC (P = 0.011, r = –0.519). Conclusion: In our study, major white matter structure changes were found in the ET patients. The results suggest that possible neurodegeneration also affects white matter structures in ET patients and that the duration of the tremor and family history are related with impaired integrity of white matter.Key words: Essential tremor, white matter, neurodegeneration, diffusion tensor imaging, fractional anisotropy, average diffusion coefficient

___

  • 1. Critchley M. Observations on essential (heredofamilial) tremor. Brain 1949; 72 (2): 113-139. doi: 10.1093/brain/72.2.113
  • 2. Louis ED, Ferreira JJ. How common is the most common adult movement disorder? Update on the worldwide prevalence of essential tremor. Movement Disorders 2010; 25 (5): 534-541. doi: 10.1002/mds.22838
  • 3. Dogu O, Sevim S, Camdeviren H, Sasmaz T, Bugdayci R et al. Prevalence of essential tremor: Door-to-door neurologic exams in Mersin Province, Turkey. Neurology 2003; 61 (12): 1804-1806. doi: 10.1212/01.WNL.0000099075.19951.8C
  • 4. Deuschl G, Elble RJ. The pathophysiology of essential tremor. Neurology 2000; 54 (11Suppl 4): 14-20.
  • 5. Benito-León J, and Louis ED. Essential tremor: emerging views of a common disorder. Nature clinical practice. Neurology 2006; 2 (12): 666-678. doi: 10.1038/ncpneuro0347
  • 6. Chandran V, Pal PK. Essential tremor: beyond the motor features. Parkinsonism Related Disorders 2012; 18 (5): 407– 413. doi: 10.1016/j.parkreldis.2011.12.003
  • 7. Benito-León J. Essential tremor: a neurodegenerative disease? Tremor Other Hyperkinetic Movements 2014; 4: 252. doi: 10.7916/D8765CG0
  • 8. Benito-León J, and Louis ED. Clinical update: diagnosis and treatment of essential tremor. Lancet 2007; 369 (9568): 1152– 1154. doi: 10.1016/S0140-6736(07)60544-3
  • 9. Benito-León J, Louis ED. Update on essential tremor. Minerva Medica 2011; 102 (6): 417-439.
  • 10. Louis ED, Benito-León J, Bermejo-Pareja F. Neurological Disorders in Central Spain Study, G. Self-reported depression and anti-depressant medication use in essential tremor: crosssectional and prospective analyses in a population-based study. European Journal of Neurology: The Official Journal of the European Federation of Neurological Societies 2007; 14 (10): 1138-1146. doi: 10.1111/j.1468-1331.2007.01923.x
  • 11. Benito-León J, Louis ED, Bermejo-Pareja F. Short sleep duration heralds’ essential tremor: a prospective, populationbased study. Movement Disorders: Official Journal of the Movement Disorder Society 2013; 28 (12): 1700-1707. doi: 10.1002/mds.25590
  • 12. Benito-León J, Louis ED, Bermejo-Pareja F. Reported hearing impairment in essential tremor: a population-based casecontrol study. Neuroepidemiology 2007; 29 (3-4): 213-217. doi: 10.1159/000112463
  • 13. Tröster AI, Fields JA, Pahwa R, Wilkinson SB, Straits–Tröster KA et al. Neuropsychological and quality of life outcome after thalamic stimulation for essential tremor. Neurology 1999; 53 (8): 1774-1780. doi: 10.1212/WNL.53.8.1774
  • 14. Louis ED, Benito-León J, Vega-Quiroga S, Bermejo-Pareja F. Cognitive and motor functional activity in non-demented community-dwelling essential tremor cases. Journal of Neurology, Neurosurgery, and Psychiatry 2010; 81 (9): 997- 1001. doi: 10.1136/jnnp.2009.202838
  • 15. Louis ED, Benito-León J, Vega-Quiroga S, Bermejo-Pareja F. Faster rate of cognitive decline in essential tremor cases than controls: a prospective study. European journal of neurology: The Official Journal of The European Federation of Neurological Societies 2010; 17 (10): 1291-1297. doi:10.1111/ j.1468-1331.2010.03122.x
  • 16. Benito-León J, Louis ED, Sánchez-Ferro A, Bermejo-Pareja F. Rate of cognitive decline during the premotor phase of essential tremor: A prospective study. Neurology 2013; 81 (1): 60-66. doi: 10.1212/WNL.0b013e318297ef2b
  • 17. Jankovic J. Essential tremor course and disability: a clinicopathologic study of 20 cases. Neurology 2004; 63 (8): 1541-1542. doi: 10.1212/WNL.63.8.1541-a
  • 18. Shill HA, Adler CH, Sabbagh MN, Connor DJ, Caviness JN et al. Pathologic findings in prospectively ascertained essential tremor subjects. Neurology 2008; 70 (16 Part 2): 1452-1455. doi: 10.1212/01.wnl.0000310425.76205.02
  • 19. Yahr MD, Orosz D, Purohit DP. Co-occurrence of essential tremor and Parkinson‟s disease: clinical study of a large kindred with autopsy findings. Parkinsonism Related Disorders 2003; 9 (4): 225-231. doi: 10.1016/S1353-8020(02)00057-3
  • 20. Samson M, and Claassen DO, Neurodegeneration and the cerebellum. Neurodegenerative Diseases 2017; 17 (4-5): 155- 165. doi: 10.1159/000460818
  • 21. Louis ED, and Faust PL, Essential tremor pathology: neurodegeneration and reorganization of neuronal connections. Nature Reviews Neurology 2020; 1-15. doi: 10.1038/s41582-019-0302-1
  • 22. Benito-León J, Alvarez-Linera J, Hernández-Tamames JA, Alonso-Navarro, H, Jiménez-Jiménez FJ et al. Brain structural changes in essential tremor: voxel-based morphometry at 3-Tesla. Journal of the Neurological Sciences 2009; 287 (1-2): 138-142. doi: 10.1016/j.jns.2009.08.037
  • 23. Cerasa A, Passamonti L, Novellino F, Salsone M, Gioia M et al. Fronto-parietal overactivation in patients with essential tremor during Stroop task. Neuroreport 2010; 21 (2): 148-151. doi: 10.1097/WNR.0b013e328335b42c
  • 24. Passamonti L, Novellino F, Cerasa A, Chiriaco C, Rocca F et al. Altered cortical-cerebellar circuits during verbal working memory in essential tremor. Brain: A Journal of Neurology 2011; 134 (8): 2274-2286. doi: 10.1093/brain/awr164
  • 25. Quattrone A, Cerasa A, Messina D, Nicoletti G, Hagberg GE et al. Essential head tremor is associated with cerebellar vermis atrophy: a volumetric and voxel-based morphometry MR imaging study. American Journal of Neuroradiology 2008; 29 (9): 1692-1697. doi: 10.3174/ajnr.A1190
  • 26. Cerasa A, Messina D, Nicoletti G, Novellino F, Lanza P et al. Cerebellar atrophy in essential tremor using an automated segmentation method. American Journal of Neuroradiology 2009; 30 (6): 1240-1243. doi: 10.3174/ajnr.A1544
  • 27. Shin H, Lee D-K, Lee J-M, Huh YE, Youn J et al. Atrophy of the cerebellar vermis in essential tremor: segmental volumetric MRI analysis. Cerebellum 2016; 15 (2): 174-181. doi: 10.1007/ s12311-015-0682-8
  • 28. Dyke JP, Cameron E, Hernandez N, Dydak U, Louis ED. Gray matter density loss in essential tremor: a lobule by lobule analysis of the cerebellum. Cerebellum Ataxias 2017; 4 (1): 10. doi: 10.1186/s40673-017-0069-3
  • 29. Cao H, Wang R, Luo X, Li X, Hallett M. A voxel-based magnetic resonance imaging morphometric study of cerebral and cerebellar graymatter in patients under 65 years with essential tremor. Medical Science Monitor 2018; 24: 3127- 3135. doi: 10.12659/MSM.906437
  • 30. Daniels C, Peller M, Wolff S, Alfke K, Witt K et al. Voxel-based morphometry shows no decreases in cerebellar gray matter volume in essential tremor. Neurology 2006; 67 (8): 1452-1456. doi: 10.1212/01.wnl.0000240130.94408.99
  • 31. Lin C-H, Chen C-M, Lu M-K, Tsai CH, Chiou JC et al. VBM reveals brain volume differences between Parkinson’s disease and essential tremor patients. Frontiers in Human Neuroscience 2013; 7: 247. doi: 10.3389/fnhum.2013.00247
  • 32. Bagepally BS, Bhatt MD, Chandran V, Saini J, Bharath RD et al. Decrease in cerebral and cerebellar gray matter in essential tremor: a voxel based morphometric analysis under 3T MRI. Journal of Neuroimaging 2012; 22 (3): 275-278. doi: 10.1111/j.1552-6569.2011.00598.x
  • 33. Cameron E, Dyke JP, Hernandez N, Louis ED, Dydak U et al. Cerebral gray matter volume losses in essential tremor: a case-control study using high resolution tissue probability maps. Parkinsonism Related Disorders 2018; 51: 85-90. doi: 10.1016/j.parkreldis.2018.03.008
  • 34. Jia L, Jia‐lin S, Qin D, Qing L, Yan Z. Diffusion tensor imaging study in essential tremor. Journal of Neuroimaging 2010; 21 (4): 370-374. doi: 10.1111/j.1552-6569.2010.00535.x
  • 35. Nicoletti G, Manners D, Novellino F, Condino F, Malucelli E et al. Diffusion tensor MRI changes in cerebellar structures of patients with familial essential tremor. Neurology 2010; 74 (12): 988-994. doi: 10.1212/WNL.0b013e3181d5a460
  • 36. Klein JC, Lorenz B, Kang JS, Baudrexel S, Seifried C. Diffusion tensor imaging of white matter involvement in essential tremor. Human Brain Mapping 2011; 32 (6): 896-904. doi: 10.1002/ hbm.21077
  • 37. Saini J, Bagepally BS, Bhatt MD, Chandran V, Bharath RD et al. Diffusion tensor imaging: Tract based spatial statistics study in essential tremor. Parkinsonism Related Disorders 2012; 18 (5): 477-482. doi: 10.1016/j.parkreldis.2012.01.006
  • 38. Nestrasil I, Svatkova A, Rudser KD, Chityala R, Wakumoto A et al. White matter measures correlate with essential tremor severity-A pilot diffusion tensor imaging study. Brain and Behavior 2018; 8 (8): e01039. doi: 10.1002/brb3.1039
  • 39. Mori S, Zhang J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 2006; 51 (5): 527-539. doi: 10.1016/j.neuron.2006.08.012
  • 40. Bhatia KP, Bain P, Bajaj N, Elble RJ, Hallett M et al. Consensus statement on the classification of tremors from the task force on tremor of the International Parkinson and Movement Disorder Society. Movement Disorders 2018; 33 (1): 75-87. doi: 10.1002/mds.27121
  • 41. Morris JC. Clinical dementia rating: a reliable and valid diagnostic and staging measure for dementia of the Alzheimer type. International Psychogeriatrics 1997; 9 (S1): 173-176. doi: 10.1017/S1041610297004870
  • 42. Stacy MA, Elble RJ, Ondo WG, Wu SC, Hulihan J. TRS study group: Assessment of interrater and intrarater reliability of the Fahn–Tolosa–Marin Tremor Rating Scale in essential tremor 2007; 22 (6): 833-838. doi: 10.1002/mds.21412
  • 43. Varga A, Di Leo G, Nagy A, Suhai FI, Apor A et al. Brain diffusion tensor imaging in patients with transcatheter aortic valve implantation: early results of the RETORIC study. In: European Congress of Radiology 2018; Vienna, Austria. doi: 10.1594/ecr2018/C-1822
  • 44. Pietracupa S, Bologna M, Bharti K, Pasqua G, Tommasin S et al. White matter rather than gray matter damage characterizes essential tremor. European Radiology 2019; 29 (12): 6634- 6642. doi: 10.1007/s00330-019-06267-9
  • 45. Hoeft F, Barnea-Goraly N, Haas BW, Golarai G, Ng D et al. More is not always better: increased fractional anisotropy of superior longitudinal fasciculus associated with poor visuospatial abilities in Williams syndrome. Journal of Neuroscience 2007; 31: 11960-11965. doi: 10.1523/JNEUROSCI.3591-07.2007
  • 46. Nath K, Husain M, Trivedi R, Kumar R, Prasad KN et al. Clinical implications of increased fractional anisotropy in meningitis associated with brain abscess. Journal of Computer Assisted Tomography 2007; 31: 888-893. doi: 10.1097/ rct.0b013e3180547118
  • 47. Mole JP, Subramanian L, Bracht T, Morris H, Metzler-Baddeley C et al. Increased fractional anisotropy in the motor tracts of Parkinson’s disease suggests compensatory neuroplasticity or selective neurodegeneration. European Radiology 2016; 26: 3327-3335. doi: 10.1007/s00330-015-4178-1
  • 48. Kumar R, Chavez AS, Macey PM, Woo MA, Yan‐Go FL et al. Altered global and regional brain mean diffusivity in patients with obstructive sleep apnea. Journal of Neuroscience Research 2012; 90 (10): 2043-2052. doi: 10.1002/jnr.23083
  • 49. Imagawa KK, Hamilton A, Ceschin R, Tokar E, Pham P et al. Characterization of microstructural injury: a novel approach in infant abusive head trauma—initial experience. Journal of Neurotrauma 2014; 31 (19): 1632-1638. doi: 10.1089/ neu.2013.3228
Turkish Journal of Medical Sciences-Cover
  • ISSN: 1300-0144
  • Yayın Aralığı: Yılda 6 Sayı
  • Yayıncı: TÜBİTAK
Sayıdaki Diğer Makaleler

Utility of the Pleth Variability Index in predicting anesthesia-induced hypotension in geriatric patients

Ahmet YÜKSEK

Effective dose of intravenous oxycodone depending on sex and age for attenuation of intubation-related hemodynamic responses

Keum Young SO, Ki Tae JUNG, Bo Hyun JANG, Sang Hun KIM

Efficacy of the in vitro splitting of human preimplantation embryos from ART programs

Marjan OMIDI, Mohammad Ali KHALILI, Azam AGHA-RAHIMI, Stefania A. NOTTOLA, Fatemeh ANBARI, Azita FARAMARZI, Maria Grazia PALMERINI

How does rerupture affect sleep and quality of life in patients undergoing arthroscopic rotator cuff repair?

İzzet BİNGÖL, Vedat BİÇİCİ

Can urinary biomarkers predict acute kidney injury in newborns with critical congenital heart disease?

Eser SÖZMEN, Mehmet YALAZ, Özgün UYGUR, Özge ALTUN KÖROĞLU, Nilgün KÜLTÜRSAY, Yüksel ATAY, Mete AKISÜ, Ertürk LEVENT, Fırat ERGİN

Family-centeredness of services for young children with Down syndrome: an observational study from Turkey

Funda AKPINAR, Emine Bahar BİNGÖLER PEKCİCİ, Ezgi ÖZALP AKIN, Gamze HAYRAN, Cansu KELEŞ, Betül YAĞBASAN, İlgi ÖZTÜRK ERTEM, Nazmiye KURŞUN

Validation of the NoSAS score for screening sleep-disordered breathing: A sleep clinicbased study in Turkey

Mehmet Nurullah ORMAN, Özgür BATUM, Burcu OKTAY ARSLAN, Zeynep Zeren UÇAR

Magnetic resonance imaging histogram analysis of corpus callosum in a functional neurological disorder

Sema BAYKARA, Murad ATMACA, Osman MERMİ, Hanefi YILDIRIM, Murat BAYKARA

Efficacy, retention, and safety of tofacitinib in real-life: Hur-bio monocentric experience

Levent KILIÇ, Emre BİLGİN, Ali AKDOĞAN, Umut KALYONCU, Sedat KİRAZ, Ömer KARADAĞ, Ali İhsan ERTENLİ, Gözde Kübra YARDIMCI, Emine DURAN, , Ertuğrul Çağrı BÖLEK, Furkan CEYLAN, Bayram FARİSOĞULLARI, Şule Apraş BİLGEN

Imaging modalities used in diagnosis and follow-up of patients with Takayasu’s arteritis

Levent KILIÇ, Abdulsamet ERDEN, Ayşe Bahar KELEŞOĞLU DİNÇER, Umut KALYONCU, Sedat KİRAZ, Ömer KARADAĞ, Tuncay HAZIROLAN