Multiple subtypes of tremor-dominant form of Parkinson’s disease: diagnostic and therapeutic significance
Z.A. ZALYALOVA1, 2, S.E. MUNASIPOVA1, 2, M.M. ERMAKOVA1
1Kazan State Medical University, Kazan
2Republic Consultative-diagnostic Center for extra-pyramid pathology and botulin therapy — Hospital for military veterans, Kazan
Contact details:
Munasipova S.E. — PhD (Medicine), Assitant Lecturer of the Department of Neurology and Rehabilitation, neurologist
Address: 49 Butlerov St., Kazan, Russian Federation, 420012, tel.: +7-960-045-53-01, e‐mail: sabina.munasipova@mail.ru
Tremor is one of the most common motor symptoms in Parkinson’s disease (PD) and affects up to 75% of patients. The tremolous form of PD is heterogeneous in clinical manifestations. Along with classic rest tremor, patients with PD may experience postural and kinetic types of the tremor, which reflects the multimodal mechanism of its formation. Classifications of PD are constantly changing, including within the tremor-dominant form. The varied responses to levodopa also reflect the role of multiple underlying pathophysiological processes. New, non-antiparkinson drugs are being studied. Evidence of the effectiveness of advanced neurosurgical, non-invasive treatment methods is not always convincing; there are no large-scale comparative studies assessing their effectiveness in patients with tremor-dominant forms of PD.
Key words: Parkinson’s disease, tremor, rest tremor, postural tremor, kinetic tremor, isometric tremor, treatment of Parkinson’s disease, levodopa.
REFERENCES
- Louis E.D. Tremor. Continuum (MinneapMinn), 2019, vol. 25 (4), pp. 959–975. DOI: 10.1212/CON.0000000000000748
- Bhatia K.P., Bain P., Bajaj N. et al. Consensus Statement on the classi- fication of tremors. from the task force on tremor of the International Parkinson and Movement Disorder Society. Mov. Disord, 2018, vol. 33 (1), pp. 75–87. DOI: 10.1002/mds.27121
- Zalyalova Z.A., Katunina E.A., Pokhabov D.V., Munasipova S.E., Ermakova M.M. Tremor-dominant form of Parkinson’s disease. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova, 2024, no. 124 (4), pp. 1–8 (in Russ.). DOI: 10.17116/jnevro20241240411
- Pasquini J., Ceravolo R., Qamhawi Z., Lee J.-Y., Deuschl G., Brooks D.J. et al. Progression of tremor in early stages of Parkinson’s disease: a clinical and neuroimaging study. Brain, 2018, vol. 141 (3), pp. 811–821. DOI: 10.1093/brain/awx376
- Luo L. et al. Motor phenotype classification in moderate to advanced PD in BioFIND study. Parkinsonism Relat. Disord, 2019, vol. 65, pp. 178–183. DOI: 10.1016/j.parkreldis.2019.06.017
- Heusinkveld L.E., Hacker M.L., Turchan M., Davis T.L., Charles D. Impact of tremor on patients with early stage Parkinson’s disease. Front. Neurol, 2018, vol. 9, p. 628. DOI: 10.3389/ fneur.2018.00628
- Tröster A.I., Pahwa R., Fields J.A., Tanner C.M., Lyons K.E. Quality of life in Essential Tremor Questionnaire (QUEST): development and initial validation. Park. Relat. Dis, 2005, vol. 11 (6), pp. 367–373. DOI: 10.1016/j. parkreldis.2005.05.009
- Zalyalova Z.A. Drozhatel’nye fenotipy bolezni Parkinsona. V kn.: 25. Bolezn’ Parkinsona i rasstroistva dvizheniiy. Ruk‐vo dlya vrachey po materialam II Natsional’nogo kongressa [Trembling phenotypes of Parkinson’s disease. In the book: 25. Parkinson’s disease and movement disorders. Guide for doctors based on the materials of the II National Congress]. Moscow, 2011. Pp. 5–59.
- Aleksovski D., Miljkovic D., Bravi D. et al. Disease progression in Parkinson subtypes: the PPMI dataset. Neurol. Sci, 2018, vol. 39 (7), pp. 1971–1976. DOI: 10.1007/s10072‐018‐3522‐z
- Levin O.S., Datieva V.K. Tremor in Parkinson’s disease: features of phenomenology and treatment. Sovremennaya terapiya v psikhiatrii i nevrologii, 2014, no. 3 (6), pp. 14–19 (in Russ.).
- Illarioshkin S.N., Ivanova‐Smolenskaya I.A Drozhatel’nye giperkinezy: rukovodstvo dlya vrachey (Seriya rukovodstv “Dvigatel’nye rasstroistva”)[]. Moscow: Izdatel’skiiy kholding “Atmosfera”, 2011.
- Madelein van der Stouwe A.M., Nieuwhof F., Helmich R.C. Tremor pathophys‐iology: lessons from neuroimaging. Curr. Opin. Neurol, 2020, vol. 33 (4), pp. 474–481. DOI: 10.1097/WCO.0000000000000829
- Hallett M. Tremor: pathophysiology. Park. Relat. Dis, 2014, vol. 20 (1), pp. S118–S122. DOI: 10.1016/S1353‐8020(13)70029‐4
- Helmich R.C., Dirkx M.F. Pathophysiology and management of Parkinsonian tremor. Semin. Neurol, 2017, vol. 37, pp. 127–134. DOI: 10.1055/s‐0037‐1601558
- Helmich R.C. The cerebral basis of Parkinsonian tremor: A network perspective. Mov. Dis, 2018, vol. 33 (7), pp. 219–231. DOI: 10.1002/mds.27224
- Dirkx M.F., Bologna M. The pathophysiology of Parkinson’s disease tremor. J. Neurol. Sci, 2022, vol. 435, 120196. DOI: 10.1016/j.jns.2022.120196
- Helmich R.C., Hallett M., Deuschl G. et al. Cerebral causes and conse‐quences of parkinsonian resting tremor: A tale of two circuits? Brain, 2012, vol. 135 (8), pp. 3206–3226. DOI: 10.1093/brain/aws023
- Jellinger K.A. Neuropathology of sporadic Parkinson’s disease: Evaluation and changes of concepts. Mov. Dis, 2012, vol. 27, pp. 8–30. DOI: 10.1002/mds.23795
- Helmich R.C., Janssen M.J.R., Oyen W.J.G. et al. Pallidal dysfunction drives a cerebellothalamic circuit into Parkinson tremor. Ann. Neurol, 2011, vol. 69, pp. 269–281. DOI: 10.1002/ana.22361
- Paulus W., Jellinger K. The neuropathologic basis of different clinical sub‐ groups of Parkinson’s disease. J. Neuropathol. Exp. Neurol, 1991, vol. 50 (6), pp. 743–755. DOI: 10.1097/00005072‐199111000‐00006
- Gironell A., Pascual‐Sedano B., Aracil I. et al. Tremor Types in Parkinson disease: a descriptive study using a new classification. Park. Dis, 2018, vol. 56 (7), pp. 45–50. DOI: 10.1155/2018/4327597
- Lenka A., Jankovic J. tremor syndromes: an updated review. Front. Neurol, 2021, vol. 12 (7), pp. 1–17. DOI: 10.3389/fneur.2021.684835
- Hess C.W., Pullman S.L. Tremor: clinical phenomenology and assessment techniques. Tremor Other Hyperkin. Mov, 2012, vol. 2, pp. 1–15. DOI: 10.5334/tohm.115
- Dirkx M.F., Zach H., Bloem B.R. et al. The nature of postural tremor in Parkinson disease. Neurology, 2018, vol. 90, pp. e1095–1102. DOI: 10.1212/WNL.0000000000005215
- Gupta D.K. et al. Prevalence and relationship of rest tremor and action tremor in Parkinson’s disease. Tremor Other Hyperkin. Mov, 2020, vol. 10 (1), pp. 1–7. DOI: 10.5334/tohm.552
- Golubev V.L. Algorithm for treating early stages of Parkinson’s disease. Atmosfera. Nervnye bolezni, 2006, no. 12 (4), pp. 9–12 (in Russ.).
- Tedeschi G. Tremor in Parkinson disease: acute response to oral levodopa. Ital. J. Neurol. Sci, 1990, vol. 11 (3), pp. 259–263. DOI: 10.1007/BF02333855
- Gigante A. Action tremor in Parkinson’s disease: frequency and relationship to motor and non‐motor signs. Eur. J. Neurol, 2015, vol. 22 (2), pp. 223–228. DOI: 10.1111/ene.12583
- Govorova T.G., Popova T.E., Tappakhov A.A. Elektrofiziologicheskie osobennosti tremora pri essentsial’nom tremore i bolezni Parkinsona [Electrophysiological features of tremor in essential tremor and Parkinson’s disease]. Botkinskie chteniya. Vserossiiskiiye terapevticheskiiy kongress s mezhdunarodnym uchastiem, 2019. Pp. 56–57.
- Stebbins G.T. How to identify tremor dominant and postural instability/gait difficulty groups with the movement disorder society unified Parkinson’s disease rating scale: comparison with the unified Parkinson’s disease rating scale. Mov. Dis, 2013, vol. 28 (5), pp. 668–670. DOI: 10.1002/mds.25383
- De Bie R.M.A., Clarke C.E., Espay A.J. et al. Initiation of pharmacological therapy in Parkinson’s disease: when, why, and how. Lancet Neurol, 2020, vol. 19, pp. 452–461. DOI: 10.1016/S1474‐4422(20)30036‐3
- Balestrino R., Schapira A.H.V. Parkinson disease. Eur. J. Neurol, 2020, vol. 27 (8), pp. 27–42. DOI: 10.1111/ene.14108
- Pringsheim T., Day G.S., Smith D.B. et al. Dopaminergic therapy for motor symptoms in early Parkinson disease practice Guideline summary. Neurology, 2021, vol. 97, pp. 942–957. DOI: 10.1212/WNL.0000000000012868
- Nonnekes J., Timmer M.H.M., de Vries N.M. et al. Unmasking levodopa re‐sistance in Parkinson’s disease. Mov. Dis, 2016, vol. 31, pp. 1602–1609. DOI: 10.1002/mds.26712
- Zach H., Dirkx M., Pasman J.W. et al. The patient’s perspective: The effect of levodopa on Parkinson symptoms. Park. Relat. Dis, 2017, vol. 35, pp. 48–54. DOI: 10.1016/j.parkreldis.2016.11.015
- Zach H., Dirkx M.F., Roth D. et al. Dopamine‐responsive and dopamine‐resis‐tant resting tremor in Parkinson disease. Neurology, 2020, vol. 95 (11), pp. e1461–e1470. DOI: 10.1212/WNL.0000000000010316
- Beckers M., Bloem B.R., Verbeek M.M. Mechanisms of peripheral levodopa resistance in Parkinson’s disease. NPJ Parkinsons Dis, 2022, vol. 8 (1), pp. 56–61. DOI: 10.1038/s41531‐022‐00321‐y
- Jankovic J., Tan E.K. Parkinson’s disease: Etiopathogenesis and treatment. J. Neurol. Neurosurg. Psychiatr, 2020, vol. 91, pp. 795–808. DOI: 10.1136/jnnp‐2019‐322338
- Titova N.V., Katunina E.A., Tairova R.T. et al. Drug-resistant tremor in Parkinson’s disease and essential tremor. Zhurnal nevrologii i psikhiatrii im. S.S. Korsakova, 2022, no. 122 (10), pp. 24–30 (in Russ.). DOI: 10.17116/jnevro202212210124
- Gupta H.V., Lyons K.E., Wachter N. et al. Long term response to levodopa in Parkinson’s disease. J. Parkinsons Dis, 2019, vol. 9 (3), pp. 525–529. DOI: 10.3233/JPD‐191633
- Caligiuri M.P., Lohr J.B. Worsening of postural tremor in patients with levodopa‐induced dyskinesia: a quantitative analysis. Clin. Neuropharmacol, 1993, vol. 16 (3), pp. 244–250. DOI: 10.1097/00002826‐199306000‐00008
- Frei K., Truong D.D. Medications used to treat tremors. J. Neurol. Sci, 2022, vol. 435, 120194. DOI: 10.1016/j.jns.2022.120194
- Bogdanov R.R. Features of drug therapy of initial manifestations of Parkinson’s disease. Nervnye bolezni, 2013, no. 1, pp. 2–5 (in Russ.).
- Pogarell O., Gasser T., van Hilten J.J. et al. Pramipexole in patients with Parkinson’s disease and marked drug resistant tremor: a randomised, double blind, placebo controlled multicentre study. J. Neurol. Neurosurg. Psychiatry, 2002, vol. 72 (6), pp. 713–720. DOI: 10.1136/jnnp.72.6.713
- Elble R.J. Tremor and dopamine agonists. Neurology, 2002, vol. 58 (1), pp. S57–S62. DOI: 10.1212/WNL.58.suppl_1.S57
- Navan P., Findley L.J., Jeffs J.A. et al. Double‐blind, single‐ dose, cross‐over study of the effects of pramipexole, pergolide, and placebo on rest tremor and UPDRS part III in Parkinson’s disease. Mov. Disord, 2003, vol. 18 (2), pp. 176–180. DOI: 10.1002/mds.10320
- Marras C., Chaudhuri K.R., Titova N. et al. Therapy of Parkinson’s disease subtypes. Neurotherapeutics, 2020, vol. 17, pp. 1366–1377. DOI: 10.1007/s13311‐020‐00894‐7
- Krishna R., Ali M., Moustafa A.A. Effects of combined MAO‐B inhibitors and levodopa vs monotherapy in Parkinson’s disease. Front. Aging Neurosci, 2014, vol. 6, pp. 1–9. DOI: 10.3389/fnagi.2014.00180
- Lew M.F. Rasagiline treatment effects on parkinsonian tremor. Int. J. Neurosci, 2013, vol. 123, pp. 859–865. DOI: 10.3109/00207454.2013.812085
- Stocchi F., Rabey J.M. Effect of rasagiline as adjunct therapy to levodopa on severity of OFF in Parkinson’s disease. Eur. J. Neurol, 2011, vol. 18 (12), pp. 1373–1378. DOI: 10.1111/j.1468‐1331.2011.03512.x
- Parkinson Study Group. Low‐dose clozapine for the treatment of drug‐induced psychosis in Parkinson’s disease. N Engl. J. Med, 1999, vol. 340 (10), pp. 757–763. DOI: 10.1056/NEJM199903113401003
- Yaw T.K., Fox S.H., Lang A.E. Clozapine in parkinsonian rest tremor: a re‐ view of outcomes, adverse reactions, and possible mechanisms of action. Mov. Dis. Clin. Prac, 2016, vol. 3 (6), pp. 116–124. DOI: 10.1002/mdc3.12266
- Trosch R.M., Friedman J.H., Lannon M.C. et al. Clozapine use in Parkinson’s disease: A retrospective analysis of a large multicentered clinical experience. Mov. Dis, 1998, vol. 13, pp. 377–382. DOI: 10.1002/mds.870130302
- Crosby N.J., Deane K., Clarke C.E. Beta‐blocker therapy for tremor in Par‐kinson’s disease. Cochrane Data base of Systematic Reviews, 2003, CD003361. DOI: 10.1002/14651858.CD003361
- Fox S.H. Non‐dopaminergic treatments for motor control in Parkinson’s disease. Drugs, 2013, vol. 7, pp. 1405–1415. DOI: 10.1007/s40265‐013‐0105‐4
- Marjama‐Lyons J., Koller W. Tremor‐predominant Parkinson’s disease. Ap‐proachestotreatment. Drugs Aging, 2000, vol. 16 (4), pp. 273–278. DOI: 10.2165/00002512‐2000160 40‐00003
- Abusrair A.H., Elsekaily W., Bohlega S. Tremor in Parkinson’s disease: from pathophysiology to advanced therapies. Tremor Other Hyperkinet Mov, 2022, vol. 12, p. 29. DOI: 10.5334/tohm.712
- Trosch R.M., Pullman S.L. Botulinum toxin A injections for the treatment of hand tremors. Mov. Dis, 1994, vol. 9 (6), pp. 601–609. Doi: 10.1002/mds.870090604
- Mittal S.O., Pandey S. Botulinum toxin for the treatment of tremor. J. Neurol. Sci, 2022, vol. 435, 120203. DOI: 10.1016/j.jns.2022.120203
- Mittal S.O., Jog M., Lee J. et al. Novel botulinum toxin injection protocols for parkinson tremor and essential tremor — the yale technique and sen‐sor‐based kinematics procedure for safe and effective treatment. Tremor Other Hyperkinet. Mov, 2020, vol. 10, pp. 1–8. DOI: 10.5334/tohm.582
- Niemann N., Jankovic J. Botulinum toxin for the treatment of hand tremor. Toxins (Basel), 2018, vol. 10, pp. 1–10. DOI: 10.3390/toxins10070299
- Samotus O., Lee J., Jog M. Long‐term tremor therapy for Parkinson and es‐sential tremor with sensor‐guided botulinum toxin type A injections. PLoS ONE, 2017, vol. 12, pp. 1–19. DOI: 10.1371/journal.pone.0178670
- Larson P.S. Deep brain stimulation for movement disorders. Neurotherapeutics, 2014, vol. 11 (3), pp. 465–474. DOI: 10.1007/s13311‐014‐0274‐1
- Uc E.Y., Follett K.A. Deep brain stimulation in movement disorders. Semin Neurol, 2007, vol. 27 (2), pp. 170–182. DOI: 10.1055/s‐2007‐971175
- Herrington T.M., Cheng J.J., Eskandar E.N. Mechanisms of deep brain stim‐ulation. J. Neurophysiol, 2016, vol. 115 (12), pp. 19–38. DOI: 10.1152/jn.00281.2015
- Chiken S., Nambu A. Mechanism of deep brain stimulation: inhibition, ex‐ citation, or disruption? Neuroscientist, 2016, vol. 22 (8), pp. 313–322. DOI: 10.1177/1073858415581986
- Walters H., Shah B.B. Focused ultrasound and other lesioning therapies in movement disorders. Curr. Neurol. Neurosci. Rep, 2019, vol. 19, pp. 66–71. DOI: 10.1007/s11910‐019‐0975‐2
- Galimova R.M., Krekotin D.K., Kachemaeva O.V. et al. Terapiya fokusirovannym ul’trazvukom pod kontrolem magnitno‐rezonansnoy navigatsii dvigatel’nykh narusheniiy pri bolezni Parkinsona i essentsial’nom tremore [Focused ultrasound therapy under magnetic resonance navigation control of movement disorders in Parkinson’s disease and essential tremor]. IX Vserossiiyskiiy s»ezd neyrokhirurgov. Sbornik tezisov. Moscow, 2021. Pp. 91–92.
- Ohye C., Higuchi Y., Shibazaki T. et al. Gamma knife thalamotomy for Parkinson disease and essential tremor: a prospective multicenter study. Neurosurg, 2012, vol. 70 (3), pp. 526–536. DOI: 10.1227/NEU.0b013e3182350893
- Chalah M.A., Lefaucheur J.P., Ayache S.S. Non‐invasive central and peripher‐ al stimulation: New hope for essential tremor? Front. Neurosci, 2015, vol. 9, pp. 1–11. doi: 10.3389/fnins.2015.00440
- Meng L., Jin M., Zhu X. et al. Peripherical electrical stimulation for Parkinsonian tremor: a systematic revie. Front. Aging Neurosci, 2022, vol. 14, pp. 1–11. DOI: 10.3389/fnagi.2022.795454