Top

Published in:

22-01-2024 | Parkinson's Disease | Neurology and Preclinical Neurological Studies - Original Article

Association between autonomic dysfunction with motor and non-motor symptoms in patients with Parkinson's disease

Authors: Yi Qin, De-Tao Meng, Zhao-Hui Jin, Wen-Jun Du, Bo-Yan Fang

Published in: Journal of Neural Transmission | Issue 4/2024

Abstract

To investigate the association between autonomic dysfunction (AutD) and motor as well as non-motor symptoms (NMS) in patients with Parkinson's disease (PD). Fifty-three PD patients were divided into two groups based on the number of domains affected by AutD: a multi-domain AutD group (AutD-M) and a single-domain AutD group (AutD-S), as evaluated using the Scale for Outcomes in Parkinson's disease-Autonomic (SCOPA-AUT), which assesses autonomic symptoms, one of the NMS. A comprehensive comparison was conducted between the two groups, including clinical measures such as clinical scales, quantitative evaluations of motor function and exercise capacity. Spearman correlation analysis was employed to investigate the relationship between AutD severity and PD symptoms. Additionally, we performed multiple linear regression model analysis to determine whether associations between SCOPA-AUT scores and clinical assessments remained significant after adjusting for Hoehn and Yahr stage, sex, and age. PD patients in the AutD-M group exhibited significantly more severe NMS and motor symptoms compared to those in the AutD-S group. In correlation analysis, SCOPA-AUT scores showed significant correlations with multiple clinical symptoms, such as most of the NMS, 10-MWT and CPET parameters. Furthermore, regression analysis also revealed that more pronounced fatigue, anxiety, depressive symptoms, worse walking speed and impaired exercise capacity were associated with higher SCOPA-AUT scores. The presence of AutD is correlated with emotional disturbances, decreased exercise endurance, and impaired gait function in patients with PD. Early management of AutD may prove beneficial in alleviating some NMS and motor symptoms in PD.

Available only for authorised users

Arnao V, Cinturino A, Valentino F, Perini V, Mastrilli S, Bellavia G, Savettieri G, Realmuto S, D’Amelio M (2015) In patient’s with Parkinson disease, autonomic symptoms are frequent and associated with other non-motor symptoms. Clin Auton Res 25(5):301–307. https://doi.org/10.1007/s10286-015-0306-xCrossRefPubMed

Asayama K, Schutte R, Li Y, Hansen TW, Staessen JA (2014) Blood pressure variability in risk stratification: what does it add? Clin Exp Pharmacol Physiol 41(1):1–8. https://doi.org/10.1111/1440-1681.12091CrossRefPubMed

Berg A, Bech S, Aasly J, Farrer MJ, Skaalum Petersen M (2022) Autonomic dysfunction in Parkinson’s disease: results from the Faroese Parkinson’s disease cohort. Neurosci Lett 785:136789. https://doi.org/10.1016/j.neulet.2022.136789CrossRefPubMed

Berganzo K, Tijero B, Somme JH, Llorens V, Sánchez-Manso JC, Low D, Iodice V, Vichayanrat E, Mathias CJ, Lezcano E, Zarranz JJ, Gómez-Esteban JC (2012) SCOPA-AUT scale in different parkinsonisms and its correlation with (123) I-MIBG cardiac scintigraphy. Parkinsonism Relat Disord 18(1):45–48. https://doi.org/10.1016/j.parkreldis.2011.08.018CrossRefPubMed

Blesa J, Foffani G, Dehay B, Bezard E, Obeso JA (2022) Motor and non-motor circuit disturbances in early Parkinson disease: which happens first? Nat Rev Neurosci 23(2):115–128. https://doi.org/10.1038/s41583-021-00542-9CrossRefPubMed

Bouça-Machado R, Duarte GS, Patriarca M, Castro Caldas A, Alarcão J, Fernandes RM, Mestre TA, Matias R, Ferreira JJ (2020) Measurement instruments to assess functional mobility in parkinson’s disease: a systematic review. Mov Disord Clin Pract 7(2):129–139. https://doi.org/10.1002/mdc3.12874CrossRefPubMed

Braak H, Braak E (2000) Pathoanatomy of Parkinson’s disease. J Neurol 247(Suppl 2):3–10. https://doi.org/10.1007/pl00007758CrossRef

Braak H, Del Tredici K, Rüb U, de Vos RA, Jansen Steur EN, Braak E (2003) Staging of brain pathology related to sporadic Parkinson’s disease. Neurobiol Aging 24(2):197–211. https://doi.org/10.1016/s0197-4580(02)00065-9CrossRefPubMed

Chaudhuri KR, Martinez-Martin P, Brown RG, Sethi K, Stocchi F, Odin P, Ondo W, Abe K, Macphee G, Macmahon D, Barone P, Rabey M, Forbes A, Breen K, Tluk S, Naidu Y, Olanow W, Williams AJ, Thomas S, Rye D, Tsuboi Y, Hand A, Schapira AH (2007) The metric properties of a novel non-motor symptoms scale for Parkinson’s disease: results from an international pilot study. Mov Disord 22(13):1901–1911. https://doi.org/10.1002/mds.21596CrossRefPubMed

Chou KL, Gilman S, Bohnen NI (2017) Association between autonomic dysfunction and fatigue in Parkinson disease. J Neurol Sci 377:190–192. https://doi.org/10.1016/j.jns.2017.04.023CrossRefPubMedPubMedCentral

Cui J, Qin Y, Tian Y, Ge X, Han H, Yang Z, Yu H (2021) Activities of daily living as a longitudinal moderator of the effect of autonomic dysfunction on anxiety and depression of Parkinson’s patients. Brain Behav 11(8):e2297. https://doi.org/10.1002/brb3.2297CrossRefPubMedPubMedCentral

De Pablo-Fernandez E, Tur C, Revesz T, Lees AJ, Holton JL, Warner TT (2017) Association of autonomic dysfunction with disease progression and survival in Parkinson disease. JAMA Neurol 74(8):970–976. https://doi.org/10.1001/jamaneurol.2017.1125CrossRefPubMedPubMedCentral

De Pablo-Fernández E, Courtney R, Warner TT, Holton JL (2018) A histologic study of the circadian system in Parkinson disease, multiple system atrophy, and progressive supranuclear palsy. JAMA Neurol 75(8):1008–1012. https://doi.org/10.1001/jamaneurol.2018.0640CrossRefPubMedPubMedCentral

Del Tredici K, Braak H (2016) Review: sporadic Parkinson’s disease: development and distribution of α-synuclein pathology. Neuropathol Appl Neurobiol 42(1):33–50. https://doi.org/10.1111/nan.12298CrossRefPubMed

Gallagher DA, Lees AJ, Schrag A (2010) What are the most important nonmotor symptoms in patients with Parkinson’s disease and are we missing them? Mov Disord 25(15):2493–2500. https://doi.org/10.1002/mds.23394CrossRefPubMed

Gibbons CH, Schmidt P, Biaggioni I, Frazier-Mills C, Freeman R, Isaacson S, Karabin B, Kuritzky L, Lew M, Low P, Mehdirad A, Raj SR, Vernino S, Kaufmann H (2017) The recommendations of a consensus panel for the screening, diagnosis, and treatment of neurogenic orthostatic hypotension and associated supine hypertension. J Neurol 264(8):1567–1582. https://doi.org/10.1007/s00415-016-8375-xCrossRefPubMedPubMedCentral

Goetz CG, Tilley BC, Shaftman SR, Stebbins GT, Fahn S, Martinez-Martin P, Poewe W, Sampaio C, Stern MB, Dodel R, Dubois B, Holloway R, Jankovic J, Kulisevsky J, Lang AE, Lees A, Leurgans S, LeWitt PA, Nyenhuis D, Olanow CW, Rascol O, Schrag A, Teresi JA, van Hilten JJ, LaPelle N (2008) Movement Disorder Society-sponsored revision of the Unified Parkinson’s Disease Rating Scale (MDS-UPDRS): scale presentation and clinimetric testing results. Mov Disord 23(15):2129–2170. https://doi.org/10.1002/mds.22340CrossRefPubMed

Guan X, Wang Y, Li Q, Wei M, Chen L, Cheng O (2018) Analysis of the clinical features of early Parkinson’s disease with comparatively integrated intestinal function. Neurol Sci 39(11):1847–1856. https://doi.org/10.1007/s10072-018-3502-3CrossRefPubMed

Gujral S, Aizenstein H, Reynolds CF 3rd, Butters MA, Erickson KI (2017) Exercise effects on depression: possible neural mechanisms. Gen Hosp Psychiatry 49:2–10. https://doi.org/10.1016/j.genhosppsych.2017.04.012CrossRefPubMedPubMedCentral

Hamilton M (1959) The assessment of anxiety states by rating. Br J Med Psychol 32(1):50–55. https://doi.org/10.1111/j.2044-8341.1959.tb00467.xCrossRefPubMed

Hamilton M (1960) A rating scale for depression. J Neurol Neurosurg Psychiatry 23(1):56–62. https://doi.org/10.1136/jnnp.23.1.56CrossRefPubMedPubMedCentral

Jeong EH, Sunwoo MK, Hyung SW, Han SK, Lee JY (2021) Correlation of dopaminergic denervation and the progression of autonomic dysfunctions in different clinical subtypes of Parkinson’s disease. Parkinson’s Dis 2021:2268651. https://doi.org/10.1155/2021/2268651CrossRef

Kanegusuku H, Silva-Batista C, Peçanha T, Nieuwboer A, Silva ND Jr, Costa LA, de Mello MT, Piemonte ME, Ugrinowitsch C, Forjaz CL (2016) Blunted maximal and submaximal responses to cardiopulmonary exercise tests in patients with Parkinson disease. Arch Phys Med Rehabil 97(5):720–725. https://doi.org/10.1016/j.apmr.2015.12.020CrossRefPubMed

Katzman R, Zhang MY, Ouang Ya Q, Wang ZY, Liu WT, Yu E, Wong SC, Salmon DP, Grant I (1988) A Chinese version of the mini-mental state examination; impact of illiteracy in a Shanghai dementia survey. J Clin Epidemiol 41(10):971–978. https://doi.org/10.1016/0895-4356(88)90034-0CrossRefPubMed

Kwon KY, Lee EJ, Lee M, Ju H, Im K (2021a) Impact of motor subtype on non-motor symptoms and fall-related features in patients with early Parkinson’s disease. Geriatr Gerontol Int 21(5):416–420. https://doi.org/10.1111/ggi.14156CrossRefPubMed

Kwon KY, Park S, Lee EJ, Lee M, Ju H (2021b) Association of fall risk factors and non-motor symptoms in patients with early Parkinson’s disease. Sci Rep 11(1):5171. https://doi.org/10.1038/s41598-021-84720-wCrossRefPubMedPubMedCentral

Kwon KY, Park S, Kim RO, Lee EJ, Lee M (2022) Associations of cognitive dysfunction with motor and non-motor symptoms in patients with de novo Parkinson’s disease. Sci Rep 12(1):11461. https://doi.org/10.1038/s41598-022-15630-8CrossRefPubMedPubMedCentral

Lai TT, Gericke B, Feja M, Conoscenti M, Zelikowsky M, Richter F (2023) Anxiety in synucleinopathies: neuronal circuitry, underlying pathomechanisms and current therapeutic strategies. NPJ Parkinson’s Dis 9(1):97. https://doi.org/10.1038/s41531-023-00547-4CrossRef

Lamotte G, Rafferty MR, Prodoehl J, Kohrt WM, Comella CL, Simuni T, Corcos DM (2015) Effects of endurance exercise training on the motor and non-motor features of Parkinson’s disease: a review. J Parkinsons Dis 5(1):21–41. https://doi.org/10.3233/jpd-140425CrossRefPubMed

Lang JT, Kassan TO, Devaney LL, Colon-Semenza C, Joseph MF (2016) Test-retest reliability and minimal detectable change for the 10-meter walk test in older adults with Parkinson’s disease. J Geriatr Phys Therapy 39(4):165–170. https://doi.org/10.1519/jpt.0000000000000068CrossRef

Leclair-Visonneau L, Magy L, Volteau C, Clairembault T, Le Dily S, Préterre C, Peyre A, Damier P, Neunlist M, Péréon Y, Derkinderen P (2018) Heterogeneous pattern of autonomic dysfunction in Parkinson’s disease. J Neurol 265(4):933–941. https://doi.org/10.1007/s00415-018-8789-8CrossRefPubMed

Ledda C, Montanaro E, Imbalzano G, Merola A, Bruno I, Artusi CA, Zibetti M, Rizzone MG, Bozzali M, Sobrero G, Vallelonga F, Maule S, Lopiano L, Romagnolo A (2022) Burden of caregiving for cardiovascular dysautonomia in Parkinson’s disease. Clin Auton Res 32(6):455–461. https://doi.org/10.1007/s10286-022-00888-9CrossRefPubMedPubMedCentral

Lee SM, Lee M, Lee EJ, Kim RO, Kim Y, Kwon KY (2023) Association Between gait and dysautonomia in patients with de novo parkinson’s disease: forward gait versus backward gait. J Mov Disord 16(1):59–67. https://doi.org/10.14802/jmd.22045CrossRefPubMed

Longardner K, Merola A, Litvan I, De Stefano AM, Maule S, Vallelonga F, Lopiano L, Romagnolo A (2022) Differential impact of individual autonomic domains on clinical outcomes in Parkinson’s disease. J Neurol 269(10):5510–5520. https://doi.org/10.1007/s00415-022-11221-9CrossRefPubMedPubMedCentral

Lou JS (2015) Fatigue in Parkinson’s disease and potential interventions. NeuroRehabilitation 37(1):25–34. https://doi.org/10.3233/nre-151238CrossRefPubMed

Malek N, Lawton MA, Grosset KA, Bajaj N, Barker RA, Burn DJ, Foltynie T, Hardy J, Morris HR, Williams NM, Ben-Shlomo Y, Wood NW, Grosset DG (2017) Autonomic dysfunction in early parkinson’s disease: results from the United Kingdom tracking Parkinson’s study. Mov Disord Clin Pract 4(4):509–516. https://doi.org/10.1002/mdc3.12454CrossRefPubMed

Marras C, Chaudhuri KR (2016) Nonmotor features of Parkinson’s disease subtypes. Mov Disord 31(8):1095–1102. https://doi.org/10.1002/mds.26510CrossRefPubMed

Mavrommati F, Collett J, Franssen M, Meaney A, Sexton C, Dennis-West A, Betts JF, Izadi H, Bogdanovic M, Tims M, Farmer A, Dawes H (2017) Exercise response in Parkinson’s disease: insights from a cross-sectional comparison with sedentary controls and a per-protocol analysis of a randomised controlled trial. BMJ Open 7(12):e017194. https://doi.org/10.1136/bmjopen-2017-017194CrossRefPubMedPubMedCentral

Merola A, Romagnolo A, Rosso M, Suri R, Berndt Z, Maule S, Lopiano L, Espay AJ (2018) Autonomic dysfunction in Parkinson’s disease: a prospective cohort study. Mov Disord 33(3):391–397. https://doi.org/10.1002/mds.27268CrossRefPubMed

Müller B, Larsen JP, Wentzel-Larsen T, Skeie GO, Tysnes OB (2011) Autonomic and sensory symptoms and signs in incident, untreated Parkinson’s disease: frequent but mild. Mov Disord 26(1):65–72. https://doi.org/10.1002/mds.23387CrossRefPubMed

Nakamura T, Hirayama M, Yamashita F, Uchida K, Hama T, Watanabe H, Sobue G (2010) Lowered cardiac sympathetic nerve performance in response to exercise in Parkinson’s disease. Mov Disord 25(9):1183–1189. https://doi.org/10.1002/mds.23127CrossRefPubMed

Nakamura T, Hirayama M, Hara T, Hama T, Watanabe H, Sobue G (2011) Does cardiovascular autonomic dysfunction contribute to fatigue in Parkinson’s disease? Mov Disord 26(10):1869–1874. https://doi.org/10.1002/mds.23744CrossRefPubMed

Nasreddine ZS, Phillips NA, Bédirian V, Charbonneau S, Whitehead V, Collin I, Cummings JL, Chertkow H (2005) The Montreal Cognitive Assessment, MoCA: a brief screening tool for mild cognitive impairment. J Am Geriatr Soc 53(4):695–699. https://doi.org/10.1111/j.1532-5415.2005.53221.xCrossRefPubMed

Pagano G, Niccolini F, Yousaf T, Wilson H, Polychronis S, Chaudhuri KR, Politis M (2017) Urinary dysfunction in early de novo patients with Parkinson’s disease. Mov Disord 32(6):939–940. https://doi.org/10.1002/mds.26967CrossRefPubMed

Palma JA, Carmona-Abellan MM, Barriobero N, Trevino-Peinado C, Garcia-Lopez M, Fernandez-Jarne E, Luquin MR (2013) Is cardiac function impaired in premotor Parkinson’s disease? A retrospective cohort study. Mov Disord 28(5):591–596. https://doi.org/10.1002/mds.25431CrossRefPubMed

Park HE, Kim JS, Oh YS, Park IS, Park JW, Song IU, Lee KS (2016) Autonomic nervous system dysfunction in patients with Parkinson disease having depression. J Geriatr Psychiatry Neurol 29(1):11–17. https://doi.org/10.1177/0891988715598234CrossRefPubMed

Podsiadlo D, Richardson S (1991) The timed “Up & Go”: a test of basic functional mobility for frail elderly persons. J Am Geriatr Soc 39(2):142–148. https://doi.org/10.1111/j.1532-5415.1991.tb01616.xCrossRefPubMed

Postuma RB, Gagnon JF, Pelletier A, Montplaisir J (2013) Prodromal autonomic symptoms and signs in Parkinson’s disease and dementia with Lewy bodies. Mov Disord 28(5):597–604. https://doi.org/10.1002/mds.25445CrossRefPubMed

Postuma RB, Berg D, Stern M, Poewe W, Olanow CW, Oertel W, Obeso J, Marek K, Litvan I, Lang AE, Halliday G, Goetz CG, Gasser T, Dubois B, Chan P, Bloem BR, Adler CH, Deuschl G (2015) MDS clinical diagnostic criteria for Parkinson’s disease. Mov Disord 30(12):1591–1601. https://doi.org/10.1002/mds.26424CrossRefPubMed

Qin Y, Jin ZH, Zhang ZY, Chen KK, Yu X, Yan HJ, Wang RD, Su Y, Liu AX, Xi JN, Fang BY (2023) Predictive value of exercise blood pressure changes for orthostatic hypotension in patients with Parkinson’s disease. J Clin Neurol (seoul, Korea) 19(1):67–75. https://doi.org/10.3988/jcn.2023.19.1.67CrossRef

Quarracino C, Otero-Losada M, Capani F, Pérez-Lloret S (2020) State-of-the-art pharmacotherapy for autonomic dysfunction in Parkinson’s disease. Expert Opin Pharmacother 21(4):445–457. https://doi.org/10.1080/14656566.2020.1713097CrossRefPubMed

Ross RM (2003) ATS/ACCP statement on cardiopulmonary exercise testing. Am J Respir Crit Care Medw 167(10):1451. https://doi.org/10.1164/ajrccm.167.10.950CrossRef

Rutten S, Ghielen I, Vriend C, Hoogendoorn AW, Berendse HW, Leentjens AF, van der Werf YD, Smit JH, van den Heuvel OA (2015) Anxiety in Parkinson’s disease: Symptom dimensions and overlap with depression and autonomic failure. Parkinsonism Relat Disord 21(3):189–193. https://doi.org/10.1016/j.parkreldis.2014.11.019CrossRefPubMed

Sabino-Carvalho JL, Fisher JP, Vianna LC (2021) Autonomic function in patients with parkinson’s disease: from rest to exercise. Front Physiol 12:626640. https://doi.org/10.3389/fphys.2021.626640CrossRefPubMedPubMedCentral

Schapira AHV, Chaudhuri KR, Jenner P (2017) Non-motor features of Parkinson disease. Nat Rev Neurosci 18(7):435–450. https://doi.org/10.1038/nrn.2017.62CrossRefPubMed

Sharabi Y, Imrich R, Holmes C, Pechnik S, Goldstein DS (2008) Generalized and neurotransmitter-selective noradrenergic denervation in Parkinson’s disease with orthostatic hypotension. Mov Disorders 23(12):1725–1732. https://doi.org/10.1002/mds.22226CrossRef

Simuni T, Caspell-Garcia C, Coffey CS, Weintraub D, Mollenhauer B, Lasch S, Tanner CM, Jennings D, Kieburtz K, Chahine LM, Marek K (2018) Baseline prevalence and longitudinal evolution of non-motor symptoms in early Parkinson’s disease: the PPMI cohort. J Neurol Neurosurg Psychiatry 89(1):78–88. https://doi.org/10.1136/jnnp-2017-316213CrossRefPubMed

Sklerov M, Shih CH, Browner N, Palma JA, Styner M, Dayan E (2020) Longitudinal change in autonomic symptoms predicts activities of daily living and depression in Parkinson’s disease. Clin Auton Res 30(3):223–230. https://doi.org/10.1007/s10286-020-00672-7CrossRefPubMed

Sklerov M, Browner N, Dayan E, Rubinow D, Frohlich F (2022) Autonomic and depression symptoms in Parkinson’s disease: clinical evidence for overlapping physiology. J Parkinsons Dis 12(3):1059–1067. https://doi.org/10.3233/jpd-213075CrossRefPubMed

Speelman AD, Groothuis JT, van Nimwegen M, van der Scheer ES, Borm GF, Bloem BR, Hopman MT, Munneke M (2012) Cardiovascular responses during a submaximal exercise test in patients with Parkinson’s disease. J Parkinsons Dis 2(3):241–247. https://doi.org/10.3233/jpd-2012-012111CrossRefPubMed

Stanković I, Petrović I, Pekmezović T, Marković V, Stojković T, Dragašević-Mišković N, Svetel M, Kostić V (2019) Longitudinal assessment of autonomic dysfunction in early Parkinson’s disease. Parkinsonism Relat Disord 66:74–79. https://doi.org/10.1016/j.parkreldis.2019.07.008CrossRefPubMed

Starkstein SE, Preziosi TJ, Forrester AW, Robinson RG (1990) Specificity of affective and autonomic symptoms of depression in Parkinson’s disease. J Neurol Neurosurg Psychiatry 53(10):869–873. https://doi.org/10.1136/jnnp.53.10.869CrossRefPubMedPubMedCentral

Stewart CB, Ledingham D, Foster VK, Anderson KN, Sathyanarayana S, Galley D, Pavese N, Pasquini J (2023) The longitudinal progression of autonomic dysfunction in Parkinson’s disease: a 7-year study. Front Neurol 14:1155669. https://doi.org/10.3389/fneur.2023.1155669CrossRefPubMedPubMedCentral

Stubendorff K, Aarsland D, Minthon L, Londos E (2012) The impact of autonomic dysfunction on survival in patients with dementia with Lewy bodies and Parkinson’s disease with dementia. PLoS ONE 7(10):e45451. https://doi.org/10.1371/journal.pone.0045451CrossRefPubMedPubMedCentral

Sun XG, Hansen JE, Beshai JF, Wasserman K (2010) Oscillatory breathing and exercise gas exchange abnormalities prognosticate early mortality and morbidity in heart failure. J Am Coll Cardiol 55(17):1814–1823. https://doi.org/10.1016/j.jacc.2009.10.075CrossRefPubMed

Tomlinson CL, Stowe R, Patel S, Rick C, Gray R, Clarke CE (2010) Systematic review of levodopa dose equivalency reporting in Parkinson’s disease. Mov Disord 25(15):2649–2653. https://doi.org/10.1002/mds.23429CrossRefPubMed

Tosserams A, Keijsers N, Kapelle W, Kessels RPC, Weerdesteyn V, Bloem BR, Nonnekes J (2022) Evaluation of compensation strategies for gait impairment in patients with Parkinson disease. Neurology 99(20):e2253-2263. https://doi.org/10.1212/wnl.0000000000201159CrossRefPubMedPubMedCentral

Verbaan D, Marinus J, Visser M, van Rooden SM, Stiggelbout AM, van Hilten JJ (2007) Patient-reported autonomic symptoms in Parkinson disease. Neurology 69(4):333–341. https://doi.org/10.1212/01.wnl.0000266593.50534.e8CrossRefPubMed

Visser M, Marinus J, Stiggelbout AM, Van Hilten JJ (2004) Assessment of autonomic dysfunction in Parkinson’s disease: the SCOPA-AUT. Mov Disord 19(11):1306–1312. https://doi.org/10.1002/mds.20153CrossRefPubMed

Wakabayashi K, Takahashi H (1997) Neuropathology of autonomic nervous system in Parkinson’s disease. Eur Neurol 38(Suppl 2):2–7. https://doi.org/10.1159/000113469CrossRefPubMed

Werner WG, DiFrancisco-Donoghue J, Lamberg EM (2006) Cardiovascular response to treadmill testing in Parkinson disease. J Neurol Phys Therapy 30(2):68–73. https://doi.org/10.1097/01.npt.0000282570.78544.00CrossRef

Zhang F, Wang F, Li CH, Wang JW, Han CL, Fan SY, Gao DM, Xing YJ, Yang C, Zhang JG, Meng FG (2022) Subthalamic nucleus-deep brain stimulation improves autonomic dysfunctions in Parkinson’s disease. BMC Neurol 22(1):124. https://doi.org/10.1186/s12883-022-02651-zCrossRefPubMedPubMedCentral

Zhou Z, Zhou X, Zhou X, Xiang Y, Zhu L, Qin L, Wang Y, Pan H, Zhao Y, Sun Q, Xu Q, Wu X, Yan X, Guo J, Tang B, Liu Z (2021) Characteristics of autonomic dysfunction in Parkinson’s disease: a large Chinese multicenter cohort study. Front Aging Neurosci 13:761044. https://doi.org/10.3389/fnagi.2021.761044CrossRefPubMedPubMedCentral

Zhou C, Wang L, Cheng W, Lv J, Guan X, Guo T, Wu J, Zhang W, Gao T, Liu X, Bai X, Wu H, Cao Z, Gu L, Chen J, Wen J, Huang P, Xu X, Zhang B, Feng J, Zhang M (2023a) Two distinct trajectories of clinical and neurodegeneration events in Parkinson’s disease. NPJ Parkinson’s Dis 9(1):111. https://doi.org/10.1038/s41531-023-00556-3CrossRef

Zhou X, Xiang Y, Song T, Zhao Y, Pan H, Xu Q, Chen Y, Sun Q, Wu X, Yan X, Guo J, Tang B, Lei L, Liu Z (2023b) Characteristics of fatigue in Parkinson’s disease: a longitudinal cohort study. Front Aging Neurosci 15:1133705. https://doi.org/10.3389/fnagi.2023.1133705CrossRefPubMedPubMedCentral

Title: Association between autonomic dysfunction with motor and non-motor symptoms in patients with Parkinson's disease
Authors: Yi Qin
De-Tao Meng
Zhao-Hui Jin
Wen-Jun Du
Bo-Yan Fang
Publication date: 22-01-2024
Publisher: Springer Vienna
Keywords: Parkinson's Disease
Fatigue
Published in: Journal of Neural Transmission / Issue 4/2024
Print ISSN: 0300-9564
Electronic ISSN: 1435-1463
DOI: https://doi.org/10.1007/s00702-024-02745-7

At a glance: The STEP trials

Springer Medicine

Association between autonomic dysfunction with motor and non-motor symptoms in patients with Parkinson's disease

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 4/2024

Validation of the Italian version of the Parkinson’s Disease- Cognitive Functional Rating Scale

High-dose glucocorticoids in COVID-19 patients with acute encephalopathy: clinical and imaging findings in a retrospective cohort study

Combined light and electron microscopy (CLEM) to quantify methamphetamine-induced alpha-synuclein-related pathology

More than fear? Brain activation patterns of dental phobic patients before and after an exposure-based treatment

Mild cognitive impairment in Huntington’s disease: challenges and outlooks

The relationship between serum prolactin levels and cognitive function in drug-naïve schizophrenia patients: a cross-sectional study