Brainstem ventilatory dysfunction: A plausible mechanism for dyspnea in Parkinson's Disease?

Parkinson's disease brainstem ventilatory dysfunction control of ventilation dyspnea non-motor symptom

Journal

Movement disorders : official journal of the Movement Disorder Society
ISSN: 1531-8257
Titre abrégé: Mov Disord
Pays: United States
ID NLM: 8610688

Informations de publication

Date de publication:
03 2020
Historique:
received: 10 07 2019
revised: 06 11 2019
accepted: 07 11 2019
pubmed: 17 1 2020
medline: 28 4 2021
entrez: 17 1 2020
Statut: ppublish

Résumé

Dyspnea is an under-recognized and debilitating symptom that is reported in up to 40% of patients with Parkinson's disease and may have multiple origins. Despite its frequency, it is poorly researched, and there is a general lack of understanding of the pathophysiology of dyspnea and respiratory dysfunction in PD. Consequently, a number of PD patients are labelled as having "unexplained dyspnea." Studies to date have focused mainly on evaluating ventilatory capacity and lung volumes, and little is known about the effects of the disease on the medullary and pontine ventilatory control centers within the brainstem. This is of particular relevance in view of neuropathological studies demonstrating early involvement of the dorsal medulla and other brainstem structures by the disease process. The possibility that impaired brainstem ventilatory control is a contributory mechanism for dyspnea and could be a premotor manifestation in some PD patients therefore warrants further attention. This review focuses on clinical, pathological, and experimental evidence for the involvement of brainstem respiratory centers in PD. We highlight the need for further research, particularly in PD patients with unexplained dyspnea. © 2020 International Parkinson and Movement Disorder Society.

Identifiants

pubmed: 31944403
doi: 10.1002/mds.27932
doi:

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

379-388

Informations de copyright

© 2020 International Parkinson and Movement Disorder Society.

Références

American Thoracic Society. Dyspnea mechanisms, assessment, and management: a consensus statement. Am J Respir Crit Care Med 1999;159:321-340.
Braak H, Del Tredici K, Rüb U, et al. Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging 2003;24:197-211.
Adler CH, Beach TG. Neuropathological basis of non-motor manifestations of Parkinson's disease. Mov Disord 2016;31(8):1114-1119.
Weiner P, Inzelberg R, Davidovich A, et al. Respiratory muscle performance and the perception of dyspnea in Parkinson's disease. Can J Neurol Sci 2002;29(1):68-72.
Gibbons CH, Freeman R. Orthostatic dyspnea: a neglected symptom of orthostatic hypotension. Clin Auton Res 2005;15(1):40-44.
Palma JA, Kaufmann H. Epidemiology, diagnosis, and management of neurogenic orthostatic hypotension. Mov Disord Clin Pract 2017;4(3):298-308.
Chaudhuri KR. Handbook of Non-motor Symptoms in Parkinson's Disease. Dordrecht: Springer; 2012.
Todorova A, Jenner P, Chaudhuri KR. Non-motor Parkinson's: integral to motor Parkinson's, yet often neglected. Pract Neurol 2014;14(5):310-322.
Chaudhuri KR, Martinez- Martin P, Schapira AHV, et al. International multicenter pilot study of the first comprehensive self-completed nonmotor symptoms questionnaire for Parkinson's disease: the NMSQuest study. Mov Disord 2006;21(7):916-923.
Chaudhuri KR, Preito-Jurcynska C, Naidu Y, et al. The nondeclaration of nonmotor symptoms of Parkinson's disease to health care professionals: an international study using the nonmotor symptoms questionnaire. Mov Disord 2010;25(6):704-709.
Baille G, Chenivesse C, Perez T, et al. Dyspnea: an underestimated symptom in Parkinson's disease. Parkinsonism Relat Disord 2019;60:162-166.
Antonini A, Barone P, Marconi R, et al. The progression of non-motor symptoms in Parkinson's disease and their contribution to motor disability and quality of life. J Neurol 2012;259(12):2621-2631.
Barone P, Antonini A, Colosimo C, et al. The PRIAMO study: a multicenter assessment of nonmotor symptoms and their impact on quality of life in Parkinson's disease. Mov Disord 2009;24(11):1641-1649.
Witjas PT, Kaphan PE, Azulay PJ, et al. Nonmotor fluctuations in Parkinson's disease: frequent and disabling. Neurology 2002;59(3):408-413.
Lee MA, Prentice WM, Hildreth AJ, et al. Measuring symptom load in idiopathic Parkinson's disease. Parkinsonism Relat Disord 2007;13(5):284-289.
Moreau C, Devos D, Baille G, et al. Are upper-body axial symptoms a feature of early Parkinson's disease? PLoS One 2016;11(9):e0162904.
Baille G, Perez T, Devos D, et al. Early occurrence of inspiratory muscle weakness in Parkinson's disease. PLoS One 2018;13(1):1-10.
Storch A, Schneider CB, Wolz M, et al. Nonmotor fluctuations in Parkinson disease. Severity and correlation with motor complications. Neurology 2013;26;80(9):800-809.
Baille G, De Jesus AM, Perez T, et al. Ventilatory dysfunction in Parkinson's disease. J Parkinsons Dis 2016;6(3):463-471.
da Silva-Júnior FP, do Prado GF, Barbosa ER, et al. Sleep disordered breathing in Parkinson's disease: a critical appraisal. Sleep Med Rev 2014;18(2):173-178.
Valko PO, Hauser S, Sommerauer M, et al. Observations on sleep-disordered breathing in idiopathic Parkinson's disease. PLoS One 2015;9(6):e100828.
De Pandis MF, Starace A, Stefanelli F, et al. Modification of respiratory funciton parameters in patients with severe Parkinson's disease. Neurol Sci 2002;23:69-70.
Herer B, Arnulf I, Housset B. Effects of levodopa on pulmonary function in Parkinson's disease. Chest 2001;119:387-393.
Polatli M, Akyol A, Çildag O, et al. Pulmonary function tests in Parkinson's disease. European Journal of Neurology. 2001;8:341-345.
Owolabi LF, Nagoda M, Babashani M. Pulmonary function tests in patients with Parkinson's disease: a case-control study. Niger J Clin Pract 2016;19(1):66-70.
Pal PK, Sathyaprabha TN, Tuhina P, et al. Pattern of subclinical pulmonary dysfunctions in Parkinson's disease and the effect of levodopa. Mov Disord 2007;22(3):420-424.
Sabaté M, González I, Ruperez F, et al. Obstructive and restrictive pulmonary dysfunctions in Parkinsons disease. J Neurol Sci. 1995;138:114-119.
Seccombe LM, Giddings HL, Rogers PG, et al. Abnormal ventilatory control in Parkinson's disease-further evidence for non-motor dysfunction. Respir Physiol Neurobiol 2011;179(2-3):300-304.
Tambasco N, Murgia N, Nigro P, et al. Levodopa-responsive breathing discomfort in Parkinson's disease patients. J Neural Transm. 2018;125(7):1033-1036.
Wang CM, Shieh WY, Weng YH, et al. Non-invasive assessment determine the swallowing and respiration dysfunction in early Parkinson's disease. Parkinsonism Relat Disord 2017;42:22-27.
Shaheen HA, Ali MA, Abd Elzaher MA, et al. Parkinson's disease and pulmonary dysfunction. Egypt J Neurol Psychiat Neurosurg 2009;46(1):129-140.
Mikaelee H, Yazdchi M, Ansarin K, et al. Pulmonary function test abnormalities in Parkinson disease. Internet J Pulm Med 2007;8(2):1.
Sathyaprabha TN, Kapavarapu PK, Pal PK, et al. Pulmonary functions in Parkinson's disease. Indian J Chest Dis Allied Sci 2005;47:251-257.
Cardoso SRX, Pereira JS. Análise da Função Respiratória na Doença de Parkinson. [Analysis of breathing function in Parkinson's disease]. Arq Neuropsiquiatr 2002;60(1):91-95.
Canning CH, Alison JA, Allen NE, et al. Parkinson's disease: an investigation of exercise capacity, respiratory function, and gait. Arch Phys Med Rehabil 1997;78:199-207.
Izquierdo-Alonso JL, Jiménez-Jiménez FJ, Cabrera-Valdivia F, et al. Airway dysfunction in patients with Parkinson's disease. Lung 1994;172(1):47-55.
Hovestadt A, Bogaard JM, Meerwaldt JD, et al. Pulmonary function in Parkinson's disease. J Neurol Neurosurg Psychiatry 1989;52:329-333.
Torsney KM, Forsyth D. Respiratory dysfunction in Parkinson's disease. J R Coll Physicians Edinb 2017;47(1):35-39.
Kanani M, Elliot M. Control of Ventilation. Cambridge: Cambridge University Press; 2004:50-54.
Kirkman E. Respiration: control of ventilation. Anaesthes Intensive Care Med 2011;12(10):446-449.
Mulkey DK, Wenker IC, Kréneisz O. Current ideas on central chemoreception by neurons and glial cells in the retrotrapezoid nucleus. J Appl Physiol 2010;108(5):1433-1439.
Moreira TS, Takakura AC, Damasceno RS, et al. Central chemoreceptors and neural mechanisms of cardiorespiratory control. Braz J Med Biol Res 2011;44(9):883-889.
Talbot NP, Smith TG, Dorrington KL. The mechanics and control of ventilation. Surgery (Oxford) 2011;29(5):212-216.
Pilowsky PM, Lung MSY, Spirovski D, et al. Differential regulation of the central neural cardiorespiratory system by metabotropic neurotransmitters. Philos Trans R Soc Lond B Biol Sci 2009;364(1529):2537-2552.
Buchanan GF, Richerson GB. Role of chemoreceptors in mediating dyspnea. Respir Physiol Neurobiol 2009;167(1):9-19.
Monteiro TC, Batuca JR, Obeso A, et al. Carotid body function in aged rats: responses to hypoxia, ischemia, dopamine, and adenosine. Age (Dordr) 2011;33(3):337-350.
Spyer KM, Gourine AV. Chemosensory pathways in the brainstem controlling cardiorespiratory activity. Philos Trans R Soc Lond B Biol Sci 2009;364(1529):2603-2610.
Burki NK, Lee LY. Mechanisms of dyspnea. Chest 2010;138(5):1196-1201.
Lunberg D, Mueller RA, Breese GR. Effects of vagotomy and glossopharyngectomy on respiratory response to dopamine-agonists. Acta Physiol Scand 1982;114:81-89.
Fisher JP, Flück D, Hilty MP, et al. Carotid chemoreceptor control of muscle sympathetic nerve activity in hypobaric hypoxia. Exp Physiol 2018;103(1):77-89.
Bairam A, Carroll JL. Neurotransmitters in carotid body development. Respir Physiol Neurobiol 2005;149:217-232.
Ward DS, Bellville JW. Reduction of hypoxic ventilatory drive by dopamine. Anesth Analg 1982;61:333-337.
Ciarka A, Vincent JL, van de Borne P. The effects of dopamine on the respiratory system: friend or foe? Pulm Pharmacol Ther 2007;20(6):607-615.
Bainbridge CW, Heistad DD. Effect of haloperidol on ventilatory responses to dopamine in man. J Pharmacol Exp Ther 1980;213:13-17.
Andrzejewski K, Budzińska K, Zaremba M, et al. Hypoxic ventilatory response after dopamine D2 receptor blockade in unilateral rat model of Parkinson's disease. Neuroscience 2016;316:192-200.
Read DJ. A clinical method for assessing the ventilatory response to carbon dioxide. Australas Ann Med 1967;16(1):20-32.
Hensley MJ, Read DJ. A test of the ventilatory response to hypoxia and hypercapnia for clinical use. Aust N Z J Med 1977;7(4):362-367.
Holle RH, Schoene RB, Pavlin EJ. Effect of respiratory muscle weakness on P0.1 induced by partial curarization. J Appl Physiol Respir Environ Exerc Physiol 1984;57(4):1150-1157.
Kuhlen R, Hausmann S, Pappert D, et al. A new method for P0.1 measurement using standard respiratory equipment. Intensive Care Med 1995;21(7):554-560.
Serebrovskaya T, Karaban I, Mankovskaya I, et al. Impaired chemosensitivity and perception of dyspnoea in Parkinson's disease. Respiration 1998;65:28-33.
Serebrovskaya T KI, Mankovskaya I, Bernardi L, et al. Hypoxic ventilatory responses and gas exchange in patients with Parkinson's disease. Respiration 1998;65:28-33.
Mizukami K, Homma T, Aonuma K, et al. Decreased ventilatory response to hypercapnia in dementia with Lewy bodies. Ann Neurol 2009;65(5):614-617.
Zhang W, Zhang L, Zhou N, et al. Dysregulation of respiratory center drive (P0.1) and muscle strength in patients with early stage idiopathic Parkinson's disease. Front Neurol 2019;10:724.
Monteiro L, Souza-Machado A, Valderramas S, et al. The effect of levodopa on pulmonary function in Parkinson's disease: a systematic review and meta-analysis. Clin Ther 2012;34(5):1049-1055.
Hampson NB, Kieburtz KD, LeWitt PA, et al. Prospective evaluation of pulmonary function in Parkinson's disease patients with motor fluctuations. Int J Neurosci 2017;127(3):276-284.
Rice JE, Antic R, Thompson PD. Disordered respiration as a levodopa-induced dyskinesia in Parkinson's disease. Mov Disord 2002;17(3):524-527.
Vercueil L, Linard JP, Wuyam B, et al. Breathing pattern in patients with Parkinson's disease. Respir Physiol 1999;118:163-172.
Dafsari HS, Reddy P, Herchenbach C, et al. Beneficial effects of bilateral subthalamic stimulation on non-motor symptoms in Parkinson's disease. Brain Stimul 2016;9(1):78-85.
Kurtis MM, Rajah T, Delgado LF, et al. The effect of deep brain stimulation on the non-motor symptoms of Parkinson's disease: a critical review of the current evidence. NPJ Parkinsons Dis 2017;2: 16024.
Chalif JI, Sitsapesan HA, Pattinson KTS, et al. Dyspnea as a side effect of subthalamic nucleus deep brain stimulation for Parkinson's disease. Respir Physiol Neurobiol 2014;192:128-133.
Tuppy M, Barna BF, Alves-Dos-Santos L, et al. Respiratory deficits in a rat model of Parkinson's disease. Neuroscience 2015;297:194-204.
Oliveira LM, Oliveira MA, Moriya HT, et al. Respiratory disturbances in a mouse model of Parkinson's disease. Exp Physiol 2019;1-11.
Benarroch EE, Schmeichel AM, Low PA, et al. Depletion of ventromedullary NK-1 receptor-immunoreactive neurons in multiple system atrophy. Brain 2003;126:2183-2190.
Andrzejewski K, Budzińska K, Kaczyńska K. Phrenic and hypoglossal nerve activity during respiratory response to hypoxia in 6-OHDA unilateral model of Parkinson's disease. Life Sci 2017;180:143-150.
Lima JC, Oliveira LM, Botelho MT, et al. The involvement of the pathway connecting the substantia nigra, the periaqueductal gray matter and the retrotrapezoid nucleus in breathing control in a rat model of Parkinson's disease. Exp Neurol 2018;302:46-56.
Dickson DW. Neuropathology of Parkinson disease. Parkinsonism Relat Disord 2018;46(s1):S30-S33.
Dexter DT, Jenner P. Parkinson disease: from pathology to molecular disease mechanisms. Free Radic Biol Med 2013;62:132-144.
Halliday GM, Blumbergs PC, Cotton RGH, et al. Loss of brainstem serotonin and substance P containing neurons in Parkinson's disease. Brain Res 1990;10:104-107.
Halliday GM, Li YW, Blumbergs PC, et al. Neuropathology of immunohistochemically identified brainstem neurons in Parkinson's disease. Ann Neurol 1990;27:373-385.
Chaudhuri KR, Schapira AHV. Non-motor symptoms of Parkinson's disease: dopaminergic pathophysiology and treatment. Lancet Neurol 2009;8:464-474.
Flabeau O, Meissner WG, Ozier A, et al. Breathing variability and brainstem serotonergic loss in a genetic model of multiple system atrophy. Mov Disord 2014;29(3):388-395.
Park A, Stacey M. Non-motor symptoms in Parkinson's disease. J Neurol 2009;256(Suppl 3):293-298.
Greene JG. Causes and consequences of degeneration of the dorsal motor nucleus of the vagus nerve in Parkinson's disease. Antioxid Redox Signal 2014;21(4):649-667.
Purdy A HA, Barnett HJ, Bratty P, et al. Familial fatal parkinsonism with alveolar hypoventilation and mental depression. Ann Neurol 1979;6:523-531.
Tsuboi Y, Dickson DW, Nabeshima K, et al. Neurodegeneration involving putative respiratory neurons in Perry syndrome. Acta Neuropathol 2008;115(2):263-268.
Benarroch EE. Brainstem respiratory control: substrates of respiratory failure of multiple system atrophy. Mov Disord 2007;22(2):155-161.
Presti MF, Schmeichel AM, Low PA, et al. Degeneration of brainstem respiratory neurons in dementia with Lewy bodies. Sleep 2014;37(2):373-378.
Schwarzacher SW, Rüb U, Deller T. Neuroanatomical characteristics of the human pre-Bötzinger complex and its involvement in neurodegenerative brainstem diseases. Brain 2011;134(Pt 1):24-35.
Perez-Lloret S, Flabeau O, Fernagut PO, et al. Current concepts in the treatment of multiple system atrophy. Mov Disord Clin Pract 2015;2(1):6-16.
Glass GA, Josephs KA, Ahlskog JE. Respiratory insufficiency as the primary presenting symptom of multiple-system atrophy. Arch Neurol 2006;63(7):978-981.
Tsuda T, Onodera H, Okabe S, et al. Impaired chemosensitivity to hypoxia is a marker of multiple system atrophy. Ann Neurol 2002;52(3):367-371.
Lipp A, Schmelzer JD, Low PA, et al. Ventilatory and cardiovascular responses to hypoxia and hypercapnia in multiple system atrophy. Arch Neurol 2010;67(2):211-216.
Postuma RB. Prodromal Parkinson's disease - using REM sleep behavior disorder as a window. Parkinsonism Relat Disord 2014;20:S1-S4.
Postuma RB, Adler CH, Dugger BN, et al. REM sleep behavior disorder and neuropathology in Parkinson's disease. Mov Disord 2015;30(10):1413-1417.
Bayulkem K, Lopez G. Clinical approach to nonmotor sensory fluctuations in Parkinson's disease. J Neurol Sci 2011;310:82-85.
Bayulkem K, Lopez G. Nonmotor fluctuations in Parkinson's disease: clinical spectrum and classification. J Neurol Sci 2010;289:89-92.
Hegland KW, Troche M, Brandimore A. Relationship between respiratory sensory perception, speech, and swallow in Parkinson's disease. Mov Disord Clin Pract 2019;6(3):243-249.

Auteurs

Srimathy Vijayan (S)

Perron Institute for Neurological and Translational Sciences, Nedlands, Perth, Western Australia, Australia.

Bhajan Singh (B)

West Australian Sleep Disorders Research Institute, Sir Charles Gairdner Hospital, Nedlands, Perth, Western Australia, Australia.
School of Human Sciences, University of Western Australia, Crawley, Western Australia, Australia.

Soumya Ghosh (S)

Perron Institute for Neurological and Translational Sciences, Nedlands, Perth, Western Australia, Australia.

Rick Stell (R)

Perron Institute for Neurological and Translational Sciences, Nedlands, Perth, Western Australia, Australia.

Frank L Mastaglia (FL)

Perron Institute for Neurological and Translational Sciences, Nedlands, Perth, Western Australia, Australia.

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