DOI QR코드

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Autonomic dysfunction in multiple sclerosis and neuromyelitis optica spectrum disorder

  • Soonwook Kwon (Department of Neurology, Inha University Hospital) ;
  • Ju-Hong Min (Department of Neurology, Samsung Medical Center, Sungkyunkwan University School of Medicine)
  • 투고 : 2022.12.12
  • 심사 : 2023.03.20
  • 발행 : 2023.04.30

초록

Autonomic dysfunction occurs frequently in multiple sclerosis (MS) and neuromyelitis optica spectrum disorder (NMOSD). Patients with either condition may present with autonomic symptoms such as bladder, sexual, cardiovascular, thermoregulatory, and gastrointestinal dysfunction, and fatigue, but autonomic symptoms that affect quality of life are underrecognized in clinical practice. The immunopathogenesis of MS has been considered to be associated with autonomic dysfunction. Applying appropriate treatment strategies for autonomic dysfunction is important to improve the quality of life of patients. Here we review autonomic dysfunction and how this is managed in patients with MS and NMOSD.

키워드

과제정보

This work was supported by an NRF grant funded by the Korea government (no. NRF-2021R1F1A1049347) and by a grant from SMC Research and Development (no. SMO1220511).

참고문헌

  1. Krbot Skoric M, Crnosija L, Gabelic T, Barun B, Adamec I, Junakovic A, et al. Autonomic symptom burden can predict disease activity in early multiple sclerosis. Mult Scler Relat Disord 2019;28:250-255. https://doi.org/10.1016/j.msard.2019.01.005
  2. Habek M, Crnosija L, Lovric M, Junakovic A, Krbot Skoric M, Adamec I. Sympathetic cardiovascular and sudomotor functions are frequently affected in early multiple sclerosis. Clin Auton Res 2016;26:385-393. https://doi.org/10.1007/s10286-016-0370-x
  3. Cortez MM, Nagi Reddy SK, Goodman B, Carter JL, Wingerchuk DM. Autonomic symptom burden is associated with MS-related fatigue and quality of life. Mult Scler Relat Disord 2015;4:258-263. https://doi.org/10.1016/j.msard.2015.03.007
  4. Mutch K, Zhao S, Hamid S, Methley A, Elsone L, Singh G, et al. Bladder and bowel dysfunction affect quality of life. A cross sectional study of 60 patients with aquaporin-4 antibody positive neuromyelitis optica spectrum disorder. Mult Scler Relat Disord 2015;4:614-618. https://doi.org/10.1016/j.msard.2015.07.015
  5. Habek M. Immune and autonomic nervous system interactions in multiple sclerosis: clinical implications. Clin Auton Res 2019;29:267-275. https://doi.org/10.1007/s10286-019-00605-z
  6. Saari A, Tolonen U, Paakko E, Suominen K, Pyhtinen J, Sotaniemi K, et al. Cardiovascular autonomic dysfunction correlates with brain MRI lesion load in MS. Clin Neurophysiol 2004;115:1473-1478. https://doi.org/10.1016/j.clinph.2004.01.012
  7. de Seze J, Stojkovic T, Gauvrit JY, Devos D, Ayachi M, Cassim F, et al. Autonomic dysfunction in multiple sclerosis: cervical spinal cord atrophy correlates. J Neurol 2001;248:297-303. https://doi.org/10.1007/s004150170204
  8. Hsu CL, Yeh JH, Lau CI. Persistent hyperthermia in a patient with aquaporin-4-antibody-positive neuromyelitis optica spectrum disorder. J Clin Neurol 2016;12:515-516. https://doi.org/10.3988/jcn.2016.12.4.515
  9. Poppe AY, Lapierre Y, Melancon D, Lowden D, Wardell L, Fullerton LM, et al. Neuromyelitis optica with hypothalamic involvement. Mult Scler 2005;11:617-621. https://doi.org/10.1191/1352458505ms1200cr
  10. Racosta JM, Kimpinski K, Morrow SA, Kremenchutzky M. Autonomic dysfunction in multiple sclerosis. Auton Neurosci 2015;193:1-6. https://doi.org/10.1016/j.autneu.2015.06.001
  11. Cosentino M, Zaffaroni M, Marino F, Bombelli R, Ferrari M, Rasini E, et al. Catecholamine production and tyrosine hydroxylase expression in peripheral blood mononuclear cells from multiple sclerosis patients: effect of cell stimulation and possible relevance for activation-induced apoptosis. J Neuroimmunol 2002;133:233-240. https://doi.org/10.1016/S0165-5728(02)00372-7
  12. Flachenecker P, Reiners K, Krauser M, Wolf A, Toyka KV. Autonomic dysfunction in multiple sclerosis is related to disease activity and progression of disability. Mult Scler 2001;7:327-334. https://doi.org/10.1177/135245850100700509
  13. Kodounis A, Stamboulis E, Constantinidis TS, Liolios A. Measurement of autonomic dysregulation in multiple sclerosis. Acta Neurol Scand 2005;112:403-408. https://doi.org/10.1111/j.1600-0404.2005.00446.x
  14. Habek M, Krbot Skoric M, Crnosija L, Gabelic T, Barun B, Adamec I. Postural orthostatic tachycardia predicts early conversion to multiple sclerosis after clinically isolated syndrome. Eur Neurol 2017;77:253-257. https://doi.org/10.1159/000469707
  15. Lensch E, Jost WH. Autonomic disorders in multiple sclerosis. Autoimmune Dis 2011;2011:803841.
  16. Nakipoglu GF, Kaya AZ, Orhan G, Tezen O, Tunc H, Ozgirgin N, et al. Urinary dysfunction in multiple sclerosis. J Clin Neurosci 2009;16:1321-1324. https://doi.org/10.1016/j.jocn.2008.12.012
  17. Castel-Lacanal E, Game X, Clanet M, Gasq D, De Boissezon X, Guillotreau J, et al. Urinary complications and risk factors in symptomatic multiple sclerosis patients. Study of a cohort of 328 patients. Neurourol Urodyn 2015;34:32-36. https://doi.org/10.1002/nau.22495
  18. Sternberg Z. Sympathetic nervous system dysfunction in multiple sclerosis, linking neurodegeneration to a reduced response to therapy. Curr Pharm Des 2012;18:1635-1644. https://doi.org/10.2174/138161212799958639
  19. Kim YH, Goodman C, Omessi E, Rivera V, Kattan MW, Boone TB. The correlation of urodynamic findings with cranial magnetic resonance imaging findings in multiple sclerosis. J Urol 1998;159:972-976. https://doi.org/10.1016/S0022-5347(01)63791-1
  20. Kragt JJ, Hoogervorst EL, Uitdehaag BM, Polman CH. Relation between objective and subjective measures of bladder dysfunction in multiple sclerosis. Neurology 2004;63:1716-1718. https://doi.org/10.1212/01.WNL.0000143062.43325.C8
  21. Sirbu CA, Mezei RM, Falup-Pecurariu C, Bratu OG, Sirbu AM, Ghinescu MC, et al. Autonomic dysfunctions in multiple sclerosis: challenges of clinical practice (review). Exp Ther Med 2020;20:196.
  22. Hornby A. The MS sufferer in the community. Nurs Times 1978;74:suppl 130-131.
  23. Preziosi G, Raptis DA, Raeburn A, Thiruppathy K, Panicker J, Emmanuel A. Gut dysfunction in patients with multiple sclerosis and the role of spinal cord involvement in the disease. Eur J Gastroenterol Hepatol 2013;25:1044-1050. https://doi.org/10.1097/MEG.0b013e328361eaf8
  24. el-Maghraby TA, Shalaby NM, Al-Tawdy MH, Salem SS. Gastric motility dysfunction in patients with multiple sclerosis assessed by gastric emptying scintigraphy. Can J Gastroenterol 2005;19:141-145. https://doi.org/10.1155/2005/103615
  25. Tepavcevic DK, Kostic J, Basuroski ID, Stojsavljevic N, Pekmezovic T, Drulovic J. The impact of sexual dysfunction on the quality of life measured by MSQoL-54 in patients with multiple sclerosis. Mult Scler 2008;14:1131-1136. https://doi.org/10.1177/1352458508093619
  26. Kessler TM, Fowler CJ, Panicker JN. Sexual dysfunction in multiple sclerosis. Expert Rev Neurother 2009;9:341-350. https://doi.org/10.1586/14737175.9.3.341
  27. Demirkiran M, Sarica Y, Uguz S, Yerdelen D, Aslan K. Multiple sclerosis patients with and without sexual dysfunction: are there any differences? Mult Scler 2006;12:209-214.  https://doi.org/10.1191/135248506ms1253oa
  28. Guo ZN, He SY, Zhang HL, Wu J, Yang Y. Multiple sclerosis and sexual dysfunction. Asian J Androl 2012;14:530-535. https://doi.org/10.1038/aja.2011.110
  29. DasGupta R, Fowler CJ. Bladder, bowel and sexual dysfunction in multiple sclerosis: management strategies. Drugs 2003;63:153-166. https://doi.org/10.2165/00003495-200363020-00003
  30. Davis SL, Wilson TE, White AT, Frohman EM. Thermoregulation in multiple sclerosis. J Appl Physiol (1985) 2010;109:1531-1537. https://doi.org/10.1152/japplphysiol.00460.2010
  31. White KD, Scoones DJ, Newman PK. Hypothermia in multiple sclerosis. J Neurol Neurosurg Psychiatry 1996;61:369-375. https://doi.org/10.1136/jnnp.61.4.369
  32. Uhthoff W. Untersuchungen uber die bei der multiplen Herdsklerose vorkommenden Angenstorungen. Archiv fur Psychiatrie und Nervenkrankheiten 1890;21:55-116. https://doi.org/10.1007/BF02162972
  33. Huang M, Morris N, Jay O, Davis S. Thermoregulatory dysfunction in multiple sclerosis patients during moderate exercise in a thermoneutral environment (1104.17). FASEB J 2014;28:1104.17.
  34. Noronha MJ, Vas CJ, Aziz H. Autonomic dysfunction (sweating responses) in multiple sclerosis. J Neurol Neurosurg Psychiatry 1968;31:19-22. https://doi.org/10.1136/jnnp.31.1.19
  35. Saari A, Tolonen U, Paakko E, Suominen K, Jauhiainen J, Sotaniemi KA, et al. Sweating impairment in patients with multiple sclerosis. Acta Neurol Scand 2009;120:358-363. https://doi.org/10.1111/j.1600-0404.2009.01164.x
  36. Cartlidge NE. Autonomic function in multiple sclerosis. Brain 1972;95:661-664. https://doi.org/10.1093/brain/95.4.661
  37. Chaseling GK, Filingeri D, Barnett M, Hoang P, Davis SL, Jay O. Cold water ingestion improves exercise tolerance of heat-sensitive people with MS. Med Sci Sports Exerc 2018;50:643-648. https://doi.org/10.1249/MSS.0000000000001496
  38. Acevedo AR, Nava C, Arriada N, Violante A, Corona T. Cardiovascular dysfunction in multiple sclerosis. Acta Neurol Scand 2000;101:85-88. https://doi.org/10.1034/j.1600-0404.2000.101002085.x
  39. Midaglia L, Juega Marino JM, Sastre-Garriga J, Rovira A, Vidal-Jordana A, Lopez-Perez MA, et al. An uncommon first manifestation of multiple sclerosis: Tako-Tsubo cardiomyopathy. Mult Scler 2016;22:842-846. https://doi.org/10.1177/1352458516638557
  40. Chagnac Y, Martinovits G, Tadmor R, Goldhammer Y. Paroxysmal atrial fibrillation associated with an attack of multiple sclerosis. Postgrad Med J 1986;62:385-387. https://doi.org/10.1136/pgmj.62.727.385
  41. Juric S, Mismas A, Mihic N, Barac AM, Habek M. Newly onset sinus bradycardia in the context of multiple sclerosis relapse. Intern Med 2012;51:1121-1124. https://doi.org/10.2169/internalmedicine.51.7139
  42. Soros P, Hachinski V. Cardiovascular and neurological causes of sudden death after ischaemic stroke. Lancet Neurol 2012;11:179-188. https://doi.org/10.1016/S1474-4422(11)70291-5
  43. Adamec I, Crnosija L, Junakovic A, Krbot Skoric M, Habek M. Progressive multiple sclerosis patients have a higher burden of autonomic dysfunction compared to relapsing remitting phenotype. Clin Neurophysiol 2018;129:1588-1594. https://doi.org/10.1016/j.clinph.2018.05.009
  44. Studer V, Rocchi C, Motta C, Lauretti B, Perugini J, Brambilla L, et al. Heart rate variability is differentially altered in multiple sclerosis: implications for acute, worsening and progressive disability. Mult Scler J Exp Transl Clin 2017;3:2055217317701317.
  45. Maciel BC, Gallo Junior L, Marin Neto JA, Martins LE. Autonomic nervous control of the heart rate during isometric exercise in normal man. Pflugers Arch 1987;408:173-177. https://doi.org/10.1007/BF00581348
  46. Damla O, Altug C, Pinar KK, Alper K, Dilek IG, Kadriye A. Heart rate variability analysis in patients with multiple sclerosis. Mult Scler Relat Disord 2018;24:64-68. https://doi.org/10.1016/j.msard.2018.06.012
  47. Sander C, Hildebrandt H, Schlake HP, Eling P, Hanken K. Subjective cognitive fatigue and autonomic abnormalities in multiple sclerosis patients. Front Neurol 2017;8:475.
  48. Bamer AM, Johnson KL, Amtmann D, Kraft GH. Prevalence of sleep problems in individuals with multiple sclerosis. Mult Scler 2008;14:1127-1130. https://doi.org/10.1177/1352458508092807
  49. Lanza G, Ferri R, Bella R, Ferini-Strambi L. The impact of drugs for multiple sclerosis on sleep. Mult Scler 2017;23:5-13. https://doi.org/10.1177/1352458516664034
  50. Fleming WE, Pollak CP. Sleep disorders in multiple sclerosis. Semin Neurol 2005;25:64-68. https://doi.org/10.1055/s-2005-867075
  51. Furlan JC. Autonomic dysreflexia following acute myelitis due to neuromyelitis optica. Mult Scler Relat Disord 2018;23:1-3. https://doi.org/10.1016/j.msard.2018.04.007
  52. Berry R, Panegyres PK. Peduncular hallucinosis and autonomic dysfunction in anti-aquaporin-4 antibody syndrome. Cogn Behav Neurol 2017;30:116-124. https://doi.org/10.1097/WNN.0000000000000132
  53. Barun B, Adamec I, Lovric M, Habek M. Postural orthostatic tachycardia syndrome: additional phenotypic feature of neuromyelitis optica spectrum disorder. Neurol Sci 2014;35:1623-1625. https://doi.org/10.1007/s10072-014-1810-9
  54. Crnosija L, Krbot Skoric M, Andabaka M, Junakovic A, Martinovic V, Ivanovic J, et al. Autonomic dysfunction in people with neuromyelitis optica spectrum disorders. Mult Scler 2020;26:688-695. https://doi.org/10.1177/1352458519837703
  55. Kwon S, Kim YS, Kim J, Kim BJ, Min JH. Clinical and MRI correlates of autonomic dysfunction in neuromyelitis optica spectrum disorder. Mult Scler Relat Disord 2020;43:102215.
  56. Vogel ER, Sandroni P, Low PA. Blood pressure recovery from Valsalva maneuver in patients with autonomic failure. Neurology 2005;65:1533-1537.  https://doi.org/10.1212/01.wnl.0000184504.13173.ef