Autonomic Dysfunction and its Diagnostic Tools in Multiple Sclerosis
Authors:
I. Šrotová; E. Vlčková; J. Bednařík
Authors place of work:
CEITEC – Středoevropský technologický institut, MU, Brno
; Neurologická klinika LF MU a FN Brno
Published in the journal:
Cesk Slov Neurol N 2016; 79/112(2): 188-198
Category:
Přehledný referát
Tato publikace vznikla na Masarykově univerzitě v rámci projektu „Diagnostika a patofyziologie neuropatické bolesti“ číslo MUNI/A/1072/2015 podpořeného z prostředků účelové podpory na specifický vysokoškolský výzkum, kterou poskytlo MŠMT v roce 2016, grantovým projektem Interní Grantové Agentury (IGA MZ ČR NT 13523-4), projektem MZ ČR – RVO (FNBr, 65269705) a interními zdroji CEITEC MUNI.
Summary
Autonomic nervous system dysfunction (AD) represents a frequent clinical presentation of multiple sclerosis (MS). According to published studies, the incidence of AD in MS patients ranges between 16 and 80% and gradually increases with the length of the demyelinating disease and with the progression of disability. However, AD can occur in any phase of MS and can even represent its first symptom in some patients. Autonomic dysfunction has a significant negative impact on the quality of life in MS patients and contributes to overall disability. Even so, autonomic nervous system dysfunction is frequently underdiagnosed in patients with multiple sclerosis. Cardiovascular and urogenital dysfunction are the most frequent types of AD in MS patients with the highest impact on their clinical status and the quality of life. Less frequently, gastrointestinal, sudomotor or pupilomotor dysfunction can be found. Autonomic (in particular cardiovascular) dysfunction in multiple sclerosis is closely related to fatigue, another frequent clinical symptom in MS patients. The aim of this paper is to sum up the spectrum of symptoms of autonomic dysfunction in multiple sclerosis and its diagnostic tools.
Key words:
multiple sclerosis – autonomic nervous system diseases – orthostatic intolerance –urinary incontinence – urinary retention –sexual dysfunction – gastrointestinal dysfunction – sweating
The authors declare they have no potential conflicts of interest concerning drugs, products, or services used in the study.
The Editorial Board declares that the manuscript met the ICMJE “uniform requirements” for biomedical papers.
Zdroje
1. McDougall AJ, McLeod JG. Autonomic nervous system function in multiple sclerosis. J Neurol Sci 2003;215(2):79– 85.
2. Thomaides TN, Zoukos Y, Chaudhuri KR, et al. Physiological assessment of aspects of autonomic function in patients with secondary progressive multiple sclerosis. J Neurol 1993;240(3):139– 43.
3. Cortez MM, Nagi Reddy SK, Goodman B, et al. Autonomic symptom burden is associated with MS-related fatigue and quality of life. Mult Scler Relat Disord 2015;4(3):258– 63. doi: 10.1016/ j.msard.2015.03.007.
4. Adamec I, Habek M. Autonomic dysfunction in multiple sclerosis. Clin Neurol Neurosurg 2013;115(Suppl 1):S73– 8. doi: 10.1016/ j.clineuro.2013.09.026.
5. Gunal DI, Afsar N, Tanridag T, et al. Autonomic dysfunction in multiple sclerosis: correlation with disease-related parameters. Eur Neurol 2002;48(1):1– 5.
6. Flachenecker P, Reiners K, Krauser M, et al. Autonomic dysfunction in multiple sclerosis is related to disease activity and progression of disability. Mult Scler 2001;7(5):327– 34.
7. Vita G, Fazio MC, Milone S, et al. Cardiovascular autonomic dysfunction in multiple sclerosis is likely related to brainstem lesions. J Neurol Sci 1993;120(1):82– 6.
8. Stenager E, Asbeth NS. Sexual aspect of multiple sclerosis. Sem Neurol 1992;12(2):120– 4.
9. Saari A, Tolonen U, Pääkkö E, et al. Cardiovascular autonomic dysfunction correlates with brain MRI lesion load in MS. Clin Neurophysiol 2004;115(6):1473– 8.
10. De Seze J, Stojkovic T, Gauvrit JY, et al. Autonomic dysfunction in multiple sclerosis: cervical spinal cord atrophy correlates. J Neurol 2001;248(4):297– 303.
11. Kurtzke JF. Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 1983;33(11):1444– 52.
12. Suarez GA, Opfer-Gehrking TL, Offord KP, et al. The Autonomic Symptom Profile: a new instrument to assess autonomic symptoms. Neurology 1999;52(3):523– 8.
13. Sletten DM, Suarez GA, Low PA, et al. COMPASS 31: a refined and abbreviated Composite Autonomic Symptom Score. Mayo Clin Proc 2012;87(12):1196– 201. doi: 10.1016/ j.mayocp.2012.10.013.
14. Treister R, O‘Neil K, Downs HM, et al. Validation of the composite autonomic symptom scale 31 (COMPASS-31) in patients with and without small fiber polyneuropathy. Eur J Neurol 2015;22(7):1124– 30. doi: 10.1111/ ene.12717.
15. Kale N, Magana S, Agaoglu J, et al. Assessment of autonomic nervous system dysfunction in multiple sclerosis and association with clinical disability. Neurol Int 2009;1(1):5– 10. doi: 10.4081/ ni.2009.e5.
16. Acevedo AR, Nava C, Arriada N, et al. Cardiovascular dysfunction in multiple sclerosis. Acta Neurol Scand 2000;101(2):85– 8.
17. Nasseri K, TenVoorde BJ, Adèr HJ, et al. Longitudinal follow-up of cardiovascular reflex tests in multiple sclerosis. J Neurol Sci 1998;155(1):50– 4.
18. Keselbrener L, Akselrod S, Ahiron A, et al. Is fatigue in patients with multiple sclerosis related to autonomic dysfunction? Clin Auton Res 2000;10(4):169– 75.
19. Flachenecker P, Rufer A, Bihler I, et al. Fatigue in MS is related to sympathetic vasomotor dysfunction. Neurology 2003;61(6):851– 3.
20. Kanjwal K, Karabin B, Kanjwal Y, et al. Autonomic dysfunction presenting as postural orthostatic tachycardia syndrome in patients with multiple sclerosis. Int J Med Sci 2010;7(1):62– 7.
21. Sörös P, Hachinski V. Cardiovascular and neurological causes of sudden death after ischaemic stroke. Lancet Neurol 2012;11(2):179– 88. doi: 10.1016/ S1474-4422(11)70291-5.
22. Juric S, Mismas A, Mihic N, et al. Newly onset sinus bradycardia in context of multiple sclerosis relapse. Intern Med 2012;51(9):1121– 4.
23. Chagnac Y, Martinovits G, Tadmor R, et al. Paroxysmal atrial fibrillation associated with an attack of multiple sclerosis. Postgrad Med J 1986;62(727):385– 7.
24. Uriel N, Kaluski E, Hendler A, et al. Cardiogenic shock in a young female with multiple sclerosis. Resuscitation 2006;70(1):153– 7.
25. Padley JR, Feneley MP, Hayward CS, et al. Neurocardiogenic pulmonary oedema: initial presentation of multiple sclerosis. Heart Lung Circ 2012;21(12):853– 5. doi: 10.1016/ j.hlc.2012.06.003.
26. Bramow S, Faber-Rod JC, Jacobsen C, et al. Fatal neurogenic pulmonary edema in a patient with progressive multiple sclerosis. Mult Scler 2008;14(5):711– 5. doi: 10.1177/ 1352458507087848.
27. Paty DW, Ebers GC, Hartung HP. Management of relapsing-remitting multiple sclerosis and treatment guidelines. Eur J Neurology 1999;1(1):1– 35.
28. Vasheghani-Farahani A, Sahraian MA, Darabi L, et al. Incidence of various cardiac arrhythmias and conduction disturbances due to high dose intravenous methylprednisolone in patients with multiple sclerosis. J Neurol Sci 2001;309(2):75– 8.
29. Štourač P. Imunomodulační léčba roztroušené sklerózy mozkomíšní v klinických a zobrazovacích parametrech. Cesk Slov Neurol N 2012;75/ 108(4):404– 10.
30. Meluzínová E. Současné možnosti léčb roztroušené sklerózy. Neurol Prax 2010;11(5):303– 7.
31. Piťha J. Imunosupresiva v léčbě neurologických onemocnění. Neurol Prax 2011;12(6):389– 93.
32. Kappos L, Radue EW, O‘Connor P, et al. A placebo-controlled trial of oral fingolimod in relapsing multiple sclerosis. N Engl J Med 2010;362(5):387– 401. doi: 10.1056/ NEJMoa0909494.
33. Budde K, Schmouder RL, Brunkhorst R, et al. First human trial of FTY720, a novel immunomodulator, in stable renal transplant patients. J Am Soc Nephrol 2002;13(4):1073– 83.
34. Gold R, Comi G, Palace J, et al. Assessment of cardiac safety during fingolimod treatment initiation in a real-world relapsing multiple sclerosis population: a phase 3b, open-label study. J Neurol 2014;261(2):267– 76. doi: 10.1007/ s00415-013-7115-8.
35. Rossi S, Rocchi C, Studer V, et al. The autonomic balance predicts cardiac responses after the first dose of fingolimod. Mult Scler 2015;21(2):206– 16. doi: 10.1177/ 1352458514538885.
36. Ambler Z, Bednařík J, Růžička E. Klinická neurologie – část obecná. Praha: Triton 2008.
37. Adamec I, Bach I, Barušić AK, et al. Assessment of prevalence and pathological response to orthostatic provocation in patients with multiple sclerosis. J Neurol Sci 2013;324(1– 2):80– 3. doi: 10.1016/ j.jns.2012.10.006.
38. Flachenecker P, Wolf A, Krauser M, et al. Cardiovascular autonomic dysfunction in multiple sclerosis: correlation with orthostatic intolerance. J Neurol 1999;246(7):578– 86.
39. Adamec I, Lovric’ M, Zaper D, et al. Postural orthostatic tachycardia syndrome associated with multiple sclerosis. Auton Neurosci 2013;173(2):65– 8. doi: 10.1016/ j.autneu.2012.11.009.
40. Martin CE, Shaver JA, Leon DF, et al. Autonomic mechanisms in hemodynamic responses to isometric exercise. J Clin Invest 1974;54(1):104– 15.
41. Ewing DJ, Clarke BF. Autonomic neuropathy: its diagnosis and prognosis. Clin Endocrinol Metab 1986;15(4):855– 88.
42. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology. Heart rate variability: standards of measurement, physiological interpretation, and clinical use. Circulation 1996;93(5):1043– 65.
43. Mahovic D, Lakusic N. Progressive impairment of autonomic control of heart rate in patients with multiple sclerosis. Arch Med Res 2007;38(3):322– 5.
44. Tombul T, Anlar O, Tuncer M, et al. Impaired heart rate variability as a marker of cardiovascular autonomic dysfunction in multiple sclerosis. Acta Neurol Belg 2011;111(2):116– 20.
45. Brezinova M, Goldenberg Z, Kucera P. Autonomic nervous system dysfunction in multiple sclerosis patients. Bratisl Lek Listy 2004;105(12):404– 7.
46. Frontoni M, Fiorini M, Strano S, et al. Power spectrum analysis contribution to the detection of cardiovascular dysautonomia in multiple sclerosis. Acta Neurol Scand 1996;93(4):241– 5.
47. Opavský J, Autonomní nervový systém a diabetická autonomní neuropatie. Praha Galén 2002.
48. Vlčková E, Bednařík J, Buršová Š, et al. Spektrální analýza variability srdeční frekvence – normativní data a variabilita metodiky. Cesk Slov Neurol N 2010;73/ 106(4):469– 70.
49. Haensch CA, Jörg J. Autonomic dysfunction in multiple sclerosis. J Neurol 2006;253(1):3– 9.
50. Thompson AJ, Toosy AT, Ciccarelli O. Pharmacological management of symptoms in multiple sclerosis: current approaches and future directions. Lancet Neurol 2010;9(12):1182– 99. doi: 10.1016/ S1474-4422(10)70249-0.
51. Betts CD, D‘Mellow MT, Fowler CJ. Urinary symptoms and the neurological features of bladder dysfunction in multiple sclerosis. J Neurol Neurosurg Psychiatry 1993;56(3):245– 50.
52. Metz LM, McGuinness SD, Harris C. Urinary tract infections may trigger relapse in multiple sclerosis. Axone 1998;19(4):67– 70.
53. Blaivas JG, Bhimani G, Labib KB. Vesicourethral dysfunction in multiple sclerosis. J Urol 1979;122(3):342– 7.
54. Podnar S, Vodusek DB. Standardization of anal sphincter electromyography: uniformity of the muscle. Muscle Nerve 2000;23(1):122– 5.
55. Podnar S, Rodi Z, Lukanovic A, et al. Standardisation of anal sphincter EMG: technique of needle examination. Muscle Nerve 1999;22(3):400– 3.
56. Thiry AJ, Deltrenre PF. Neurophysiological assessment of the central motor pathway to the external urethral sphincter in man. Br J Urol 1989;63(5):515– 9.
57. Kadaňka Z jr. Elektrofyziologické vyšetření pánevního dna. Cesk Slov Neurol N 2013;76/ 109(2):155– 61.
58. Rodi Z, Vodusek DB, Denislic M. Clinical uro-neurophysiological investigation in multiple sclerosis. Eur J Neurol 1996;3(6):574– 80.
59. Vodusek DB, Zidar J. Perineal motor evoked responses. Neurourol Urodynamic 1988;7(1):236– 7.
60. Eardley I, Nagendran K, Lecky B, et al. Neurophysiology of the striated urethral sphincter in multiple sclerosis. Br J Urol 1991;68(1):81– 8.
61. Haldeman S, Bradley WE, Bhatia N. Evoked responses from the pudendal nerve. J Urol 1982;128(5):974– 80.
62. Bojar M, Mazanec R, Kučera Z. Role neurologa v diagnostice, léčbě a rehabilitaci osob trpících inkontinencí moči (část I). Neurol Prax 2006;4(1):212– 9.
63. Sau G, Siracusano S, Aiello I, et al. The usefulness of the somatosensory evoked potentials of the pudendal nerve in diagnosis of probable multiple sclerosis. Spinal Cord 1999;37(4):258– 63.
64. Sau GF, Aiello I, Siracusano S, et al. Pudendal nerve somatosensory evoked potentials in probable multiple sclerosis. Ital J Neurol Sci 1997;18(5):289– 91.
65. Ertekin C, Reel F. Bulbocavernosus reflex in normal men and in patients with neurogenic bladder and/ or impotence. J Neurol Sci 1976;28(1):1– 15.
66. Hinds JP, Eidelman BH, Wald A. Prevalence of bowel dysfunction in multiple sclerosis. A population survey. Gastroenterology 1990;98(6):1538– 42.
67. Chia YW, Gill KP, Jameson JS, et al. Paradoxical puborectalis contraction is a feature of constipation in patients with multiple sclerosis. J Neurol Neurosurg Psychiatry 1996;60(1):31– 5.
68. Levinthal DJ, Rahman A, Nusrat S, et al. Adding to the burden: gastrointestinal symptoms and syndromes in multiple sclerosis. Mult Scler Int 2013;2013:319201. doi: 10.1155/ 2013/ 319201.
69. Gold R, Kappos L, Arnold DL, et al. Placebo-controlled phase 3 study of oral BG-12 for relapsing multiple sclerosis. N Engl J Med 2012;367(12):1098– 107.
70. Preziosi G, Raptis DA, Raeburn A, et al. Gut dysfunction in patients with multiple sclerosis and the role of spinal cord involvement in the disease. Eur J Gastroenterol Hepatol 2013;25(9):1044– 50. doi: 10.1097/ MEG.0b013e328361eaf8.
71. Marrie RA, Reider N, Stuve O, et al. The incidence and prevalence of comorbid gastrointestinal, musculoskeletal, ocular, pulmonary, and renal disorders in multiple sclerosis: a systematic review. Mult Scler 2015;21(3):332– 41. doi: 10.1177/ 1352458514564488.
72. Mlčáková L, Bednařík J, Ošlejšková E, et al. Spektrální analýza variability srdeční frekvence a elektrogastrografie – metody popisující funkce autonomního nervového systému. Cesk Slov Neurol N 2008;71/ 104(5):621– 22.
73. Riezzo G, Russo F, Indrio F. Electrogastrography in adults and children: the strength, pitfalls, and clinical significance of the cutaneous recording of the gastric electrical activity. Biomed Res Int 2013;2013:282757. doi: 10.1155/ 2013/ 282757.
74. Chang J, Rayner CK, Jones KL, et al. Diabetic gastroparesis-backwards and forwards. J Gastroenterol Hepatol 2011;26(Suppl 1):46– 57. doi: 10.1111/ j.1440-1746.2010.06573.x.
75. El-Maghraby TA, Shalaby NM, Al-Tawdy MH, et al. Gastric motility dysfunction in patients with multiple sclerosis assessed by gastric emptying scintigraphy. Can J Gastroenterol 2005;9(1):141– 5.
76. Zorzon M, Zivadinov R, Monti Bragadin L, et al. Sexual dysfunction in multiple sclerosis: a 2-year follow-up study. J Neurol Sci 2001;187(1– 2):1-5.
77. Šrotová I, Crha I, Vlčková E, et al. Roztroušená skleróza, neplodnost a její léčba. Cesk Slov Neurol N 2015;78/ 11(6):655– 60.
78. Foley FW, Zemon V, Campagnolo D, et al. The Multiple Sclerosis Intimacy and Sexuality Questionnaire – re-validation and development of a 15-item version with a large US sample. Mult Scler 2013;19(9):1197– 203. doi: 10.1177/ 1352458512471876.
79. Confavreux C, Hutchinson M, Hours MM, et al. Rate of pregnancy-related relapse in multiple sclerosis. Pregnancy in Multiple Sclerosis Group. N Engl J Med 1998;339(5):285– 91.
80. Grinsted L, Heltberg A, Hagen C, et al. Serum sex hormone and gonadotropin concentrations in premenopausal women with multiple sclerosis. J Intern Med 1989;226(4):241– 4.
81. Falaschi P, Martocchia A, Proietti A, et al. High incidence of hyperandrogenism-related clinical signs in patients with multiple sclerosis. Neuro Endocrinol Lett 2001;22(4):248– 50.
82. Fode M, Krogh-Jespersen S, Brackett NL, et al. Male sexual dysfunction and infertility associated with neurological disorders. Asian J Androl 2012;14(1):61– 8. doi: 10.1038/ aja.2011.70.
83. Cocco E, Sardu C, Gallo P, et al. Frequency and risk factors of mitoxantrone-induced amenorrhea in multiple sclerosis: the FEMIMS study. Mult Scler 2008;14(9):1225– 33. doi: 10.1177/ 1352458508094882.
84. Cavalla P, Rovei V, Masera S, et al. Fertility in patients with multiple sclerosis: current knowledge and future perspectives. Neurol Sci 2006;27(4):231– 9.
85. Zivadinov R, Zorzon M, Locatelli L, et al. Sexual dysfunction in multiple sclerosis: a MRI, neurophysiological and urodynamic study. J Neurol Sci 2003;210(1– 2):73– 6.
86. Ghezzi A, Malvestiti GM, Baldini S, et al. Erectile impotence in multiple sclerosis: a neurophysiological study. J Neurol 1995;242(3):123– 6.
87. Yang CC, Bowen JR, Kraft GH, et al. Cortical evoked potentials of the dorsal nerve of the clitoris and female sexual dysfunction in multiple sclerosis. J Urol 2000;164(6):2010– 3.
88. Saari A, Tolonen U, Pääkkö E, et al. Sympathetic skin responses in multiple sclerosis. Acta Neurol Scand 2008;118(4):226– 31.
89. Saari A, Tolonen U, Pääkkö E, et al. Sweating impairment in patients with multiple sclerosis. Acta Neurol Scand 2009;120(5):358– 63. doi: 10.1111/ j.1600-0404.2009.01164.x.
90. Noronha MJ, Vas CJ, Aziz H. Autonomic dysfunction (sweating responses) in multiple sclerosis. J Neurol Neurosurg Psychiatry 1968;31(1):19– 22.
91. Guthrie TC, Nelson DA. Influence of temperature changes on multiple sclerosis: critical review of mechanisms and research potential. J Neurol Sci 1995;129(1):1– 8.
92. Davis SL, Wilson TE, Vener JM, et al. Pilocarpine-induced sweat gland function in individuals with multiple sclerosis. J Appl Physiol 1985;98(5):1740– 4.
93. Shahani BT, Halperin JJ, Boulu P, et al. Sympathetic skin response – a method of assessing unmyelinated axon dysfunction in peripheral neuropathies. J Neurol Neurosurg Psychiatry 1984;47(5):536– 42.
94. Wang GH. The galvanic skin reflex; a review of old and recent works from a physiologic point of view. Am J Phys Med 1957;36(5):295– 320.
95. Illigens BM, Gibbons CH. Sweat testing to evaluate autonomic function. Clin Auton Res 2009;19(2):79– 87. doi: 10.1007/ s10286-008-0506-8.
96. Vlčková E, Šrotová I, Bednařík J. Sympatická kožní odpověď v diagnostice neuropatie tenkých vláken. Cesk Slov Neurol N 2016;79/ 112(1):52– 60.
97. Claus D, Schondorf R. Sympathetic skin response. The International Federation of Clinical Neurophysiology. Electroencephalogr Clin Neurophysiol Suppl 1999;52(1):277– 82.
98. Knezevic W, Bajada S. Peripheral autonomic surface potential. A quantitative technique for recording sympathetic conduction in man. J Neurol Sci 1985;67(2):239– 51.
99. Vinik AI, Nevoret M, Casellini C, et al. Neurovascular function and sudorimetry in health and disease. Curr Diab Rep 2013;13(4):517– 32. doi: 10.1007/ s11892-013-0392-x.
100. Aghamollaii V, Harirchian MH, Modabbernia A, et al. Sympathetic skin response (SSR) in multiple sclerosis and clinically isolated syndrome: a case-control study. Neurophysiol Clin 2011;41(4):161– 71. doi: 10.1016/ j.neucli.2011.08.003.
101. Saari A, Tolonen U, Pääkkö E, et al. Sudomotor dysfunction in patients with optic neuritis. Clin Auton Res 2010;20(3):199– 204. doi: 10.1007/ s10286-009-0052-z.
102. Pintér A, Cseh D, Sárközi A, et al. Autonomic dysregulation in multiple sclerosis. Int J Mol Sci 2015;16(8):16920– 52. doi: 10.3390/ ijms160816920.
103. Crnošija L, Adamec I, Lovrić M, et al. Autonomic dysfunction in clinically isolated syndrome suggestive of multiple sclerosis. Clin Neurophysiol 2016;127(1):864– 9. doi: 10.1016/ j.clinph.2015.06.010.
104. Blazek P, Davis SL, Greenberg BM, et al. Objective characterization of the relative afferent pupillary defect in MS. J Neurol Sci 2012;323(1– 2):193– 200. doi: 10.1016/ j.jns.2012.09.015.
105. Surakka J, Ruutiainen J, Romberg A, et al. Pupillary function in early multiple sclerosis. Clin Auton Re 2008;18(3):150– 4. doi: 10.1007/ s10286-008-0471-2.
106. Ampapová M, Ampapa R. Optická neuritida a roztroušená skleróza. Klin Farmakol Farm 2013;27(2):75– 9.
107. Pozzessere G, Rossi P, Valle E, et al. Autonomic involvement in multiple sclerosis: a pupillometric study. Clin Auton Res 1997;7(6):315– 9.
108. Bamer AM, Johnson KL, Amtmann D, et al. Prevalence of sleep problems in individuals with multiple sclerosis. Mult Scler 2008;14(8):1127– 30. doi: 10.1177/ 1352458508092807.
109. Oka Y, Kanbayashi T, Mezaki T, et al. Low CSF hypocretin-1/ orexin-A associated with hypersomnia secondary to hypothalamic lesion in a case of multiple sclerosis. J Neurol 2004;251(7):885– 6.
110. Tachibana N, Howard RS, Hirsch NP, et al. Sleep problems in multiple sclerosis. Eur Neurol 1994;34(6):320– 3.
111. Fleming WE, Pollak CP. Sleep disorders in multiple sclerosis. Semin Neurol 2005;25(1):64– 8.
112. Vališ M, Taláb R, Masopust J. Únava u roztroušené sklerózy mozkomíšní a možnosti jejího ovlivnění. Neurol Prax 2005;1(1):40– 1.
113. Zellini F, Niepel G, Tench CR, et al. Hypothalamic involvement assessed by T1 relaxation time in patients with relapsing-remitting multiple sclerosis. Mult Scler 2009;15(12):1442– 9. doi: 10.1177/ 1352458509350306.
114. Krupp LB, LaRocca NG, Muir-Nash J, et al. The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol 1989;46(10):1121– 3.
115. Kos D, Kerckhofs E, Ketelaer P, et al. Self-report assessment of fatigue in multiple sclerosis: A critical evaluation. Occupational Therapy in Health Care 2004;17(3– 4):45– 62.
Štítky
Dětská neurologie Neurochirurgie NeurologieČlánek vyšel v časopise
Česká a slovenská neurologie a neurochirurgie
2016 Číslo 2
Nejčtenější v tomto čísle
- Ramsay-Huntov syndróm – vzácna manifestácia pomerne častého ochorenia
- Management tranzitorní ischemické ataky a minor stroke
- Neurosarkoidóza u muže středního věku – kazuistika
- Autonomní dysfunkce a její diagnostika u roztroušené sklerózy