Top

Published in:

21-04-2023 | Multiple Sclerosis | Review

Autonomic nervous system disorders in multiple sclerosis

Authors: Effrosyni Koutsouraki, Koukoulidis Theodoros, Georgiadou Eleni, Kalampouka Marianna, Nikolaidou Areti, Koukoulidou Ariadni, Michmizos Dimitrios

Published in: Journal of Neurology | Issue 8/2023

Abstract

Multiple sclerosis (MS) is a chronic progressive demyelinating disease of the central nervous system (CNS), which also affects the autonomic nervous system (ANS). Manifestations of MS in the ANS include urological, sexual, gastrointestinal, cardiovascular, and thermoregulatory disorders as well as increased fatigue. These problems are common yet are often underestimated due to the non-specificity of the symptoms and the limited evaluation of the ANS in the usual clinical practice. Most of these symptoms seem to be related to localized lesions in the CNS. However, the mechanisms by which these disorders are caused in MS have not been fully investigated, thus preventing any focused etiological treatment. The most common disorders of the ANS in MS represent a challenge for clinicians due to the variability of the clinical picture and our minimal data on their diagnosis and treatment. Early diagnosis and initiation of individualized treatment regimens, often in need of multiple approaches, seem to yield the best results in managing ANS dysfunction in MS patients.

Abrams P, Cardozo L, Fall M, Griffiths D, Rosier P, Ulmsten U, van Kerrebroeck P, Victor A, Wein A (2003) Standardisation Sub-Committee of the International Continence Society. The standardization of terminology in lower urinary tract function: report from the standardization sub-committee of the international continence society. Urology 61:37–49. https://doi.org/10.1016/S0090-4295(02)02243-4CrossRefPubMed

Adamec I, Habek M (2013) Autonomic dysfunction in multiple sclerosis. Clin Neurol Neurosurg 115(1):S73–S78. https://doi.org/10.1016/j.clineuro.2013.09.026CrossRefPubMed

Adamec I, Bach I, Barušić AK, Mišmaš A, Habek M (2013) Assessment of prevalence and pathological response to orthostatic provocation in patients with multiple sclerosis. J Neurol Sci 324:80–83. https://doi.org/10.1016/j.jns.2012.10.006CrossRefPubMed

Adamec I, Crnošija L, Junaković A, KrbotSkorić M, Habek M (2018) Progressive multiple sclerosis patients have a higher autonomic dysfunction burden than the relapsing-remitting phenotype. Clin Neurophysiol 129(8):1588–1594. https://doi.org/10.1016/j.clinph.2018.05.009CrossRefPubMed

Amarenco G, Raibaut P, Hubeaux K, Jousse M, Sheikh IS, Lapeyre E (2013) Autonomic nervous system alteration in multiple sclerosis patients with urinary symptoms. Clinical, urodynamic, and cardiovascular study. Prog Urol 23:1505–1510. https://doi.org/10.1016/j.purol.2013.06.010CrossRefPubMed

Anema JR, Heijenbrok MW, Faes TJ, Heimans JJ, Lanting P, Polman CH (1991) Cardiovascular autonomic function in multiple sclerosis. J Neurol Sci 104:129–134. https://doi.org/10.1016/0022-510X(91)90301-MCrossRefPubMed

Bakke A, Myhr KM, Gronning M, Nyland H (1996) Bladder, bowel and sexual dysfunction in patients with multiple sclerosis—a cohort study. Scand J Urol Nephrol Suppl 179:61–66PubMed

Barak Y, Achiron A, Elizur A, Gabbay U, Noy S, Sarova-Pinhas I (1996) Sexual dysfunction in relapsing-remitting multiple sclerosis: magnetic resonance imaging, clinical, and psychological correlates. J Psychiatry Neurosci 21:255–258PubMedPubMedCentral

Beenakker EA, Oparina TI, Hartgring A, Teelken A, Arutjunyan AV, de Keyser J (2001) Cooling garment treatment in MS: clinical improvement and decrease in leukocyte no production. Neurology 57:892–894. https://doi.org/10.1212/WNL.57.5.892CrossRefPubMed

10.

Beer S, Kesselring J (1988) Die multiple sklerose im kanton bern. Fortschritte der Neurologie Psychiatrie 56(12):390–397CrossRef

11.

Betts CD, Jones SJ, Fowler CG, Fowler CJ (1994) Erectile dysfunction in multiple sclerosis. Associated neurological and neurophysiological deficits, and treatment of the condition. Brain 117(6):1303–1310. https://doi.org/10.1093/brain/117.6.1303CrossRefPubMed

12.

Bratu O, Mischianu D, Constantinoiu S (2013) Transobturator urethral suspension surgical treatment of urinary incontinence in men. Chirurgia (Bucur) 108:250–255PubMed

13.

Bratu O, Marcu D, Spinu D, Radulescu A, Oprea I, Mischianu D (2015) TOT versus TVT-mesh surgical treatment in stress urinary incontinence. Rom J Mil Med 118:40–44

14.

Celik DB, Poyraz EC, Bingol A, Idiman E, Ozakbas S, Kaya D (2013) Sexual dysfunction in multiple sclerosis: gender differences. J Neurol Sci 324:17–20. https://doi.org/10.1016/j.jns.2012.08.019CrossRefPubMed

15.

Cetinel B, Tarcan T, Demirkesen O, Ozyurt C, Sen I, Erdogan S, Siva A (2013) Management of lower urinary tract dysfunction in multiple sclerosis: a systematic review and Turkish consensus report. Neurourol Urodyn 32:1047–1057. https://doi.org/10.1002/nau.22374CrossRefPubMed

16.

Chagnac Y, Martinovits G, Tadmor R, Goldhammer Y (1986) Paroxysmal atrial fibrillation is associated with an attack of multiple sclerosis. Postgrad Med J 62:385–387. https://doi.org/10.1136/pgmj.62.727.385CrossRefPubMedPubMedCentral

17.

Chancellor MB, Blaivas JG (1994) Urological and sexual problems in multiple sclerosis. Clin Neurosci 2(3–4):189–195PubMed

18.

Chaseling GK, Filingeri D, Barnett M, Hoang P, Davis SL, Jay O (2018) Cold water ingestion improves exercise tolerance of heat-sensitive people with MS. Med Sci Sports Exerc 50:643–648. https://doi.org/10.1249/MSS.0000000000001496CrossRefPubMed

19.

Chehensse C, Bahrami S, Denys P, Clement P, Bernabe J, Giuliano F (2013) The spinal control of ejaculation revisited: a systematic review and meta-analysis of anejaculation in spinal cord injured patients. Hum Reprod Update 19:507–526. https://doi.org/10.1093/humupd/dmt029CrossRefPubMed

20.

Chen AY, Frankowski R, Bishop-Leone J, Hebert T, Leyk S, Lewin J, Goepfert H (2001) The development and validation of a dysphagia-specific quality-of-life questionnaire for patients with head and neck cancer: the M.D. Anderson dysphagia inventory. Arch Otolaryngol Head Neck Surg 127:870–876PubMed

21.

Christogianni A, Bibb R, Davis S, Jay O, Barnett M, Evangelou N, Filingeri D (2018) Temperature sensitivity in multiple sclerosis: an overview of its impact on sensory and cognitive symptoms. Temperature (Austin) 5:208–223. https://doi.org/10.1080/23328940.2018.1475831CrossRefPubMed

22.

Crayton HJ, Rossman HS (2006) Managing the symptoms of multiple sclerosis: a multimodal approach. Clin Ther 28:445–460. https://doi.org/10.1016/j.clinthera.2006.04.005CrossRefPubMed

23.

Crnošija L, Adamec I, Lovrić M, Junaković A, KrbotSkorić M (2016) Autonomic dysfunction in clinically isolated syndrome suggestive of multiple sclerosis. Clin Neurophysiol 127:864CrossRefPubMed

24.

De RodezBenavent S, Nygaard G, Nilsen K, Etholm L, Sowa P, Wendel-Haga M, Harbo H, Drolsum L, Laeng B, Kerty E, Celius E (2019) Neurodegenerative interplay of cardiovascular autonomic dysregulation and the retina in early multiple sclerosis. Front Neurol 10:1–9. https://doi.org/10.3389/fneur.2019.00507CrossRef

25.

Dasgupta R, Fowler CJ (2003) Bladder, bowel and sexual dysfunction in multiple sclerosis: management strategies. Drugs 63:153–166. https://doi.org/10.2165/00003495-200363020-00003CrossRefPubMed

26.

Dasgupta R, Wiseman OJ, Kanabar G, Fowle CJ, Mikol D (2004) Efficacy of sildenafil in the treatment of female sexual dysfunction due to multiple sclerosis. J Urol 171:1189–1193. https://doi.org/10.1097/01.ju.0000113145.43174.24CrossRefPubMed

27.

Davis SL, Wilson TE, Vener JM, Crandall CG, Petajan JH, White AT (2005) Pilocarpine-induced sweat gland function in individuals with multiple sclerosis. J Appl Physiol 98:1740–1744. https://doi.org/10.1152/japplphysiol.00860.2004CrossRefPubMed

28.

Davis SL, Wilson TE, White AT, Frohman EM (2010) Thermoregulation in multiple sclerosis. J Appl Physiol 109:1531–1537. https://doi.org/10.1152/japplphysiol.00460.2010CrossRefPubMedPubMedCentral

29.

de Sèze J, Stojkovic T, Gauvrit JY et al (2001) Autonomic dysfunction in multiple sclerosis: cervical spinal cord atrophy correlates. J Neurol 248(4):297–303CrossRefPubMed

30.

de Seze M, Ruffion A, Denys P, Joseph PA, Perrouin-Verbe B, GENULF (2007) The neurogenic bladder in multiple sclerosis: Review of the literature and proposal of management guidelines. Mult Scler 13(7):915–928. https://doi.org/10.1177/1352458506075651CrossRefPubMed

31.

Demirkiran M, Sarica Y, Uguz S, Yerdelen D, Aslan K (2006) Multiple sclerosis patients with and without sexual dysfunction: Are there any differences? Mult Scler 12:209–214. https://doi.org/10.1191/135248506ms1253oaCrossRefPubMed

32.

Drossman DA (2006) The functional gastrointestinal disorders and the Rome III process. Gastroenterology 130:1377–1390. https://doi.org/10.1053/j.gastro.2006.03.008CrossRefPubMed

33.

Fanciulli A, Campese N, Wenning G (2019) The Schellong test: detecting orthostatic blood pressure and heart rate changes in German-speaking countries. Clin Auton Res 29:363–366CrossRefPubMed

34.

Flachenecker P, Reiners K, Krauser M, Wol A, Toyka KV (2001) Autonomic dysfunction in multiple sclerosis is related to disease activity and the progression of disability. Mult Scler 7:327–334. https://doi.org/10.1177/135245850100700509CrossRefPubMed

35.

Flachenecker P, Rufer A, Bihler I, Hippel C, Reiners K, Toyka KV, Kesselring J (2003) Fatigue in MS is related to sympathetic vasomotor dysfunction. Neurology 61(6):851–853. https://doi.org/10.1212/01.WNL.0000080365.95436.B8CrossRefPubMed

36.

Foley FW, LaRocca NG, Sanders AS, Zemon V (2001) Rehabilitation of intimacy and sexual dysfunction in couples with multiple sclerosis. Mult Scler 7:417–421. https://doi.org/10.1177/135245850100700612CrossRefPubMed

37.

Forbes MK, Baillie AJ, Schniering CA (2014) Critical flaws in the female sexual function index and the international index of erectile function. J Sex Res 51:485–491. https://doi.org/10.1080/00224499.2013.876607CrossRefPubMed

38.

Fowler C et al (2009) A UK consensus of the management of the bladder in multiple sclerosis. J Neurol Neurosurg Psychiatry 80:470–477PubMed

39.

Freeman R (2005) Autonomic peripheral neuropathy. Lancet 365:1259–1270. https://doi.org/10.1016/S0140-6736(05)74815-7CrossRefPubMed

40.

Frontoni M, Fiorini M, Strano S, Cerutti S, Giubilei F, Urani C, Bastianello S, Pozzilli C (1996) Power spectrum analysis contribution to the detection of cardiovascular dysautonomia in multiple sclerosis. Acta Neurol Scand 93:241–245. https://doi.org/10.1111/j.1600-0404.1996.tb00514.xCrossRefPubMed

41.

Gallien P, Robineau S, Nicolas B, le Bot MP, Brissot R, Verin M (1998) Vesicourethral dysfunction and urodynamic findings in multiple sclerosis: a study of 149 cases. Arch Phys Med Rehabil 79:255–257. https://doi.org/10.1016/S0003-9993(98)90003-XCrossRefPubMed

42.

Gibbons CH, Illigens BM, Centi J, Freeman R (2008) QDIRT: quantitative direct and indirect test of sudomotor function. Neurology 70:2299–2304. https://doi.org/10.1212/01.wnl.0000314646.49565.c0CrossRefPubMed

43.

Goit RK, Paudel BH, Khadka R, Roy RK, Shrewastwa MK (2014) Mild-to-moderate intensity exercise improves cardiac autonomic drive-in type 2 diabetes. J Diabetes Investig 5:722–727. https://doi.org/10.1111/jdi.12238CrossRefPubMedPubMedCentral

44.

Gruenwald I, Vardi Y, Gartman I, Juven E, Sprecher E, Yarnitsky D, Miller A (2007) Sexual dysfunction in females with multiple sclerosis: quantitative sensory testing. Mult Scler 13:95–105. https://doi.org/10.1177/1352458506071134CrossRefPubMed

45.

Guadalupe G, Haupts M, Duning T, Hildebrandt H (2023) Heart rate variability and fatigue in MS: two parallel pathways representing disseminated inflammatory processes. Neurol Sci 44:83–98CrossRef

46.

Gulick EE (2011) Bowel management related quality of life in people with multiple sclerosis: psychometric evaluation of the QoL-BM measure. Int J Nurs Stud 48:1066–1070. https://doi.org/10.1016/j.ijnurstu.2011.02.002CrossRefPubMed

47.

Gumus H, Akpinar Z, Yilmaz H (2014) Effects of multiple sclerosis on female sexuality: a controlled study. J Sex Med 11:481–486. https://doi.org/10.1111/jsm.12397CrossRefPubMed

48.

Guo ZN, He SY, Zhang HL, Wu J, Yang Y (2012) Multiple sclerosis and sexual dysfunction. Asian J Androl 14:530–535. https://doi.org/10.1038/aja.2011.110CrossRefPubMedPubMedCentral

49.

Gutrecht JA, Suarez GA, Denny BE (1993) Sympathetic skin response in multiple sclerosis. J Neurol Sci 118:88–91. https://doi.org/10.1016/0022-510X(93)90251-SCrossRefPubMed

50.

Hanken K, Eling P, Hildebrandt H (2014) The representation of inflammatory signals in the brain—a model for subjective fatigue in multiple sclerosis. Front Neurol 5:264. https://doi.org/10.3389/fneur.2014.00264CrossRefPubMedPubMedCentral

51.

Heller L, Keren O, Aloni R, Davidoff G (1992) An open trial of vacuum penile tumescence: constriction therapy for neurological impotence. Paraplegia 30:550–553. https://doi.org/10.1038/sc.1992.113CrossRefPubMed

52.

Hennessey A, Robertson NP, Swingler R, Compston DAS (1999) Urinary, faecal, and sexual dysfunction in patients with multiple sclerosis. J Neurol 246(11):1027–1032CrossRefPubMed

53.

Hirsch IH, Smith RL, Chancellor MB, Bagley DH, Carsello J, Staas WE Jr (1994) Use of intracavernous injection of prostaglandin E1 for neuropathic erectile dysfunction. Paraplegia 32:661–664. https://doi.org/10.1038/sc.1994.106CrossRefPubMed

54.

Hornby A (1978) The MS sufferer in the community. Nurs Times 74(Suppl):130–131

55.

House JG, Stiens SA (1997) Pharmacologically initiated defecation for persons with spinal cord injury: effectiveness of three agents. Arch Phys Med Rehabil 78:1062–1065. https://doi.org/10.1016/S0003-9993(97)90128-3CrossRefPubMed

56.

Illigens BM, Gibbons CH (2009) Sweat testing to evaluate autonomic function. Clin Auton Res 19:79–87. https://doi.org/10.1007/s10286-008-0506-8CrossRefPubMed

57.

Illigens BM, Siepmann T, Roofeh J, Gibbons CH (2013) Laser Doppler imaging in the detection of peripheral neuropathy. Auton Neurosci 177:286–290. https://doi.org/10.1016/j.autneu.2013.06.006CrossRefPubMedPubMedCentral

58.

John EH (2015) Textbook of medical physiology, vol 293, 13th edn. Parisianou, Athens

59.

John EH (2015) Textbook of medical physiology, vol 835, 13th edn. Parisianou, Athens

60.

John EH (2015) Textbook of medical physiology, vol 837, 13th edn. Parisianou, Athens

61.

Joyner MJ, Charkoudian N, Wallin BG (2010) Sympathetic nervous system and blood pressure in humans: individualized patterns of regulation and their implications. Hypertension 56:10–16CrossRefPubMed

62.

Judge SI, Bever CT (2006) Potassium channel blockers in multiple sclerosis: neuronal Kv channels and effects of symptomatic treatment. Pharmacol Ther 111:224–259. https://doi.org/10.1016/j.pharmthera.2005.10.006CrossRefPubMed

63.

Jurić S, Mišmaš A, Mihić N, Barać AM, Habek M (2012) Newly onset sinus bradycardia in the context of multiple sclerosis relapse. Intern Med 51:1121–1124. https://doi.org/10.2169/internalmedicine.51.7139CrossRefPubMed

64.

Kale N, Setty M, Jale A, Osman T (2009) Assessment of autonomic nervous system dysfunction in multiple sclerosis and the association with clinical disability. Neurol Int. https://doi.org/10.4081/ni.2009.e4CrossRefPubMedPubMedCentral

65.

Kanjwal K, Karabin B, Kanjwal Y, Grubb BP (2010) Autonomic dysfunction presents as postural orthostatic tachycardia syndrome in patients with multiple sclerosis. Int J Med Sci 7:62–67. https://doi.org/10.7150/ijms.7.62CrossRefPubMedPubMedCentral

66.

Keller DM, Fadel PJ, Harnsberger MA, Remington GM, Frohman EM, Davis SL (2014) Reduced spontaneous sympathetic nerve activity in multiple sclerosis patients. J Neurol Sci 344:210–214. https://doi.org/10.1016/j.jns.2014.06.053CrossRefPubMedPubMedCentral

67.

Kessler TM, Fowler CJ, Panicker JN (2009) Sexual dysfunction in multiple sclerosis. Expert Rev Neurother 9:341–350. https://doi.org/10.1586/14737175.9.3.341CrossRefPubMed

68.

Krogh K, Christensen P, Sabroe S, Laurberg S (2006) Neurogenic bowel dysfunction score. Spinal Cord 44:625–631. https://doi.org/10.1038/sj.sc.3101887CrossRefPubMed

69.

Ku YT, Montgomery LD, Lee HC, Luna B, Webbon BW (2000) Physiologic and functional responses of MS patients to body cooling. Am J Phys Med Rehabil 79:427–434. https://doi.org/10.1097/00002060-200009000-00004CrossRefPubMed

70.

Khurana R, Setty A (1996) The value of the isometric hand-grip test–studies in various autonomic disorders. Clin Auton Res 6(4):211–218CrossRefPubMed

71.

Lensch E, Jost WH (2011) Autonomic disorders in multiple sclerosis. Autoimmune Dis 2011:803–841. https://doi.org/10.4061/2011/803841CrossRef

72.

Levinthal DJ, Rahman A, Nusrat S, O’Leary M, Heyman R, Bielefeldt K (2013) Adding to the burden: Gastrointestinal symptoms and syndromes in multiple sclerosis. Mult Scler Int 2013:319201. https://doi.org/10.1155/2013/319201CrossRefPubMedPubMedCentral

73.

Lilius HG, Valtonen EJ, Wikstrom J (1976) Sexual problems in patients suffering from multiple sclerosis. Scand J Soc Med 4(1):41–44CrossRefPubMed

74.

Linden D, Diehl RR, Berlit P (1995) Subclinical autonomic disturbances in multiple sclerosis. J Neurol 242:374–378. https://doi.org/10.1007/BF00868392CrossRefPubMed

75.

Linden D, Diehl RR, Kretzschmar A, Berlit P (1997) Autonomic evaluation using standard tests and power spectral analysis in multiple sclerosis. Muscle Nerve 20:809–814. https://doi.org/10.1002/(SICI)1097-4598(199707)20:7%3c809::AID-MUS4%3e3.0.CO;2-BCrossRefPubMed

76.

Litwiller SE, Frohman EM, Zimmern PE (1999) Multiple sclerosis and the urologist. J Urol 161:743–757. https://doi.org/10.1016/S0022-5347(01)61760-9CrossRefPubMed

77.

Lombardi G, Macchiarella A, del Popolo G (2010) Efficacy and safety of tadalafil for erectile dysfunction in patients with multiple sclerosis. J Sex Med 7:2192–2200. https://doi.org/10.1111/j.1743-6109.2010.01797.xCrossRefPubMed

78.

Lombardi G, Nelli F, Celso M, Mencarini M, del Popolo G (2012) Treating erectile dysfunction and central neurological diseases with oral phosphodiesterase type 5 inhibitors. Review of the literature. J Sex Med 9:970–985. https://doi.org/10.1111/j.1743-6109.2011.02615.xCrossRefPubMed

79.

Low PA (2004) Evaluation of sudomotor function. Clin Neurophysiol 115:1506–1513. https://doi.org/10.1016/j.clinph.2004.01.023CrossRefPubMed

80.

Lucio AC, D’Ancona CA, Lopes MH, Perissinotto MC, Damasceno BP (2014) The effect of pelvic floor muscle training alone or in combination with electrostimulation in the treatment of sexual dysfunction in women with multiple sclerosis. Mult Scler 20:1761–1768. https://doi.org/10.1177/1352458514531520CrossRefPubMed

81.

Mahajan ST, Patel PB, Marrie RA (2010) Under treatment of overactive bladder symptoms in patients with multiple sclerosis: an ancillary analysis of the NARCOMS patient registry. J Urol 183:1432–1437. https://doi.org/10.1016/j.juro.2009.12.029CrossRefPubMed

82.

Mahovic D, Lakusic N (2007) Progressive impairment of autonomic control of heart rate in patients with multiple sclerosis. Arch Med Res 38:322–325. https://doi.org/10.1016/j.arcmed.2006.11.009CrossRefPubMed

83.

Marrie RA, Cutter G, Tyry T, Vollmer T, Campagnolo D (2007) Disparities in the management of multiple sclerosis-related bladder symptoms. Neurology 68(23):1971–1978CrossRefPubMed

84.

Mayo ME, Chetner MP (1992) Lower urinary tract dysfunction in multiple sclerosis. Urology 39:67–70. https://doi.org/10.1016/0090-4295(92)90045-XCrossRefPubMed

85.

McDougall AJ, McLeod JG (2003) Autonomic nervous system function in multiple sclerosis. J Neurol Sci 215:79–85. https://doi.org/10.1016/S0022-510X(03)00205-3CrossRefPubMed

86.

Merghati-Khoei E, Qaderi K, Amini L, Korte JE (2013) Sexual problems among women with multiple sclerosis. J Neurol Sci 331:81–85. https://doi.org/10.1016/j.jns.2013.05.014CrossRefPubMedPubMedCentral

87.

Merkelbach S, Dillmann U, Kölmel C, Holz J, Müller M (2001) Cardiovascular autonomic dysregulation and fatigue in multiple sclerosis. Mult Scler 7(5):320–326CrossRefPubMed

88.

Munteis E, Andreu M, Tellez MJ, Mon D, Ois A, Roquer J (2006) Anorectal dysfunction in multiple sclerosis. Mult Scler 12:215–218. https://doi.org/10.1191/135248506ms1254oaCrossRefPubMed

89.

Noronha MJ, Vas CJ, Aziz H (1968) Autonomic dysfunction (sweating responses) in multiple sclerosis. J Neurol Neurosurg Psychiatry 31:19–22. https://doi.org/10.1136/jnnp.31.1.19CrossRefPubMedPubMedCentral

90.

Norton C, Chelvanayagam S (2010) Bowel problems and coping strategies in people with multiple sclerosis. Br J Nurs 19(220):221–226. https://doi.org/10.12968/bjon.2010.19.4.46783CrossRef

91.

Novak P (2011) Quantitative autonomic testing. J Vis Exp 53:e2502. https://doi.org/10.3791/2502CrossRef

92.

Orasanu B, Frasure H, Wyman A, Mahajan ST (2013) Sexual dysfunction in patients with multiple sclerosis. Mult Scler Relat Disord 2:117–123. https://doi.org/10.1016/j.msard.2012.10.005CrossRefPubMed

93.

Pellizzer AM, Straznicky NE, Lim S, Kamen PW, Krum H (1999) Reduced dietary fat intake increases parasympathetic activity in healthy premenopausal women. Clin Exp Pharmacol Physiol 26:656–660. https://doi.org/10.1046/j.1440-1681.1999.03103.xCrossRefPubMed

94.

Pintér A, Cseh D, Sárközi A, Illigens B, Siepmann T (2015) Autonomic dysregulation in multiple sclerosis. Int J Mol Sci 16(8):16920–16952. https://doi.org/10.3390/ijms160816920CrossRefPubMedPubMedCentral

95.

Polak P, Kalinin S, Feinstein D (2011) Locus coeruleus damage and noradrenaline reductions in multiple sclerosis and experimental autoimmune encephalomyelitis. Brain 134:665CrossRefPubMedPubMedCentral

96.

Poser CM, Paty DW, Scheinberg LC, McDonald WI, Ebers GC (1984) The diagnosis of multiple sclerosis. Thieme-Stratton, New York

97.

Poser S, Poser W, Schlaf G (1986) Prognostic indicators in multiple sclerosis. Acta Neurol Scand 74(5):387–392CrossRefPubMed

98.

Preziosi G, Raptis DA, Raeburn A, Thiruppathy K, Panicker J, Emmanuel A (2013) Gut dysfunction in patients with multiple sclerosis and the role of spinal cord involvement in the disease. Eur J Gastroenterol Hepatol 25:1044–1050. https://doi.org/10.1097/MEG.0b013e328361eaf8CrossRefPubMedPubMedCentral

99.

Preziosi G, Gordon-Dixon A, Emmanuel A (2018) Neurogenic bowel dysfunction in patients with multiple sclerosis: prevalence, impact, and management strategies. Degener Neurol Neuromuscul Dis. 8:79–90. https://doi.org/10.2147/DNND.S138835. (Published online 2018 Dec 6)CrossRefPubMedPubMedCentral

100.

Racosta JM, Kimpinski K, Morrow SA, Kremenchutzky M (2015) Autonomic dysfunction in multiple sclerosis. Auton Neurosci 193:1–6. https://doi.org/10.1016/j.autneu.2015.06.001CrossRefPubMed

101.

Rockwood TH, Church JM, Fleshman JW, Kane RL, Mavrantonis C, Thorson AG, Wexner SD, Bliss D, Lowry AC (1999) Patient and surgeon ranking of the severity of symptoms associated with fecal incontinence: the fecal incontinence severity index. Dis Colon Rectum 42:1525–1532. https://doi.org/10.1007/BF02236199CrossRefPubMed

102.

Rosman AS, Chaparala G, Monga A, Spungen AM, Bauman WA, Korsten MA (2008) Intramuscular neostigmine and glycopyrrolate safely accelerated bowel evacuation in patients with spinal cord injury and defecatory disorders. Dig Dis Sci 53:2710–2713. https://doi.org/10.1007/s10620-008-0216-zCrossRefPubMed

103.

Saari A, Tolonen U, Pääkkö E, Suominen K, Pyhtinen J, Sotaniemi K, Myllylä V (2004) Cardiovascular autonomic dysfunction correlates with brain MRI lesion load in MS. Clin Neurophysiol 115:1473–1478. https://doi.org/10.1016/j.clinph.2004.01.012CrossRefPubMed

104.

Saari A, Tolonen U, Pääkkö E, Suominen K, Pyhtinen J, Sotaniemi KA, Jauhiainen J, Myllylä VV (2008) Sympathetic skin responses in multiple sclerosis. Acta Neurol Scand 118:226–231. https://doi.org/10.1111/j.1600-0404.2008.01003.xCrossRefPubMed

105.

Saari A, Tolonen U, Pääkkö E, Suominen K, Jauhiainen J, Sotaniemi KA, Myllylä VV (2009) Sweating impairment in patients with multiple sclerosis. Acta Neurol Scand 120:358–363. https://doi.org/10.1111/j.1600-0404.2009.01164.xCrossRefPubMed

106.

Saari A, Tolonen U, Pääkkö E, Suominen K, Jauhiainen J, Sotaniemi KA, Myllylä VV (2010) Sudomotor dysfunction in patients with optic neuritis. Clin Auton Res 20:199–204. https://doi.org/10.1007/s10286-009-0052-zCrossRefPubMed

107.

Sander C, Hildebrandt H, Schlake HP, Eling P, Hanken K (2017) Subjective cognitive fatigue and autonomic abnormalities in multiple sclerosis patients. Front Neurol. https://doi.org/10.3389/fneur.2017.00475CrossRefPubMedPubMedCentral

108.

Sanders AS, Foley FW, LaRocca GL, Zemon V (2000) The multiple sclerosis intimacy and sexuality questionnaire-19 (MSISQ-19) Sex. Disabil 18:3–26. https://doi.org/10.1023/A:1005421627154CrossRef

109.

Sanya EO, Tutaj M, Brown CM, Goel N, Neundörfer B, Hilz MJ (2005) Abnormal heart rate and blood pressure responses to baroreflex stimulation in multiple sclerosis patients. Clin Auton Res 15:213–218. https://doi.org/10.1007/s10286-005-0274-7CrossRefPubMed

110.

Safarinejad MR (2008) Evaluation of endocrine profile, hypothalamic-pituitary-testis axis, and semen quality in multiple sclerosis. J Neuroendocrinol 20:1368–1375. https://doi.org/10.1111/j.1365-2826.2008.01791.xCrossRefPubMed

111.

Schroth WS, Tenner SM, Rappaport BA, Mani R (1992) Multiple sclerosis as a cause of atrial fibrillation and electrocardiographic changes. Arch Neurol 49:422–424. https://doi.org/10.1001/archneur.1992.00530280116034CrossRefPubMed

112.

Shy M, Frohman E, So Y, Arezzo J, Cornblath D, Giuliani M, Kincaid J, Ochoa J, Parry G, Weimer L (2003) Quantitative sensory testing: report of the Therapeutics and Technology Assessment Subcommittee of the American Academy of Neurology. Neurology 60(6):898–904CrossRefPubMed

113.

Siepmann T, Ziemssen T, Mueck-Weymann M, Kirch W, Siepmann M (2007) The effects of venlafaxine on autonomic functions in healthy volunteers. J Clin Psychopharmacol 27:687–691. https://doi.org/10.1097/jcp.0b013e31815a255bCrossRefPubMed

114.

Siepmann T, Gibbons CH, Illigens BM, Lafo JA, Brown CM, Freeman R (2012) Quantitative pilomotor axon reflex test: a novel test of pilomotor function. Arch Neurol 69:1488–1492. https://doi.org/10.1001/archneurol.2012.1092CrossRefPubMedPubMedCentral

115.

Sirbu CA, Mezei RM, Falup-Pecurariu C et al (2020) Autonomic dysfunctions in multiple sclerosis: challenges of clinical practice (Review). Exp Ther Med 20(6):196. https://doi.org/10.3892/etm.2020.9326CrossRefPubMedPubMedCentral

116.

Skorić MK, Crnošija L, Gabelić T, Barun B, Adamec I, Junaković A, Pavičić T, Ruška B, Habek M (2019) Autonomic symptom burden can predict disease activity in early multiple sclerosis. Mult Scler Relat Disord 28:250–255. https://doi.org/10.1016/j.msard.2019.01.005CrossRef

117.

Soler JM, Previnaire JG, Plante P, Denys P, Chartier-Kastler E (2007) Midodrine improves ejaculation in spinal cord-injured men. J Urol 178:2082–2086. https://doi.org/10.1016/j.juro.2007.07.047CrossRefPubMed

118.

Spinu D, Bratu O, Marcu D, Mischianu D, Huica R, Surcel M, Munteanu A, Socea B, Bodean O, Ursaciuc C (2018) The use of ELISA and PCR in identifying correlations between viral infections and benign prostatic hypertrophy. Rev Chim 69:645–649CrossRef

119.

Staerman F, Guiraud P, Coeurdacier P, Menard D, Edan G, Lobel B (1996) Value of nocturnal penile tumescence and rigidity (NPTR) recording in impotent patients with multiple sclerosis. Int J Impot Res 8:241–245PubMed

120.

Sternberg Z (2015) Promoting sympathovagal balance in multiple sclerosis; pharmacological, non-pharmacological, and surgical strategies. Autoimmun Rev. https://doi.org/10.1016/j.autrev.2015.04.012CrossRefPubMed

121.

Stohrer M, Blok B, Castro-Diaz D, Chartier-Kastler E, Del Popolo G, Kramer G, Pannek J, Radziszewski P, Wyndaele JJ (2009) EAU guidelines on neurogenic lower urinary tract dysfunction. Eur Urol 56:81–88. https://doi.org/10.1016/j.eururo.2009.04.028CrossRefPubMed

122.

Swash M, Snooks SJ, Chalmers DH (1987) Parity as a factor in incontinence in multiple sclerosis. Arch Neurol 44:504–508. https://doi.org/10.1001/archneur.1987.00520170034018CrossRefPubMed

123.

Tepavcevic DK, Kostic J, Basuroski ID, Stojsavljevic N, Pekmezovic T, Drulovic J (2008) The impact of sexual dysfunction on the quality of life measured by MSQoL-54 in patients with multiple sclerosis. Mult Scler 14:1131–1136. https://doi.org/10.1177/1352458508093619CrossRefPubMed

124.

Tornic J, Panicker J (2018) The management of lower urinary tract dysfunction in multiple sclerosis. Curr Neurol Neurosci Rep 18(8):54CrossRefPubMedPubMedCentral

125.

Vieira B, Costa A, Videira G, Sa MJ, Abreu P (2015) Prevalence of autonomic dysfunction in patients with multiple sclerosis. Acta Med Port 28:51–55CrossRefPubMed

126.

Vita G, Fazio MC, Milone S, Blandino A, Salvi L, Messina C (1993) Cardiovascular autonomic dysfunction in multiple sclerosis is likely related to brainstem lesions. J Neurol Sci 120:82–86. https://doi.org/10.1016/0022-510X(93)90029-XCrossRefPubMed

127.

White AT, VanHaitsma TA, Vener J, Davis SL (2013) Effect of passive whole-body heating on central conduction and cortical excitability in multiple sclerosis patients and healthy controls. J Appl Physiol 1985(114):1697–1704. https://doi.org/10.1152/japplphysiol.01119.2012CrossRef

128.

Wiesel PH, Norton C, Glickman S, Kamm MA (2001) Pathophysiology and management of bowel dysfunction in multiple sclerosis. Eur J Gastroenterol Hepatol 13:441–448. https://doi.org/10.1097/00042737-200104000-00025CrossRefPubMed

129.

Zangaglia R, Martignoni E, Glorioso M, Ossola M, Riboldazzi G, Calandrella D, Brunetti G, Pacchetti C (2007) Macrogol for the treatment of constipation in Parkinson’s disease. A randomized placebo-controlled study. Mon Disord 22:1239–1244. https://doi.org/10.1002/mds.21243CrossRef

130.

Zemishlany Z, Weizman A (2008) The impact of mental illness on sexual dysfunction. Adv Psychosom Med 29:89–106CrossRefPubMed

131.

Zivadinov R, Zorzon M, Bosco A, Bragadin LM, Moretti R, Bonfigli L, Iona LG, Cazzato G (1999) Sexual dysfunction in multiple sclerosis: II. Correlation analysis. Mult Scler 5:428–431. https://doi.org/10.1191/135245899678846465CrossRefPubMed

132.

Zorzon M, Zivadinov R, Bragadin LM, Moretti R, de Masi R, Nasuelli D, Cazzato G (2001) Sexual dysfunction in multiple sclerosis: a 2-year follow-up study. J Neurol Sci 187:1–5. https://doi.org/10.1016/S0022-510X(01)00493-2CrossRefPubMed

133.

Zorzon M, Zivadinov R, Locatelli L, Stival B, Nasuelli D, Bratina A, Bosco A, Tommasi MA, PozziMucelli RS, Ukmar M et al (2003) Correlation of sexual dysfunction and brain magnetic resonance imaging in multiple sclerosis. Mult Scler 9:108–110. https://doi.org/10.1191/1352458503ms881srCrossRefPubMed

Title: Autonomic nervous system disorders in multiple sclerosis
Authors: Effrosyni Koutsouraki
Koukoulidis Theodoros
Georgiadou Eleni
Kalampouka Marianna
Nikolaidou Areti
Koukoulidou Ariadni
Michmizos Dimitrios
Publication date: 21-04-2023
Publisher: Springer Berlin Heidelberg
Keywords: Multiple Sclerosis
Fatigue
Published in: Journal of Neurology / Issue 8/2023
Print ISSN: 0340-5354
Electronic ISSN: 1432-1459
DOI: https://doi.org/10.1007/s00415-023-11725-y

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Autonomic nervous system disorders in multiple sclerosis

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 8/2023

Long-term efficacy and safety of ravulizumab in adults with anti-acetylcholine receptor antibody-positive generalized myasthenia gravis: results from the phase 3 CHAMPION MG open-label extension

Myelin oligodendrocyte glycoprotein antibody-associated disease (MOGAD): current understanding and challenges

Duchenne muscular dystrophy: pathogenesis and promising therapies

Recent advances in novel mutation genes of Parkinson's disease

Large diameter hemicraniectomy does not improve long-term outcome in malignant infarction

Antiplatelet therapy may improve the prognosis of patients with moyamoya disease: a 12-year retrospective study