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08.04.2019 | Review Article

Immune and autonomic nervous system interactions in multiple sclerosis: clinical implications

verfasst von: Mario Habek

Erschienen in: Clinical Autonomic Research | Ausgabe 3/2019

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Abstract

Multiple sclerosis is characterized by a wide spectrum of clinical manifestations, among which dysfunction of the autonomic nervous system represents an important cause of multiple sclerosis-related disability. The aim of this review is to provide an overview of autonomic dysfunction in people with multiple sclerosis, and to discuss the interactions between the immune and autonomic nervous systems and the effects of these interactions on various aspects of multiple sclerosis. Autonomic dysfunction in people with multiple sclerosis can be demonstrated clinically and on a molecular level. Clinically, it can be demonstrated by measuring autonomic symptoms with the Composite Autonomic Symptom Score (COMPASS-31), and neurophysiologically, with different autonomic nervous system tests. Both symptomatic and objectively determined autonomic dysfunction can be associated with increased risk of multiple sclerosis disease activity. Further supporting these clinical observations are molecular changes in immune cells. Changes in the sympathetic autonomic system, such as different expression of dopaminergic and adrenergic receptors on immune cells, or modulation of the cholinergic anti-inflammatory pathway over different subunits of the nicotinic acetylcholine receptor in the peripheral immune system, may mediate different effects on multiple sclerosis disease activity.
Literatur
2.
Zurück zum Zitat Adamec I, Habek M (2013) Autonomic dysfunction in multiple sclerosis. Clin Neurol Neurosurg 115(Suppl 1):S73–S78CrossRefPubMed Adamec I, Habek M (2013) Autonomic dysfunction in multiple sclerosis. Clin Neurol Neurosurg 115(Suppl 1):S73–S78CrossRefPubMed
3.
Zurück zum Zitat Racosta JM, Kimpinski K (2016) Autonomic dysfunction, immune regulation, and multiple sclerosis. Clin Auton Res 26:23–31CrossRefPubMed Racosta JM, Kimpinski K (2016) Autonomic dysfunction, immune regulation, and multiple sclerosis. Clin Auton Res 26:23–31CrossRefPubMed
4.
Zurück zum Zitat Suarez GA, Opfer-Gehrking TL, Offord KP, Atkinson EJ, O’Brien PC, Low PA (1999) The autonomic symptom profile: a new instrument to assess autonomic symptoms. Neurology 52:523–528CrossRefPubMed Suarez GA, Opfer-Gehrking TL, Offord KP, Atkinson EJ, O’Brien PC, Low PA (1999) The autonomic symptom profile: a new instrument to assess autonomic symptoms. Neurology 52:523–528CrossRefPubMed
5.
Zurück zum Zitat Sletten DM, Suarez GA, Low PA, Mandrekar J, Singer W (2012) COMPASS 31: a refined and abbreviated composite autonomic symptom score. Mayo Clin Proc 87:1196–1201CrossRefPubMedPubMedCentral Sletten DM, Suarez GA, Low PA, Mandrekar J, Singer W (2012) COMPASS 31: a refined and abbreviated composite autonomic symptom score. Mayo Clin Proc 87:1196–1201CrossRefPubMedPubMedCentral
6.
Zurück zum Zitat Drulović J, Gavrilović A, Crnošija L, Kisić-Tepavčević D, Krbot Skorić M, Ivanović J, Adamec I, Dujmović I, Junaković A, Marić G, Martinović V, Pekmezović T, Habek M (2017) Validation and cross-cultural adaptation of the COMPASS-31 in croatian and serbian patients with multiple sclerosis. Croat Med J 58:342–348CrossRefPubMed Drulović J, Gavrilović A, Crnošija L, Kisić-Tepavčević D, Krbot Skorić M, Ivanović J, Adamec I, Dujmović I, Junaković A, Marić G, Martinović V, Pekmezović T, Habek M (2017) Validation and cross-cultural adaptation of the COMPASS-31 in croatian and serbian patients with multiple sclerosis. Croat Med J 58:342–348CrossRefPubMed
7.
Zurück zum Zitat Vieira B, Costa A, Videira G, Sá MJ, Abreu P (2015) Prevalence of autonomic dysfunction in patients with multiple sclerosis. Acta Med Port 28:51–55CrossRefPubMed Vieira B, Costa A, Videira G, Sá MJ, Abreu P (2015) Prevalence of autonomic dysfunction in patients with multiple sclerosis. Acta Med Port 28:51–55CrossRefPubMed
8.
Zurück zum Zitat Cortez MM, Nagi Reddy SK, Goodman B, Carter JL, Wingerchuk DM (2015) Autonomic symptom burden is associated with MS-related fatigue and quality of life. Mult Scler Relat Disord 4:258–263CrossRefPubMed Cortez MM, Nagi Reddy SK, Goodman B, Carter JL, Wingerchuk DM (2015) Autonomic symptom burden is associated with MS-related fatigue and quality of life. Mult Scler Relat Disord 4:258–263CrossRefPubMed
9.
Zurück zum Zitat Ruška B, Pavičić T, Pavlović I, Junaković A, Adamec I, Crnošija L, Krbot Skorić M, Habek M (2018) Performance of the COMPASS-31 questionnaire with regard to autonomic nervous system testing results and medication use: a prospective study in a real-life setting. Neurol Sci 39:2079–2084CrossRefPubMed Ruška B, Pavičić T, Pavlović I, Junaković A, Adamec I, Crnošija L, Krbot Skorić M, Habek M (2018) Performance of the COMPASS-31 questionnaire with regard to autonomic nervous system testing results and medication use: a prospective study in a real-life setting. Neurol Sci 39:2079–2084CrossRefPubMed
10.
Zurück zum Zitat Acevedo AR, Nava C, Arriada N, Violante A, Corona T (2000) Cardiovascular dysfunction in multiple sclerosis. Acta Neurol Scand 101:85–88CrossRefPubMed Acevedo AR, Nava C, Arriada N, Violante A, Corona T (2000) Cardiovascular dysfunction in multiple sclerosis. Acta Neurol Scand 101:85–88CrossRefPubMed
11.
Zurück zum Zitat de Seze J, Stojkovic T, Gauvrit JY, Devos D, Ayachi M, Cassim F, Saint Michel T, Pruvo JP, Guieu JD, Vermersch P (2001) Autonomic dysfunction in multiple sclerosis: cervical spinal cord atrophy correlates. J Neurol 248:297–303CrossRefPubMed de Seze J, Stojkovic T, Gauvrit JY, Devos D, Ayachi M, Cassim F, Saint Michel T, Pruvo JP, Guieu JD, Vermersch P (2001) Autonomic dysfunction in multiple sclerosis: cervical spinal cord atrophy correlates. J Neurol 248:297–303CrossRefPubMed
12.
Zurück zum Zitat Flachenecker P, Wolf A, Krauser M, Hartung HP, Reiners K (1999) Cardiovascular autonomic dysfunction in multiple sclerosis: correlation with orthostatic intolerance. J Neurol 246:578–586CrossRefPubMed Flachenecker P, Wolf A, Krauser M, Hartung HP, Reiners K (1999) Cardiovascular autonomic dysfunction in multiple sclerosis: correlation with orthostatic intolerance. J Neurol 246:578–586CrossRefPubMed
13.
Zurück zum Zitat Low PA (1993) Composite autonomic scoring scale for laboratory quantification of generalized autonomic failure. Mayo Clin Proc 68:748–752CrossRefPubMed Low PA (1993) Composite autonomic scoring scale for laboratory quantification of generalized autonomic failure. Mayo Clin Proc 68:748–752CrossRefPubMed
14.
Zurück zum Zitat Habek M, Crnošija L, Lovrić M, Junaković A, Krbot Skorić M, Adamec I (2016) Sympathetic cardiovascular and sudomotor functions are frequently affected in early multiple sclerosis. Clin Auton Res 26:385–393CrossRefPubMed Habek M, Crnošija L, Lovrić M, Junaković A, Krbot Skorić M, Adamec I (2016) Sympathetic cardiovascular and sudomotor functions are frequently affected in early multiple sclerosis. Clin Auton Res 26:385–393CrossRefPubMed
15.
Zurück zum Zitat Adamec I, Crnošija L, Junaković A, Krbot Skorić M, Habek M (2018) Progressive multiple sclerosis patients have a higher burden of autonomic dysfunction compared to relapsing remitting phenotype. Clin Neurophysiol 129:1588–1594CrossRefPubMed Adamec I, Crnošija L, Junaković A, Krbot Skorić M, Habek M (2018) Progressive multiple sclerosis patients have a higher burden of autonomic dysfunction compared to relapsing remitting phenotype. Clin Neurophysiol 129:1588–1594CrossRefPubMed
16.
Zurück zum Zitat Arbogast SD, Alshekhlee A, Hussain Z, McNeeley K, Chelimsky TC (2009) Hypotension unawareness in profound orthostatic hypotension. Am J Med 122:574–580CrossRefPubMed Arbogast SD, Alshekhlee A, Hussain Z, McNeeley K, Chelimsky TC (2009) Hypotension unawareness in profound orthostatic hypotension. Am J Med 122:574–580CrossRefPubMed
17.
Zurück zum Zitat 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 120:82–86CrossRefPubMed 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 120:82–86CrossRefPubMed
18.
Zurück zum Zitat Illigens BM, Gibbons CH (2009) Sweat testing to evaluate autonomic function. Clin Auton Res 19:79–87CrossRefPubMed Illigens BM, Gibbons CH (2009) Sweat testing to evaluate autonomic function. Clin Auton Res 19:79–87CrossRefPubMed
19.
Zurück zum Zitat Davis SL, Wilson TE, Vener JM, Crandall CG, Petajan JH, White AT (1985) Pilocarpine-induced sweat gland function in individuals with multiple sclerosis. J Appl Physiol 2005(98):1740–1744 Davis SL, Wilson TE, Vener JM, Crandall CG, Petajan JH, White AT (1985) Pilocarpine-induced sweat gland function in individuals with multiple sclerosis. J Appl Physiol 2005(98):1740–1744
20.
Zurück zum Zitat 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 115:1473–1478CrossRefPubMed 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 115:1473–1478CrossRefPubMed
21.
Zurück zum Zitat Nasseri K, TenVoorde BJ, Adèr HJ, Uitdehaag BM, Polman CH (1998) Longitudinal follow-up of cardiovascular reflex tests in multiple sclerosis. J Neurol Sci 155:50–54CrossRefPubMed Nasseri K, TenVoorde BJ, Adèr HJ, Uitdehaag BM, Polman CH (1998) Longitudinal follow-up of cardiovascular reflex tests in multiple sclerosis. J Neurol Sci 155:50–54CrossRefPubMed
22.
Zurück zum Zitat Nasseri K, Uitdehaag BM, van Walderveen MA, Ader HJ, Polman CH (1999) Cardiovascular autonomic function in patients with relapsing remitting multiple sclerosis: a new surrogate marker of disease evolution? Eur J Neurol 6:29–33CrossRefPubMed Nasseri K, Uitdehaag BM, van Walderveen MA, Ader HJ, Polman CH (1999) Cardiovascular autonomic function in patients with relapsing remitting multiple sclerosis: a new surrogate marker of disease evolution? Eur J Neurol 6:29–33CrossRefPubMed
23.
Zurück zum Zitat Flachenecker P, Reiners K, Krauser M, Wolf A, Toyka KV (2001) Autonomic dysfunction in multiple sclerosis is related to disease activity and progression of disability. Mult Scler 7:327–334CrossRefPubMed Flachenecker P, Reiners K, Krauser M, Wolf A, Toyka KV (2001) Autonomic dysfunction in multiple sclerosis is related to disease activity and progression of disability. Mult Scler 7:327–334CrossRefPubMed
24.
Zurück zum Zitat Habek M, Krbot Skorić M, Crnošija L, Gabelić T, Barun B, Adamec I (2017) Postural orthostatic tachycardia predicts early conversion to multiple sclerosis after clinically isolated syndrome. Eur Neurol 77:253–257CrossRefPubMed Habek M, Krbot Skorić M, Crnošija L, Gabelić T, Barun B, Adamec I (2017) Postural orthostatic tachycardia predicts early conversion to multiple sclerosis after clinically isolated syndrome. Eur Neurol 77:253–257CrossRefPubMed
25.
Zurück zum Zitat Krbot Skorić M, 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 28:250–255CrossRefPubMed Krbot Skorić M, 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 28:250–255CrossRefPubMed
26.
Zurück zum Zitat Disanto G, Zecca C, MacLachlan S, Sacco R, Handunnetthi L, Meier UC, Simpson A, McDonald L, Rossi A, Benkert P, Kuhle J, Ramagopalan SV, Gobbi C (2018) Prodromal symptoms of multiple sclerosis in primary care. Ann Neurol 83:1162–1173CrossRefPubMed Disanto G, Zecca C, MacLachlan S, Sacco R, Handunnetthi L, Meier UC, Simpson A, McDonald L, Rossi A, Benkert P, Kuhle J, Ramagopalan SV, Gobbi C (2018) Prodromal symptoms of multiple sclerosis in primary care. Ann Neurol 83:1162–1173CrossRefPubMed
27.
Zurück zum Zitat Marrie RA, Reider N, Cohen J, Stuve O, Trojano M, Cutter G, Reingold S, Sorensen PS (2015) A systematic review of the incidence and prevalence of cardiac, cerebrovascular, and peripheral vascular disease in multiple sclerosis. Mult Scler 21:318–331CrossRefPubMedPubMedCentral Marrie RA, Reider N, Cohen J, Stuve O, Trojano M, Cutter G, Reingold S, Sorensen PS (2015) A systematic review of the incidence and prevalence of cardiac, cerebrovascular, and peripheral vascular disease in multiple sclerosis. Mult Scler 21:318–331CrossRefPubMedPubMedCentral
28.
Zurück zum Zitat Christiansen CF, Christensen S, Farkas DK, Miret M, Sørensen HT, Pedersen L (2010) Risk of arterial cardiovascular diseases in patients with multiple sclerosis: a population-based cohort study. Neuroepidemiology 35:267–274CrossRefPubMed Christiansen CF, Christensen S, Farkas DK, Miret M, Sørensen HT, Pedersen L (2010) Risk of arterial cardiovascular diseases in patients with multiple sclerosis: a population-based cohort study. Neuroepidemiology 35:267–274CrossRefPubMed
30.
Zurück zum Zitat Grassi G, Seravalle G, Brambilla G, Pini C, Alimento M, Facchetti R, Spaziani D, Cuspidi C, Mancia G (2014) Marked sympathetic activation and baroreflex dysfunction in true resistant hypertension. Int J Cardiol 177:1020–1025CrossRefPubMed Grassi G, Seravalle G, Brambilla G, Pini C, Alimento M, Facchetti R, Spaziani D, Cuspidi C, Mancia G (2014) Marked sympathetic activation and baroreflex dysfunction in true resistant hypertension. Int J Cardiol 177:1020–1025CrossRefPubMed
31.
32.
Zurück zum Zitat Mutani R, Clemente S, Lamberti A, Monaco F (1982) Assessment of autonomic disturbances in multiple sclerosis by measurement of heart rate responses to deep breathing and to standing. Ital J Neurol Sci 3:111–114CrossRefPubMed Mutani R, Clemente S, Lamberti A, Monaco F (1982) Assessment of autonomic disturbances in multiple sclerosis by measurement of heart rate responses to deep breathing and to standing. Ital J Neurol Sci 3:111–114CrossRefPubMed
33.
Zurück zum Zitat Senaratne MP, Carroll D, Warren KG, Kappagoda T (1984) Evidence for cardiovascular autonomic nerve dysfunction in multiple sclerosis. J Neurol Neurosurg Psychiatry 47:947–952CrossRefPubMedPubMedCentral Senaratne MP, Carroll D, Warren KG, Kappagoda T (1984) Evidence for cardiovascular autonomic nerve dysfunction in multiple sclerosis. J Neurol Neurosurg Psychiatry 47:947–952CrossRefPubMedPubMedCentral
34.
Zurück zum Zitat Pentland B, Ewing DJ (1987) Cardiovascular reflexes in multiple sclerosis. Eur Neurol 26:46–50CrossRefPubMed Pentland B, Ewing DJ (1987) Cardiovascular reflexes in multiple sclerosis. Eur Neurol 26:46–50CrossRefPubMed
35.
Zurück zum Zitat Yokota T, Matsunaga T, Okiyama R, Hirose K, Tanabe H, Furukawa T, Tsukagoshi H (1991) Sympathetic skin response in patients with multiple sclerosis compared with patients with spinal cord transection and normal controls. Brain 114:1381–1394CrossRefPubMed Yokota T, Matsunaga T, Okiyama R, Hirose K, Tanabe H, Furukawa T, Tsukagoshi H (1991) Sympathetic skin response in patients with multiple sclerosis compared with patients with spinal cord transection and normal controls. Brain 114:1381–1394CrossRefPubMed
36.
Zurück zum Zitat Anema JR, Heijenbrok MW, Faes TJ, Heimans JJ, Lanting P, Polman CH (1991) Cardiovascular autonomic function in multiple sclerosis. J Neurol Sci 104:129–134CrossRefPubMed Anema JR, Heijenbrok MW, Faes TJ, Heimans JJ, Lanting P, Polman CH (1991) Cardiovascular autonomic function in multiple sclerosis. J Neurol Sci 104:129–134CrossRefPubMed
37.
Zurück zum Zitat Thomaides TN, Zoukos Y, Chaudhuri KR, Mathias CJ (1993) Physiological assessment of aspects of autonomic function in patients with secondary progressive multiple sclerosis. J Neurol 240:139–143CrossRefPubMed Thomaides TN, Zoukos Y, Chaudhuri KR, Mathias CJ (1993) Physiological assessment of aspects of autonomic function in patients with secondary progressive multiple sclerosis. J Neurol 240:139–143CrossRefPubMed
38.
Zurück zum Zitat Gutrecht JA, Suarez GA, Denny BE (1993) Sympathetic skin response in multiple sclerosis. J Neurol Sci 118:88–91CrossRefPubMed Gutrecht JA, Suarez GA, Denny BE (1993) Sympathetic skin response in multiple sclerosis. J Neurol Sci 118:88–91CrossRefPubMed
39.
Zurück zum Zitat Elie B, Louboutin JP (1995) Sympathetic skin response (SSR) is abnormal in multiple sclerosis. Muscle Nerve 18(2):185–189CrossRefPubMed Elie B, Louboutin JP (1995) Sympathetic skin response (SSR) is abnormal in multiple sclerosis. Muscle Nerve 18(2):185–189CrossRefPubMed
40.
Zurück zum Zitat Linden D, Diehl RR, Berlit P (1995) Subclinical autonomic disturbances in multiple sclerosis. J Neurol 242:374–378CrossRefPubMed Linden D, Diehl RR, Berlit P (1995) Subclinical autonomic disturbances in multiple sclerosis. J Neurol 242:374–378CrossRefPubMed
41.
Zurück zum Zitat Caminero AB, Pérez-Jiménez A, Barreiro P, Ferrer T (1995) Sympathetic skin response: correlation with autonomic and somatic involvement in multiple sclerosis. Electromyogr Clin Neurophysiol 35:457–462PubMed Caminero AB, Pérez-Jiménez A, Barreiro P, Ferrer T (1995) Sympathetic skin response: correlation with autonomic and somatic involvement in multiple sclerosis. Electromyogr Clin Neurophysiol 35:457–462PubMed
42.
Zurück zum Zitat Linden D, Diehl RR, Kretzschmar A, Berlit P (1997) Autonomic evaluation by means of standard tests and power spectral analysis in multiple sclerosis. Muscle Nerve 20:809–814CrossRefPubMed Linden D, Diehl RR, Kretzschmar A, Berlit P (1997) Autonomic evaluation by means of standard tests and power spectral analysis in multiple sclerosis. Muscle Nerve 20:809–814CrossRefPubMed
43.
Zurück zum Zitat Merkelbach S, Dillmann U, Kölmel C, Holz I, Muller M (2001) Cardiovascular autonomic dysregulation and fatigue in multiple sclerosis. Mult Scler 7:320–326CrossRefPubMed Merkelbach S, Dillmann U, Kölmel C, Holz I, Muller M (2001) Cardiovascular autonomic dysregulation and fatigue in multiple sclerosis. Mult Scler 7:320–326CrossRefPubMed
44.
Zurück zum Zitat Gunal DI, Afsar N, Tanridag T, Aktan S (2002) Autonomic dysfunction in multiple sclerosis: correlation with disease-related parameters. Eur Neurol 48:1–5CrossRefPubMed Gunal DI, Afsar N, Tanridag T, Aktan S (2002) Autonomic dysfunction in multiple sclerosis: correlation with disease-related parameters. Eur Neurol 48:1–5CrossRefPubMed
45.
Zurück zum Zitat McDougall AJ, McLeod JG (2003) Autonomic nervous system function in multiple sclerosis. J Neurol Sci 215(1–2):79–85CrossRefPubMed McDougall AJ, McLeod JG (2003) Autonomic nervous system function in multiple sclerosis. J Neurol Sci 215(1–2):79–85CrossRefPubMed
46.
Zurück zum Zitat Labuz-Roszak B, Pierzchala K (2007) Difficulties in the diagnosis of autonomic dysfunction in multiple sclerosis. Clin Auton Res 17:375–377CrossRefPubMed Labuz-Roszak B, Pierzchala K (2007) Difficulties in the diagnosis of autonomic dysfunction in multiple sclerosis. Clin Auton Res 17:375–377CrossRefPubMed
47.
Zurück zum Zitat Lorberboym M, Lampl Y, Nikolov G, Sadeh M, Gilad R (2008) I-123 MIBG cardiac scintigraphy and autonomic test evaluation in multiple sclerosis patients. J Neurol 255:211–216CrossRefPubMed Lorberboym M, Lampl Y, Nikolov G, Sadeh M, Gilad R (2008) I-123 MIBG cardiac scintigraphy and autonomic test evaluation in multiple sclerosis patients. J Neurol 255:211–216CrossRefPubMed
48.
Zurück zum Zitat 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 118:226–231CrossRefPubMed 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 118:226–231CrossRefPubMed
49.
Zurück zum Zitat Hale LA, Nukada H, Du Plessis LJ, Peebles KC (2009) Clinical screening of autonomic dysfunction in multiple sclerosis. Physiother Res Int 14:42–55CrossRefPubMed Hale LA, Nukada H, Du Plessis LJ, Peebles KC (2009) Clinical screening of autonomic dysfunction in multiple sclerosis. Physiother Res Int 14:42–55CrossRefPubMed
50.
Zurück zum Zitat Aghamollaii V, Harirchian MH, Modabbernia A, Ghaffarpour M, Mousavi M, Tafakhori A (2011) Sympathetic skin response (SSR) in multiple sclerosis and clinically isolated syndrome: a case-control study. Neurophysiol Clin 41:161–171CrossRefPubMed Aghamollaii V, Harirchian MH, Modabbernia A, Ghaffarpour M, Mousavi M, Tafakhori A (2011) Sympathetic skin response (SSR) in multiple sclerosis and clinically isolated syndrome: a case-control study. Neurophysiol Clin 41:161–171CrossRefPubMed
51.
Zurück zum Zitat 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 324:80–83CrossRefPubMed 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 324:80–83CrossRefPubMed
52.
Zurück zum Zitat Crnošija L, Adamec I, Lovrić M, Junaković A, Krbot Skorić M, Lušić I, Habek M (2016) Autonomic dysfunction in clinically isolated syndrome suggestive of multiple sclerosis. Clin Neurophysiol 127:864–869CrossRefPubMed Crnošija L, Adamec I, Lovrić M, Junaković A, Krbot Skorić M, Lušić I, Habek M (2016) Autonomic dysfunction in clinically isolated syndrome suggestive of multiple sclerosis. Clin Neurophysiol 127:864–869CrossRefPubMed
54.
55.
Zurück zum Zitat Cosentino M, Zaffaroni M, Ferrari M, Marino F, Bombelli R, Rasini E, Frigo G, Ghezzi A, Comi G, Lecchini S (2005) Interferon-gamma and interferon-beta affect endogenous catecholamines in human peripheral blood mononuclear cells: implications for multiple sclerosis. J Neuroimmunol 162:112–121CrossRefPubMed Cosentino M, Zaffaroni M, Ferrari M, Marino F, Bombelli R, Rasini E, Frigo G, Ghezzi A, Comi G, Lecchini S (2005) Interferon-gamma and interferon-beta affect endogenous catecholamines in human peripheral blood mononuclear cells: implications for multiple sclerosis. J Neuroimmunol 162:112–121CrossRefPubMed
56.
Zurück zum Zitat Karaszewski JW, Reder AT, Anlar B, Arnason GW (1993) Increased high affinity beta-adrenergic receptor densities and cyclic AMP responses of CD8 cells in multiple sclerosis. J Neuroimmunol 43:1–7CrossRefPubMed Karaszewski JW, Reder AT, Anlar B, Arnason GW (1993) Increased high affinity beta-adrenergic receptor densities and cyclic AMP responses of CD8 cells in multiple sclerosis. J Neuroimmunol 43:1–7CrossRefPubMed
57.
Zurück zum Zitat Zoukos Y, Thomaides TN, Kidd D, Cuzner ML, Thompson A (2003) Expression of beta 2 adrenoreceptors on peripheral blood mononuclear cells in patients with primary and secondary progressive multiple sclerosis: a longitudinal 6 month study. J Neurol Neurosurg Psychiatry 74:197–202CrossRefPubMedPubMedCentral Zoukos Y, Thomaides TN, Kidd D, Cuzner ML, Thompson A (2003) Expression of beta 2 adrenoreceptors on peripheral blood mononuclear cells in patients with primary and secondary progressive multiple sclerosis: a longitudinal 6 month study. J Neurol Neurosurg Psychiatry 74:197–202CrossRefPubMedPubMedCentral
58.
Zurück zum Zitat Giorelli M, Livrea P, Trojano M (2004) Post-receptorial mechanisms underlie functional disregulation of beta2-adrenergic receptors in lymphocytes from multiple sclerosis patients. J Neuroimmunol 155:143–149CrossRefPubMed Giorelli M, Livrea P, Trojano M (2004) Post-receptorial mechanisms underlie functional disregulation of beta2-adrenergic receptors in lymphocytes from multiple sclerosis patients. J Neuroimmunol 155:143–149CrossRefPubMed
59.
Zurück zum Zitat Zaffaroni M, Marino F, Bombelli R, Rasini E, Monti M, Ferrari M, Ghezzi A, Comi G, Lecchini S, Cosentino M (2008) Therapy with interferon-beta modulates endogenous catecholamines in lymphocytes of patients with multiple sclerosis. Exp Neurol 214:315–321CrossRefPubMed Zaffaroni M, Marino F, Bombelli R, Rasini E, Monti M, Ferrari M, Ghezzi A, Comi G, Lecchini S, Cosentino M (2008) Therapy with interferon-beta modulates endogenous catecholamines in lymphocytes of patients with multiple sclerosis. Exp Neurol 214:315–321CrossRefPubMed
60.
Zurück zum Zitat Marino F, Cosentino M (2013) Adrenergic modulation of immune cells: an update. Amino Acids 45:55–71CrossRefPubMed Marino F, Cosentino M (2013) Adrenergic modulation of immune cells: an update. Amino Acids 45:55–71CrossRefPubMed
61.
Zurück zum Zitat Cosentino M, Zaffaroni M, Legnaro M, Bombelli R, Schembri L, Baroncini D, Bianchi A, Clerici R, Guidotti M, Banfi P, Bono G, Marino F (2016) Dopaminergic receptors and adrenoceptors in circulating lymphocytes as putative biomarkers for the early onset and progression of multiple sclerosis. J Neuroimmunol 298:82–89CrossRefPubMed Cosentino M, Zaffaroni M, Legnaro M, Bombelli R, Schembri L, Baroncini D, Bianchi A, Clerici R, Guidotti M, Banfi P, Bono G, Marino F (2016) Dopaminergic receptors and adrenoceptors in circulating lymphocytes as putative biomarkers for the early onset and progression of multiple sclerosis. J Neuroimmunol 298:82–89CrossRefPubMed
62.
Zurück zum Zitat Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81:1–5CrossRefPubMed Bianchi ME (2007) DAMPs, PAMPs and alarmins: all we need to know about danger. J Leukoc Biol 81:1–5CrossRefPubMed
64.
Zurück zum Zitat De Jonge WJ, Ulloa L (2007) The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation. Br J Pharmacol 151:915–929CrossRefPubMedPubMedCentral De Jonge WJ, Ulloa L (2007) The alpha7 nicotinic acetylcholine receptor as a pharmacological target for inflammation. Br J Pharmacol 151:915–929CrossRefPubMedPubMedCentral
65.
Zurück zum Zitat Nicolussi EM, Huck S, Lassmann H, Bradl M (2009) The cholinergic anti-inflammatory system limits T cell infiltration into the neurodegenerative CNS, but cannot counteract complex CNS inflammation. Neurobiol Dis 35:24–31CrossRefPubMed Nicolussi EM, Huck S, Lassmann H, Bradl M (2009) The cholinergic anti-inflammatory system limits T cell infiltration into the neurodegenerative CNS, but cannot counteract complex CNS inflammation. Neurobiol Dis 35:24–31CrossRefPubMed
66.
Zurück zum Zitat Hao J, Simard AR, Turner GH et al (2011) Attenuation of CNS inflammatory responses by nicotine involves α7 and non-α7 nicotinic receptors. Exp Neurol 227:110–119CrossRefPubMed Hao J, Simard AR, Turner GH et al (2011) Attenuation of CNS inflammatory responses by nicotine involves α7 and non-α7 nicotinic receptors. Exp Neurol 227:110–119CrossRefPubMed
67.
Zurück zum Zitat Simard AR, Gan Y, St-Pierre S, Kousari A, Patel V, Whiteaker P, Morley BJ, Lukas RJ, Shi FD (2013) Differential modulation of EAE by α9*- and β2*-nicotinic acetylcholine receptors. Immunol Cell Biol 91:195–200CrossRefPubMedPubMedCentral Simard AR, Gan Y, St-Pierre S, Kousari A, Patel V, Whiteaker P, Morley BJ, Lukas RJ, Shi FD (2013) Differential modulation of EAE by α9*- and β2*-nicotinic acetylcholine receptors. Immunol Cell Biol 91:195–200CrossRefPubMedPubMedCentral
68.
Zurück zum Zitat Liu Q, Whiteaker P, Morley BJ, Shi FD, Lukas RJ (2017) Distinctive Roles for α7*- and α9*-Nicotinic acetylcholine receptors in inflammatory and autoimmune responses in the murine experimental autoimmune encephalomyelitis model of multiple sclerosis. Front Cell Neurosci 11:287CrossRefPubMedPubMedCentral Liu Q, Whiteaker P, Morley BJ, Shi FD, Lukas RJ (2017) Distinctive Roles for α7*- and α9*-Nicotinic acetylcholine receptors in inflammatory and autoimmune responses in the murine experimental autoimmune encephalomyelitis model of multiple sclerosis. Front Cell Neurosci 11:287CrossRefPubMedPubMedCentral
69.
Zurück zum Zitat Rosas-Ballina M, Olofsson PS, Ochani M et al (2011) Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 334:98–101CrossRefPubMedPubMedCentral Rosas-Ballina M, Olofsson PS, Ochani M et al (2011) Acetylcholine-synthesizing T cells relay neural signals in a vagus nerve circuit. Science 334:98–101CrossRefPubMedPubMedCentral
70.
Zurück zum Zitat Degelman ML, Herman KM (2017) Smoking and multiple sclerosis: a systematic review and meta-analysis using the Bradford Hill criteria for causation. Mult Scler Relat Disord 17:207–216CrossRefPubMed Degelman ML, Herman KM (2017) Smoking and multiple sclerosis: a systematic review and meta-analysis using the Bradford Hill criteria for causation. Mult Scler Relat Disord 17:207–216CrossRefPubMed
71.
Zurück zum Zitat Gomes JP, Watad A, Shoenfeld Y (2018) Nicotine and autoimmunity: the lotus’ flower in tobacco. Pharmacol Res 128:101–109CrossRefPubMed Gomes JP, Watad A, Shoenfeld Y (2018) Nicotine and autoimmunity: the lotus’ flower in tobacco. Pharmacol Res 128:101–109CrossRefPubMed
72.
Zurück zum Zitat Gao Z, Nissen JC, Ji K, Tsirka SE (2014) The experimental autoimmune encephalomyelitis disease course is modulated by nicotine and other cigarette smoke components. PLoS One 9:e107979CrossRefPubMedPubMedCentral Gao Z, Nissen JC, Ji K, Tsirka SE (2014) The experimental autoimmune encephalomyelitis disease course is modulated by nicotine and other cigarette smoke components. PLoS One 9:e107979CrossRefPubMedPubMedCentral
73.
Zurück zum Zitat Khezri S, Abtahi Froushani SM, Shahmoradi M (2018) Nicotine augments the beneficial effects of mesenchymal stem cell-based therapy in rat model of multiple sclerosis. Immunol Invest 47(2):113–124CrossRefPubMed Khezri S, Abtahi Froushani SM, Shahmoradi M (2018) Nicotine augments the beneficial effects of mesenchymal stem cell-based therapy in rat model of multiple sclerosis. Immunol Invest 47(2):113–124CrossRefPubMed
Metadaten
Titel
Immune and autonomic nervous system interactions in multiple sclerosis: clinical implications
verfasst von
Mario Habek
Publikationsdatum
08.04.2019
Verlag
Springer Berlin Heidelberg
Erschienen in
Clinical Autonomic Research / Ausgabe 3/2019
Print ISSN: 0959-9851
Elektronische ISSN: 1619-1560
DOI
https://doi.org/10.1007/s10286-019-00605-z