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Published in: Neurological Sciences 1/2020

01-01-2020 | Multiple Sclerosis | Original Article

Combined upper limb and breathing exercise programme for pain management in ambulatory and non-ambulatory multiple sclerosis individuals: part II analyses from feasibility study

Authors: Tanja Grubić Kezele, Matea Babić, Tamara Kauzlarić-Živković, Tamara Gulić

Published in: Neurological Sciences | Issue 1/2020

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Abstract

Purpose

The present small semi-controlled feasibility study investigated a possible efficacy of a combined upper limb and breathing exercise programme in managing pain in ambulatory and non-ambulatory patients with EDSS from 0.0–8.0.

Method

People with MS (N = 19) were enrolled in this single-blind randomized controlled study and divided into 2 groups: exercise group (5 ambulatory, 5 non-ambulatory; Expanded Disability Status Scale (EDSS), 1.0–8.0) and related control group that performed no exercise (4 ambulatory, 5 non-ambulatory; EDSS, 1.0–7.5). The exercise group performed combined upper limb and breathing exercises in a group led by a physiotherapist (2 days/week, 60 min/session) accompanied by independent home exercises (3 days/week, ≥ 20 min/session). Participants underwent measures of pain level (visual analogue scale) for physical pain, functional independence of daily activities (Barthel index) and handgrip strength (HGS) for dominant (D) and non-dominant (ND) hand evaluated by a dynamometer before and after the 4-week period by the blinded assessor.

Results

The VAS for pain showed statistically significant group-by-time interaction only in non-ambulatory (p = .049) individuals, but with large intervention effects on both subgroups (ambulatory, p = .159; non-ambulatory, d = 0.97). Functional independence in daily activities (Barthel index) showed statistically non-significant group-by-time interaction in ambulatory (p = .195, d = 0.89) and non-ambulatory (p = .102, d = 1.64) individuals, but despite the absence of statistical significance, there were large intervention effects. Handgrip strength was significantly improved for both hands in ambulatory (D, p = .012; d = 2.07; ND, p = .025, d = 1.77) and only non-dominant hand in non-ambulatory individuals (D, p = .288, d = 0.83; ND, p = .012, d = 2.21).

Conclusion

This small pilot study provides preliminary proof-of-concept data supporting low-intensity upper limb and breathing exercise programme for potential reduction of pain and improvement of functional independence in both ambulatory and non-ambulatory individuals with MS in a larger sample and that strengthening the upper limbs might be an additional pain relief mechanism.

Trial registration

NTC03222596
Literature
1.
go back to reference Ramagopalan SV, Dobson R, Meier UC, Giovannoni G (2010) Multiple sclerosis: risk factors, prodromes, and potential causal pathways. Lancet Neurol 9:727–739PubMed Ramagopalan SV, Dobson R, Meier UC, Giovannoni G (2010) Multiple sclerosis: risk factors, prodromes, and potential causal pathways. Lancet Neurol 9:727–739PubMed
2.
go back to reference Baldin E, Riise T, Mattarozzi K, Gajofatto A, Granella F, Leone M, Lugaresi A, Malagù S, Motti L, Neri W, Pesci I, Santangelo M, Scandellari C, Tola MR, Vignatelli L, Zenesini C, D’Alessandro R15; G.E.Ro.N.I.Mu.S. study group (2019) Health-related quality of life in clinically isolated syndrome and risk of conversion to multiple sclerosis. Neurol Sci 40:75–80PubMed Baldin E, Riise T, Mattarozzi K, Gajofatto A, Granella F, Leone M, Lugaresi A, Malagù S, Motti L, Neri W, Pesci I, Santangelo M, Scandellari C, Tola MR, Vignatelli L, Zenesini C, D’Alessandro R15; G.E.Ro.N.I.Mu.S. study group (2019) Health-related quality of life in clinically isolated syndrome and risk of conversion to multiple sclerosis. Neurol Sci 40:75–80PubMed
3.
go back to reference Hentati E, Ben Sassi S, Nabli F, Mabrouk T, Zouari M, Hentati F (2018) Disability progression in multiple sclerosis: a Tunisian prospective cohort study. Neurol Sci 39:879–884PubMed Hentati E, Ben Sassi S, Nabli F, Mabrouk T, Zouari M, Hentati F (2018) Disability progression in multiple sclerosis: a Tunisian prospective cohort study. Neurol Sci 39:879–884PubMed
4.
go back to reference Drulovic J, Basic-Kes V, Grgic S, Vojinovic S, Dincic E (2015) The prevalence of pain in adults with multiple sclerosis: a multicenter cross-sectional survey. Pain Med 16:1597–1602PubMed Drulovic J, Basic-Kes V, Grgic S, Vojinovic S, Dincic E (2015) The prevalence of pain in adults with multiple sclerosis: a multicenter cross-sectional survey. Pain Med 16:1597–1602PubMed
5.
go back to reference Demaneuf T, Aitken Z, Karahalios A, Leong TI, De Livera AM, Jelinek GA, Weiland TJ, Marck CH (2019) Effectiveness of exercise interventions for pain reduction in people with multiple sclerosis: a systematic review and meta-analysis of randomized controlled trials. Arch Phys Med Rehabil 100:128–139PubMed Demaneuf T, Aitken Z, Karahalios A, Leong TI, De Livera AM, Jelinek GA, Weiland TJ, Marck CH (2019) Effectiveness of exercise interventions for pain reduction in people with multiple sclerosis: a systematic review and meta-analysis of randomized controlled trials. Arch Phys Med Rehabil 100:128–139PubMed
6.
go back to reference Ferraro D, Plantone D, Morselli F, Dallari G, Simone AM, Vitetta F, Sola P, Primiano G, Nociti V, Pardini M, Mirabella M, Vollono C (2018) Systematic assessment and characterization of chronic pain in multiple sclerosis patients. Neurol Sci 39:445–453PubMed Ferraro D, Plantone D, Morselli F, Dallari G, Simone AM, Vitetta F, Sola P, Primiano G, Nociti V, Pardini M, Mirabella M, Vollono C (2018) Systematic assessment and characterization of chronic pain in multiple sclerosis patients. Neurol Sci 39:445–453PubMed
7.
go back to reference Solaro C, Trabucco E, Messmer Uccelli M (2013) Pain and multiple sclerosis: pathophysiology and treatment. Curr Neurol Neurosci Rep 13:320PubMed Solaro C, Trabucco E, Messmer Uccelli M (2013) Pain and multiple sclerosis: pathophysiology and treatment. Curr Neurol Neurosci Rep 13:320PubMed
8.
go back to reference Halabchi F, Alizadeh Z, Sahraian MA, Abolhasani M (2017) Exercise prescription for patients with multiple sclerosis; potential benefits and practical recommendations. BMC Neurol 17:185PubMedPubMedCentral Halabchi F, Alizadeh Z, Sahraian MA, Abolhasani M (2017) Exercise prescription for patients with multiple sclerosis; potential benefits and practical recommendations. BMC Neurol 17:185PubMedPubMedCentral
9.
go back to reference Motl RW, McAuley E, Snook EM, Gliottoni RC (2009) Physical activity and quality of life in multiple sclerosis: intermediary roles of disability, fatigue, mood, pain, self-efficacy and social support. Psychol Health Med 14:111–124PubMedPubMedCentral Motl RW, McAuley E, Snook EM, Gliottoni RC (2009) Physical activity and quality of life in multiple sclerosis: intermediary roles of disability, fatigue, mood, pain, self-efficacy and social support. Psychol Health Med 14:111–124PubMedPubMedCentral
10.
go back to reference Turner AP, Kivlahan DR, Haselkorn JK (2009) Exercise and quality of life among people with multiple sclerosis: looking beyond physical functioning to mental health and participation in life. Arch Phys Med Rehabil 90:420–428PubMed Turner AP, Kivlahan DR, Haselkorn JK (2009) Exercise and quality of life among people with multiple sclerosis: looking beyond physical functioning to mental health and participation in life. Arch Phys Med Rehabil 90:420–428PubMed
11.
go back to reference Tacchino A, Brichetto G, Zaratin P, Battaglia MA, Ponzio M (2019) Self-assessment reliability in multiple sclerosis: the role of socio-demographic, clinical, and quality of life aspects. Neurol Sci 40:617-20; Di Cara M, Lo Buono V, Corallo F, Cannistraci C, Rifici C, Sessa E, D’Aleo G, Bramanti P, Marino S. (2019) Body image in multiple sclerosis patients: a descriptive review. Neurol Sci 40:923–928 Tacchino A, Brichetto G, Zaratin P, Battaglia MA, Ponzio M (2019) Self-assessment reliability in multiple sclerosis: the role of socio-demographic, clinical, and quality of life aspects. Neurol Sci 40:617-20; Di Cara M, Lo Buono V, Corallo F, Cannistraci C, Rifici C, Sessa E, D’Aleo G, Bramanti P, Marino S. (2019) Body image in multiple sclerosis patients: a descriptive review. Neurol Sci 40:923–928
12.
go back to reference Amtmann D, Askew RL, Kim J, Chung H, Ehde DM, Bombardier CH, Kraft GH, Jones SM, Johnson KL (2015) Pain affects depression through anxiety, fatigue, and sleep in multiple sclerosis. Rehabil Psychol 60:81–90PubMedPubMedCentral Amtmann D, Askew RL, Kim J, Chung H, Ehde DM, Bombardier CH, Kraft GH, Jones SM, Johnson KL (2015) Pain affects depression through anxiety, fatigue, and sleep in multiple sclerosis. Rehabil Psychol 60:81–90PubMedPubMedCentral
13.
go back to reference Shahrbanian S, Duquette P, Ahmed S, Mayo NE (2016) Pain acts through fatigue to affect participation in individuals with multiple sclerosis. Qual Life Res 25:477–491PubMed Shahrbanian S, Duquette P, Ahmed S, Mayo NE (2016) Pain acts through fatigue to affect participation in individuals with multiple sclerosis. Qual Life Res 25:477–491PubMed
14.
go back to reference Marck CH, De Livera AM, Weiland TJ, Jelinek PL, Neate SL, Brown CR, Taylor KL, Khan F, Jelinek GA (2017) Pain in people with multiple sclerosis: associations with modifiable lifestyle factors, fatigue, depression, anxiety, and mental health quality of life. Front Neurol 8:461PubMedPubMedCentral Marck CH, De Livera AM, Weiland TJ, Jelinek PL, Neate SL, Brown CR, Taylor KL, Khan F, Jelinek GA (2017) Pain in people with multiple sclerosis: associations with modifiable lifestyle factors, fatigue, depression, anxiety, and mental health quality of life. Front Neurol 8:461PubMedPubMedCentral
15.
go back to reference Pilutti LA, Greenlee TA, Motl RW, Nickrent MS, Petruzzello SJ (2013) Effects of exercise training on fatigue in multiple sclerosis: a meta-analysis. Psychosom Med 75:575–580PubMed Pilutti LA, Greenlee TA, Motl RW, Nickrent MS, Petruzzello SJ (2013) Effects of exercise training on fatigue in multiple sclerosis: a meta-analysis. Psychosom Med 75:575–580PubMed
16.
go back to reference Safari R, Van der Linden ML, Mercer TH (2017) Effect of exercise interventions on perceived fatigue in people with multiple sclerosis: synthesis of meta-analytic reviews. Neurodegener Dis Manag 7:219–230PubMed Safari R, Van der Linden ML, Mercer TH (2017) Effect of exercise interventions on perceived fatigue in people with multiple sclerosis: synthesis of meta-analytic reviews. Neurodegener Dis Manag 7:219–230PubMed
17.
go back to reference Afkar A, Ashouri A, Rahmani M, Emami Sigaroudi A (2017) Effect of exercise therapy on quality of life of patients with multiple sclerosis in Iran: a systematic review and meta-analysis. Neurol Sci 38:1901–1911PubMed Afkar A, Ashouri A, Rahmani M, Emami Sigaroudi A (2017) Effect of exercise therapy on quality of life of patients with multiple sclerosis in Iran: a systematic review and meta-analysis. Neurol Sci 38:1901–1911PubMed
18.
go back to reference Barry A, Cronin O, Ryan AM, Sweeney B, O’Toole O, Allen AP, Clarke G, O’Halloran KD, Downer EJ (2018) Impact of short-term cycle ergometer training on quality of life, cognition and depressive symptomatology in multiple sclerosis patients: a pilot study. Neurol Sci 39:461–469PubMed Barry A, Cronin O, Ryan AM, Sweeney B, O’Toole O, Allen AP, Clarke G, O’Halloran KD, Downer EJ (2018) Impact of short-term cycle ergometer training on quality of life, cognition and depressive symptomatology in multiple sclerosis patients: a pilot study. Neurol Sci 39:461–469PubMed
19.
go back to reference Motl RW, Gosney JL (2008) Effect of exercise training on quality of life in multiple sclerosis: a meta-analysis. Mult Scler 14:129–135PubMed Motl RW, Gosney JL (2008) Effect of exercise training on quality of life in multiple sclerosis: a meta-analysis. Mult Scler 14:129–135PubMed
20.
go back to reference Heine M, van de Port I, Rietberg MB, van Wegen EE, Kwakkel G (2015) Exercise therapy for fatigue in multiple sclerosis. Cochrane Database Syst Rev 2015:1–128 Heine M, van de Port I, Rietberg MB, van Wegen EE, Kwakkel G (2015) Exercise therapy for fatigue in multiple sclerosis. Cochrane Database Syst Rev 2015:1–128
21.
go back to reference Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33:1444–1452PubMed Kurtzke JF (1983) Rating neurologic impairment in multiple sclerosis: an expanded disability status scale (EDSS). Neurology 33:1444–1452PubMed
22.
go back to reference Motl RW, Sandroff BM (2015) Benefits of exercise training in multiple sclerosis. Curr Neurol Neurosci Rep 15:62PubMed Motl RW, Sandroff BM (2015) Benefits of exercise training in multiple sclerosis. Curr Neurol Neurosci Rep 15:62PubMed
23.
go back to reference Hasanpour Dehkordi A (2016) Influence of yoga and aerobics exercise on fatigue, pain and psychosocial status in patients with multiple sclerosis: a randomized trial. J Sports Med Phys Fitness 56:1417–1422PubMed Hasanpour Dehkordi A (2016) Influence of yoga and aerobics exercise on fatigue, pain and psychosocial status in patients with multiple sclerosis: a randomized trial. J Sports Med Phys Fitness 56:1417–1422PubMed
24.
go back to reference Grubić Kezele T, Babić M, Štimac D (2019) Exploring the feasibility of a mild and short 4-week combined upper limb and breathing exercise program as a possible home base program to decrease fatigue and improve quality of life in ambulatory and non-ambulatory multiple sclerosis individuals. Neurol Sci 40:733–743PubMed Grubić Kezele T, Babić M, Štimac D (2019) Exploring the feasibility of a mild and short 4-week combined upper limb and breathing exercise program as a possible home base program to decrease fatigue and improve quality of life in ambulatory and non-ambulatory multiple sclerosis individuals. Neurol Sci 40:733–743PubMed
25.
go back to reference Klaren RE, Motl RW, Woods JA, Miller SD (2014) Effects of exercise in experimental autoimmune encephalomyelitis (an animal model of multiple sclerosis). J Neuroimmunol 274:14–19PubMedPubMedCentral Klaren RE, Motl RW, Woods JA, Miller SD (2014) Effects of exercise in experimental autoimmune encephalomyelitis (an animal model of multiple sclerosis). J Neuroimmunol 274:14–19PubMedPubMedCentral
26.
go back to reference Vertesi A, Lever JA, Molloy DW, Sanderson B, Tuttle I, Pokoradi L, Principi E (2001) Standardized mini-mental state examination. Use and interpretation. Can Fam Physician 47:2018–2023PubMedPubMedCentral Vertesi A, Lever JA, Molloy DW, Sanderson B, Tuttle I, Pokoradi L, Principi E (2001) Standardized mini-mental state examination. Use and interpretation. Can Fam Physician 47:2018–2023PubMedPubMedCentral
27.
go back to reference Ortiz-Rubio A, Cabrera-Martos I, Rodríguez-Torres J, Fajardo-Contreras W, Díaz-Pelegrina A, Valenza MC (2016) Effects of a home-based upper limb training program in patients with multiple sclerosis: a randomized controlled trial. Arch Phys Med Rehabil 97:2027–2033PubMed Ortiz-Rubio A, Cabrera-Martos I, Rodríguez-Torres J, Fajardo-Contreras W, Díaz-Pelegrina A, Valenza MC (2016) Effects of a home-based upper limb training program in patients with multiple sclerosis: a randomized controlled trial. Arch Phys Med Rehabil 97:2027–2033PubMed
28.
go back to reference Sandroff BM, Balto JM, Klaren RE, Sommer SK, DeLuca J, Motl RW (2016) Systematically developed pilot randomized controlled trial of exercise and cognition in persons with multiple sclerosis. Neurocase 22:443–450PubMed Sandroff BM, Balto JM, Klaren RE, Sommer SK, DeLuca J, Motl RW (2016) Systematically developed pilot randomized controlled trial of exercise and cognition in persons with multiple sclerosis. Neurocase 22:443–450PubMed
29.
go back to reference Grau-López L, Sierra S, Martínez-Cáceres E, Ramo-Tello C (2011) Analysis of the pain in multiple sclerosis patients. Neurologia 26:208–213PubMed Grau-López L, Sierra S, Martínez-Cáceres E, Ramo-Tello C (2011) Analysis of the pain in multiple sclerosis patients. Neurologia 26:208–213PubMed
30.
go back to reference Svendsen KB, Jensen TS, Hansen HJ, Bach FW (2005) Sensory function and quality of life in patients with multiple sclerosis and pain. Pain 114:473–481PubMed Svendsen KB, Jensen TS, Hansen HJ, Bach FW (2005) Sensory function and quality of life in patients with multiple sclerosis and pain. Pain 114:473–481PubMed
31.
go back to reference Mori F, Codecà C, Kusayanagi H, Monteleone F, Buttari F, Fiore S, Bernardi G, Koch G, Centonze D (2010) Effects of anodal transcranial direct current stimulation on chronic neuropathic pain in patients with multiple sclerosis. J Pain 11:436–442PubMed Mori F, Codecà C, Kusayanagi H, Monteleone F, Buttari F, Fiore S, Bernardi G, Koch G, Centonze D (2010) Effects of anodal transcranial direct current stimulation on chronic neuropathic pain in patients with multiple sclerosis. J Pain 11:436–442PubMed
32.
go back to reference Tomasović Mrčela N, Massari D, Vlak T (2010) Functional independence, diagnostic groups, hospital stay, and modality of payment in three Croatian seaside inpatient rehabilitation centers. Croat Med J 51:534–542PubMed Tomasović Mrčela N, Massari D, Vlak T (2010) Functional independence, diagnostic groups, hospital stay, and modality of payment in three Croatian seaside inpatient rehabilitation centers. Croat Med J 51:534–542PubMed
33.
go back to reference Mahoney FI, Barthel DW (1965) Functional evaluation: the Barthel index. Md State Med J 14:56–61 Mahoney FI, Barthel DW (1965) Functional evaluation: the Barthel index. Md State Med J 14:56–61
34.
go back to reference Lusardi MM, Bohannon RW (1991) Hand grip strength: comparability of measurements obtained with a jamar dynamometer and a modified sphygmomanometer. J Hand Ther 4:117–122 Lusardi MM, Bohannon RW (1991) Hand grip strength: comparability of measurements obtained with a jamar dynamometer and a modified sphygmomanometer. J Hand Ther 4:117–122
35.
go back to reference Fess EE, Moran CA (1981) American society of hand therapists clinical assessment recommendations. American Society of Hand Therapists, USA Fess EE, Moran CA (1981) American society of hand therapists clinical assessment recommendations. American Society of Hand Therapists, USA
36.
go back to reference Ray AD, Udhoji S, Mashtare TL, Fisher NM (2013) A combined inspiratory and expiratory muscle training program improves respiratory muscle strength and fatigue in multiple sclerosis. Arch Phys Med Rehabil 94:1964–1970PubMed Ray AD, Udhoji S, Mashtare TL, Fisher NM (2013) A combined inspiratory and expiratory muscle training program improves respiratory muscle strength and fatigue in multiple sclerosis. Arch Phys Med Rehabil 94:1964–1970PubMed
37.
go back to reference Rutledge T, Loh C (2004) Effect sizes and statistical testing in the determination of clinical significance in behavioral medicine research. Ann Behav Med 27:138–145PubMed Rutledge T, Loh C (2004) Effect sizes and statistical testing in the determination of clinical significance in behavioral medicine research. Ann Behav Med 27:138–145PubMed
38.
go back to reference Cohen J (1988) Statistical power analysis for the behavioral sciences. Lawrence Erlbaum Associates, Hillsdale NJ Cohen J (1988) Statistical power analysis for the behavioral sciences. Lawrence Erlbaum Associates, Hillsdale NJ
39.
go back to reference Severijns D, Lamers I, Kerkhofs L, Feys P (2015) Hand grip fatigability in persons with multiple sclerosis according to hand dominance and disease progression. J Rehabil Med 47:154–160PubMed Severijns D, Lamers I, Kerkhofs L, Feys P (2015) Hand grip fatigability in persons with multiple sclerosis according to hand dominance and disease progression. J Rehabil Med 47:154–160PubMed
40.
go back to reference Cramer H, Lauche R, Azizi H, Dobos G, Langhorst J (2014) Yoga for multiple sclerosis: a systematic review and meta-analysis. PLoS One 9:e112414PubMedPubMedCentral Cramer H, Lauche R, Azizi H, Dobos G, Langhorst J (2014) Yoga for multiple sclerosis: a systematic review and meta-analysis. PLoS One 9:e112414PubMedPubMedCentral
41.
go back to reference Perciavalle V, Blandini M, Fecarotta P, Buscemi A, Di Corrado D, Bertolo L, Fichera F, Coco M (2017) The role of deep breathing on stress. Neurol Sci 38:451–458PubMed Perciavalle V, Blandini M, Fecarotta P, Buscemi A, Di Corrado D, Bertolo L, Fichera F, Coco M (2017) The role of deep breathing on stress. Neurol Sci 38:451–458PubMed
42.
go back to reference Castro-Sánchez AM, Matarán-Peñarrocha GA, Lara-Palomo I, Saavedra-Hernández M, Arroyo-Morales M, Moreno-Lorenzo C (2012) Hydrotherapy for the treatment of pain in people with multiple sclerosis: a randomized controlled trial. Evid Based Complement Alternat Med 2012:473963PubMed Castro-Sánchez AM, Matarán-Peñarrocha GA, Lara-Palomo I, Saavedra-Hernández M, Arroyo-Morales M, Moreno-Lorenzo C (2012) Hydrotherapy for the treatment of pain in people with multiple sclerosis: a randomized controlled trial. Evid Based Complement Alternat Med 2012:473963PubMed
43.
go back to reference Rogers KA, MacDonald M (2015) Therapeutic yoga: symptom management for multiple sclerosis. J Altern Complement Med 21:655–659PubMedPubMedCentral Rogers KA, MacDonald M (2015) Therapeutic yoga: symptom management for multiple sclerosis. J Altern Complement Med 21:655–659PubMedPubMedCentral
44.
go back to reference Clarke R, Coote S (2015) Perceptions of participants in a group, community, exercise programme for people with multiple sclerosis. Rehabil Res Pract 2015:123494PubMedPubMedCentral Clarke R, Coote S (2015) Perceptions of participants in a group, community, exercise programme for people with multiple sclerosis. Rehabil Res Pract 2015:123494PubMedPubMedCentral
45.
go back to reference Miller L, Paul L, Mattison P, McFadyen A (2011) Evaluation of a home-based physiotherapy programme for those with moderate to severe multiple sclerosis: a randomized controlled pilot study. Clin Rehabil 25:720–730PubMed Miller L, Paul L, Mattison P, McFadyen A (2011) Evaluation of a home-based physiotherapy programme for those with moderate to severe multiple sclerosis: a randomized controlled pilot study. Clin Rehabil 25:720–730PubMed
46.
go back to reference El-Sayes J, Harasym D, Turco CV, Locke MB, Nelson AJ (2018) Exercise-induced neuroplasticity: a mechanistic model and prospects for promoting plasticity. Neuroscientist 25:65–85PubMed El-Sayes J, Harasym D, Turco CV, Locke MB, Nelson AJ (2018) Exercise-induced neuroplasticity: a mechanistic model and prospects for promoting plasticity. Neuroscientist 25:65–85PubMed
47.
go back to reference Kerschensteiner M (2017) Neuroplasticity and its relevance for multiple sclerosis. Neurodegener Dis Manag 7:31–33PubMed Kerschensteiner M (2017) Neuroplasticity and its relevance for multiple sclerosis. Neurodegener Dis Manag 7:31–33PubMed
48.
go back to reference Vivar C, Potter MC, van Praag H (2013) All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis. Curr Top Behav Neurosci 15:189–210PubMedPubMedCentral Vivar C, Potter MC, van Praag H (2013) All about running: synaptic plasticity, growth factors and adult hippocampal neurogenesis. Curr Top Behav Neurosci 15:189–210PubMedPubMedCentral
49.
go back to reference Nokia MS, Lensu S, Ahtiainen JP (2016) Physical exercise increases adult hippocampal neurogenesis in male rats provided it is aerobic and sustained. J Physiol 594:1855–1873PubMedPubMedCentral Nokia MS, Lensu S, Ahtiainen JP (2016) Physical exercise increases adult hippocampal neurogenesis in male rats provided it is aerobic and sustained. J Physiol 594:1855–1873PubMedPubMedCentral
50.
go back to reference Jakovac H, Grubić Kezele T, Radošević-Stašić B (2018) Expression profiles of metallothionein I/II and megalin in cuprizone model of de- and remyelination. Neuroscience 388:69–86PubMed Jakovac H, Grubić Kezele T, Radošević-Stašić B (2018) Expression profiles of metallothionein I/II and megalin in cuprizone model of de- and remyelination. Neuroscience 388:69–86PubMed
51.
go back to reference Jakovac H, Grubić Kezele T, Šućurović S, Mulac-Jeričević B, Radošević-Stašić B (2017) Osteopontin-metallothionein I/II interactions in experimental autoimmune encephalomyelitis. Neuroscience 350:133–145PubMed Jakovac H, Grubić Kezele T, Šućurović S, Mulac-Jeričević B, Radošević-Stašić B (2017) Osteopontin-metallothionein I/II interactions in experimental autoimmune encephalomyelitis. Neuroscience 350:133–145PubMed
52.
go back to reference Grubić Kezele T, Fužinac-Smojver A, Ćurko-Cofek B, Jakovac H, Turković K (2017) Adult neurogenesis-accent on subgranular and subventricular zone in mammals. Medicina 53:136–146 Grubić Kezele T, Fužinac-Smojver A, Ćurko-Cofek B, Jakovac H, Turković K (2017) Adult neurogenesis-accent on subgranular and subventricular zone in mammals. Medicina 53:136–146
Metadata
Title
Combined upper limb and breathing exercise programme for pain management in ambulatory and non-ambulatory multiple sclerosis individuals: part II analyses from feasibility study
Authors
Tanja Grubić Kezele
Matea Babić
Tamara Kauzlarić-Živković
Tamara Gulić
Publication date
01-01-2020
Publisher
Springer International Publishing
Published in
Neurological Sciences / Issue 1/2020
Print ISSN: 1590-1874
Electronic ISSN: 1590-3478
DOI
https://doi.org/10.1007/s10072-019-04046-4

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