Upper-lower limb and breathing exercise program for improving sleep quality and psychological status in multiple sclerosis: a pilot randomized controlled trial
Tanja Grubić Kezele
A * , Zrinka Trope B , Valentina Ahel B , Natali Ružić B , Hrvoje Omrčen C , Luka Đudarić D and Ariana Fužinac-Smojver E
A Department of Physiology and Immunology,
B
C Department of Anatomy,
D Department of Radiology,
E Department of Basic Sciences,
Abstract
To examine the feasibility and possible effect of an 8-week exercise program on sleep quality, insomnia and psychological distress in individuals with multiple sclerosis (MS).
Twenty-four individuals with MS were recruited into a controlled pre-post feasibility study and divided into 2 groups: exercise (n = 13; Expanded Disability Status Scale (EDSS): 1.0–7.5) and a related control group with no exercise (n = 11; EDSS: 1.0–7.0). The exercise group performed combined upper limb, lower limb and breathing exercises in a controlled group (2d/week, 60 min/session) for 8 weeks. Participants were administered measures to evaluate sleep quality (Pittsburgh Sleep Quality Index, PSQI), insomnia severity (Insomnia Severity Index, ISI), psychological distress (Clinical Outcomes in Routine Evaluation–Outcome Measure, CORE-OM) and additionally impact of fatigue (Modified Fatigue Impact Scale, MFIS) after 8-weeks.
Insomnia severity measured with ISI (F(1;22)=5.95, p = 0.023, ηp2 = 0.213, 90% CI = 0.02–0.42) and psychological distress measured with the CORE-OM (F(1;22)=4.82, p = 0.039, ηp2 = 0.179, 90% CI = 0.01–0.40) showed statistically significant group-by-time interaction. Sleep quality measured with the PSQI showed statistically significant group-by-time interaction only in an aspect of daytime sleep dysfunction (F(1;22)=5.33, p = 0.031, ηp2 = 0.195, 90% CI = 0.01–0.40). The fatigue impact measured with the MFIS showed statistically significant group-by-time interaction in physical (F(1;22)=6.80, p = 0.016, ηp2 = 0.236, 90% CI = 0.02–0.44) and cognitive aspects (F(1;22)=9.12, p = 0.006, ηp2 = 0.293, 90% CI = 0.05–0.49), and total score (F(1;22)=11.29, p = 0.003, ηp2 = 0.339, 90% CI = 0.08–0.52).
Our 8-week program reduced insomnia severity, psychological distress and some aspects of fatigue (physical; cognitive; total), and improved sleep quality in an aspect of daytime sleep dysfunction in a small group of individuals with MS. Good feasibility and significant positive changes from baseline warrant further exploratory work.
Keywords: insomnia, multiple sclerosis, sleep quality, psychological distress, quality of life, fatigue.
References
Abbott, J. H. (2014) The distinction between randomized clinical trials (RCTs) and preliminary feasibility and pilot studies: What they are and are not. Journal of Orthopaedic & Sports Physical Therapy 44, 555-558.
| Crossref | Google Scholar |
Alhazzani, A., Alshahrani, A., Alqahtani, M., Alamri, R., Alqahtani, R., Alqahtani, M., Alahmarii, M. (2018) Insomnia among non-depressed multiple sclerosis patients: A cross-sectional study. The Egyptian Journal of Neurology, Psychiatry and Neurosurgery 54, 17.
| Crossref | Google Scholar |
Al-Sharman, A., Khalil, H., El-Salem, K., Aldughmi, M., Aburub, A. (2019) The effects of aerobic exercise on sleep quality measures and sleep-related biomarkers in individuals with Multiple Sclerosis: A pilot randomised controlled trial. NeuroRehabilitation 45, 107-115.
| Crossref | Google Scholar |
Bastien, C., Vallières, A., Morin, C. M. (2001) Validation of the insomnia severity index as an outcome measure for insomnia research. Sleep Medicine 2, 297-307.
| Crossref | Google Scholar |
Bøe Lunde, H., Aae, T., Indrevåg, W., Aarseth, J., Bjorvatn, B., Myhr, K., Bø, L. (2012) Poor sleep in patients with multiple sclerosis. PLoS One 7, e49996.
| Crossref | Google Scholar |
Brass, S., Li, C., Auerbach, S. (2014) The underdiagnosis of sleep disorders in patients with multiple sclerosis. Journal of Clinical Sleep Medicine 10, 1025-1031.
| Crossref | Google Scholar |
Buysse, D., Reynolds, C., Monk, T., Berman, S., Kupfer, D. (1989) The Pittsburgh sleep quality index: A new instrument for psychiatric practice and research. Psychiatry Research 28, 193-213.
| Crossref | Google Scholar |
Clarke, R., Coote, S. (2015) Perceptions of participants in a group, community, exercise programme for people with multiple sclerosis. Rehabilitation Research and Practice 2015, 123494.
| Crossref | Google Scholar |
Cramer, H., Lauche, R., Azizi, H., Dobos, G., Langhorst, J. (2014) Yoga for multiple sclerosis: A systematic review and meta-analysis. PLoS One 9, e112414.
| Crossref | Google Scholar |
Evans, C., Connell, J., Barkham, M., Margison, F., McGrath, G., Mellor-Clark, J., Audin, K. (2002) Towards a standardised brief outcome measure: Psychometric properties and utility of the CORE-OM. The British Journal of Psychiatry 180, 51-60.
| Crossref | Google Scholar |
Fisk, J. D., Ritvo, P. G., Ross, L., Haase, D. A., Marrie, T. J., Schlech, W. F. (1994) Measuring the functional impact of fatigue: Initial validation of the fatigue impact scale. Clinical Infectious Diseases 18, S79-S83.
| Google Scholar |
Grubić Kezele, T., Babić, M., Kauzlarić-Živković, T., Gulić, T. (2020) Combined upper limb and breathing exercise programme for pain management in ambulatory and non-ambulatory multiple sclerosis individuals: Part II analyses from feasibility study. Neurological Sciences 41, 65-74.
| Google Scholar |
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. Neurological Sciences 40, 733-743.
| Google Scholar |
Grubić Kezele, T., Fužinac-Smojver, A., Kauzlarić-Živković, T. (2019) Mild and motivational exercise in a social supporting environment for over passing primary fatigue in patients with multiple sclerosis. International Physical Medicine & Rehabilitation Journal 4, 152-154.
| Google Scholar |
Grubić Kezele, T., Fužinac-Smojver, A., Zoretić, K., Frank, S. (2018) Determination of the levels of fatigue, pain, functional independence and quality of life in people with multiple sclerosis (MS) compared to non-MS individuals: Use of standard. Medicina Fluminensis 54, 210-216.
| Crossref | Google Scholar |
Grubić Kezele,T., Medjimurec, S., Bukarica, M., Čorapović, A., Fužinac-Smojver, A. (2019) Quality of life and level of physical activity in primary school children with juvenile idiopathic arthritis in Primorje-Gorski Kotar County. Paediatria Croatica 63, 145-152.
| Google Scholar |
Howard, R. S., Wiles, C. M., Hirsch, N. P., Loh, L., Spencer, G. T., Newsom-Davis, J. (1992) Respiratory involvement in multiple sclerosis. Brain 115, 479-494.
| Crossref | Google Scholar |
Kaymaz, D., Candemir, İ. ç., Ergün, P., Demir, N., Taşdemir, F., Demir, P. (2018) Relation between upper-limb muscle strength with exercise capacity, quality of life and dyspnea in patients with severe chronic obstructive pulmonary disease. The Clinical Respiratory Journal 12, 1257-1263.
| Crossref | Google Scholar |
Kurtzke, J. F. (1983) Rating neurologic impairment in multiple sclerosis: An expanded disability status scale (EDSS). Neurology 33, 1444-1452.
| Google Scholar |
Larson, R. (2013) Psychometric properties of the modified fatigue impact scale. International Journal of MSCare 15, 15-20.
| Google Scholar |
Lobentanz, I. S., Asenbaum, S., Vass, K., Sauter, C, Klösch, G., Kollegger, H., Kristoferitsch, W., Zeitlhofer, J. (2004) Factors influencing quality of life in multiple sclerosis patients: Disability, depressive mood, fatigue and sleep quality. Acta Neurologica Scandinavica 110, 6-13.
| Crossref | Google Scholar |
McDonald, W. I., Compston, A., Edan, G., Goodkin, D., Hartung, H. P., Lublin, F. D., Wolinsky, J. S. (2001) Recommended diagnostic criteria for multiple sclerosis: Guidelines from the International Panel on the diagnosis of multiple sclerosis. Annals of Neurology 50, 121-127.
| Crossref | Google Scholar |
Morin, C., Belleville, G., Bélanger, L., Ivers, H. (2011) The insomnia severity index: Psychometric indicators to detect insomnia cases and evaluate treatment response. Sleep 34, 601-608.
| Crossref | Google Scholar |
Nicholas, R., Rashid, W. (2013) Multiple sclerosis. American Academy of Family Physicians 87, 712-714.
| Google Scholar |
Pekić, V., Kragujević, J., Kampić, I., & Ukić, I. (2017). Poor quality of sleep and fatigue and their relationship with the functional status of patients with Multiple sclerosis. 12th Quadrennial Congress of the World Federation of Neuroscience Nurses “Neuroscience clinical excellence”. Opatija, Croatia, pp. 204–205.
Perciavalle, V., Blandini, M., Fecarotta, P., Buscemi, A., Di Corrado, D., Bertolo, L., Coco, M. (2017) The role of deep breathing on stress. Neurological Sciences 38, 451-458.
| Crossref | Google Scholar |
Pilutti, L. A., Greenlee, T. A., Motl, R. W., Nickrent, M. S., Petruzzello, S. J. (2013) Effects of exercise training on fatigue in multiple sclerosis: A meta-analysis. Psychosomatic Medicine 75, 575-580.
| Google Scholar |
Ray, A. D., Udhoji, S., Mashtare, T. L., Fisher, N. M. (2013) A combined inspiratory and expiratory muscle training program improves respiratory muscle strength and fatigue in multiple sclerosis. Archives of Physical Medicine and Rehabilitation 94, 1964-1970.
| Google Scholar |
Sadeghi Bahmani, D., Kesselring, J., Papadimitriou, M., Bansi, J., Pühse, U., Gerber, M., Brand, S. (2019) In patients with multiple sclerosis, both objective and subjective sleep, depression, fatigue, and paresthesia improved after 3 weeks of regular exercise. Frontiers in Psychiatry 10, 265.
| Crossref | Google Scholar |
Sakkas, G. K., Giannaki, C. D., Karatzaferi, C., Manconi, M. (2019) Sleep abnormalities in multiple sclerosis. Current Treatment Options in Neurology 21, 4.
| Crossref | Google Scholar |
Sandroff, B. M., Balto, J. M., Klaren, R. E., Sommer, S. K., DeLuca, J., Motl, R. W. (2016) Systematically developed pilot randomized controlled trial of exercise and cognition in persons with multiple sclerosis. Neurocase 22, 443-450.
| Google Scholar |
Schellaert, V., Labauge, P., Lebrun, C., Maudarbocus, K., Bernard, J., Blache, J., Bayard, S. (2018) Psychological processes associated with insomnia in patients with multiple sclerosis. Sleep 41(3),.
| Crossref | Google Scholar |
Siengsukon, C., Aldughmi, M., Kahya, M., Bruce, J., Lynch, S., Ness Norouzinia, A., Billinger, S. (2016) Randomized controlled trial of exercise interventions to improve sleep quality and daytime sleepiness in individuals with multiple sclerosis: A pilot study. Multiple Sclerosis Journal – Experimental, Translational and Clinical 24, 2.
| Crossref | Google Scholar |
Strober, L. B., Arnett, P. A. (2005) An examination of four models predicting fatigue in multiple sclerosis. Archives of Clinical Neuropsychology 20, 631-646.
| Crossref | Google Scholar |
Tzelepis, G. E., McCool, F. D. (2015) Respiratory dysfunction in multiple sclerosis. Respiratory Medicine 109, 671-679.
| Crossref | Google Scholar |
Uhlig, B., Sand, T., ødegård, S., Hagen, K. (2014) Prevalence and associated factors of DSM-V insomnia in Norway: The Nord-Trøndelag Health Study (HUNT 3). Sleep Medicine 15, 708-713.
| Crossref | Google Scholar |
Vertesi, A., Lever, J. A., Molloy, D. W., Sanderson, B., Tuttle, I., Pokoradi, L., & Principi, E. (2001). Standardized mini-mental state examination. Use and interpretation. Canadian Family Physician, 47, 2018–2023. https://www.ncbi.nlm.nih.gov/pmc/articles/PMC2018449/
Vitkova, M., Rosenberger, J., Gdovinova, Z., Szilasiova, J., Mikula, P., Groothoff, J., van Dijk, J. (2016) Poor sleep quality in patients with multiple sclerosis: Gender differences. Brain and Behavior 6, e00553.
| Crossref | Google Scholar |
