Document Type : Original Article
Authors
1 Ph.D Student in Exercise Physiology , Department of Physical Education and Sport Sciences, Bojnourd Branch, Islamic Azad University, Bojnourd, Iran.
2 Assistant Professor at Department of Physical Education and Sport Sciences, Bojnourd Branch, Islamic Azad University, Bojnourd, Iran.
Abstract
Background and Aim: Multiple sclerosis (MS) is a chronic disease of the central nervous system that affects the brain and spinal cord and cause disturbances in the conduction of nerve and electrical currents. The aim of this study was to investigate the effect of eight weeks of combined training on the expression of neuregulin-1 gene, balance and body composition in patients with MS. Materials and Methods: Thirty women with MS mean age 47.7±4.79 year and weight 69.70±5.5 kg living in Mashhad city were randomly divided into two experimental (15 people) and control (15 people) groups. The experimental group performed combined exercises including resistance exercises with an intensity of 65 to 85% of a one maximum repetition and aerobic exercises with 60 to 70% of maximum heart rate for eight weeks, three days a week, and 45 minutes in each session while the control group did not participate in any sports program during this period. Blood samples were taken from the brachial vein before and 48 hours after exercise in a fasting state. Neuroglin-1 gene expression were determined using Real Time PCR method. Balance index was measured by BDI and TUG tests, and body composition also was measured using a body composition analyzer. Data were analyzed using independent t-test and paired t-test at the significant level of p≤0.05. Results: Combined training significantly increased neuregulin-1 gene expression (p=0.001), static balance (p=0.001), dynamic balance (p=0.001), lean body mass (p=0.001) and significantly decreased fat body mass (p=0.001) in MS people. Conclusion: Based on the findings of the present research, combined exercises can improve the conditions of MS patients by increasing the influencing factors in the illness.
Keywords
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Amiri Parsa, T., Attarzadeh Hoseini, S.R., Bijeh, Nahid., & Hamdinia, M.R. (2020). The effect of combined exercise (resistance-aerobic) valume on neurotrophic changes, neuropathic pain and some performance indicators in postmenopausal women with diabetic peripheral neuropathy. The Iranian Journal of Obstetrics, Gynecology and Infertility, 22(12), 24-37. [In Persian]. https://doi.org/10.22038/IJOGI.2020.15550
Atre, J.J., & Ganvir, S.S. (2020). Effect of functional strength training versus proprioceptive neuromuscular facilitation on balance and gait in patients with diabetic neuropathy. Indian Journal of Physical Therapy and Research, 2(1), 47. https://doi.org/10.4103/ijptr.ijptr_76_19
Baar, K. (2014). Using molecular biology to maximize concurrent training. Sports Medicine, 44(2), 117-125. https://doi.org/10.1007/s40279-014-0252-0
Bahmani, D.S., & Motl, R.W. (2021). Rate, burden, and treatment of sexual dysfunction in multiple sclerosis: The case for exercise training as a new treatment approach. Multiple Sclerosis and Related Disorders, 51, 102878. https://doi.org/10.1016/j.msard.2021.102878
Batvandi, A., & Kaki, A. (2021). The effect of aerobic exercise on Nrg1/Erbb2 signaling pathway in male rats with diabetic neuropathic pain. Iranian Journal of Diabetes & Metabolism. 21(4): 229-239. [In Persian]. http://ijdld.tums.ac.ir/article-1-6075-en.html
Bo, B., Zhou, Y., Zheng, Q., Wang, G., Zhou, K., & Wei, J. (2020). The molecular mechanisms associated with aerobic exercise-induced cardiac regeneration. Biomolecules, 11(1), 19.
Bombardier, C.H., Motl, R.W., Benedict, R.H., Temkin, N., Qian, P., Alexander, K., ... & Carey, C.M. (2021). Exercise training and cognition in multiple sclerosis: The GET Smart trial protocol. Contemporary Clinical Trials, 104, 106331. https://doi.org/10.1016/j.cct.2021.106331
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Chantler, S., Griffiths, A., Matu, J., Davison, G., Jones, B., & Deighton, K. (2021). The effects of exercise on indirect markers of gut damage and permeability: A systematic review and meta-analysis. Sports Medicine, 51(1), 113-124. https://doi.org/10.1007/s40279-020-01348-y
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Dalgas, U., Stenager, E., & Ingemann-Hansen, T. (2008). Multiple sclerosis and physical exercise: recommendations for the application of resistance-, endurance-and combined training. Multiple Sclerosis Journal, 14(1), 35-53. https://doi.org/10.1177/1352458507079445
Dalgas, U., Stenager, E., Jakobsen, J., Petersen, T., Overgaard, K., & Ingemann-Hansen, T. (2010). Muscle fiber size increases following resistance training in multiple sclerosis. Multiple Sclerosis Journal, 16(11), 1367-1376. https://doi.org/10.1177/1352458510377222
du Plessis, R., Dembskey, N., & Bassett, S.H. (2023). Effects of an isometric exercise training program on muscular strength, ankle mobility, and balance in patients with diabetic peripheral neuropathy in the lower legs in South Africa. International Journal of Diabetes in Developing Countries, 43(2), 252-257. https://doi.org/10.1007/s13410-022-01068-1
Ennequin, G., Boisseau, N., Caillaud, K., Chavanelle, V., Etienne, M., Li, X., & Sirvent, P. (2015). Neuregulin 1 improves glucose tolerance in db/db mice. Plos One, 10(7), e0130568. https://doi.org/10.1371/journal.pone.0130568
Ennequin, G., Capel, F., Caillaud, K., Chavanelle, V., Etienne, M., Teixeira, A., . . . & Sirvent, P. (2017). Neuregulin 1 improves complex 2-mediated mitochondrial respiration in skeletal muscle of healthy and diabetic mice. Scientific Reports, 7(1), 1-9. https://doi.org/ 10.1038/s41598-017-02029-z
Fattahi, Z., TaheriChadorneshin, H., Rashidi, E., & Abtahi-Eivary, S.-H. (2020). Effect of two different volumes of resistance training on serum level of fibroblast growth factor-21, body fat percentage and mobility in obese elderly women. The Iranian Journal of Obstetrics, Gynecology and Infertility, 23(10), 61-71 . https://doi.org/ 10.22038/IJOGI.2020.17490
Froozandeh, E., Tofighi, A., & Tolouei Azar, J. (2020). The effect of 8 weeks of resistance and aerobic interval training on levels of GLP-1, NRG-1 and IL-33 in type 2 diabetic women. Sport Physiology, 12(46), 117-138. https://doi.org/10.22089/spj.2019.7434.1913
Ghahramanloo, E., Midgley, A.W., & Bentley, D.J. (2009). The effect of concurrent training on blood lipid profile and anthropometrical characteristics of previously untrained men. Journal of Physical Activity & Health, 6(6), 760. https://doi.org/10.1123/jpah.6.6.760
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Harbo, H.F., Gold, R., & Tintoré, M. (2013). Sex and gender issues in multiple sclerosis. Ther Adv Neurol Disord, 6(4),237-48. https://doi.org/10.1177/1756285613488434
Hedayati, A., Rashidlamir, A., Hashemi Javaheri, A., & Ehsaei, M. (2015). The effect of eight weeks of resistance training on static and dynamic balance as well as power of the foot muscles in diabetic women with peripheral neuropathy. Journal Shahid Sadughi University, 23 (9), 833-843. [In Persian]. http://jssu.ssu.ac.ir/article-1-2932-en.html
Izaias Marcelo, H., Henrique Aleixo, P., Pereira da Silva, R., Lopes Pacagnelli, F., Brinholi Victorino Da Silva, R. B., Camargo Filho, S., . . . & Chacon Castoldi, R. (2021). Effects of concurrent training and intermittent fasting on structural, functional, and morphological parameters of the heart. International Journal of Morphology, 39(4). https://doi.org/10.4067/S0717-95022021000401190
Kataria, H., Hart, C.G., Alizadeh, A., Cossoy, M., Kaushik, D.K., Bernstein, C.N., . . . & Karimi-Abdolrezaee, S. (2021). Neuregulin-1 beta 1 is implicated in pathogenesis of multiple sclerosis. Brain, 144(1), 162-185. https://doi.org/10.1093/brain/awaa385
Kim, H.J., Lee, H.J., So, B., Son, J. S., Yoon, D., & Song, W. (2016). Effect of aerobic training and resistance training on circulating irisin level and their association with change of body composition in overweight/obese adults: a pilot study. Physiological Research, 65(2), 271. https://doi.org/10.33549/physiolres.932997
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MacNeil, L.G., Glover, E., Bergstra, T.G., Safdar, A., & Tarnopolsky, M.A. (2014). The order of exercise during concurrent training for rehabilitation does not alter acute genetic expression, mitochondrial enzyme activity or improvements in muscle function. PloS One, 9(10), e109189. https://doi.org/10.1371/journal.pone.0109189
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Picon, C., Jayaraman, A., James, R., Beck, C., Gallego, P., Witte, M. E., . . . & Reynolds, R. (2021). Neuron-specific activation of necroptosis signaling in multiple sclerosis cortical grey matter. Acta Neuropathologica, 141(4), 585-604. https://doi.org/10.1007/s00401-021-02274-7
Rossi, F., Diniz, T., Neves, L., Fortaleza, A., Gerosa-Neto, J., Inoue, D., . . . & Freitas, I. (2017). The beneficial effects of aerobic and concurrent training on metabolic profile and body composition after detraining: a 1-year follow-up in postmenopausal women. European Journal of Clinical Nutrition, 71(5), 638-645. https://doi.org/10.1038/ejcn.2016.263
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Amiri Parsa, T., Attarzadeh Hoseini, S.R., Bijeh, Nahid., & Hamdinia, M.R. (2020). The effect of combined exercise (resistance-aerobic) valume on neurotrophic changes, neuropathic pain and some performance indicators in postmenopausal women with diabetic peripheral neuropathy. The Iranian Journal of Obstetrics, Gynecology and Infertility, 22(12), 24-37. [In Persian]. https://doi.org/10.22038/IJOGI.2020.15550
Atre, J.J., & Ganvir, S.S. (2020). Effect of functional strength training versus proprioceptive neuromuscular facilitation on balance and gait in patients with diabetic neuropathy. Indian Journal of Physical Therapy and Research, 2(1), 47. https://doi.org/10.4103/ijptr.ijptr_76_19
Baar, K. (2014). Using molecular biology to maximize concurrent training. Sports Medicine, 44(2), 117-125. https://doi.org/10.1007/s40279-014-0252-0
Bahmani, D.S., & Motl, R.W. (2021). Rate, burden, and treatment of sexual dysfunction in multiple sclerosis: The case for exercise training as a new treatment approach. Multiple Sclerosis and Related Disorders, 51, 102878. https://doi.org/10.1016/j.msard.2021.102878
Batvandi, A., & Kaki, A. (2021). The effect of aerobic exercise on Nrg1/Erbb2 signaling pathway in male rats with diabetic neuropathic pain. Iranian Journal of Diabetes & Metabolism. 21(4): 229-239. [In Persian]. http://ijdld.tums.ac.ir/article-1-6075-en.html
Bo, B., Zhou, Y., Zheng, Q., Wang, G., Zhou, K., & Wei, J. (2020). The molecular mechanisms associated with aerobic exercise-induced cardiac regeneration. Biomolecules, 11(1), 19.
Bombardier, C.H., Motl, R.W., Benedict, R.H., Temkin, N., Qian, P., Alexander, K., ... & Carey, C.M. (2021). Exercise training and cognition in multiple sclerosis: The GET Smart trial protocol. Contemporary Clinical Trials, 104, 106331. https://doi.org/10.1016/j.cct.2021.106331
Bouamra, M., Zouhal, H., Ratel, S., Makhlouf, I., Bezrati, I., Chtara, M., … & Chaouachi, A. (2022). Concurrent training promotes greater gains on body composition and components of physical fitness than single-mode training (endurance or resistance) in youth with obesity. Frontiers in Physioogyl.13, 1-16. https://doi.org/10.3389/fphys.2022.869063
Cantó, C., Suárez, E., Lizcano, J. M., Griñó, E., Shepherd, P.R., Fryer, L.G., ... & Zorzano, A. (2004). Neuregulin signaling on glucose transport in muscle cells. Journal of Biological Chemistry, 279(13), 12260-12268. https://doi.org/10.1074/jbc.M308554200
Chantler, S., Griffiths, A., Matu, J., Davison, G., Jones, B., & Deighton, K. (2021). The effects of exercise on indirect markers of gut damage and permeability: A systematic review and meta-analysis. Sports Medicine, 51(1), 113-124. https://doi.org/10.1007/s40279-020-01348-y
Chua, Y., Ito, Y., Pole, J., Newman, S., Chin, S.-F., Stein, R., ... & Murrell, A. (2009). The NRG-1 gene is frequently silenced by methylation in breast cancers and is a strong candidate for the 8p tumour suppressor gene. Oncogene, 28(46), 4041-4052. https://doi.org/10.1038/onc.2009.259
Dalgas, U., Stenager, E., & Ingemann-Hansen, T. (2008). Multiple sclerosis and physical exercise: recommendations for the application of resistance-, endurance-and combined training. Multiple Sclerosis Journal, 14(1), 35-53. https://doi.org/10.1177/1352458507079445
Dalgas, U., Stenager, E., Jakobsen, J., Petersen, T., Overgaard, K., & Ingemann-Hansen, T. (2010). Muscle fiber size increases following resistance training in multiple sclerosis. Multiple Sclerosis Journal, 16(11), 1367-1376. https://doi.org/10.1177/1352458510377222
du Plessis, R., Dembskey, N., & Bassett, S.H. (2023). Effects of an isometric exercise training program on muscular strength, ankle mobility, and balance in patients with diabetic peripheral neuropathy in the lower legs in South Africa. International Journal of Diabetes in Developing Countries, 43(2), 252-257. https://doi.org/10.1007/s13410-022-01068-1
Ennequin, G., Boisseau, N., Caillaud, K., Chavanelle, V., Etienne, M., Li, X., & Sirvent, P. (2015). Neuregulin 1 improves glucose tolerance in db/db mice. Plos One, 10(7), e0130568. https://doi.org/10.1371/journal.pone.0130568
Ennequin, G., Capel, F., Caillaud, K., Chavanelle, V., Etienne, M., Teixeira, A., . . . & Sirvent, P. (2017). Neuregulin 1 improves complex 2-mediated mitochondrial respiration in skeletal muscle of healthy and diabetic mice. Scientific Reports, 7(1), 1-9. https://doi.org/ 10.1038/s41598-017-02029-z
Fattahi, Z., TaheriChadorneshin, H., Rashidi, E., & Abtahi-Eivary, S.-H. (2020). Effect of two different volumes of resistance training on serum level of fibroblast growth factor-21, body fat percentage and mobility in obese elderly women. The Iranian Journal of Obstetrics, Gynecology and Infertility, 23(10), 61-71 . https://doi.org/ 10.22038/IJOGI.2020.17490
Froozandeh, E., Tofighi, A., & Tolouei Azar, J. (2020). The effect of 8 weeks of resistance and aerobic interval training on levels of GLP-1, NRG-1 and IL-33 in type 2 diabetic women. Sport Physiology, 12(46), 117-138. https://doi.org/10.22089/spj.2019.7434.1913
Ghahramanloo, E., Midgley, A.W., & Bentley, D.J. (2009). The effect of concurrent training on blood lipid profile and anthropometrical characteristics of previously untrained men. Journal of Physical Activity & Health, 6(6), 760. https://doi.org/10.1123/jpah.6.6.760
Ghanbari-Niaki, A. (2016). Neuregulins response to exercise: a mini review. Annals of Applied Sport Science, 4(1), 3-7. https://doi.org/10.7508/aass.2016.01.002
Harbo, H.F., Gold, R., & Tintoré, M. (2013). Sex and gender issues in multiple sclerosis. Ther Adv Neurol Disord, 6(4),237-48. https://doi.org/10.1177/1756285613488434
Hedayati, A., Rashidlamir, A., Hashemi Javaheri, A., & Ehsaei, M. (2015). The effect of eight weeks of resistance training on static and dynamic balance as well as power of the foot muscles in diabetic women with peripheral neuropathy. Journal Shahid Sadughi University, 23 (9), 833-843. [In Persian]. http://jssu.ssu.ac.ir/article-1-2932-en.html
Izaias Marcelo, H., Henrique Aleixo, P., Pereira da Silva, R., Lopes Pacagnelli, F., Brinholi Victorino Da Silva, R. B., Camargo Filho, S., . . . & Chacon Castoldi, R. (2021). Effects of concurrent training and intermittent fasting on structural, functional, and morphological parameters of the heart. International Journal of Morphology, 39(4). https://doi.org/10.4067/S0717-95022021000401190
Kataria, H., Hart, C.G., Alizadeh, A., Cossoy, M., Kaushik, D.K., Bernstein, C.N., . . . & Karimi-Abdolrezaee, S. (2021). Neuregulin-1 beta 1 is implicated in pathogenesis of multiple sclerosis. Brain, 144(1), 162-185. https://doi.org/10.1093/brain/awaa385
Kim, H.J., Lee, H.J., So, B., Son, J. S., Yoon, D., & Song, W. (2016). Effect of aerobic training and resistance training on circulating irisin level and their association with change of body composition in overweight/obese adults: a pilot study. Physiological Research, 65(2), 271. https://doi.org/10.33549/physiolres.932997
Kjølhede, T., Vissing, K., & Dalgas, U. (2012). Multiple sclerosis and progressive resistance training: a systematic review. Multiple Sclerosis Journal, 18(9), 1215-1228. https://doi.org/10.1177/1352458512437418
Lebrasseur, N.K., Coté, G.M., Miller, T.A., Fielding, R.A., & Sawyer, D.B. (2003). Regulation of neuregulin/ErbB signaling by contractile activity in skeletal muscle. American Journal of Physiology-Cell Physiology, 28(5), C1149-C1155. https://doi.org/10.1152/ajpcell.00487.2002
Li, L., Shang, L., Kang, W., Du, L., & Ge, S. (2022). Neuregulin‐1 promotes the proliferation, migration, and angiogenesis of human periodontal ligament stem cells in vitro. Cell Biology International, 46(5), 792-805. https://doi.org/10.1002/cbin.11770
MacNeil, L.G., Glover, E., Bergstra, T.G., Safdar, A., & Tarnopolsky, M.A. (2014). The order of exercise during concurrent training for rehabilitation does not alter acute genetic expression, mitochondrial enzyme activity or improvements in muscle function. PloS One, 9(10), e109189. https://doi.org/10.1371/journal.pone.0109189
Marjani, F., Rahnama, N., Etemadifar, M., & Shoaei, M. (2022). Comparison of the effect of selected exercises with TRX and aerofitness on balance and proprioception in patients with multiple sclerosis. Journal of Ilam University of Medical Sciences, 30(1), 42-54. [In Persian]. http://sjimu.medilam.ac.ir/article-1-7036-en.html
Mokhtarzade, M., Agha-Alinejad, H., Motl, R.W., Negaresh, R., Baker, J.S., & Zimmer, P. (2019). Weight control and physical exercise in people with multiple sclerosis: current knowledge and future perspectives. Complementary Therapies in Medicine, 43, 240-246. https://doi.org/10.1016/j.ctim.2019.02.006
Odiete, O., Hill, M.F., & Sawyer, D.B. (2012). Neuregulin in cardiovascular development and disease. Circulation Research, 111(10), 1376-1385. https://doi.org/10.1161/CIRCRESAHA.112.267286
Picon, C., Jayaraman, A., James, R., Beck, C., Gallego, P., Witte, M. E., . . . & Reynolds, R. (2021). Neuron-specific activation of necroptosis signaling in multiple sclerosis cortical grey matter. Acta Neuropathologica, 141(4), 585-604. https://doi.org/10.1007/s00401-021-02274-7
Rossi, F., Diniz, T., Neves, L., Fortaleza, A., Gerosa-Neto, J., Inoue, D., . . . & Freitas, I. (2017). The beneficial effects of aerobic and concurrent training on metabolic profile and body composition after detraining: a 1-year follow-up in postmenopausal women. European Journal of Clinical Nutrition, 71(5), 638-645. https://doi.org/10.1038/ejcn.2016.263
Safari, E., Sokhanguei, Y., & Fatahi, A. (2022). Effect of a combined exercise program on balance and respiratory fitness of active older men. The Scientific Journal of Rehabilitation Medicine, 11(5), 822-834. https://doi.org/10.32598/SJRM.11.5.5
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