The Curative Effect of Swimming Exercise on Electrophysiological Parameters after Sciatic Nerve Injury
Year 2023,
, 37 - 50, 31.10.2023
Osman Özocak
,
Sevil Kestane
,
Huriye Humeyra Duran
,
Bekir Coksevim
Abstract
The sciatic nerve damage can cause symptoms such as loss of muscle strength and pain as a result of trauma to the nerve due to pressure, stretching or cutting, as well as lifelong disability. Despite the increasing knowledge about sciatic nerve regeneration mechanisms, full functional recovery is still insufficient. It is well known that exercise improves overall health. The current study aimed to reveal the therapeutic effects of swimming exercises using electrophysiological methods in rats with experimental sciatic nerve injury. Eighteen male Wistar Albino rats were used in this study. The subjects were randomly divided into three groups (n=6): 1-Control (C), 2-Intact Exercise (IntE), 3-Operated Exercise (OpE) groups. Sciatic nerve injury was performed by inducing experimental damage to the left hind extremity sciatic nerve of rats. Swimming exercise was applied for 45 minutes a day, five days a week (25°C) for four weeks. The level of regeneration was evaluated by taking motor function test-sciatic function index and EMG recording performed at the beginning of the experiment (day 0), after nerve damage (day 3), and at the end of the experiment (day 35). It was determined that sciatic function index, amplitude of motor and sensory nerves, peak-peak amplitude, percentage of compound muscle action potential, motor and sensory nerve conduction velocities, which decreased after sciatic nerve injury, increased with swimming exercise (p<0.05). Positive and significant effects were observed in terms of nerve regeneration, motor functional recovery, and electrophysiological parameters in the swimming exercise groups. This study showed that swimming exercise has effective results in the level of recovery after sciatic nerve injury.
Supporting Institution
Erciyes University Scientific Research Projects Unit (BAP)
Project Number
TDK-2019-9480
Thanks
The authors wish to thank Prof. Dr .Bekir Çoksevim for guiding during this study, the participants who supported the study and the Erciyes University support.
References
- Andrade, I. R. S., Nakachima, L. R., Fernandes, M., Fernandes, C. H., Santos, J. B. G. D., & Valente, S. G. (2020). Assessment of the effects of swimming as a postoperative rehabilitation on nerve regeneration of wistar rats submitted to grafting of autologous nerves after injury to the sciatic nerve. Revista brasileira de ortopedia, 55(3), 323–328. https://doi.org/10.1055/s-0039-1692711
- Arabzadeh, E., Rahimi, A., Zargani, M., Feyz Simorghi, Z., Emami, S., Sheikhi, S., Zaeri Amirani, Z., Yousefi, P., Sarshin, A., Aghaei, F., & Feizolahi, F. (2022). Resistance exercise promotes functional test via sciatic nerve regeneration, and muscle atrophy improvement through GAP-43 regulation in animal model of traumatic nerve injuries. Neuroscience letters, 787, 136812. https://doi.org/10.1016/j.neulet.2022.136812
- Asensio-Pinilla, E., Udina, E., Jaramillo, J., & Navarro, X. (2009). Electrical stimulation combined with exercise increase axonal regeneration after peripheral nerve injury. Experimental neurology, 219(1), 258–265. https://doi.org/10.1016/j.expneurol.2009.05.034
- Ashoura, FA., Elbazb, AA., Sabeck, NA., Hazzaad, SM., Metwallyd, EM. (2015). Effect of electrical stimulation and stem cells on experimentally induced peripheral nerve injury in rats. Menoufia Med J, 28, 742-747.
- Bain, J. R., Mackinnon, S. E., & Hunter, D. A. (1989). Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plastic and reconstructive surgery, 83(1), 129–138. https://doi.org/10.1097/00006534-198901000-00024
- Bobinski, F., Martins, D. F., Bratti, T., Mazzardo-Martins, L., Winkelmann-Duarte, E. C., Guglielmo, L. G., & Santos, A. R. (2011). Neuroprotective and neuroregenerative effects of low-intensity aerobic exercise on sciatic nerve crush injury in mice. Neuroscience, 194, 337–348. https://doi.org/10.1016/j.neuroscience.2011.07.075
- Boeltz, T., Ireland, M., Mathis, K., Nicolini, J., Poplavski, K., Rose, S. J., Wilson, E., & English, A. W. (2013). Effects of treadmill training on functional recovery following peripheral nerve injury in rats. Journal of neurophysiology, 109(11), 2645–2657. https://doi.org/10.1152/jn.00946.2012
- Bonetti, L. V., Korb, A., Da Silva, S. A., Ilha, J., Marcuzzo, S., Achaval, M., & Faccioni-Heuser, M. C. (2011). Balance and coordination training after sciatic nerve injury. Muscle & nerve, 44(1), 55–62. https://doi.org/10.1002/mus.21996
- Brandt, J., Evans, J. T., Mildenhall, T., Mulligan, A., Konieczny, A., Rose, S. J., & English, A. W. (2015). Delaying the onset of treadmill exercise following peripheral nerve injury has different effects on axon regeneration and motoneuron synaptic plasticity. Journal of neurophysiology, 113(7), 2390–2399. https://doi.org/10.1152/jn.00892.2014
- Cai, J., Na, S., & Hwangbo, G. (2015). The effects of exercise intensity and initial timing on functional recovery after sciatic nerve crush injury in rats. Journal of the Korean Society of Physical Medicine. The Korean Society of Physical Medicine. https://doi.org/10.13066/kspm.2015.10.3.1
- Cannoy, J., Crowley, S., Jarratt, A., Werts, K. L., Osborne, K., Park, S., & English, A. W. (2016). Upslope treadmill exercise enhances motor axon regeneration but not functional recovery following peripheral nerve injury. Journal of Neurophysiology, 116(3), 1408–1417. https://doi.org/10.1152/jn.00129.2016
- Celebi, MT. (2013). The effects of low dose radiation and VEGF (Vascular Endothelial Growth Factor) on the repairment of sciatic nerve injury in rats. Unpublished Master Thesis. Pamukkale University, Medical Faculty Department Of Plastic Reconstructive and Aesthetic Surgery, Denizli.
- Chatzi, C., Zhang, Y., Hendricks, W. D., Chen, Y., Schnell, E., Goodman, R. H., & Westbrook, G. L. (2019). Exercise-induced enhancement of synaptic function triggered by the inverse BAR protein, Mtss1L. eLife, 8, e45920. https://doi.org/10.7554/eLife.45920
- Cobianchi, S., Casals-Diaz, L., Jaramillo, J., & Navarro, X. (2013). Differential effects of activity dependent treatments on axonal regeneration and neuropathic pain after peripheral nerve injury. Experimental neurology, 240, 157–167. https://doi.org/10.1016/j.expneurol.2012.11.023
- Dai, C., Tang, S., Li, J., Wang, J., & Xiao, X. (2014). Effects of colistin on the sensory nerve conduction velocity and F-wave in mice. Basic & clinical pharmacology & toxicology, 115(6), 577–580. https://doi.org/10.1111/bcpt.12272
- Debastiani, J. C., Santana, A. J., Ribeiro, L. F. C., Brancalhão, R. M. C., & Bertolini, G. R. F. (2019). Sericin silk protein in peripheral nervous repair associated with the physical exercise of swimming in Wistar rats. Neurological research, 41(4), 326–334. https://doi.org/10.1080/01616412.2018.1564187
- English, A. W., Chen, Y., Carp, J. S., Wolpaw, J. R., & Chen, X. Y. (2007). Recovery of electromyographic activity after transection and surgical repair of the rat sciatic nerve. Journal of neurophysiology, 97(2), 1127–1134. https://doi.org/10.1152/jn.01035.2006
- Farzamfar, S., Salehi, M., Tavangar, S. M., Verdi, J., Mansouri, K., Ai, A., Malekshahi, Z. V., & Ai, J. (2019). A novel polycaprolactone/carbon nanofiber composite as a conductive neural guidance channel: an in vitro and in vivo study. Progress in biomaterials, 8(4), 239–248. https://doi.org/10.1007/s40204-019-00121-3
- Figueiredo, G. S. L., Fernandes, M., Atti, V. N., Valente, S. G., Roth, F., Nakachima, L. R., Santos, J. B. G. D., & Fernandes, C. H. (2022). Use of aerobic treadmill exercises on nerve regeneration after sciatic nerve injury in spontaneously hypertensive rats. Acta Cirurgica Brasileira, 37(8), e370804. https://doi.org/10.1590/acb370804
- Goulart, C. O., Jürgensen, S., Souto, A., Oliveira, J. T., de Lima, S., Tonda-Turo, C., Marques, S. A., de Almeida, F. M., & Martinez, A. M. (2014). A combination of Schwann-cell grafts and aerobic exercise enhances sciatic nerve regeneration. PloS one, 9(10), e110090. https://doi.org/10.1371/journal.pone.0110090
- Han, D., Lu, J., Xu, L., & Xu, J. (2015). Comparison of two electrophysiological methods for the assessment of progress in a rat model of nerve repair. International Journal of Clinical and Experimental Medicine, 8(2), 2392–2398.
- Hirata, K., & Kawabuchi, M. (2002). Myelin phagocytosis by macrophages and nonmacrophages during Wallerian degeneration. Microscopy Research and Technique, 57(6), 541–547. https://doi.org/10.1002/jemt.10108
- Hu, J., Zhu, Q. T., Liu, X. L., Xu, Y. B., & Zhu, J. K. (2007). Repair of extended peripheral nerve lesions in rhesus monkeys using acellular allogenic nerve grafts implanted with autologous mesenchymal stem cells. Experimental Neurology, 204(2), 658–666. https://doi.org/10.1016/j.expneurol.2006.11.018
- Iijima, Y., Ajiki, T., Murayama, A., & Takeshita, K. (2016). Effect of artificial nerve conduit vascularization on peripheral nerve in a necrotic bed. plastic and reconstructive surgery. Global Open, 4(3), e665. https://doi.org/10.1097/GOX.0000000000000652
- Ilha, J., Araujo, R. T., Malysz, T., Hermel, E. E., Rigon, P., Xavier, L. L., & Achaval, M. (2008). Endurance and resistance exercise training programs elicit specific effects on sciatic nerve regeneration after experimental traumatic lesion in rats. Neurorehabilitation and Neural Repair, 22(4), 355–366. https://doi.org/10.1177/1545968307313502
- Kavlak, E., Belge, F., Unsal, C., Uner, A. G., Cavlak, U., & Cömlekçi, S. (2014). Effects of pulsed electromagnetic field and swimming exercise on rats with experimental sciatic nerve injury. Journal of Physical Therapy Science, 26(9), 1355–1361. https://doi.org/10.1589/jpts.26.1355
- Kuzay, D., Kestane, S., Kemerli MZ., Ozocak, O., Aktoprak, M., Coksevim, B (2022). The effect of exercise and mesenchimal stem cell application on plasma oxidative stress levels in experimental neuropathy. Turkish Journal of Health and Sport. 3 (1), 20-25.
- Lee, S. K., & Wolfe, S. W. (2000). Peripheral nerve injury and repair. The Journal of the American Academy of Orthopaedic Surgeons, 8(4), 243–252. https://doi.org/10.5435/00124635-200007000-00005
- Liao, C. F., Yang, T. Y., Chen, Y. H., Yao, C. H., Way, T. D., & Chen, Y. S. (2017). Effects of swimming exercise on nerve regeneration in a rat sciatic nerve transection model. BioMedicine, 7(1), 3. https://doi.org/10.1051/bmdcn/2017070103
- López-Álvarez, V. M., Modol, L., Navarro, X., & Cobianchi, S. (2015). Early increasing-intensity treadmill exercise reduces neuropathic pain by preventing nociceptor collateral sprouting and disruption of chloride cotransporters homeostasis after peripheral nerve injury. Pain, 156(9), 1812–1825.
- Marqueste, T., Alliez, J. R., Alluin, O., Jammes, Y., & Decherchi, P. (2004). Neuromuscular rehabilitation by treadmill running or electrical stimulation after peripheral nerve injury and repair. Journal of applied physiology (Bethesda, Md. : 1985), 96(5), 1988–1995. https://doi.org/10.1152/japplphysiol.00775.2003
- Martins, D. F., Martins, T. C., Batisti, A. P., Dos Santos Leonel, L., Bobinski, F., Belmonte, L. A. O., Mazzardo-Martins, L., Cargnin-Ferreira, E., & Santos, A. R. S. (2018). Long-Term regular eccentric exercise decreases neuropathic pain-like behavior and improves motor functional recovery in an axonotmesis mouse model: the role of insulin-like growth factor-1. Molecular Neurobiology, 55(7), 6155–6168. https://doi.org/10.1007/s12035-017-0829-3
- Mendonça, A. C., Barbieri, C. H., & Mazzer, N. (2003). Directly applied low intensity direct electric current enhances peripheral nerve regeneration in rats. Journal of Neuroscience Methods, 129(2), 183–190. https://doi.org/10.1016/s0165-0270(03)00207-3
- Minegishi, Y., Nishimoto, J., Uto, M., Ozone, K., Oka, Y., Kokubun, T., Murata, K., Takemoto, H., & Kanemura, N. (2022). Effects of exercise on muscle reinnervation and plasticity of spinal circuits in rat sciatic nerve crush injury models with different numbers of crushes. Muscle & Nerve, 65(5), 612–620. https://doi.org/10.1002/mus.27512
- Mohammadi, R., Vahabzadeh, B., & Amini, K. (2014). Sciatic nerve regeneration induced by transplantation of in vitro bone marrow stromal cells into an inside-out artery graft in rat. Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery, 42(7), 1389–1396. https://doi.org/10.1016/j.jcms.2014.03.031
- Oliveira, L. S., Sobral, L. L., Takeda, S. Y., Betini, J., Guirro, R. R., Somazz, M. C., & Teodori, R. M. (2008). Electrical stimulation and swimming in the acute phase of axonotmesis: their influence on nerve regeneration and functional recovery. Revista de Neurologia, 47(1), 11–15.
- Ozocak, O. (2022). The effect of exercise and mesenchymal stem cell (MSC) Applications on muscular performance in sciatic nerve damage. Unpublished Doctoral Thesis. Erciyes University Health Sciences Institute. Kayseri.
- Park, J. S., & Höke, A. (2014). Treadmill exercise induced functional recovery after peripheral nerve repair is associated with increased levels of neurotrophic factors. PloS one, 9(3), e90245. https://doi.org/10.1371/journal.pone.0090245
- Pollari, E., Prior, R., Robberecht, W., Van Damme, P., & Van Den Bosch, L. (2018). In vivo electrophysiological measurement of compound muscle action potential from the forelimbs in mouse models of motor neuron degeneration. Journal of visualized experiments : JoVE, (136), 57741. https://doi.org/10.3791/57741
- Rodinskii, A. G., Serdyuchenko, I. Y., & Demchenko, T. V. (2013). Electrical and force responses of the shin muscles of rats after unilateral compression of the sciatic nerve and systemic introduction of gamma-hydroxybutyrate. Neurophysiology, 45(2), 157-167. https://doi.org/10.1007/s11062-013-9352-y
- Rosa Junior, G. M.; Magalhães, R. M. G.; Rosa, V. C.; Bueno, C. R. de S.; Simionato, L. H.; Bortoluci, C. H. F. (2016). Effect of the laser therapy in association with swimming for a morphological nerve repair and functional recovery in rats submitted to sciatic axonotmesis, SciELO Journals. Dataset. https://doi.org/10.6084/m9.figshare.20015447.v1
- Sabatier, M. J., Redmon, N., Schwartz, G., & English, A. W. (2008). Treadmill training promotes axon regeneration in injured peripheral nerves. Experimental Neurology, 211(2), 489–493. https://doi.org/10.1016/j.expneurol.2008.02.013
- Sakar M. (2010). The effect of poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) PHBHHX and mesenchymal stem cell ( MSC ) on axonal regeneration in experimental sciatic nerve damage. Master Hacettepe University Faculty Of Medicine, in Neurosurgery. Ankara.
- Selagzi, H., Buyukakilli, B., Cimen, B., Yilmaz, N., & Erdogan, S. (2008). Protective and therapeutic effects of swimming exercise training on diabetic peripheral neuropathy of streptozotocin-induced diabetic rats. Journal of Endocrinological Investigation, 31(11), 971–978. https://doi.org/10.1007/BF03345634
- Silva, L. E., Valim, V., Pessanha, A. P., Oliveira, L. M., Myamoto, S., Jones, A., & Natour, J. (2008). Hydrotherapy versus conventional land-based exercise for the management of patients with osteoarthritis of the knee: a randomized clinical trial. Physical Therapy, 88(1), 12–21. https://doi.org/10.2522/ptj.20060040
- Teodori, R. M., Betini, J., de Oliveira, L. S., Sobral, L. L., Takeda, S. Y., & de Lima Montebelo, M. I. (2011). Swimming exercise in the acute or late phase after sciatic nerve crush accelerates nerve regeneration. Neural Plasticity, 783901. https://doi.org/10.1155/2011/783901
- Tsai, S. W., Chen, C. J., Chen, H. L., Chen, C. M., & Chang, Y. Y. (2012). Effects of treadmill running on rat gastrocnemius function following botulinum toxin A injection. Journal of Orthopaedic Research : Official Publication of the Orthopaedic Research Society, 30(2), 319–324. https://doi.org/10.1002/jor.21509
- Udina, E., Cobianchi, S., Allodi, I., & Navarro, X. (2011). Effects of activity-dependent strategies on regeneration and plasticity after peripheral nerve injuries. Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft, 193(4), 347–353. https://doi.org/10.1016/j.aanat.2011.02.012
- Van Meeteren, N. L., Brakkee, J. H., Hamers, F. P., Helders, P. J., & Gispen, W. H. (1997). Exercise training improves functional recovery and motor nerve conduction velocity after sciatic nerve crush lesion in the rat. Archives of Physical Medicine and Rehabilitation, 78(1), 70–77. https://doi.org/10.1016/s0003-9993(97)90013-7
- Wang, J., Yang, C. C., Chen, S. C., & Hsieh, Y. L. (2010). No synergistic effect of mesenchymal stem cells and exercise on functional recovery following sciatic nerve transection. Functional Neurology, 25(1), 33–43.
- Wariyar, S. S., Brown, A. D., Tian, T., Pottorf, T. S., & Ward, P. J. (2022). Angiogenesis is critical for the exercise-mediated enhancement of axon regeneration following peripheral nerve injury. Experimental Neurology, 353, 114029. https://doi.org/10.1016/j.expneurol.2022.114029
- Widick, M. H., Tanabe, T., Fortune, S., & Zealear, D. L. (1994). Awake evoked electromyography recording from the chronically implanted rat. The Laryngoscope, 104(4), 420–425. https://doi.org/10.1288/00005537-199404000-00005
- Yang, C. C., Wang, J., Chen, S. C., Jan, Y. M., & Hsieh, Y. L. (2015). Enhanced functional recovery from sciatic nerve crush injury through a combined treatment of cold-water swimming and mesenchymal stem cell transplantation. Neurological Research, 37(9), 816–826.
Yüzme Egzersizinin Siyatik Sinir Hasarı Sonrasında Elektrofizyolojik Parametreler Üzerindeki İyileştirici Etkisi
Year 2023,
, 37 - 50, 31.10.2023
Osman Özocak
,
Sevil Kestane
,
Huriye Humeyra Duran
,
Bekir Coksevim
Abstract
Siyatik sinir hasarı, sinirin basınç, gerilme veya kesilme gibi nedenlerle travmaya uğraması sonucu kas gücü kaybı ve ağrı gibi semptomlara neden olduğu gibi hatta yaşam boyu sakatlığa da neden olabilmektedir. Rejenerasyon mekanizmaları hakkındaki bilgilerin artmasına rağmen tam fonksiyonel iyileşme hala yetersizdir. Egzersizin genel sağlığı iyileştirerek fiziksel ve psikolojik refahı arttırdığı iyi bilinmektedir. Bu çalışmada yüzme egzersizlerinin, deneysel siyatik sinir yaralanması olan sıçanlarda elektrofizyolojik yöntemler kullanılarak terapötik etkilerinin ortaya çıkarılması amaçlandı. Bu çalışmada 18 adet erkek Wistar Albino rat kullanıldı. Denekler rastgele üç gruba (n=6) ayrıldı: 1-Kontrol (K) grubu, 2-İntak Egzersiz (IntE) grubu, 3-Opere Egzersiz (OpE) grubu. Siyatik sinir hasarı, sıçanların sol arka ekstremite siyatik sinirinde deneysel hasar oluşturularak gerçekleştirildi. Dört hafta süresince, haftada beş gün, günde 45 dakika yüzme egzersizi uygulandı (25°C). Rejenerasyon düzeyi, deney başında (0. gün), sinir hasarı sonrası (3. gün) ve deney sonunda (35. gün) yapılan motor fonksiyon testi-siyatik fonksiyon indeksi ve EMG kaydı alınarak değerlendirildi. Siyatik sinir hasarı sonrası azalan siyatik fonksiyon indeksi, motor ve duyu sinirlerinin amplitüdü, peak-peak amplitüdü, bileşik kas aksiyon potansiyeli yüzdesi, motor ve duyusal sinir iletim hızlarının yüzme egzersizi ile arttığı belirlendi (p<0,05). Yüzme Egzersizi yapılan gruplarda sinir rejenerasyonu, motor fonksiyonel iyileşme ve elektrofizyolojik parametreler açısından olumlu ve anlamlı etkiler gözlendi. Bu çalışma yüzme egzersizinin siyatik sinir hasarı sonrasında toparlanma düzeyinde etkili sonuçlar olduğunu gösterdi.
Project Number
TDK-2019-9480
References
- Andrade, I. R. S., Nakachima, L. R., Fernandes, M., Fernandes, C. H., Santos, J. B. G. D., & Valente, S. G. (2020). Assessment of the effects of swimming as a postoperative rehabilitation on nerve regeneration of wistar rats submitted to grafting of autologous nerves after injury to the sciatic nerve. Revista brasileira de ortopedia, 55(3), 323–328. https://doi.org/10.1055/s-0039-1692711
- Arabzadeh, E., Rahimi, A., Zargani, M., Feyz Simorghi, Z., Emami, S., Sheikhi, S., Zaeri Amirani, Z., Yousefi, P., Sarshin, A., Aghaei, F., & Feizolahi, F. (2022). Resistance exercise promotes functional test via sciatic nerve regeneration, and muscle atrophy improvement through GAP-43 regulation in animal model of traumatic nerve injuries. Neuroscience letters, 787, 136812. https://doi.org/10.1016/j.neulet.2022.136812
- Asensio-Pinilla, E., Udina, E., Jaramillo, J., & Navarro, X. (2009). Electrical stimulation combined with exercise increase axonal regeneration after peripheral nerve injury. Experimental neurology, 219(1), 258–265. https://doi.org/10.1016/j.expneurol.2009.05.034
- Ashoura, FA., Elbazb, AA., Sabeck, NA., Hazzaad, SM., Metwallyd, EM. (2015). Effect of electrical stimulation and stem cells on experimentally induced peripheral nerve injury in rats. Menoufia Med J, 28, 742-747.
- Bain, J. R., Mackinnon, S. E., & Hunter, D. A. (1989). Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plastic and reconstructive surgery, 83(1), 129–138. https://doi.org/10.1097/00006534-198901000-00024
- Bobinski, F., Martins, D. F., Bratti, T., Mazzardo-Martins, L., Winkelmann-Duarte, E. C., Guglielmo, L. G., & Santos, A. R. (2011). Neuroprotective and neuroregenerative effects of low-intensity aerobic exercise on sciatic nerve crush injury in mice. Neuroscience, 194, 337–348. https://doi.org/10.1016/j.neuroscience.2011.07.075
- Boeltz, T., Ireland, M., Mathis, K., Nicolini, J., Poplavski, K., Rose, S. J., Wilson, E., & English, A. W. (2013). Effects of treadmill training on functional recovery following peripheral nerve injury in rats. Journal of neurophysiology, 109(11), 2645–2657. https://doi.org/10.1152/jn.00946.2012
- Bonetti, L. V., Korb, A., Da Silva, S. A., Ilha, J., Marcuzzo, S., Achaval, M., & Faccioni-Heuser, M. C. (2011). Balance and coordination training after sciatic nerve injury. Muscle & nerve, 44(1), 55–62. https://doi.org/10.1002/mus.21996
- Brandt, J., Evans, J. T., Mildenhall, T., Mulligan, A., Konieczny, A., Rose, S. J., & English, A. W. (2015). Delaying the onset of treadmill exercise following peripheral nerve injury has different effects on axon regeneration and motoneuron synaptic plasticity. Journal of neurophysiology, 113(7), 2390–2399. https://doi.org/10.1152/jn.00892.2014
- Cai, J., Na, S., & Hwangbo, G. (2015). The effects of exercise intensity and initial timing on functional recovery after sciatic nerve crush injury in rats. Journal of the Korean Society of Physical Medicine. The Korean Society of Physical Medicine. https://doi.org/10.13066/kspm.2015.10.3.1
- Cannoy, J., Crowley, S., Jarratt, A., Werts, K. L., Osborne, K., Park, S., & English, A. W. (2016). Upslope treadmill exercise enhances motor axon regeneration but not functional recovery following peripheral nerve injury. Journal of Neurophysiology, 116(3), 1408–1417. https://doi.org/10.1152/jn.00129.2016
- Celebi, MT. (2013). The effects of low dose radiation and VEGF (Vascular Endothelial Growth Factor) on the repairment of sciatic nerve injury in rats. Unpublished Master Thesis. Pamukkale University, Medical Faculty Department Of Plastic Reconstructive and Aesthetic Surgery, Denizli.
- Chatzi, C., Zhang, Y., Hendricks, W. D., Chen, Y., Schnell, E., Goodman, R. H., & Westbrook, G. L. (2019). Exercise-induced enhancement of synaptic function triggered by the inverse BAR protein, Mtss1L. eLife, 8, e45920. https://doi.org/10.7554/eLife.45920
- Cobianchi, S., Casals-Diaz, L., Jaramillo, J., & Navarro, X. (2013). Differential effects of activity dependent treatments on axonal regeneration and neuropathic pain after peripheral nerve injury. Experimental neurology, 240, 157–167. https://doi.org/10.1016/j.expneurol.2012.11.023
- Dai, C., Tang, S., Li, J., Wang, J., & Xiao, X. (2014). Effects of colistin on the sensory nerve conduction velocity and F-wave in mice. Basic & clinical pharmacology & toxicology, 115(6), 577–580. https://doi.org/10.1111/bcpt.12272
- Debastiani, J. C., Santana, A. J., Ribeiro, L. F. C., Brancalhão, R. M. C., & Bertolini, G. R. F. (2019). Sericin silk protein in peripheral nervous repair associated with the physical exercise of swimming in Wistar rats. Neurological research, 41(4), 326–334. https://doi.org/10.1080/01616412.2018.1564187
- English, A. W., Chen, Y., Carp, J. S., Wolpaw, J. R., & Chen, X. Y. (2007). Recovery of electromyographic activity after transection and surgical repair of the rat sciatic nerve. Journal of neurophysiology, 97(2), 1127–1134. https://doi.org/10.1152/jn.01035.2006
- Farzamfar, S., Salehi, M., Tavangar, S. M., Verdi, J., Mansouri, K., Ai, A., Malekshahi, Z. V., & Ai, J. (2019). A novel polycaprolactone/carbon nanofiber composite as a conductive neural guidance channel: an in vitro and in vivo study. Progress in biomaterials, 8(4), 239–248. https://doi.org/10.1007/s40204-019-00121-3
- Figueiredo, G. S. L., Fernandes, M., Atti, V. N., Valente, S. G., Roth, F., Nakachima, L. R., Santos, J. B. G. D., & Fernandes, C. H. (2022). Use of aerobic treadmill exercises on nerve regeneration after sciatic nerve injury in spontaneously hypertensive rats. Acta Cirurgica Brasileira, 37(8), e370804. https://doi.org/10.1590/acb370804
- Goulart, C. O., Jürgensen, S., Souto, A., Oliveira, J. T., de Lima, S., Tonda-Turo, C., Marques, S. A., de Almeida, F. M., & Martinez, A. M. (2014). A combination of Schwann-cell grafts and aerobic exercise enhances sciatic nerve regeneration. PloS one, 9(10), e110090. https://doi.org/10.1371/journal.pone.0110090
- Han, D., Lu, J., Xu, L., & Xu, J. (2015). Comparison of two electrophysiological methods for the assessment of progress in a rat model of nerve repair. International Journal of Clinical and Experimental Medicine, 8(2), 2392–2398.
- Hirata, K., & Kawabuchi, M. (2002). Myelin phagocytosis by macrophages and nonmacrophages during Wallerian degeneration. Microscopy Research and Technique, 57(6), 541–547. https://doi.org/10.1002/jemt.10108
- Hu, J., Zhu, Q. T., Liu, X. L., Xu, Y. B., & Zhu, J. K. (2007). Repair of extended peripheral nerve lesions in rhesus monkeys using acellular allogenic nerve grafts implanted with autologous mesenchymal stem cells. Experimental Neurology, 204(2), 658–666. https://doi.org/10.1016/j.expneurol.2006.11.018
- Iijima, Y., Ajiki, T., Murayama, A., & Takeshita, K. (2016). Effect of artificial nerve conduit vascularization on peripheral nerve in a necrotic bed. plastic and reconstructive surgery. Global Open, 4(3), e665. https://doi.org/10.1097/GOX.0000000000000652
- Ilha, J., Araujo, R. T., Malysz, T., Hermel, E. E., Rigon, P., Xavier, L. L., & Achaval, M. (2008). Endurance and resistance exercise training programs elicit specific effects on sciatic nerve regeneration after experimental traumatic lesion in rats. Neurorehabilitation and Neural Repair, 22(4), 355–366. https://doi.org/10.1177/1545968307313502
- Kavlak, E., Belge, F., Unsal, C., Uner, A. G., Cavlak, U., & Cömlekçi, S. (2014). Effects of pulsed electromagnetic field and swimming exercise on rats with experimental sciatic nerve injury. Journal of Physical Therapy Science, 26(9), 1355–1361. https://doi.org/10.1589/jpts.26.1355
- Kuzay, D., Kestane, S., Kemerli MZ., Ozocak, O., Aktoprak, M., Coksevim, B (2022). The effect of exercise and mesenchimal stem cell application on plasma oxidative stress levels in experimental neuropathy. Turkish Journal of Health and Sport. 3 (1), 20-25.
- Lee, S. K., & Wolfe, S. W. (2000). Peripheral nerve injury and repair. The Journal of the American Academy of Orthopaedic Surgeons, 8(4), 243–252. https://doi.org/10.5435/00124635-200007000-00005
- Liao, C. F., Yang, T. Y., Chen, Y. H., Yao, C. H., Way, T. D., & Chen, Y. S. (2017). Effects of swimming exercise on nerve regeneration in a rat sciatic nerve transection model. BioMedicine, 7(1), 3. https://doi.org/10.1051/bmdcn/2017070103
- López-Álvarez, V. M., Modol, L., Navarro, X., & Cobianchi, S. (2015). Early increasing-intensity treadmill exercise reduces neuropathic pain by preventing nociceptor collateral sprouting and disruption of chloride cotransporters homeostasis after peripheral nerve injury. Pain, 156(9), 1812–1825.
- Marqueste, T., Alliez, J. R., Alluin, O., Jammes, Y., & Decherchi, P. (2004). Neuromuscular rehabilitation by treadmill running or electrical stimulation after peripheral nerve injury and repair. Journal of applied physiology (Bethesda, Md. : 1985), 96(5), 1988–1995. https://doi.org/10.1152/japplphysiol.00775.2003
- Martins, D. F., Martins, T. C., Batisti, A. P., Dos Santos Leonel, L., Bobinski, F., Belmonte, L. A. O., Mazzardo-Martins, L., Cargnin-Ferreira, E., & Santos, A. R. S. (2018). Long-Term regular eccentric exercise decreases neuropathic pain-like behavior and improves motor functional recovery in an axonotmesis mouse model: the role of insulin-like growth factor-1. Molecular Neurobiology, 55(7), 6155–6168. https://doi.org/10.1007/s12035-017-0829-3
- Mendonça, A. C., Barbieri, C. H., & Mazzer, N. (2003). Directly applied low intensity direct electric current enhances peripheral nerve regeneration in rats. Journal of Neuroscience Methods, 129(2), 183–190. https://doi.org/10.1016/s0165-0270(03)00207-3
- Minegishi, Y., Nishimoto, J., Uto, M., Ozone, K., Oka, Y., Kokubun, T., Murata, K., Takemoto, H., & Kanemura, N. (2022). Effects of exercise on muscle reinnervation and plasticity of spinal circuits in rat sciatic nerve crush injury models with different numbers of crushes. Muscle & Nerve, 65(5), 612–620. https://doi.org/10.1002/mus.27512
- Mohammadi, R., Vahabzadeh, B., & Amini, K. (2014). Sciatic nerve regeneration induced by transplantation of in vitro bone marrow stromal cells into an inside-out artery graft in rat. Journal of cranio-maxillo-facial surgery : official publication of the European Association for Cranio-Maxillo-Facial Surgery, 42(7), 1389–1396. https://doi.org/10.1016/j.jcms.2014.03.031
- Oliveira, L. S., Sobral, L. L., Takeda, S. Y., Betini, J., Guirro, R. R., Somazz, M. C., & Teodori, R. M. (2008). Electrical stimulation and swimming in the acute phase of axonotmesis: their influence on nerve regeneration and functional recovery. Revista de Neurologia, 47(1), 11–15.
- Ozocak, O. (2022). The effect of exercise and mesenchymal stem cell (MSC) Applications on muscular performance in sciatic nerve damage. Unpublished Doctoral Thesis. Erciyes University Health Sciences Institute. Kayseri.
- Park, J. S., & Höke, A. (2014). Treadmill exercise induced functional recovery after peripheral nerve repair is associated with increased levels of neurotrophic factors. PloS one, 9(3), e90245. https://doi.org/10.1371/journal.pone.0090245
- Pollari, E., Prior, R., Robberecht, W., Van Damme, P., & Van Den Bosch, L. (2018). In vivo electrophysiological measurement of compound muscle action potential from the forelimbs in mouse models of motor neuron degeneration. Journal of visualized experiments : JoVE, (136), 57741. https://doi.org/10.3791/57741
- Rodinskii, A. G., Serdyuchenko, I. Y., & Demchenko, T. V. (2013). Electrical and force responses of the shin muscles of rats after unilateral compression of the sciatic nerve and systemic introduction of gamma-hydroxybutyrate. Neurophysiology, 45(2), 157-167. https://doi.org/10.1007/s11062-013-9352-y
- Rosa Junior, G. M.; Magalhães, R. M. G.; Rosa, V. C.; Bueno, C. R. de S.; Simionato, L. H.; Bortoluci, C. H. F. (2016). Effect of the laser therapy in association with swimming for a morphological nerve repair and functional recovery in rats submitted to sciatic axonotmesis, SciELO Journals. Dataset. https://doi.org/10.6084/m9.figshare.20015447.v1
- Sabatier, M. J., Redmon, N., Schwartz, G., & English, A. W. (2008). Treadmill training promotes axon regeneration in injured peripheral nerves. Experimental Neurology, 211(2), 489–493. https://doi.org/10.1016/j.expneurol.2008.02.013
- Sakar M. (2010). The effect of poly(3-hydroxybutyrate-co-3-hydroxyhexanoate) PHBHHX and mesenchymal stem cell ( MSC ) on axonal regeneration in experimental sciatic nerve damage. Master Hacettepe University Faculty Of Medicine, in Neurosurgery. Ankara.
- Selagzi, H., Buyukakilli, B., Cimen, B., Yilmaz, N., & Erdogan, S. (2008). Protective and therapeutic effects of swimming exercise training on diabetic peripheral neuropathy of streptozotocin-induced diabetic rats. Journal of Endocrinological Investigation, 31(11), 971–978. https://doi.org/10.1007/BF03345634
- Silva, L. E., Valim, V., Pessanha, A. P., Oliveira, L. M., Myamoto, S., Jones, A., & Natour, J. (2008). Hydrotherapy versus conventional land-based exercise for the management of patients with osteoarthritis of the knee: a randomized clinical trial. Physical Therapy, 88(1), 12–21. https://doi.org/10.2522/ptj.20060040
- Teodori, R. M., Betini, J., de Oliveira, L. S., Sobral, L. L., Takeda, S. Y., & de Lima Montebelo, M. I. (2011). Swimming exercise in the acute or late phase after sciatic nerve crush accelerates nerve regeneration. Neural Plasticity, 783901. https://doi.org/10.1155/2011/783901
- Tsai, S. W., Chen, C. J., Chen, H. L., Chen, C. M., & Chang, Y. Y. (2012). Effects of treadmill running on rat gastrocnemius function following botulinum toxin A injection. Journal of Orthopaedic Research : Official Publication of the Orthopaedic Research Society, 30(2), 319–324. https://doi.org/10.1002/jor.21509
- Udina, E., Cobianchi, S., Allodi, I., & Navarro, X. (2011). Effects of activity-dependent strategies on regeneration and plasticity after peripheral nerve injuries. Annals of anatomy = Anatomischer Anzeiger : official organ of the Anatomische Gesellschaft, 193(4), 347–353. https://doi.org/10.1016/j.aanat.2011.02.012
- Van Meeteren, N. L., Brakkee, J. H., Hamers, F. P., Helders, P. J., & Gispen, W. H. (1997). Exercise training improves functional recovery and motor nerve conduction velocity after sciatic nerve crush lesion in the rat. Archives of Physical Medicine and Rehabilitation, 78(1), 70–77. https://doi.org/10.1016/s0003-9993(97)90013-7
- Wang, J., Yang, C. C., Chen, S. C., & Hsieh, Y. L. (2010). No synergistic effect of mesenchymal stem cells and exercise on functional recovery following sciatic nerve transection. Functional Neurology, 25(1), 33–43.
- Wariyar, S. S., Brown, A. D., Tian, T., Pottorf, T. S., & Ward, P. J. (2022). Angiogenesis is critical for the exercise-mediated enhancement of axon regeneration following peripheral nerve injury. Experimental Neurology, 353, 114029. https://doi.org/10.1016/j.expneurol.2022.114029
- Widick, M. H., Tanabe, T., Fortune, S., & Zealear, D. L. (1994). Awake evoked electromyography recording from the chronically implanted rat. The Laryngoscope, 104(4), 420–425. https://doi.org/10.1288/00005537-199404000-00005
- Yang, C. C., Wang, J., Chen, S. C., Jan, Y. M., & Hsieh, Y. L. (2015). Enhanced functional recovery from sciatic nerve crush injury through a combined treatment of cold-water swimming and mesenchymal stem cell transplantation. Neurological Research, 37(9), 816–826.