Effect of short-term low-frequency electrical stimulation on nerve regeneration of delayed nerve defect during operation_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

 JIAO Haishan ¹ , XIAO Bo ¹ , WANG Xiaodong ² , LI Dongyin ¹ , SONG Yuening ¹ , ZHENG Hui ¹ , LIU Xiaomei ¹

1. Department of Basic Medicine, Suzhou Vocational Health College, Suzhou Jiangsu, 215009, P.R.China;
2. Department of Histology and Embryology, Medical College, Nantong University, Nantong Jiangsu, 226001, P.R.China;

Corresponding author：

JIAO Haishan, Email: jiaohaishan@szhct.edu.cn

Keywords：

Short-time low-frequency electrical stimulation; peripheral nerve; chronic injury; nerve defect repair; rat

DOI：

10.7507/1002-1892.201609024

Video：

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Objective To explore the effect of short-term low-frequency electrical stimulation (SLES) during operation on nerve regeneration in delayed peripheral nerve injury with long gap. Methods Thirty female adult Sprague Dawley rats, weighing 160-180 g, were used to prepare 13-mm defect model by trimming the nerve stumps. Then all rats were randomly divided into 2 groups, 15 rats in each group. After nerve defect was bridged by the contralateral normal sciatic nerve, SLES was applied in the experimental group, but was not in the control group. The spinal cords and dorsal root ganglions (DRGs) were harvested to carry out immunofluorescence histochemistry double staining for growth-associated proteins 43 (GAP-43) and brain-derived neurotrophic factor (BDNF) at 1, 2, and 7 days after repair. Fluorogold (FG) retrograde tracing was performed at 3 months after repair. The mid-portion regenerated segments were harvested to perform Meyer’s trichrome staining, immunofluorescence double staining for neurofilament (NF) and soluble protein 100 (S-100) on the transversely or longitudinal sections at 3 months after repair. The segment of the distal sciatic nerve trunk was harvested for electron microscopy and morphometric analyses to measure the diameter of the myelinated axons, thickness of myelin sheaths, the G ratio, and the density of the myelinated nerve fibers. The gastrocnemius muscles of the operated sides were harvested to measure the relative wet weight ratios. Karnovsky-Root cholinesterase staining of the motor endplate was carried out. Results In the experimental group, the expressions of GAP-43 and BDNF were higher than those in the control group at 1 and 2 days after repair. The number of labeled neurons in the anterior horn of gray matter in the spinal cord and DRGs at the operated side from the experimental group was more than that from the control group. Meyer’s trichrome staining, immunofluorescence double staining, and the electron microscopy observation showed that the regenerated nerves were observed to develop better in the experimental group than the control group. The relative wet weight ratio of experimental group was significantly higher than that of the control group (t=4.633,P=0.000). The size and the shape of the motor endplates in the experimental group were better than those in the control group. Conclusion SLES can promote the regeneration ability of the short-term (1 month) delayed nerve injury with long gap to a certain extent.

Citation： JIAO Haishan, XIAO Bo, WANG Xiaodong, LI Dongyin, SONG Yuening, ZHENG Hui, LIU Xiaomei. Effect of short-term low-frequency electrical stimulation on nerve regeneration of delayed nerve defect during operation. Chinese Journal of Reparative and Reconstructive Surgery, 2017, 31(3): 335-344. doi: 10.7507/1002-1892.201609024 Copy

1.	Fu SY, Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged axotomy. J Neurosci, 1995, 15(5 Pt 2): 3876-3885.
2.	Jiao HS, Yao J, Yang Y, et al. Chitosan/polyglycolic acid nerve grafts for axon regeneration from prolonged axotomized neurons to chronically denervated segments. Biomaterials, 2009, 30(28): 5004-5018.
3.	Furey MJ, Midha R, Xu QG, et al. Prolonged target deprivation reduces the capacity of injured motoneurons to regenerate. Neurosurgery, 2007, 60(4): 723-733.
4.	Gordon T, Brushart TM, Amirjani N, et al. The potential of electrical stimulation to promote functional recovery after peripheral nerve injury—comparisons between rats and humans. Acta Neurochir Suppl, 2007, 100: 3-11.
5.	Gordon T, Amirjani N, Edwards DC, et al. Brief post-surgical electrical stimulation accelerates axon regeneration and muscle reinnervation without affecting the functional measures in carpal tunnel syndrome patients. Exp Neurol, 2010, 223(1): 192-202.
6.	Sharma N, Marzo SJ, Jones KJ, et al. Electrical stimulation and testosterone differentially enhance expression of regeneration-associated genes. Exp Neurol, 2010, 223(1): 183-191.
7.	焦海山, 肖波, 刘晓梅. 术中低频电刺激对周围神经再生的影响. 神经解剖学杂志, 2013, 29(4): 475-478.
8.	Jiao H, Yao J, Song Y, et al. Morphological Proof of nerve regeneration after long-term defects of rat sciatic nerves. Int J Neurosci, 2015, 125(11): 861-874.
9.	焦海山, 姚健, 刘晓梅, 等. 自体神经桥接陈旧性周围神经缺损后雪旺细胞的组织学观察. 神经解剖学杂志, 2011, 27(4): 409-413.
10.	张艳, 熊希凯. 骨骼肌运动终板和神经纤维的酶组织化学及镀银双重显示. 中国组织化学与细胞化学杂志, 1998, 7(3): 364-365.
11.	Manivannan S, Terakawa S. Rapid sprouting of filopodia in nerve terminals of chromaffin cells, PC12 cells, and dorsal root neurons induced by electrical stimulation. J Neurosci, 1994, 14(10): 5917-5928.
12.	Nix WA, Hopf HC. Electrical stimulation of regenerating nerve and its effect on motor recovery. Brain Res, 1983, 272(1): 21-25.
13.	Brushart TM, Hoffman PN, Royall RM, et al. Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron. J Neurosci, 2002, 22(15): 6631-6638.
14.	Gordon T, Chan KM, Sulaiman OA, et al. Accelerating axon growth to overcome limitations in functional recovery after peripheral nerve injury. Neurosurgery, 2009, 65(4 Suppl): A132-144.
15.	Gordon T. The role of neurotrophic factors in nerve regeneration. Neurosurg Focus, 2009, 26(2): E3.
16.	Al-Majed AA, Tam SL, Gordon T. Electrical stimulation accelerates and enhances expression of regeneration-associated genes in regenerating rat femoral motoneurons. Cell Mol Neurobiol, 2004, 24(3): 379-402.
17.	Al-Majed AA, Brushart TM, Gordon T. Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating rat femoral motoneurons. Eur J Neurosci, 2000, 12(12): 4381-4390.
18.	Huang J, Hu X, Lu L, et al. Electrical stimulation accelerates motor functional recovery in autograft-repaired 10 mm femoral nerve gap in rats. J Neurotrauma, 2009, 26(10): 1805-1813.
19.	Huang J, Lu L, Hu X, et al. Electrical stimulation accelerates motor functional recovery in the rat model of 15-mm sciatic nerve gap bridged by scaffolds with longitudinally oriented microchannels. Neurorehabil Neural Repair, 2010, 24(8): 736-745.
20.	Haastert-Talini K, Schmitte R, Korte N, et al. Electrical stimulation accelerates axonal and functional peripheral nerve regeneration across long gaps. J Neurotrauma, 2011, 28(4): 661-674.
21.	Lundborg G, Dahlin LB, Danielsen N, et al. Nerve regeneration in silicone chambers: influence of gap length and of distal stump components. Exp Neurol, 1982, 76(2): 361-375.
22.	Al-Majed AA, Neumann CM, Brushart TM, et al. Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J Neurosci, 2000, 20(7): 2602-2608.
23.	Peyronnard JM, Charron L, Lavoie J, et al. Differences in horseradish peroxidase labeling of sensory, motor and sympathetic neurons following chronic axotomy of the rat sural nerve. Brain Res, 1986, 364(1): 137-150.
24.	姚健, 李云恺, 肖永华, 等. 陈旧性坐骨神经损伤后相关结构的组织学变化. 神经解剖学杂志, 2005, 21(5): 456-462.

1. Fu SY, Gordon T. Contributing factors to poor functional recovery after delayed nerve repair: prolonged axotomy. J Neurosci, 1995, 15(5 Pt 2): 3876-3885.
2. Jiao HS, Yao J, Yang Y, et al. Chitosan/polyglycolic acid nerve grafts for axon regeneration from prolonged axotomized neurons to chronically denervated segments. Biomaterials, 2009, 30(28): 5004-5018.
3. Furey MJ, Midha R, Xu QG, et al. Prolonged target deprivation reduces the capacity of injured motoneurons to regenerate. Neurosurgery, 2007, 60(4): 723-733.
4. Gordon T, Brushart TM, Amirjani N, et al. The potential of electrical stimulation to promote functional recovery after peripheral nerve injury—comparisons between rats and humans. Acta Neurochir Suppl, 2007, 100: 3-11.
5. Gordon T, Amirjani N, Edwards DC, et al. Brief post-surgical electrical stimulation accelerates axon regeneration and muscle reinnervation without affecting the functional measures in carpal tunnel syndrome patients. Exp Neurol, 2010, 223(1): 192-202.
6. Sharma N, Marzo SJ, Jones KJ, et al. Electrical stimulation and testosterone differentially enhance expression of regeneration-associated genes. Exp Neurol, 2010, 223(1): 183-191.
7. 焦海山, 肖波, 刘晓梅. 术中低频电刺激对周围神经再生的影响. 神经解剖学杂志, 2013, 29(4): 475-478.
8. Jiao H, Yao J, Song Y, et al. Morphological Proof of nerve regeneration after long-term defects of rat sciatic nerves. Int J Neurosci, 2015, 125(11): 861-874.
9. 焦海山, 姚健, 刘晓梅, 等. 自体神经桥接陈旧性周围神经缺损后雪旺细胞的组织学观察. 神经解剖学杂志, 2011, 27(4): 409-413.
10. 张艳, 熊希凯. 骨骼肌运动终板和神经纤维的酶组织化学及镀银双重显示. 中国组织化学与细胞化学杂志, 1998, 7(3): 364-365.
11. Manivannan S, Terakawa S. Rapid sprouting of filopodia in nerve terminals of chromaffin cells, PC12 cells, and dorsal root neurons induced by electrical stimulation. J Neurosci, 1994, 14(10): 5917-5928.
12. Nix WA, Hopf HC. Electrical stimulation of regenerating nerve and its effect on motor recovery. Brain Res, 1983, 272(1): 21-25.
13. Brushart TM, Hoffman PN, Royall RM, et al. Electrical stimulation promotes motoneuron regeneration without increasing its speed or conditioning the neuron. J Neurosci, 2002, 22(15): 6631-6638.
14. Gordon T, Chan KM, Sulaiman OA, et al. Accelerating axon growth to overcome limitations in functional recovery after peripheral nerve injury. Neurosurgery, 2009, 65(4 Suppl): A132-144.
15. Gordon T. The role of neurotrophic factors in nerve regeneration. Neurosurg Focus, 2009, 26(2): E3.
16. Al-Majed AA, Tam SL, Gordon T. Electrical stimulation accelerates and enhances expression of regeneration-associated genes in regenerating rat femoral motoneurons. Cell Mol Neurobiol, 2004, 24(3): 379-402.
17. Al-Majed AA, Brushart TM, Gordon T. Electrical stimulation accelerates and increases expression of BDNF and trkB mRNA in regenerating rat femoral motoneurons. Eur J Neurosci, 2000, 12(12): 4381-4390.
18. Huang J, Hu X, Lu L, et al. Electrical stimulation accelerates motor functional recovery in autograft-repaired 10 mm femoral nerve gap in rats. J Neurotrauma, 2009, 26(10): 1805-1813.
19. Huang J, Lu L, Hu X, et al. Electrical stimulation accelerates motor functional recovery in the rat model of 15-mm sciatic nerve gap bridged by scaffolds with longitudinally oriented microchannels. Neurorehabil Neural Repair, 2010, 24(8): 736-745.
20. Haastert-Talini K, Schmitte R, Korte N, et al. Electrical stimulation accelerates axonal and functional peripheral nerve regeneration across long gaps. J Neurotrauma, 2011, 28(4): 661-674.
21. Lundborg G, Dahlin LB, Danielsen N, et al. Nerve regeneration in silicone chambers: influence of gap length and of distal stump components. Exp Neurol, 1982, 76(2): 361-375.
22. Al-Majed AA, Neumann CM, Brushart TM, et al. Brief electrical stimulation promotes the speed and accuracy of motor axonal regeneration. J Neurosci, 2000, 20(7): 2602-2608.
23. Peyronnard JM, Charron L, Lavoie J, et al. Differences in horseradish peroxidase labeling of sensory, motor and sympathetic neurons following chronic axotomy of the rat sural nerve. Brain Res, 1986, 364(1): 137-150.
24. 姚健, 李云恺, 肖永华, 等. 陈旧性坐骨神经损伤后相关结构的组织学变化. 神经解剖学杂志, 2005, 21(5): 456-462.

Chinese Journal of Reparative and Reconstructive Surgery

Effect of short-term low-frequency electrical stimulation on nerve regeneration of delayed nerve defect during operation

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