Experimental study of the effect of the sciatic nerve elongation on pain in rats_Chinese Journal of Reparative and Reconstructive Surgery

Authors：

LI Xingwei , SHA Rula , BAO Bingbo , GAO Tao , LIN Junqing ,  ZHENG Xianyou

Department of Orthopedics, Shanghai Jiao Tong University Affiliated Sixth People’s Hospital, Shanghai, 200233, P.R.China;

Corresponding author：

ZHENG Xianyou, Email: zhengxianyou@126.com

Keywords：

Peripheral nerve defect; nerve elongation; autotomy; pain; rat

DOI：

10.7507/1002-1892.2018120912

Video：

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Objective To investigate the effect of the sciatic nerve elongation on pain in rats. Methods Thirty-six adult male Wistar rats of SPF grade, weighing 250-300 g. Eighteen of them were randomly divided into 3 groups, 6 rats in each group. They were sciatic nerve elongation group (group A), nerve no-elongation group (group B), and nerve ligation group (group C). The model of 10-mm sciatic nerve defect was established in all 3 groups. The sciatic nerve was extended at a speed of 1 mm/d for 14 days in group A. The group B was only installed with external fixation. The nerve stumps were ligated in the group C. At 3, 7, 10, and 14 days after operation, the foot injury was evaluated by the autotomy scoring scale. At 14 days after operation, the dorsal root ganglia (DRG) of L₄-S₁ spinal cord of rats in each group was observed by tumor necrosis factor α (TNF-α) immunohistochemical staining, and the primary antibodies were replaced by pure serum as negative control group. Another 18 rats were randomly divided into 3 groups, 6 rats in each group. They were sciatic nerve elongation group (group A1), nerve no-elongation group (group B1), positive control group (group C1). In groups A1 and B1, the 10-mm long sciatic nerve defect model was established by the same method as groups A and B, and then fixed with external fixation. Nerve elongation was done or not done without anesthesia at 3 days after operation. In group C1, no modeling was done and 20 μL 2.5% formaldehyde was injected into the toes. After 90 minutes, the dorsal horn of spinal cord of L₄-S₁ segment of rats was cutting for c-Fos immunohistochemical staining and the number of positive cells was counted. Primary antibodies were replaced with pure serum as negative control group. Results The autotomy scores of rats in groups B and C gradually increased postoperatively, and group A remained stable at 0.25±0.50. The scores of group C were significantly higher than those of group A and group B at each time point postoperatively (P<0.05). The scores of group A were significantly lower than those of group B at 10 and 14 days postoperatively (P<0.05). TNF-α immunohistochemical staining showed that the TNF-α expression in group A was weak, slightly positive (+/-); in group B was positive (+); in group C was strongly positive (++); and the negative control group had no TNF-α expression (-). c-Fos immunohistochemical staining showed that the c-Fos expressions in groups A1 and B1 were weak positive, in group C1 was strong positive, and negative control group had no c-Fos positive expression. The number of c-Fos positive cells in groups A1, B1, C1, and negative control group were (21.5±6.6), (19.3±8.1), (95.6±7.4), and 0 cells/field, respectively, and group C1 was significantly higher than groups A1 and B1 (P<0.05), there was no significant difference between group A1 and group B1 (P>0.05). Conclusion Nerve elongation does not cause obvious pain neither during the operation of elongation nor throughout the whole elongation.

Citation： LI Xingwei, SHA Rula, BAO Bingbo, GAO Tao, LIN Junqing, ZHENG Xianyou. Experimental study of the effect of the sciatic nerve elongation on pain in rats. Chinese Journal of Reparative and Reconstructive Surgery, 2019, 33(7): 894-900. doi: 10.7507/1002-1892.2018120912 Copy

1.	Battiston B, Titolo P, Ciclamini D, et al. Peripheral nerve defects: overviews of practice in europe. Hand Clin, 2017, 33(3): 545-550.
2.	顾玉东. 周围神经缺损的基本概念与治疗原则. 中华手外科杂志, 2002, 18(3): 129-130.
3.	顾玉东. 周围神经缺损的治疗现状与进展. 中华创伤杂志, 2002, 18(9): 517-519.
4.	Winfree CJ. Peripheral nerve injury evaluation and management. Curr Surg, 2005, 62(5): 469-476.
5.	侯春林. 长段周围神经缺损的治疗策略. 中华创伤杂志, 2007, 23(6): 401-402.
6.	Wolford LM, Rodrigues DB. Autogenous grafts/allografts/conduits for bridging peripheral trigeminal nerve gaps. Atlas Oral Maxillofac Surg Clin North Am, 2011, 19(1): 91-107.
7.	徐筑秋, 杨晓楠, 祁佐良. 细胞自噬在周围神经损伤及再生中研究进展. 中国修复重建外科杂志, 2017, 31(1): 122-125.
8.	Saijilafu, Nishiura Y, Hara Y, et al. Gradual stretching of the proximal nerve stump induces the growth of regenerating sprouts in rats. J Orthop Res, 2008, 26(7): 1012-1017.
9.	Loverde JR, Ozoka VC, Aquino R, et al. Live imaging of axon stretch growth in embryonic and adult neurons. J Neurotrauma, 2011, 28(11): 2389-2403.
10.	Manders EK, Saggers GC, Diaz-Alonso P, et al. Elongation of peripheral nerve and viscera containing smooth muscle. Clin Plast Surg, 1987, 14(3): 551-562.
11.	寇玉辉, 姜保国. 周围神经缺损修复新方法—神经延长术. 北京大学学报: 医学版, 2016, 48(5): 753-755.
12.	Pfister BJ, Iwata A, Meaney DF, et al. Extreme stretch growth of integrated axons. J Neurosci, 2004, 24(36): 7978-7983.
13.	Baoguo J, Shibata M, Matsuzaki H, et al. Proximal nerve elongation vs nerve grafting in repairing segmental nerve defects in rabbits. Microsurgery, 2004, 24(3): 213-217.
14.	Wall PD, Devor M, Inbal R, et al. Autotomy following peripheral nerve lesions: experimental anaesthesia dolorosa. Pain, 1979, 7(2): 103-111.
15.	Uehara J, Kuboki T, Fujisawa T, et al. Soluble tumour necrosis factor receptors in synovial fluids from temporomandibular joints with painful anterior disc displacement without reduction and osteoarthritis. Arch Oral Biol, 2004, 49(2): 133-142.
16.	Hunt SP, Pini A, Evan G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature, 1987, 328(6131): 632-634.
17.	Bereiter DA, Bereiter DF. Morphine and NMDA receptor antagonism reduce c-fos expression in spinal trigeminal nucleus produced by acute injury to the TMJ region. Pain, 2000, 85(1-2): 65-77.
18.	丁小谋, 王宏, 邹宏恩. 神经延长修复周围神经长段缺损. 中国修复重建外科杂志, 2000, 14(6): 380.
19.	Delorme E. The treatment of gunshot wounds of nerves. Br Med J, 1915, 1(2837): 853-855.
20.	Highet WB, Sanders FK. The effects of stretching nerves after suture. Br J Surg, 1943, 30: 355-369.
21.	Abe I, Ochiai N, Ichimura H, et al. Internodes can nearly double in length with gradual elongation of the adult rat sciatic nerve. J Orthop Res, 2004, 22(3): 571-577.
22.	Kubota S, Nishiura Y, Hara Y, et al. Functional and morphological effects of indirect gradual elongation of peripheral nerve: electrophysiological and morphological changes at different elongation rates. Hand Surg, 2011, 16(2): 105-111.
23.	Simpson AH, Halliday J, Hamilton DF, et al. Limb lengthening and peripheral nerve function-factors associated with deterioration of conduction. Acta Orthop, 2013, 84(6): 579-584.
24.	马宏敏, 王锦玲, 黄维国, 等. 实验性面神经损伤后的神经再生速度. 中国耳鼻咽喉颅底外科杂志, 2000, 6(1): 17-19.
25.	莎茹拉, 沈俊, 张长青. 神经延长术修复周围神经缺损实验研究. 国际骨科学杂志, 2017, 38(2): 110-114.
26.	Jeudy J, Raimbeau G, Rabarin F, et al. Neuroma-in-continuity of the median nerve managed by nerve expansion and direct suture with vein conduit. Orthop Traumatol Surg Res, 2014, 100(4 Suppl): S267-S270.
27.	Murata Y, Onda A, Rydevik B, et al. Changes in pain behavior and histologic changes caused by application of tumor necrosis factor-alpha to the dorsal root ganglion in rats. Spine (Phila Pa 1976), 2006, 31(5): 530-535.
28.	Emshoff R, Brandlmaier I, Gerhard S, et al. Magnetic resonance imaging predictors of temporomandibular joint pain. J Am Dent Assoc, 2003, 134(6): 705-714.

1. Battiston B, Titolo P, Ciclamini D, et al. Peripheral nerve defects: overviews of practice in europe. Hand Clin, 2017, 33(3): 545-550.
2. 顾玉东. 周围神经缺损的基本概念与治疗原则. 中华手外科杂志, 2002, 18(3): 129-130.
3. 顾玉东. 周围神经缺损的治疗现状与进展. 中华创伤杂志, 2002, 18(9): 517-519.
4. Winfree CJ. Peripheral nerve injury evaluation and management. Curr Surg, 2005, 62(5): 469-476.
5. 侯春林. 长段周围神经缺损的治疗策略. 中华创伤杂志, 2007, 23(6): 401-402.
6. Wolford LM, Rodrigues DB. Autogenous grafts/allografts/conduits for bridging peripheral trigeminal nerve gaps. Atlas Oral Maxillofac Surg Clin North Am, 2011, 19(1): 91-107.
7. 徐筑秋, 杨晓楠, 祁佐良. 细胞自噬在周围神经损伤及再生中研究进展. 中国修复重建外科杂志, 2017, 31(1): 122-125.
8. Saijilafu, Nishiura Y, Hara Y, et al. Gradual stretching of the proximal nerve stump induces the growth of regenerating sprouts in rats. J Orthop Res, 2008, 26(7): 1012-1017.
9. Loverde JR, Ozoka VC, Aquino R, et al. Live imaging of axon stretch growth in embryonic and adult neurons. J Neurotrauma, 2011, 28(11): 2389-2403.
10. Manders EK, Saggers GC, Diaz-Alonso P, et al. Elongation of peripheral nerve and viscera containing smooth muscle. Clin Plast Surg, 1987, 14(3): 551-562.
11. 寇玉辉, 姜保国. 周围神经缺损修复新方法—神经延长术. 北京大学学报: 医学版, 2016, 48(5): 753-755.
12. Pfister BJ, Iwata A, Meaney DF, et al. Extreme stretch growth of integrated axons. J Neurosci, 2004, 24(36): 7978-7983.
13. Baoguo J, Shibata M, Matsuzaki H, et al. Proximal nerve elongation vs nerve grafting in repairing segmental nerve defects in rabbits. Microsurgery, 2004, 24(3): 213-217.
14. Wall PD, Devor M, Inbal R, et al. Autotomy following peripheral nerve lesions: experimental anaesthesia dolorosa. Pain, 1979, 7(2): 103-111.
15. Uehara J, Kuboki T, Fujisawa T, et al. Soluble tumour necrosis factor receptors in synovial fluids from temporomandibular joints with painful anterior disc displacement without reduction and osteoarthritis. Arch Oral Biol, 2004, 49(2): 133-142.
16. Hunt SP, Pini A, Evan G. Induction of c-fos-like protein in spinal cord neurons following sensory stimulation. Nature, 1987, 328(6131): 632-634.
17. Bereiter DA, Bereiter DF. Morphine and NMDA receptor antagonism reduce c-fos expression in spinal trigeminal nucleus produced by acute injury to the TMJ region. Pain, 2000, 85(1-2): 65-77.
18. 丁小谋, 王宏, 邹宏恩. 神经延长修复周围神经长段缺损. 中国修复重建外科杂志, 2000, 14(6): 380.
19. Delorme E. The treatment of gunshot wounds of nerves. Br Med J, 1915, 1(2837): 853-855.
20. Highet WB, Sanders FK. The effects of stretching nerves after suture. Br J Surg, 1943, 30: 355-369.
21. Abe I, Ochiai N, Ichimura H, et al. Internodes can nearly double in length with gradual elongation of the adult rat sciatic nerve. J Orthop Res, 2004, 22(3): 571-577.
22. Kubota S, Nishiura Y, Hara Y, et al. Functional and morphological effects of indirect gradual elongation of peripheral nerve: electrophysiological and morphological changes at different elongation rates. Hand Surg, 2011, 16(2): 105-111.
23. Simpson AH, Halliday J, Hamilton DF, et al. Limb lengthening and peripheral nerve function-factors associated with deterioration of conduction. Acta Orthop, 2013, 84(6): 579-584.
24. 马宏敏, 王锦玲, 黄维国, 等. 实验性面神经损伤后的神经再生速度. 中国耳鼻咽喉颅底外科杂志, 2000, 6(1): 17-19.
25. 莎茹拉, 沈俊, 张长青. 神经延长术修复周围神经缺损实验研究. 国际骨科学杂志, 2017, 38(2): 110-114.
26. Jeudy J, Raimbeau G, Rabarin F, et al. Neuroma-in-continuity of the median nerve managed by nerve expansion and direct suture with vein conduit. Orthop Traumatol Surg Res, 2014, 100(4 Suppl): S267-S270.
27. Murata Y, Onda A, Rydevik B, et al. Changes in pain behavior and histologic changes caused by application of tumor necrosis factor-alpha to the dorsal root ganglion in rats. Spine (Phila Pa 1976), 2006, 31(5): 530-535.
28. Emshoff R, Brandlmaier I, Gerhard S, et al. Magnetic resonance imaging predictors of temporomandibular joint pain. J Am Dent Assoc, 2003, 134(6): 705-714.

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