The effect of lycopene in egg shell membrane guidance channel on sciatic nerve regeneration in rats

Document Type: Original Article

Authors

1 Neurophysiology Research Center, Department of Anatomy, Faculty of Medicine, Urmia University of Medical Sciences, Urmia, Iran

2 Department of Anatomy, Faculty of Medicine, Urmia University of Medical Sciences, Urmia, Iran

Abstract

Objective(s): Peripheral nerves are commonly damaged. Although the nerve autograft still subsists the gold standard in surgery of nerve injury gaps, it has severe detriment. The egg shell membrane (ESM) is a natural material, which has a great potential in practice. The aim of this survey was to appraise the effect of lycopene and the ESM nerve guidance channel on sciatic nerve regeneration.
Materials and Methods: In this study, 32 male rats were randomized into four groups: sham surgery, autograft, ESM+ dimethyl sulfoxide (DMSO), and ESM+lycopene. One centimeter of sciatic nerve was removed, and the gap was grafted by ESM channel or autograft. The sciatic function index (SFI) was evaluated at days 7, 21, 30, 49, 60 and 90 after surgery.  Nerve regeneration and gastroknemius muscle fibers were evaluated at days 30 and 90 after surgery by withdrawal reflex latency (WRL), histology and immunohistology assessments.
Results: At  49, 60 and 90 days after surgery, the mean SFI in ESM+lycopene group was significantly greater than ESM+DMSO group (P<0.05). On day 90, the mean muscle fiber diameters and the mean number of myelinated axons in ESM+lycopene and autograft groups were significantly greater than ESM+DMSO group (P<0.05). In addition, the mean WRL was significantly lower in ESM+lycopene group than in the ESM+DMSO group 90 days after surgery (P<0.05).
Conclusion: The results of this study show that the affirmative effects of ESM+lycopene may be beneficial for treating peripheral nerve damages.

Keywords


1. Cheng Xl, Wang P, Sun B, Li Sb, Gao Yf, He Xz, et al. The longitudinal epineural incision and complete nerve transaction method for modeling sciatic nerve injury. Neural Regen Res 2015;10:1663-1668.
2. Panagopoulos GN, Megaloikonomos PD, Mavrogenis AF. The present and future for peripheral nerve regeneration. Orthopedics 2017; 40:141-156.
3. Griffin MF, Malahias M, Hindocha S, Khan WS. Peripheral nerve injury: principles for repair and regeneration. Open Orthop J 2014; 8:199-203.
4. Mohammadi J, Delaviz H, Mohammadi B, Delaviz H, Rad P. Comparison of repair of peripheral nerve transaction in predegenerated muscle with and without a vein graft. BMC Neurol 2016; 16: 237-244.
5. Xue C, Zhu H, Tan D, Ren H, Gu X, Zhao Y, et al. Electrospun silk fibroin-based neural scaffold for bridging a long sciatic nerve gap in dogs. J Tissue Eng Regen Med 2018; 12:31143-e1153.
6. Bian YZWY, Aibaidoula G, Chen GQ, Wu Q. Evaluation of poly (з-hydroxybutyrate-co-з-hydroxyhexanoate) conduits for peripheral nerve regeneration. Biomaterials 2009; 30:217-225.
7. Farjah GH, Heshmatian B, Karimipour M, Saberi A. Using egg shell membrane as nerve guide channels in peripheral nerve regeneration. Iran J Basic Med Sci 2013; 16:901-905.
8. Konofaos P, Ver Halen JP. Nerve repair by means of tubulization: past, present, future. J Reconstr Microsurg 2013; 29: 149-164.
9. Farjah GH, Dolatkhah MA, Pourheidar B, Heshmatian B. The effect of cerebro-spinal fluid in collagen guide channel on sciatic nerve regeneration in rat. Turk Neurosurg 2017; 27:453-459.
10. Kehoe SZX, Boyd D. FDA approved guidance conduits and wraps for peripheral nerve injury: A review of materials and efficacy. Injury Int J Care Injured 2012; 43:553-572.
11. Ruff KJ, Morrison D, Duncan SA, Back M, Aydogan C, Theodosakis J. Beneficial effects of natural egg shell membrane versus placebo in exercise-induced joint pain, stiffness, and cartilage turnover in healthy, postmenopausal women. Clin Interv Aging 2018; 13:285-295.
12. Cordeiro CM, Hincke MT. Recent patents on eggshell: shell and membrane applications. Recent. Pat Food Nutr Agric 2011; 3:1-8.
13. Liu M, Luo G, Wang Y, Xu R, wang Y, He W, et al. Nano-silver-decorated microfibrous egg shell membrane: processing, cytotoxicity assessment and optimization, antibacterial activity and wound healing. Sci Rep 2017; 7:436-449.
14. Nakano T, Ikawa NI; Ozimek L. Chemical composition of chicken eggshell and shell membranes. Poult Sci 2003; 82:510-514.
15. Torres FG, Troncoso OP, Piaggio F, Higar A. Structer-property relationships of a biopolymer network: the eggshell membrane. Acta Biomater 2010; 6: 3687-3693.
16. Sharma N, Goswami UC. Functional of lycopene in mammalian system: a review. Proc Zool Soc 2011; 64:1-7.
17. Renju GL, Muraleedhara Kurup G, Saritha Kumari CH. Anti-inflammatory activity of lycopene isolated from Chlorella marina on type II collagen induced arthritis in Sprague Dawley rats. Immunopharmacol Immunotoxicol 2013; 35: 282-291.
18. Voutilainen S, Numi T, Mursu J, Rissanen TH. Carotenoids and cardiovascular health. Am J Clin Nutr  2006; 83:1265-71.
19. Pandir D, Unal B, Bas H. Lycopene protects the diabetic rat kidney against oxidative stress-mediated oxidative damage induced by furan. Braz Arch Boil Technol 2016; 59:e16150794.
20. Li W, Zho P, Wang G, Lu X, Jiang Y, Zhao X. Anti-inflammatory effects of lycopene prevents cardiac dysfunction in streptozotocin-diabetic rats. Int J Clin Exp Med 2016; 9:8047-8054.
21. Subhash K, Bose C, Agrawal BK. Effect of short term supplementation of tomatoes on antioxidant enzymes and lipid peroxidation in type-II diabetes. Indian J Clin Biochem 2007; 22:95-98.
22. Mordente A, Guantario B, Meucci E, Silvestrini A, Lombardi E, Martorana G, et al. Free radicals and cardiovascular diseases: An Update. Curr Med Chem 2011; 18:1146-1163.
23. Göncü T, Oğuz E, Sezen H, Koçarslan S, Oğuz H, Akal A, et al. Anti-inflammatory effect of lycopene on endotoxin-induced uveitis in rats. Arq Bras Oftalmol 2016;79:357-362.
24. Bain JR, Mackinnon SE, Hunter DA. Functional evaluation of complete sciatic, peroneal, and posterior tibial nerve lesions in the rat. Plast Reconstr Surg 1989; 83: 129-138.
25. Farjah GH, Fazli F, Karimipour M, Pourheidar B, Heshmatiyan B, Pourheidar M. The effect of bone marrow mesenchymal stem cells on recovery of skeletal muscle after neurotization surgery in rat.  Iran J Basic Med Sci 2018; 21:236-243.
26. Farjah GH, Naeimi M, Saberi A. Comparison outcome of nerve regeneration across an eggshell membrane guide channel and autograft. Caspian J Neurol Sci 2016; 2:1-8.
27. Konya D, Liao WL, Choi H, Yu D, Woodard MC, Newton KM, et al. Functional recovery in T13-L1 hemisected rats resulting from peripheral nerve rerouting: role of neuroplasticity. Regen Med 2008; 3:309-327.
28. Li L, Li Y, Fan Z, Wang X, Li z, Wen J, et al. Ascorbic acid facilitates neural regeneration after sciatic nerve crush injury. Front Cell Neurosci 2019; 13:108. Doi: 10.3389/fncel.2019.00108.
29. Ohto-Fujita E, Schimizu M, Sano S, Kurimoto M, Yamazawa K, Atomi T, et al. Solubilized eggshell membrane supplies a type III collagen-rich elastic dermal papilla. Cell Tissue Res 2019; 376:123-135.
30. Vuong TT, Rønning SB, Suso HP, Schmidt R, Prydz K, Lundström M, et al. The extracellular matrix of eggshell displays anti-inflammatory activities through NF-kB in LPS-triggered human immune cells. J Inflamm Res 2017; 10:83-96.
31. Makkar S, Liyanage R, Kannan L, Packialakshmi B, Lay JO Jr, Rath NC. Chicken egg shell membrane associated proteins peptides. J Agric Food Chem 2015; 63: 9888-9896.
32. Li R, Liu H, Huang H, Bi W, Yan R, Tan X, et al. Chitosan conduit combined hyaluronic acid prevent sciatic nerve scar in a rat model of peripheral nerve crush injury. Mol Med Rep 2018; 17:4360-4368.
33. Minge D, Senkov O, Kaushik R, Herde MK, Tikhobrazova O, Wulff AB, et al. Heparan sulfates support pyramidal cell excitability, synaptic plasticity, and context discrimination. Cereb Cortex 2017; 27:903-918.
34. Itoh S, Takakuda K, Kawabatta S, Aso Y, Kasai K, Itoh H, et al. Evaluation of cross-linking procedures of collagen tubes used in peripheral nerve repair. Biomaterials 2002; 23:4475-4481.
35. Yao L, de Ruiter GC, Wang H, Knight AM, Spinner RJ, Yaszemski MJ, et al. Controlling dispersion of axonal regeneration using a multichannel collagen nerve conduit. Biomaterials 2010; 31:5789-5797.
36. Pan HC, Yang DY, Chiu YT, Lai SZ, Wang YC, Chang MH, Cheng FC. Enhanced regeneration in injured sciatic nerve by human amniotic mesenchymal stem cell. J Clin Neurosci 2006; 13:570-575.
37. Hu W, Wang H, Liu Z, Wang R, Luo X, Huang Y. Neuroprotective effects of lycopene in spinal cord injury in rats via antioxidative and anti-apoptotic pathway. Neurosci Lett 2017; 642:107-112.
38. Castaneda F; Kinne RK. Omental graft improves functional recovery of transected peripheral nerve. Muscle Nerve 2002; 26:527-532.
39. Wessely R, Paschalidis M, Wagenpfeil S, Wegener F, Neumann FJ, Theiss W. A comprehensive approach to visual and functional assessment of experimental vascular lesions in vivo. Am J Physiol Heart Circ Physiol 2004; 286:H2461-7.
40. de Ménorval MA, Mir LM, Fernández ML, Reigada R. Effects od dimethyl sulfoxide in cholesterol-containing lipid membrans: a comparative study of experiments in silico and with cells. PloS One 2012; 7: e41733.
41. Lanza C, Raimondo S, Verganil L, Catena L, Senes F, Tos P, et al. Expression of antioxidant molecules after peripheral nerve injury and regeneration. J Neurosci Res 2012;90:842-848.
42. Hsu S, Yao C, Hsu Y, Lin J, Chen Y, Chen Y. Effects of taxol on regeneration in a rat sciatic nerve transection model. Sci Rep 2017; 7:42280.
43. Takano S, Uchida K, Inoue G, Miyagi M, Aikawa J, Iwase D, et al. Nerve growth factor regulation and production by macrophages in osteoarthritic synovium. Clin Exp Immunol 2017; 190: 235-243.
44. Chang YJ, Hsu CM, Lin CH, Lu MS, Chen L. Electrical stimulation promotes nerve growth factor-induced neurite outgrowth and signaling. Biochim. Biophys Acta 2013; 1830: 4130-4136.
45. Goel R, Tyagi N. Potential contribution of antioxidant mechanism in the defensive effect of lycopene against partial sciatic nerve ligation induced behavioral, biochemical and histological modification in wistar rats. Drug Res 2016; 66:633-638.
46. Fregnan F, Muratori L, Simoes AR, Giacobini-Robecchi MG, Raimondo S. Role of inflammatory cytokines in peripheral nerve injury. Neural Regeneration Res 2012;7:2259-2266.
47. Aziz S, Heshmatiyan B, Amini K, Raisi A, Azimzadeh M. Alpha-lipoic acid loaded in chitosan conduit enhances sciatic nerve regeneration in rat. Iran J Basic Med Sci 2015;18:228-233.
48. Leon AS. Attenuation of adverse effects of aging on skeletal muscle by regular exercise and nutritional support. Am J Lifestyle Med 2017; 11:4-16.
49. Brazil DP, Yang ZZ, Hemmings, BA. Advances in protein kinase B signaling: AKTion on multiple fronts. Trends Biochem Sci 2004; 29:233-242.
50. Xu H, Yan Y, Li S. PDLLA/chondroitin sulfate/chitosan/NGF conduits for peripheral nerve regeneration. Biomaterials 2011; 32:4506-4516.