Morphological Foundations of Restoration of Motor Innervation in Injuries of Peripheral Nerves
https://doi.org/10.18499/2225-7357-2019-8-4-66-73
Abstract
The problem of restoration of motor innervation is considered to be challenging due to a significant proportion of the peripheral nerve damage in the general structure of peacetime and wartime injuries, as well as a high risk of permanent function loss of the affected limb. Injuries of the peripheral nerves result in a complex of pathophysiological processes from both – the side of damaged nerve stems and the side of denervated target tissues. Moreover, the morphological picture of tissue changes is both degenerative and regenerative simultaneously. The process of secondary degeneration of the distal segments of crossed axons is similar to aseptic inflammation and is a prerequisite for the subsequent regeneration of nerve fibers. The process of reinnervation of the distal segment of the crossed nerve stem has a certain similarity with the development of peripheral nerves in the embryonic period, but the branches of regenerating axons move in the distal direction along the preserved neuriluminal tubes. A prolonged absence of motor innervation causes pronounced dystrophic changes in muscle fibers and intercellular spaces filling with the fibrous connective tissue; this, in turns, may result in a lack of functional limb restoration even if the terminal branches of the damaged nerve are adequately reinnervated. The restoration of contractile activity of reinnervated muscles is morphologically determined by the functional hypertrophy of the preserved muscle fibers, since the complete restoration of the innervation of all muscle fibers is practically not achievable due to the peculiarities of the peripheral nerve suture technique and the patterns of nerve fiber regeneration. Thus, an understanding of the patterns and morphological manifestations of degenerative-regenerative processes in tissues with injuries of peripheral nerves will allow substantiating the need for reconstructive plastic interventions on nerve stems from morphological points of view, based on the possibilities of achieving significant functional results.
About the Authors
A. Y. NishtRussian Federation
Aleksei Nisht.
ul. Lebedeva, 6, St. Petersburg, 194044.
V. S. Chirsky
Russian Federation
ul. Lebedeva, 6, St. Petersburg, 194044.
N. F. Fomin
Russian Federation
ul. Lebedeva, 6, St. Petersburg, 194044.
References
1. Alekseev ED. Differentsirovannoe lechenie sovremennykh boevykh ognestrel'nykh povrezhdenii perifericheskikh nervov: avtoref. dis. … kand. med. nauk. Sankt-Peterburg; 1998. 16 (in Russian).
2. Baitinger VF, Baitinger AV. End-To-Side Nerve Suture: Strategy Of «Obtaining» Axons From The Intact Nerve (Part III). Issues of Reconstructive and Plastic Surgery. 2013; 3(46): 6–16 (in Russian).
3. Bersnev VP, Kokin GS, Izvekova TO. Prakticheskoe rukovodstvo po khirurgii nervov. Moscow: Umnyi doktor; 2017. 552 (in Russian).
4. Goven'ko FS. Khirurgiya povrezhdenii perifericheskikh nervov. Saint-Petersburg: VMedA; 2010. 384 (in Russian).
5. Govenko FS, Monashenko DN, Lukin DS, Komantsev VN. Neuroticism three major nerves in the brachial plexus traction injury. Herald of the Russian Academy of Military Medicine. 2012; 4: 12–9 (in Russian).
6. Grigorovich KA. Khirurgiya nervov. Leningrad: Meditsina; 1969. 447 (in Russian).
7. Grigorovskii VV, Strafun SS, Gaiko OG, Gaiovich VV, Blinova EN. Histopathological changes and correlations of the morphological values of limb muscle status and clinical data in patients with the consequences of innervation traumatic disorders. Genij Ortopedii. 2014; 4: 49–57 (in Russian).
8. Gubochkin NG. The reparative treatment of the wounded and injured with multisystem injuries to the tendons and nerves of the upper extremity. IKBFU's Vestnik. Ser. Natural and Medical Sciences. 2011; 7: 45–51 (in Russian).
9. Doinikov BS. Izbrannye trudy po neiromorfologii i nevropatologii. Moscow: Meditsina; 1955. 468 (in Russian).
10. Zhivolupov SA, Rashidov NA, Samartsev IN, Yakovlev EV. Peculiarities of development of denervation-reinervation process in traumatic neuropathies and plexopathies. Herald of the Russian Academy of Military Medicine. 2013; 3: 190–8 (in Russian).
11. Masgutov RF, Rizvanov AA, Bogov AA, Gallyamov AR, Kiyasov AP, Bogov AA. Current trends for treatment of peripheral nerves injuries. Practical medicine. 2013; 1–2:99–103 (in Russian).
12. Nikitin SS. Electromyographic stages of denervation/reinnervation process at neuromuscular diseases: need for revision. Neuromuscular Diseases. 2015; 5(2):16–24 (in Russian).
13. Nozdrachev AD, Chumasov EI. Perifericheskaya nervnaya sistema. Struktura, razvitie, transplantatsiya i regeneratsiya. Moscow: Nauka; 1999. 272 (in Russian).
14. Trofimova SI, Baindurashvili AG, Agranovich OE. The use of triceps brachii muscle flaps in reconstructive surgery. Detskaya Khirurgiya. 2012; 6: 48–51 (in Russian).
15. Khodzhamuradov GМ, Davlatov АA, Ismoilov MM, Odinayev МF, Gulin AV. Prognosis of motor results of nerve grafting of upper extremity. Tambov University Reports. Series Natural and Technical Sciences. 2012; 17(3): 898–900 (in Russian).
16. Khem A, Kormak D. Gistologiya. Per. s angl. M.: Mir; 1983. 3:293 (in Russian).
17. Shchanitsyn IN, Ivanov AN, Bazhanov SP, Ninel' VG, Puchin'jan DM, Norkin IA. Stimulation of Peripheral Nerve Regeneration: Current Status, Problems and Perspectives. Successes of Physiological Sciences. 2017; 48(3): 92–111 (in Russian).
18. Shchanitsyn IN, Ivanov AN, Bajanov SP, Ulyanov VJ, Norkin IA, Ninel VG, Puchinyan DM. Methods for studying changes in the spinal cord after traumatic injuries of peripheral nerves. Regional blood circulation and microcirculation. 2014; 1(49):13–22 (in Russian).
19. Iurchenko NN. Sudeck''s Syndrome, Reflex Sympathetic Dystrophy. University Clinic. 2016; 12(1–2): 70–73 (in Russian).
20. Ashley Z, Sutherland H, Lanmüller H, Russold MF, Unger E, Bijak M, et al. Atrophy, but not necrosis, in rabbit skeletal muscle denervated for periods up to one year. American Journal of Physiology-Cell Physiology. 2007 Jan;292(1):C440–51. doi: 10.1152/ajpcell.00085.2006
21. Boncompagni S, Kern H, Rossini K, Hofer C, Mayr W, Carraro U, et al. Structural differentiation of skeletal muscle fibers in the absence of innervation in humans. Proceedings of the National Academy of Sciences. 2007 Nov 27;104(49):19339–44. doi: 10.1073/pnas.0709061104
22. Borisov AB, Huang S-K, Carlson BM. Remodeling of the vascular bed and progressive loss of capillaries in denervated skeletal muscle. The Anatomical Record. 2000 Mar 1;258(3):292. doi: 10.1002/(sici)1097-0185(20000301)258:3<292
23. Carlson BM, Billington L, Faulkner JA. Studies on the regenerative recovery of long-term denervated muscle in rats. Restorative Neurology and Neuroscience. 1996 Jan 1;10(2):77-84. doi: 10.3233/RNN-1996-10203
24. Carlson BM, Borisov AB, Dedkov EI, et al. The biology and restorative capacity of long-term denervated skeletal muscle. Basic and applied myology. 2002; 12(6):247–54.
25. Cattin A-L, Lloyd AC. The multicellular complexity of peripheral nerve regeneration. Current Opinion in Neurobiology. 2016 Aug;39:38–46. doi: 10.1016/j.conb.2016.04.005
26. Gaudet AD, Popovich PG, Ramer MS. Wallerian degeneration: gaining perspective on inflammatory events after peripheral nerve injury. Journal of Neuroinflammation. 2011;8(1):110–23. doi: 10.1186/1742-2094-8-110
27. Kenyon LC. Skeletal Muscle. In: Rubin E, Reisner HM. (Eds.). Essentials of Rubin’s pathology. Philadelphia: Wolters Kluwer Health/Lippincott Williams & Wilkins; 2014.
28. Lu D, Huang S, Carlson BM. Electron microscopic study of long-term denervated rat skeletal muscle. The Anatomical Record. 1997 Jul;248(3):355–65. doi: 10.1002/(sici)1097-0185(199707)248:3<355
29. McKay Hart A, Brannstrom T, Wiberg M, Terenghi G. Primary sensory neurons and satellite cells after peripheral axotomy in the adult rat. Experimental Brain Research. 2002 Feb 1;142(3):308–18. 2002; 142: 308–318. doi: 10.1007/s00221-001-0929-0
30. Noble J, Munro CA, Prasad VSSV, Midha R. Analysis of Upper and Lower Extremity Peripheral Nerve Injuries in a Population of Patients with Multiple Injuries. The Journal of Trauma: Injury, Infection, and Critical Care. 1998 Jul;45(1):116–22. doi: 10.1097/00005373-199807000-00025
31. Sferrazza R, Vindigni V, Adami N, Carraro U, Mazzoleni F. Myofiber regeneration in a denervated human muscle 3,5 years after posttraumatic free flap reconstruction. Basic Applied Myology. 2007; 17(3–4):137–9.
32. Stoll G, Müller HW. Nerve Injury, Axonal Degeneration and Neural Regeneration: Basic Insights. Brain Pathology. 2006 Apr 5;9(2):313–25. doi: 10.1111/j.1750-3639.1999.tb00229.x
33. Viguie CA, Lu D-X, Huang S-K, Rengen H, Carlson BM. Quantitative study of the effects of long-term denervation on the extensor digitorum longus muscle of the rat. The Anatomical Record. 1997 Jul;248(3):346–54. doi: 10.1002/(sici)1097-0185(199707)248
34. Wong K, Babetto E, Beirowski B. Axon degeneration: make the Schwann cell great again. Neural Regeneration Research. 2017;12(4):518. doi: 10.4103/1673-5374.205000
35. Winkler T, von Roth P, Matziolis G, Schumann MR, Hahn S, Strube P, et al. Time course of skeletal muscle regeneration after severe trauma. Acta Orthopaedica. 2010 Dec 13;82(1):102–11. doi: 10.3109/17453674.2010.539498
36. Zochodne DW, Levy D. Nitric oxide in damage, disease and repair of the peripheral nervous system. Cellular and molecular biology. 2005 Sep5;51(3):255–67
Review
For citations:
Nisht A.Y., Chirsky V.S., Fomin N.F. Morphological Foundations of Restoration of Motor Innervation in Injuries of Peripheral Nerves. Journal of Anatomy and Histopathology. 2019;8(4):66-73. (In Russ.) https://doi.org/10.18499/2225-7357-2019-8-4-66-73