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J Brachial Plex Peripher Nerve Inj 2008; 03(01): e39-e44
DOI: 10.1186/1749-7221-3-13
Research article
Gundogdu et al; licensee BioMed Central Ltd.

Vascular mechanism of axonal degeneration in peripheral nerves in hemiplegic sides after cerebral hemorrhage: An experimental study[*]

Cemal Gundogdu
1   Department of Pathology, Medical Faculty, Ataturk University, Erzurum, Turkey
,
Memet Dumlu Aydin
2   Department of Neurosurgery, Medical Faculty, Ataturk University, Erzurum, Turkey
,
Dilcan Kotan
3   Department of Neurology, Medical Faculty, Ataturk University, Erzurum, Turkey
,
Nazan Aydin
4   Department of Psychiatry, Medical Faculty, Ataturk University, Erzurum, Turkey
,
Ednan Bayram
5   Cardiology Clinic of Erzurum State Hospital, Erzurum, Turkey
,
Hızır Ulvi
3   Department of Neurology, Medical Faculty, Ataturk University, Erzurum, Turkey
,
Recep Aygul
3   Department of Neurology, Medical Faculty, Ataturk University, Erzurum, Turkey
› Author Affiliations
Subject Editor:
Further Information

Publication History

05 December 2007

28 April 2008

Publication Date:
17 September 2014 (online)

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Abstract

Background Though retrograde neuronal death and vascular insufficiency have been well established in plegics following intracerebral hemorrhage, the effects of plegia on arterial nervorums of peripheral nerves have not been reported. In this study, the histopathological effects of the intracerebral hemorrhage on the dorsal root ganglions and sciatic nerves via affecting the arterial nervorums were investigated.

Methods This study was conducted on 13 male hybrid rabbits. Three animals were taken as control group and did not undergo surgery. The remaining 10 subjects were anesthetized and were injected with 0.50 ml of autologous blood into their right sensory-motor region. All rabbits were followed-up for two months and then sacrificed. Endothelial cell numbers and volume values were estimated a three dimensionally created standardized arterial nervorums model of lumbar 3. Neuron numbers of dorsal root ganglions, and axon numbers in the lumbar 3 nerve root and volume values of arterial nervorums were examined histopathologically. The results were analyzed by using a Mann-Whitney-U test.

Results Left hemiplegia developed in 8 animals. On the hemiplegic side, degenerative vascular changes and volume reduction in the arterial nervorums of the sciatic nerves, neuronal injury in the dorsal root ganglions, and axonal injury in the lumbar 3 were detected. Statistical analyses showed a significant correlation between the normal or nonplegic sides and plegic sides in terms of the neurodegeneration in the dorsal root ganglions (p < 0.005), axonal degeneration in the lumbar 3 nerve roots (p < 0.005), endothelial cell degeneration in the arterial nervorums (p < 0.001), and volume reduction in the arterial nervorums (p < 0.001).

Conclusion Intracerebral hemorrhage resulted in neurodegeneration in the dorsal root ganglion and axonolysis in the sciatic nerves, endothelial injury, and volume reduction of the arterial nervorums in the sciatic nerves. The interruption of the neural network connection in the walls of the arterial nervorums in the sciatic nerves may be responsible for circulation disorders of the arterial nervorums, and arterial nervorums degeneration could result in sciatic nerves injury.

*This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.


 

  • References

  • 1 De Groot PC, Van Kuppevelt DH, Pons C, Snoek G, Woude LHVan Der, Hopman MT. Time course of arterial vascular adaptations to inactivity and paralyses in humans. Med Sci Sports Exerc 2003; 35: 1977-85 10.1249/01.MSS.0000099088.21547.67 14652491
    CrossrefPubMedGoogle Scholar
  • 2 Olive JL, McCully KK, Dudley GA. Blood flow response in individuals with incomplete spinal cord injuries. Spinal Cord 2002; 40: 639-45 10.1038/sj.sc.3101379 12483497
    CrossrefPubMedGoogle Scholar
  • 3 Olive JL, Dudley GA. Vascular remodeling after spinal cord injury. Med Sci Sports Exerc 2003; 35: 901-7 10.1249/01.MSS.0000069755.40046.96 12783036
    CrossrefPubMedGoogle Scholar
  • 4 Lackova M, Schreiberova A, Kolesar D, Lukacova N, Marsala J. Moderately Different NADPH-Diaphorase Positivity in the Selected Peripheral Nerves after Ischemia/Reperfusion Injury of the Spinal Cord in Rabbit. Cell Mol Neurobiol 2006; 26: 1309-23 10.1007/s10571-006-9088-y
    CrossrefPubMedGoogle Scholar
  • 5 Groothuis JT, Boot CR, Houtman S, van Langen H, Hopman MT. Does peripheral nerve degeneration affect circulatory responses to head-up tilt in spinal cord-injured individuals?. Clin Auton Res 2005; 15: 99-106 10.1007/s10286-005-0248-9 15834766
    CrossrefPubMedGoogle Scholar
  • 6 Beggs J, Johnson PC, Olafsen A, Watkins CJ, Cleary C. Transperineurial arterioles in human sural nerve. J Neuropathol Exp Neurol 1991; 50: 704-18 10.1097/00005072-199111000-00003 1748879
    CrossrefPubMedGoogle Scholar
  • 7 Lincoln J, Milner P, Appenzeller O, Burnstock G, Qualls C. Innervation of normal human sural and optic nerves by noradrenaline- and peptide-containing nervi vasorum and. Brain Res 1993; 632: 48-56 10.1016/0006-8993(93)91137-H 7511981
    CrossrefPubMedGoogle Scholar
  • 8 Low PA, Lagerlund TD, Mc Manis PG. Nerve blood flow and oxygen delivery in normal, diabetic, and ischemic neuropathy. Int Rev Neurobiol 1989; 31: 355-438 2557297
    PubMedGoogle Scholar
  • 9 Lundborg G. Structure and function of the intraneural microvessels as related to trauma, edema formation, and nerve function. J Bone Joint Surg 1975; 57: 938-48 171272
    PubMedGoogle Scholar
  • 10 Low PA, Tuck RR. Effects of changes of blood pressure, respiratory acidosis and hypoxia on blood flow in the sciatic nerve of the rat. J Physiol Lond 1984; 347: 513-24 1199460 6423817
    CrossrefPubMedGoogle Scholar
  • 11 Smith DR, Kobrine AI, Rizzoli HV. Absence of autoregulation in peripheral nerve blood flow. J Neurol Sci 1977; 33: 347-52 10.1016/0022-510X(77)90132-0 915522
    CrossrefPubMedGoogle Scholar
  • 12 Sundqvist T, Oberg PA, Rapoport SI. Blood flow in rat sciatic nerve during hypotension. Exp Neurol 1985; 90: 138-43 10.1016/0014-4886(85)90047-0
    PubMedGoogle Scholar
  • 13 Rodriguez Sanchez C, Medina Sanchez M, Malik RA, Ah See AK, Sharma AK. Morphological abnormalities in the sural nerve from patients with peripheral vascular disease. Histol Histopathol 1991; 6: 63-71 1666855
    PubMedGoogle Scholar
  • 14 Ishikawa H, Honda T, Toriyama K, Torii S, Sugiura Y. Origin and course of nerves immunoreactive for calcitonin gene-related peptide surrounding the femoral artery in rat. Anat Embryol 2003; 207: 299-305 10.1007/s00429-003-0359-9 14618400
    CrossrefPubMedGoogle Scholar
  • 15 Aydin MD, Erdoğan AR, Cevli SC, Gundogdu C, Dane S, Diyarbakýrlý S. Ganglionary mechanism of spasticity and ileus in cerebral hemorrhage: An experimental study. Int J Dev Neurosci 2006; 24 (7) 455-9 10.1016/j.ijdevneu.2006.07.001 16963220
    CrossrefPubMedGoogle Scholar
  • 16 Bell MA, Weddell AG. A descriptive study of the blood vessels of the sciatic nerve in the rat, man and other mammals. Brain 1984; 107: 871-98 10.1093/brain/107.3.871 6478181
    CrossrefPubMedGoogle Scholar
  • 17 Bell MA, Weddell AG. A morphometric study of intrafascicular vessels of mammalian sciatic nerve. Muscle Nerve 1993; 7: 524-34 10.1002/mus.880070703
    PubMedGoogle Scholar
  • 18 Johnson PC, Beggs JL. Pathology of the autonomic nerve innervating the vasa nervorum in diabetic neuropathy. Diabet Med 1993; 10: 56-61 8435989
    CrossrefPubMedGoogle Scholar
  • 19 Kihara M, Low PA. Regulation of rat nerve blood flow: role of epineurial a-receptors. J Physiol 1990; 422: 145-52 1190125 2352176
    CrossrefPubMedGoogle Scholar
  • 20 Rechthand E, Hervonen A, Sato S, Rapoport SI. Distribution of adrenergic innervation of blood vessels in peripheral nerve. Brain Res 1986; 374: 185-9 10.1016/0006-8993(86)90409-9 3719326
    CrossrefPubMedGoogle Scholar
  • 21 Schaafsma L, Sun H, Zochodne D. Exogenous opioids influence the microcirculation of injured peripheral nerves. Am J Physiol 1997; 272: H76-H82 9038924
    PubMedGoogle Scholar
  • 22 Zochodne DW, Ho LT. Influence of perivascular peptides on endoneurial blood flow and microvascular resistance in the sciatic nerve of the rat. J Physiol 1991; 444: 615-30 1179952 1726597
    CrossrefPubMedGoogle Scholar
  • 23 Zochodne DW, Low PA. Adrenergic control of nerve blood flow. Exp Neurol 1990; 109: 300-7 10.1016/S0014-4886(05)80021-4 2285433
    CrossrefPubMedGoogle Scholar
  • 24 Appenzeller O, Dhital K, Cowen T, Burnstock G. The nerves to blood vessels supplying blood to nerves: The innervation vasa nervorum. Brain Res 1984; 304: 383-6 10.1016/0006-8993(84)90344-5 6204720
    CrossrefPubMedGoogle Scholar
  • 25 Dhital K, Lincoln J, Appenzeller O, Burnstock G. Adrenergic innervation of vasa and nervi nervorum of optic, sciatic, vagus and sympathetic nerve trunks in normal and streptozotocin-diabetic rats. Brain Res 1986; 367: 39-44 10.1016/0006-8993(86)91576-3 2938665
    CrossrefPubMedGoogle Scholar
  • 26 Ma J, Novikov LN, Wiberg M, Kellerth JO. Delayed loss of spinal motoneurons after peripheral nerve injury in adult rats: a quantitative morphological study. Exp Brain Res 2001; 139: 216-23 10.1007/s002210100769 11497064
    CrossrefPubMedGoogle Scholar
  • 27 Suzuki H, Oyanagi K, Takahashi H, Kono M, Yokoyama M, Ikuta FA. Quantitative pathological investigation of the cervical cord, roots and ganglia after long-term amputation of the unilateral upper arm. Acta Neuropathol 1993; 86: 546-8
    PubMedGoogle Scholar
  • 28 McKay HA, Brannstrom T, Wiberg M, Terenghi G. Primary sensory neurons and satellite cells after peripheral axotomy in the adult rat: timecourse of cell death and elimination. Exp Brain Res 2002; 142: 308-18 10.1007/s00221-001-0929-0 11819038
    CrossrefPubMedGoogle Scholar
  • 29 Taiushev KG. Segment-by-segment histological analysis of the cervical part of the spinal cord, roots of the cerebrospinal nerves and ganglia in severe cranio-cerebral trauma. Arkh Anat Gistol Embriol 1989; 96: 16-23 2751438
    PubMedGoogle Scholar
  • 30 Ganchrow D, Ornoy A. Possible evidence for secondary degeneration of central nervous system in the pathogenesis of anencephaly and brain dysraphia. A study in young human fetuses. Pathol Anat Histol 1979; 384: 285-94 10.1007/BF00428230
    PubMedGoogle Scholar
  • 31 Teunissen L, Veldink J, Notermans NC, Bleys RL. Quantitative assessment of the innervation of epineurial arteries in the peripheral nerve by immunofluorescence: differences between controls and patients with peripheral arterial disease. Acta Neuropathol 2002; 103: 475-80 10.1007/s00401-001-0492-6 11935263
    CrossrefPubMedGoogle Scholar
  • 32 Tandrup T, Woolf CJ, Coggeshall RE. Delayed loss of small dorsal root ganglion cells after transection of the rat sciatic nerve. Comp Neurol 2000; 422: 172-80 10.1002/(SICI)1096-9861(20000626)422:2<172::AID-CNE2>3.0.CO;2-H
    CrossrefPubMedGoogle Scholar
  • 33 Shi TJ, Tandrup T, Bergman E, Xu ZQ, Ulfhake B, Hokfelt T. Effect of peripheral nerve injury on dorsal root ganglion neurons in the C57 BL/6J mouse: marked changes both in cell numbers and neuropeptide expression. Neuroscience 2001; 105: 249-63 10.1016/S0306-4522(01)00148-8 11483316
    CrossrefPubMedGoogle Scholar
  • 34 Bahadori MH, Al-Tiraihi T, Valojerdi MR. Sciatic nerve transection in neonatal rats induces apoptotic neuronal death in L5 dorsal root ganglion. J Neurocytol 2001; 30: 125-30 10.1023/A:1011935122963 11577250
    CrossrefPubMedGoogle Scholar
  • 35 Tandan R, Bradley WG. Amyotrophic lateral sclerosis: Part 2. Etiopathogenesis. Ann Neurol 2000; 18: 419-31 10.1002/ana.410180402
    PubMedGoogle Scholar
  • 36 Bendsen E, Byskov AG, Laursen SB, Larsen HP, Andersen CY, Westergaard LG. Number of germ cells and somatic cells in human fetal testes during the first weeks after sex differentiation. Hum Reprod 2003; 18: 13-8 10.1093/humrep/deg057 12525434
    CrossrefPubMedGoogle Scholar
  • 37 Cruz-Orive LM, Weibel ER. Recent stereological methods for cell biology: a brief survey. Am J Physiol 1990; 258: 148-56
    PubMedGoogle Scholar
  • 38 Sterio DC. The unbiased estimation of number and sizes of arbitrary particles using the disector. J Microsc 1984; 134: 127-36 6737468
    CrossrefPubMedGoogle Scholar