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

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.

Figure 1

A nerve root and its supplying artery of a normal rabbit are represented, which were reconstructed three dimensionally by using consecutive sections of the same artery specimen. The reconstructed artery is accepted as a cylinder, and its surface area is calculated as: S = 2∏rh; the endothelial cell density was calculated in a part of ANs. Volumetric changes of the ANs were calculated as the volume of the cylinder-shaped artery by the following formula: V = ∏r²h. Vascular luminal changes of the arteries were calculated by using volume changes of the ANs instead of changes in vessel diameter.

Figure 2

Normal appearance of a nerve root and epineural arteries at the level of L₃ (H&E, ×100, LM). (AN_1,2: Arterial nervorum, NR: Nerve Root, E: Endothel) (H&E, ×100, LM).

Figure 3

Appearance of a nerve root (NR), arterial nervorum (AN), and endothelial cells of the ANs (E) at the L₃ level on the non-plegic side. Minimallly endothelial swelling, cellular loss, and axonal injury are observed (H&E, ×200, LM).

Figure 4

Appearance of a nerve root (NR), arterial nervorum (AN), and endothelial cells of the ANs (E) at the L₃ level on the non-plegic side. Endothelial shrinkage, angulation, and cellular loss are seen in ANs of the nerve root at the level of L₆ on the plegic side (H&E, ×100, LM). Degenerated axons, myelin sheath derangements, and axonal loss are seen on the plegic side (H&E, ×200, LM).