Paradoxic Relations between Basilar Artery Reconfiguration and Superior Cervical Ganglia Ischemia After Bilateral Common Carotid Artery Ligation

doi:10.1016/j.wneu.2019.01.144

World Neurosurgery

Volume 125, May 2019, Pages e658-e664

https://doi.org/10.1016/j.wneu.2019.01.144 Get rights and content

Background

The relationship between superior cervical ganglia (SCG) ischemia due to bilateral common carotid artery ligation (BCCAL) and basilar artery (BA) reconfiguration was investigated.

Methods

Twenty-three rabbits were randomly divided into 3 groups: group III rabbits underwent BCCAL (n = 13), group II rabbits were sham-operated controls (n = 5), and group I rabbits did not undergo surgery (n = 5). Degenerated neuron densities (DND) within the SCG were correlated with the BA vasodilatation index (VDI).

Results

Mean live and DND in SCG of group I rabbits were 11.235 ± 982/μm³ and 11 ± 3/μm³, respectively, with a mean heart rate of 294 ± 21 beats/min. Mean SCG DND and heart rates were 213 ± 42/μm³ and 242 ± 17 beats/min for the sham group (group II) rabbits and 1743 ± 285/μm³ and 199 ± 19 beats/min for the study group (group III) rabbits, respectively. The BA VDI values in the sham group (group II) (1.32 ± 0.10) and the study group (group III) (0.976 ± 0.112) significantly differed from those in the control group (group I) (1.65 ± 0.12; P < 0.005) versus the sham group (group II) (P < 0.0001) versus the BCCAL applied group (group III) and between group II and group III (P < 0.005).

Conclusions

A meaningful and paradoxic correlation was detected between the BA VDI values and degenerated neuron density of SCG after BCCAL. Although a low degenerated neuron density within SCG may provoke excessive sympathetic activity and prevent excessive BA dilatation with steno-occlusive carotid artery diseases, a high degenerated neuron density may cause dangerous vasodilatation of BA.

Introduction

Cerebral arteries are innervated by several systems contributing to the autonomic control of cerebral blood flow1, 2 and brain vessel diameter. Parasympathetic fibers have vasodilatory effects, and sympathetic fibers are vasospastic on cerebral arteries.2, 3 Vasospastic sympathetic innervation of cerebral vessels originates from the postganglionic fibers of the superior sympathetic ganglion rise with its biggest efferent branch and the carotid nerve that assists the carotid plexus.⁴ In the pathogenesis of vasospasms, the sympathetic nervous system plays a critical role,⁵ because sympathetic innervation promotes cerebral vasoconstriction in response to sharp increases in arterial pressure.⁶ In addition, the sympathetic system has trophic effects on cerebral vascular smooth muscle cells.⁷ Bilateral common carotid artery ligation (BCCAL) increases blood pressure, generates retrograde blood flow, causes ischemic degenerative variations in target tissues, and leads to significant histomorphologic and hemodynamic variations in the carotid-vertebrobasilar vasculature.⁸ Within 2 to 4 months after BCCAL, aneurysm, neovascularization, and vital collateral circulation can form.9, 10, 11 BCCA occlusion causes carotid artery system loss and cervical sympathetic trunk ischemia. Ischemic degeneration of the superior cervical ganglia (SCG) inhibits the sympathetic nervous system, which decreases the heart rate, causing bradycardia and rhythm disorders.9, 12, 13 Additionally, SCG ischemia may cause sympathetic hypoactivitiy in the cerebral vasculature.¹⁴ Morphometric examination of the basilar arteries (BAs) clearly reveals the critical role of sympathetic nerve innervation in determining BA characteristics after BCCAL.¹⁵ In this study, we investigated whether there is a relationship between SCG ischemia due to BCCAL, heart rate variations after permanent BCCAL, and volumetric changes in BAs.

Section snippets

Animal Models

Twenty-three adult male albino New Zealand rabbits (mean weight, 3.7 ± 0.4 kg) were used. The animal protocols used were certified by the Atatürk University Medical Faculty Ethics Committee (Erzurum, Turkey), and all guidelines regarding animal care and experiments were followed. The rabbits were randomly divided into 3 groups: group I rabbits did not undergo surgery (control, n = 5), group II rabbits were sham operated (n = 5), and group III rabbits underwent BCCAL (n = 13). The rabbits were

Results

Within 1 week after surgery, 2 BCCAL-applied rabbits in group III died. Prior to death, breathing disturbances, loss of consciousness, ischemic attacks, convulsions, and cardiac arrhythmia were observed. The BCCAL-applied (group III) rabbits that survived the 1-month observation period (n = 11) were included in the stereologic and histopathologic analysis.

Interpretation and Scientific Implications

BCCAL produces primary redistribution of blood to the brain, with retrograde and increased blood flow in the basilar and vertebral arteries. Important histopathologic and morphologic vertebral, posterior cerebral, posterior communicating, and neck vessel and artery changes occur within 4 months after BCCAL in BA. Intracranial vascular variations mostly regress to their earlier state after 4 months. However, the mechanism(s) that clarify trophic vessel variations in response to changed blood

Conclusion

BCCAL can cause dangerous histomorphologic changes in the SCG. Ischemic neurodegeneration of the SCG may have beneficial effects by decreasing the amount of sympathetic products therein, which enables greater blood flow to the brain through a more dilatated BA. However, low degenerated neuron density in the SCG may provoke excessive sympathetic activity and prevent excessive BA dilatation during steno-occlusive carotid artery diseases. Whereas a low degenerated neuron density in the SCG may

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: Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

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Original ArticleParadoxic Relations between Basilar Artery Reconfiguration and Superior Cervical Ganglia Ischemia After Bilateral Common Carotid Artery Ligation

Background

Methods

Results

Conclusions

Introduction

Section snippets

Animal Models

Results

Interpretation and Scientific Implications

Conclusion

Auton Neurosci

World Neurosurg

World Neurosurg

Auton Neurosci

World Neurosurg

World Neurosurg

World Neurosurg

Brain Res

Auton Neurosci

Neurol Neurochir Pol

World Neurosurg

Exp Neurol

Role of degenerated neuron density of dorsal root ganglion on anterior spinal artery vasospasm in subarachnoid hemorrhage: Experimental study

Acta Neurochir (Wien)

Predictive role of external carotid artery vasospasm on cerebral ischemia after subarachnoid hemorrhage: Experimental study

Turk Neurosurg

How reliable is pupillary evaluation following subarachnoid hemorrhage? Effect of oculomotor nerve degeneration secondary to posterior communicating artery vasospasm: First experimental study

J Neurol Surgery, A Cent Eur Neurosurg

Original Article
Paradoxic Relations between Basilar Artery Reconfiguration and Superior Cervical Ganglia Ischemia After Bilateral Common Carotid Artery Ligation