Altered arterial homeostasis and cerebral aneurysms: a molecular epidemiology study

Neurosurgery. 2004 Jun;54(6):1450-60; discussion 1460-2. doi: 10.1227/01.neu.0000125005.67850.f8.

Abstract

Objective: We hypothesized that patients with intracranial cerebral aneurysms (IAs) harbor a molecular defect in the process responsible for maintaining arterial integrity (arterial homeostasis). In this study, we undertook a preliminary assessment of differential expression of key molecules involved with each phase of homeostasis: arterial flow modulation, arterial tear and repair, and the ensuing extracellular matrix.

Methods: Key molecules from each phase of the arterial homeostatic process were selected: prostacyclin-stimulating factor, implicated with arterial flow modulation; PNUT and RAI, involved with tissue repair and arterial remodeling; and Type III collagen and fibronectin, which are key constituents of the extracellular matrix. A small sample of the IA dome was harvested at the time of surgical repair from both ruptured and unruptured domes. Pericranial vascular tissue was harvested from a sample of the superficial temporal artery (STA) or occipital artery from aneurysmal and nonaneurysmal patients undergoing craniotomy for unrelated conditions. Statistical analysis examining expression of each marker was performed initially using dichotomous analysis (presence or absence of expression), followed by an assessment of quantitative differences in expression. Initial analysis was restricted to the pair consisting of dome and STA harvested from each individual patient. This was followed by a pooled analysis in which all domes and STAs were respectively pooled.

Results: A total of 86 tissue samples were studied, including 24 IA domes, STA samples from 43 aneurysmal patients, and STA samples from 19 nonaneurysmal patients. We found that the degree of prostacyclin-stimulating factor and RAI expression was reduced in ruptured aneurysm domes when compared with STAs from IA patients (odds ratio, 0.26; 95% confidence interval [CI], 0.08-0.89; and odds ratio, 0.18; 95% CI, 0.03-0.94, respectively). Type III collagen expression also was reduced among ruptured domes when compared with STA (P = 0.042). These differences were found to be independent of the effects of smoking with adjusted odds ratios of 0.25 (95% CI, 0.08-0.77) and 0.18 (95% CI, 0.04-0.79), respectively, for prostacyclin-stimulating factor and RAI. No statistically significant differences were noted among the unruptured domes.

Conclusion: These preliminary data suggest an impaired ability to express proteins responsible for flow modulation and arterial repair within the ruptured domes when compared with control pericranial tissue. The study generates a hypothesis of impaired arterial homeostasis with a reduced ability to modulate hemodynamic flow with perhaps increased microinjury. This is exacerbated further by an impaired molecular ability to repair the vessel wall, culminating in aneurysm rupture. The study has limitations based on the use of pericranial tissue as the control and the relatively small sample size. Nevertheless, this study suggests that altered arterial homeostasis warrants further investigation in hopes of better understanding IA pathogenesis.

MeSH terms

  • Adult
  • Aged
  • Biological Factors / genetics
  • Biological Factors / metabolism*
  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism*
  • Case-Control Studies
  • DNA-Binding Proteins
  • Extracellular Matrix Proteins / genetics
  • Extracellular Matrix Proteins / metabolism*
  • Female
  • Genetic Predisposition to Disease
  • Homeostasis / genetics
  • Humans
  • Intracellular Signaling Peptides and Proteins*
  • Intracranial Aneurysm / genetics
  • Intracranial Aneurysm / metabolism*
  • Male
  • Middle Aged
  • Nuclear Proteins / genetics
  • Nuclear Proteins / metabolism*
  • Osteonectin / genetics
  • Osteonectin / metabolism*
  • RNA, Messenger / genetics
  • RNA-Binding Proteins
  • Repressor Proteins
  • Temporal Arteries / metabolism

Substances

  • Biological Factors
  • Carrier Proteins
  • DNA-Binding Proteins
  • Extracellular Matrix Proteins
  • Intracellular Signaling Peptides and Proteins
  • Nuclear Proteins
  • Osteonectin
  • PPP1R10 protein, human
  • PPP1R13L protein, human
  • RNA, Messenger
  • RNA-Binding Proteins
  • Repressor Proteins
  • prostacyclin synthesis stimulating plasma factor