The Falcate Artery: Its Dynamics in Vasospasm

Abstract

Background

Moyamoya disease demonstrates angiographically enlarged anterior falcine artery (AFA) participating in anastomotic dural–pial collateralization along parasagittal locations. It is conceivable that in vasospasm following subarachnoid hemorrhage (SAH-V), this AFA may responsively enlarge to perfuse ischemic parenchyma. We investigate the angiographic attributes of AFA and its reactive functions in post-SAH-V.

Materials and Methods

A retrospective assessment of clinical and imaging data was done on patients with SAH with angiographic vasospasm (modified Fisher scale [mFS]: 1–4; graded subjectively as either “mild”/“moderate”/“severe”), who were offered nimodipine infusion chemical angioplasty (NCA). Digital subtraction (biplane) angiography (DSA) characteristics studied were visibility of AFA and its length from the skull base. The mixed effect analysis methodology was used for comparison.

Results

The AFA was visualized in 59% of patients (n = 100; age: 26–75 years; M:F = 48:52;) in pre-NCA angiograms (47% in angiographic control group; p = 0.004). A trend was noted tending to longer AFA lengths in SAH-V in cases of anterior communicating artery (ACom) aneurysms (p = 0.7237), and higher mFS (increased by ∼0.99 cm in mFS grade 4; p = 0.276). Post-NCA, the average reduction in AFA length in “mild,” “moderate,” and “severe” subgroups of vasospasm was 0.49, 0.78, and 0.81 cm, respectively. The length reduction for AFA after NCA was statistically significant (p < 0.001). An 18.9% increase in the odds of vasospasm was estimated per centimeter increase in AFA length.

Conclusion

The AFA is angiographically demonstrable in greater than 58% of SAH-V cases. On DSA, the AFA was substantially longer and prominent in SAH-V cases and its post-NCA dimensions reduced, especially with severe vasospasm.

 

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Keywords

falx artery - vasospasm - nimodipine - subarachnoid hemorrhage

Introduction

The falx cerebri is a multilayered interhemispheric invagination of the dura. Anchored at the crista galli anteriorly and internal occipital protuberance posteriorly, it assumes a sickle-like morphology as it traverses the supratentorial midline fissure.[1] Unopposed layers of the falcine dura enclose blood-filled sagittal sinuses. The superior sagittal sinus (SSS) is enclosed in its superior margin of the falx cerebri, while the inferior sagittal sinus rides along the free margin just rostral to the corpus callosum.[2] The most common pathology afflicting the falx is a falcine meningioma (not invading the SSS) that constitutes approximately 9% of all intracranial meningiomas.[3]

Until the latter half of the last century, the general impression of the falcine dura was that of an avascular membranous structure, similar to fascia. It is now acknowledged that the dura is indeed a vascularized sheet and that the anterior segment of the falx is perfused by the anterior falcine artery (AFA), a branch of the anterior ethmoidal artery (AEA), a branch of the ophthalmic artery (OA).[4] Moyamoya disease, a progressive neurovascular pathology of the distal internal carotid arteries (ICA), is characterized by hypertrophic AEA and AFA that subserve dural–pial anastomoses in the ischemic anterior parasagittal parenchyma.[5] It is then not unreasonable to hypothesize that in other ischemic states, as with post-subarachnoid hemorrhage vasospasm (SAH-V), the AFA may reactively increase in dimensions to perfuse the at-risk ischemic parenchyma. In present study, we tried to evaluate the angiographic attributes of the AFA and its reactionary role in post-SAH-V and the effect of chemical angioplasty on AFA.

 

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Materials and Methods

This was a retrospective observational study performed at a tertiary referral center. Cases were defined as patients with clinical and angiographic evidence of vasospasm, whose age at evaluation was between 18 and 85 years, for whom chemical angioplasty was achieved with intra-arterial nimodipine infusion (Nimodipine chemical angioplasty [NCA]). One hundred cases whose digital subtraction angiography (DSA) was performed between July 2019 and March 2020 were retrieved from the Picture Archiving and Communication System (PACS). Informed consent was taken from all participants. All angiographies were done on either Artis Zee (Siemens Healthineers AG, Erlangen, Germany) or Allura (Koninklijke Philips N.V., Amsterdam, the Netherlands) biplane DSA systems at six frames per second as a standard. The institutional intra-arterial NCA protocol involves infusion of nimodipine (3 mg maximum dose diluted in 35 mL normal saline) over a period of 20 minutes) via a 5-Fr vertebral catheter placed in the distal cervical ICA under strict blood pressure monitoring and intermittent fluoroscopy. A subjective/visual grading of angiographic vasospasm into (1) mild, (2) moderate, and (3) severe categories was performed for the angiograms obtained before and after NCA. The imaging and angiographic attributes that were tabulated included the following: presence/absence of AFA; length of AFA from the anterior cranial fossa (ACF) base computed from freehand tracing with the available tools in the institutional Radiology Information System (Centricity RIS-I, GE Healthcare) in the corresponding DSA frame in which the AFA was visualized to its longest ([Fig. 1A, B]), change in length of AFA after nimodipine, aneurysm location (anterior cerebral artery vs. other), treatment methods (surgical clipping and endovascular coiling), and involved territory in vasospasm (anterior cerebral artery [ACA] vs. others). Angiograms of an equivalent number of “disease controls” defined by patients without subarachnoid hemorrhage (in whom elective angiography was done for indications other than acute subarachnoid hemorrhage and in which the vascular abnormality was restricted to the posterior fossa and wherein the pathological vessels involved were not anterior cerebral artery) were evaluated on the same lines.

Fig. 1 (A–C) A 56-year-old male patient following anterior communicating artery aneurysm clipping. The lateral angiogram shows clip in situ (white arrow in A) with mild vasospasm in the A2–A3 segments of the anterior cerebral artery. The anterior falcine artery (AFA) is demonstrated (encircled in B). The AFA length was measured by joining multiple small segments along its course starting from the anterior cranial fossa base (gray dashed line in C).

Statistical Analysis

Data were entered in Excel Spreadsheet 2010 (Microsoft, Redmond, Washington, United States). Mean and standard deviation were calculated for the variables. Mixed effect analysis was adopted for pre- and postintervention comparisons among different groups. For comparison of paired categorical data, the chi-squared test was used, while the Mann–Whitney U test was used for comparison of paired nonparametric data. A p-value of ≤0.05 was considered significant. The binary logistic regression model was used to model the probability of vasospasm with respect to the length of the AFA.

 

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Results

One hundred cases the fulfilled inclusion criteria (M:F= 48:52; age: 26–75 years; mean age: 53.07 years). Eighty-nine patients were treated by surgical clipping, while the remaining were managed with endovascular coiling. Preclipping/coiling DSA was available for 82 cases, among which 43 (52.4%) had a demonstrable AFA. The AFA was present in 59/100 cases in pre-NCA DSA (with a mean length of 3.45 ± 3.3 cm from the ACF base) and in 57/100 cases in post-NCA DSA. Forty-seven (47%) cases of the angiographic controls had AFA visualized on DSA (2.19 ± 2.54 cm from the ACF base). This intergroup difference was statistically significant (p = 0.004). Although there was a trend for a longer length of AFA in the cases with aneurysms located in the ACA territory (3.68 vs. 3.33 cm, with p = 0.7237), and when the vasospasm primarily involved the ACA and its branches (3.50 vs. 3.03 cm, respectively, with p = 0.6308), and cases with a higher modified Fisher grade of SAH (longer by 0.99 cm in grade 4 SAH; p = 0.276), the differences were not statistically significant.

Following NCA, the mean reduction in AFA length was 0.49 cm in “mild,” 0.78 cm in “moderate,” and 0.81 cm in cases with “severe” vasospasm ([Table 1], [Figs. 2] [3] [4]). Mixed effect analysis results for the pre- and postintervention comparison for the various degrees of vasospasm were the following: irrespective of the severity of the vasospasm, the reduction in the length of the AFA on post-nimodipine DSA was significant (p < 0.001). The intergroup differences in the absolute change in the length of the AFA post-NCA was significant (“mild” vs. “severe”: 3.653 cm; p = 0; “mild” vs. “moderate”: 0.629 cm in moderate; p = 0.354). There was no significant interaction effect in the “moderate versus mild” spasm and “severe versus mild” spasm comparison. There was a trend toward more reduction in the AFA length post-NCA in a higher-grade SAH (0.458 cm in grade 4 SAH, [p = 0.088] vs. 0.338 cm [p = 0.144], 0.09 cm [p = 0.84], and 0.192 cm [p = 0.493] in grades 1, 2, and 3, respectively; [Table 2]).

Table 1 Mean lengths of anterior falcine artery (AFA) according to vasospasm severity (length in cm)

Time point	Vasospasm severity	Mean length of AFA	Standard deviation
Pre-nimodipine	Mild	2.74	3.17
Post-nimodipine	Mild	2.25	2.75
Pre-nimodipine	Moderate	3.37	3.15
Post-nimodipine DSA	Moderate	2.59	2.55
Pre-nimodipine	Severe	6.39	2.72
Post-nimodipine DSA	Severe	5.58	2.64

Abbreviation: DSA, digital subtraction angiography.

Fig. 2 Line graph of mixed effect analysis of the length of the anterior falcine artery before and after administration of intra-arterial nimodipine in mild, moderate, and severe vasospasm groups.

Fig. 3 A 51-year-old male patient. Following anterior communicating artery aneurysm clipping, (A) the pre-nimodipine lateral angiogram shows clip in situ (white arrow) with mild vasospasm in the A2–A3 segments of the anterior cerebral artery. (B) Decrease in the length and prominence of the anterior falcine artery (black arrows) above the anterior cranial fossa base is demonstrated after administration of intra-arterial nimodipine. Note the improvement of brain perfusion after intra-arterial nimodipine infusion.

Fig. 4 A 35-year-old female patient following anterior communicating artery aneurysm clipping. (A) The pre-nimodipine anteroposterior angiogram shows severe spasm of the supraclinoid internal carotid artery, A1 segment of the anterior cerebral artery, and M1–M2 segments of the middle cerebral artery. (B) The pre-nimodipine lateral angiogram shows clip in situ (white arrow) with conspicuously visualized the anterior falcine artery (AFA; black arrow). (C) Marked decrease in the length of the AFA and its poor visualization (black arrow) are demonstrated after administration of intra-arterial nimodipine.

Table 2 Results of mixed effect analysis in pre- and post-nimodipine data with different degrees of vasospasms (length in cm)

Variable (length of AFA from ACF base)	Estimate	p
Main effect: change in AFA length with nimodipine infusion irrespective of vasospasm severity	−0.488	< 0.001
Main effect: change in AFA length in moderate spasm compared with mild spasm (irrespective of nimodipine infusion)	0.629	0.354
Main effect: change in AFA length in severe spasm compared with mild spasm (irrespective of nimodipine infusion)	3.653	< 0.001
Interaction effect: moderate vs. mild spasm (with nimodipine infusion, pre vs. post)	−0.295	0.171
Interaction effect: severe vs. mild spasm (with nimodipine infusion, pre vs. post)	−0.326	0.224

Abbreviations: ACF, anterior cranial fossa; AFA, anterior falcine artery.

Binary logistic regression analysis revealed that for every centimeter increase in the length of the AFA, there was an 18.9% increase in the probability of angiographic vasospasm.

 

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Discussion

A summary of the key results from our study is presented thus: the AFA was visualized on ICA angiography in higher than 53% of all subjects who underwent angiography. The mean length of the AFA from the ACF base was significantly higher in patients with SAH-V compared with the angiographic controls. The AFA significantly reduced in length following intra-arterial nimodipine/vasodilator infusion in patients with severe angiographic vasospasm, compared with those with milder degrees of vasospasm. The AFA is in essence the continuation of the AEA supplying the midline falx dura around the SSS as far posterior as the coronal suture.[6] The AEA, the parent artery of the AFA, has been studied in cadaveric dissections by White et al.[7] The definition of the origin of the anterior falx artery in their work is as follows: the AEA originates from the OA, approaches the medial wall of the orbit, and via the anterior ethmoidal foramen (AEF) courses through the ethmoid air cells. At the cribriform plate, it turns superiorly forming the anterior falx artery to travel between the two layers of dura. In this work, they demonstrate three sites for hemostatic control of the AEA, namely, (1) AEF in the medial orbital wall (lamina papyracea), (2) anterior ethmoid canal (in the location of the lateral ethmoid wall), and (3) at the cribriform plate (extradural). The third site denotes the origin of the AFA for hemostatic control of lesions of the ACF base via a single-flap craniotomy in the fronto-orbital location. In another prior work, Müller had highlighted that the AFA is a continuation of the AEA and that the course may be further posterior than what was once believed. A continuation into the parietal dura of the SSS later uniting with the branches (frontal) of the middle meningeal artery (MMA) at the coronal suture was found. The surgical anatomy of the AEA leading onto the AFA has also been reported by Moon et al with similar observations.[8] Cross-connections with the companion AFA (paired) exist.[9] Venae comitantes are absent in these paired vessels. The AFA is also involved in anastomosis with the posterior ethmoidal artery.[10] In OA occlusion, the AFA, by virtue of its connections with the MMA, can restitute orbital collateral circulation.[9] Collateralization with the branches of the lacrimal artery has also been described. Displacement of the AFA by intracranial masses is rare.[4] The vessel is usually opacified only from one side. Given that the course of the AFA is not leptomeningeal, it is unlikely to be compromised by post-SAH-V.

During 1979, Müller described the AFA and its anatomic relationships to the dural veins, the SSS, and the arachnoid granulations. Histology of the artery highlighted its modification to be compliant to longitudinal stretching. The intricacy of its relationships hinted a functional importance greater than just nourishment of the dura.[6] Thick walled arteries were noted flanking the SSS whose pulsations would help with moving the venous blood. It is reasonable to believe that the description alludes to the AFA.[11]

The angiographic visibility of the anterior falx artery has been variably reported, ranging from 8.7 to 21% in apparently normal clinical conditions.[4] [12] Across all the groups evaluated in the current study (including the angiographic controls), the percentage of angiograms with AFA visualization was consistently higher. It ought to be noted that the percentages cited above are sourced from angiographic literature from ethnically different populations and from a time when the angiographic resolution and the sophistication for digital subtraction was lesser. The rates of AFA visibility that we report are to be interpreted in light of these determinants. While it is now considered that the AFA does not invariably regress in its entirety after the period of development, definite data regarding its identification (percentages) in surgical/dissection specimen are lacking.

We refer to the literature on the dynamically responsive nature of the caliber of the AFA. Quite understandably, a greater proportion of patients (up to 35%) whose pathologies are locoregionally related to the anterior falx show a prominent falcine artery.[12] Hypertrophy of the AFA has hitherto been reported in pathological contexts of dural arteriovenous fistulas of the anterior cranial fossa base,[13] arteriovenous malformations,[14] subdural empyema in the interhemispheric region,[15] primary neoplasms (meningiomas and glioblastomas),[16] metastasis,[17] Paget's disease,[4] and dural–pial collateralization.[5] In their report of a case of anterior subdural (interhemispheric) empyema, Mitsuoka et al interpreted that exaggerated angiographic dimension of the AFA was a reactive/reversible phenomenon to pachymeningeal inflammation/irritation.[15] Such observations testify the sensitive nature of the AFA.

Dural–pial collateralization between the AFA and the mediofrontal/parasagittal branches of the callosomarginal trunk are well described by Hawkins.[18] Proof of their existence and compensatory nature is drawn from moyamoya disease, wherein this dural–pial collateralization hypertrophies to sustain the at-risk ischemic parenchyma. In fact, OA collaterals via the AFA are among the most frequent in moyamoya disease with their development and dimensions in balance with the perfusion needs of the at-risk anterior cerebral artery territories.[5] While it seems incongruent to compare collateralization in moyamoya disease (an indolent slow-progressing disease) to the acute course of post-SAH-V, it is worth noting that in stroke collaterals do develop in as early approximately 3 to 5 days.[17] Post-SAH-V is unusual before 3 days of the ictus.[19] Cerebral vasospasm is maximally symptomatic and angiographically most evident in the ACA territory.[20] That the anterior communicating artery is among the most common sites for ruptured intracranial aneurysms is known.[21] Summarizing by taking into account the time course of the SAH-V evolution, at-risk parenchyma being the distal ACA territory, the availability of dural–pial collateralization from the AFA, and the evidence for reactive/sympathetic nature of the AFA in locoregional pathology (alluded to earlier), we state that the observed statistically significant higher percentage of AFA visualization in our study testifies the AFA as a key contributor to sustain the vasospastic territory. We substantiate the a priori hypothesis of our study by emphasizing that AFA dural–pial collaterals hypertrophy due to their reciprocal balance with the constricted pial vasculature is in cases with SAH-V especially if the latter involves ACA territory. The correlation between the degree of vasospasm with the length of the AFA that we noted also is in line with these observations. Our purpose of using the “length” of the AFA above the anterior cranial fossa floor as the objective parameter as against the “diameter” was to ensure better reproducibility and eliminate the possible chances of error in calibration/measurement of the extremely small girth of the AFA.

The reciprocal balance between the AFA and the pial vasculature is discussed earlier. Intra-arterial vasodilators, such as nimodipine, decrease resistance and increase blood flow through the circle of Willis. With such changes, it is expected that postinfusion of vasodilators, dural–pial collateralization, although transient, becomes less vigorous. The postinfusion decrease in the length of the AFA that we noted to be significant in the group with severe vasospasm aligns with the prediction. It thus reaffirms the socialist role of the AFA for deprived brain parenchyma. Although not statistically significant, we found a trend of longer lengths of the AFA if aneurysm and subsequent vasospasm involve the ACA territory, higher grades of SAH, and clipping as compared with coiling. In binary logistic regression analysis also, we found a positive correlation between the probability of the presence of vasospasm with the length of the AFA and patient age. To the best of our knowledge, no report of the role of AFA in SAH-V and its dynamic changes in angiography exists in the literature.

We acknowledge shortcomings of this retrospective study. The control population that was included were diseased controls (not matched for age) who had no clinical/angiographic evidence of vasospasm and in whom in the vascular abnormality was remote from the AFA/ACA/anterior parasagittal territory. “Healthy controls” in angiography, given the radiation/ethical concerns, are not feasible. Vasospasm was judged based on visual assessment and may be prone to observation errors. The numbers of participants in the case and control groups were not matched. The case group was heterogeneous with regard to the location of aneurysm and treatment offered. Further influence of gender, ethnicity, etc., on the skull shape can affect the AFA measurements. Other potential dural–cortical collaterals, which can potentially supply the at-risk cerebral parenchyma, were not evaluated in our study. Also, subgroup analysis of the clipped versus coiled group and the effect of location of the aneurysm and the associated hematoma on AFA was not performed.

 

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Conclusion

The AFA is visualized on ICA angiography at a greater frequency than has been earlier reported in the literature. As an angiographic equivalent to the presence of vasospasm, the mean length of the AFA from the ACF base was significantly higher in patients with SAH-V compared with angiographic controls. The AFA significantly reduced in length following intra-arterial nimodipine infusion in patients with severe angiographic vasospasm, compared with those with milder degrees of vasospasm, further substantiating this claim of its role in autoregulation in vasospasm. A trend toward a longer length of the AFA is seen in grade 4 SAH, ACA territory aneurysms, and vasospasm involving the ACA territory. Further studies are needed for exploring and validating the compensatory role of the anterior falx artery in cerebral vasospasm and to probe its significance as an angiographic sign that antedates the onset of angiographic vasospasm.

 

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Conflict of Interest

None declared.

Data Availability Statement

The data will be made available upon reasonable request to authors.

Authors' Contributions

All the authors have made substantial contributions to all of the following: (1) the conception and design of the study, acquisition of data, or analysis and interpretation of data; (2) drafting the article or revising it critically for important intellectual content; and (3) final approval of the version to be submitted.

Ethical Approval

The study was approved by the institute's ethical board.

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31. März 2025