Collateral leptomeningeal arteries: where are the anastomosis?

Key point:

  • To provide a review of existing (and often conflicting) knowledge concerning human leptomeningeal arteries (LMA) from an anatomical and physiological standpoints.

Vascular architecture of leptomeningeal arteries
The leptomeningeal arteries are localized within the pia–arachnoid, they are surrounded by cerebrospinal fluid and give rise to smaller arteries that penetrate into the Virchow-Robin spaces of the the brain tissue (penetrating arteries). The penetrating arteries become parenchymal arterioles once they penetrate into the brain tissue and become almost completely surrounded by astrocytic end-feet. There are several important structural and functional differences between pial arteries on the surface of the brain and smaller parenchymal arterioles:

  • Pial arteries receive “extrinsic” innervation from the peripheral nervous system, whereas parenchymal arterioles are “intrinsically” innervated from within the brain neuropil.
  • Parenchymal arterioles have only one layer of circumferentially smooth muscle, a greater basal tone and are unresponsive to at least some neurotransmitters that can have large effects on pial vessels.
  • Pial vessel architecture forms an effective collateral network, whereas penetrating and parenchymal arterioles are long and largely unbranched; for this reason the occlusion of one LMA does not appreciably decrease cerebral blood flow and the occlusion of an individual arteriole results in significant reductions in flow and infarction of the surrounding local tissue.

More than 300 years ago, Willis T. characterized the arterial ring at the base of the brain and began debate concerning whether the circle functions primarily as a flow equalizer or as an anastomosis. Heubner O., in 1874, was the first to produce a well-documented study demonstrating the existence of LMA; he was trying to establish the ACA, MCA, and PCA territories by injecting 1 of these arteries and, unexpectedly, the whole cerebral arterial system was filled. Despite this evidence, other contemporary anatomists, like Duret, Charcot and Testut, were not convinced of the importance of LMA. Vander Eecken H.M. and Adams R.D., in 1953, were the first to provide a comprehensive anatomic description of LMA; they showed their microscopic anatomy, defined their number and diameter, studied inter- and intra-individual variability, between the two hemispheres of same brain, in LMA size, number, and localization.

Anatomic Evidence of LMA
1684 Willis T. the first to describe LMA in Cerebri Anatome
1699 Ruysch F. he described LMA in Epistola anatomica, problematica, duodecima, authore Mich. Ernesto Ettmullero etc., as virum clarissimum Fredericum Ruysch, etc., De cerebri corticali substantia
1754 Von Haller A. he described LMA in Iconum anatomicarum
1808 Von Haller A. he described LMA in Anatomical Plates of the Human Body
1874 Heubner O. he produced the first well-documented study demonstrating the presence of LMA (Die luetischen Erkrankungen der Hirnarterien)
1931 Cobb S. he reported a study performed by Fray in 1925 similar to the Heubner’s study (The cerebral circulation, XIII: the question of “end arteries” of the brain and the mechanism of infarction)
1953 Vander Eecken H.M., Adams R.D. they were the first to provide a comprehensive anatomic description of LMA in The anatomy and functional significance of the meningeal arterial anastomoses of the human brain
1959 Vander Eecken H.M., Adams R.D. they were the first to provide a comprehensive functional description of LMA in The Anastomoses Between the Leptomeningeal Arteries of the Brain: Their Morphological, Pathological, and Clinical Significance.
1963 Kameyama M. et al. they confirmed the presence of LMA in Collateral circulation of the brain: with special reference to atherosclerosis of the major cervical and cerebral arteries
1966 Wollschlaeger G. et al. they confirmed the presence of LMA in an anatomically or postmortem radiographically study Arterial anastomoses of the human brain: a radiographic-anatomic study
1968 Van Den Bergh R. et al. they confirmed the presence of LMA in the Anatomy and embriology of cerebral circulation
1974 Gillilan L.A. et al. they confirmed the presence of LMA in the Potential collateral circulation to the human cerebral cortex
1976 Lazorthes G. et al. they confirmed the presence of LMA and also found several other anastomosis at the level of the occipital lobe (Vascularization et circulation de l’encèphale. In: Tome premier: Anatomie descriptive et fonctionelle)
1990 Van der Zwan A., Hillen B. they studied the variability of the vascular territories in human cadaver brains (Araldite F as injection material for quantitative morphology of cerebral vascularization).

Really, what distinguished anatomists (Testut, Duret, etc.) questioned from the beginning of these investigations was the compensatory capacity of LMA. De Seze S., in 1931, gave the first evidence of this capacity in Pression artérielle et ramollisement cerebral: Recherches cliniques physiopathologiques et therapeutiques; he radiographically observed, in cadaveric study, that injected fluid in ACA or PCA retrogradely filled the MCA branches. However, due to an extreme variability in patients outcomes associated with an almost constant presence of LMA on arteriography, it was not reached a common opinion. A different perspective on the hemodynamic functionality of LMA came from Viñuela et al. (1986), who observed refilling of arteriovenous malformations in conditions of complete occlusion of feeding vessels as a result of LMA and other vessels. Studies about stroke gave great importance to LMA compensatory capacity; in 1992 Ringelstein et al. hypothesized that LMA could influence penumbra extension and therapeutic window in MCA occlusion, observing that wider distal end-to-end anastomoses appear to correlate with more tissue protection. Nowadays, mechanisms controlling luminal size of the distal anastomoses are unknown.

Factors Influencing the Compensatory Capacity of LMA
  • Variability in diameter and number of LMA. This factor depends on the evidences, collected during decades of studies and animal experiments, that the variability of LMA affects the outcome of MCA occlusion and it depends on the individual variation of these anastomoses.

  • Systemic blood pressure. Occlusion of an artery leads to a decreased pressure in that territory and to a pressure gradient between the surrounding healthy territories and the territory of the occluded artery. It is known that Cerebral Perfusion Pressure (CPP)=Mean Arterial Pressure (MAP) -Intracranial Pressure (ICP) and that CPP is maintained above 70-80mmHg. This means that in hypertensive patients with an increase in blood pressure after stroke have an higher ICP and an higher pressure gradient between healthy territories and occluded territory. It was demonstrated that this condition leads to a better outcome after stroke.

  • Vascular dynamics. When an occlusion occur gradually, as in the case of a stenosis, LMA have enough time to develop and the compensatory capacity will be better than in sudden occlusion. This assumption is confirmed by the presence of compensatory LMA in other cerebrovascular diseases (moyamoya).

  • Age of patient. Several authors stressed the importance of the patient’s age as an independent factor in the compensatory capacity of LMA. They considered the functional state of the circulation of aged patients as altered and the compensatory capacity as very low.

 In conclusion,with the introduction of the concept of penumbra there was great interest to understand physiological behavior of LMA. It is known that there is great interindividual variability in distribution, size and number of LMA, but no study shows the range of this variability and associates variability to compensatory capacity.

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