Leptomeningeal collateral circulation
{{Infobox anatomy
| name = Leptomeningeal collateral circulation
| image = Sobo 1909 3 548.png
| caption = Arterial supply of the brain
| location = around the brain
| function = small connections ({{wt|en|anastamoses}}) between the areas supplied by the major arteries of the brain.
}}
The leptomeningeal collateral circulation (also known as leptomeningeal anastomoses or pial collaterals) is a network of small blood vessels in the brain that connects branches of the middle, anterior and posterior cerebral arteries (MCA, ACA, and PCA),{{Cite journal|last1=Brozici Mariana|last2=van der Zwan Albert|last3=Hillen Berend|date=2003-11-01|title=Anatomy and Functionality of Leptomeningeal Anastomoses|journal=Stroke|volume=34|issue=11|pages=2750–2762|doi=10.1161/01.STR.0000095791.85737.65|pmid=14576375|doi-access=free|citeseerx=10.1.1.574.8896}} with variation in its precise anatomy between individuals. During a stroke, leptomeningeal collateral vessels allow limited blood flow when other, larger blood vessels provide inadequate blood supply to a part of the brain.
Structure
Leptomeningeal collaterals lie within the leptomeninges, the two deep layers of the meninges called the pia mater and the arachnoid mater.{{Cite journal|last1=Patel|first1=Neel|last2=Kirmi|first2=Olga|date=2009|title=Anatomy and imaging of the normal meninges|journal=Seminars in Ultrasound, CT and MRI|volume=30|issue=6|pages=559–564|issn=0887-2171|pmid=20099639|doi=10.1053/j.sult.2009.08.006}} Their diameter has been measured at approximately 300 micrometers,{{Cite journal|last1=Phan|first1=Thanh G.|last2=Hilton|first2=James|last3=Beare|first3=Richard|last4=Srikanth|first4=Velandai|last5=Sinnott|first5=Matthew|date=2014-09-19|title=Computer Modeling of Anterior Circulation Stroke: Proof of Concept in Cerebrovascular Occlusion|journal=Frontiers in Neurology|volume=5|pages=176|doi=10.3389/fneur.2014.00176|pmid=25285093|pmc=4168699|issn=1664-2295|doi-access=free }} but there is variability between individuals in the size, quantity and location of these vessels, and between either hemisphere within the same subject.
Inter-territorial end to end anastomoses exist between branches of the anterior cerebral artery and middle cerebral artery, the posterior cerebral artery and middle cerebral artery, the anterior cerebral artery and posterior cerebral artery, and the right and left anterior cerebral arteries.{{Cite book|url=https://www.ncbi.nlm.nih.gov/books/NBK53086/|title=Anatomy and Ultrastructure|last=Cipolla|first=Marilyn J.|date=2009|publisher=Morgan & Claypool Life Sciences|language=en}}{{Cite journal|last1=Türe|first1=Uğur|last2=Yaşargil|first2=M. Gazi|last3=Krisht|first3=Ali F.|date=1996-12-01|title=The Arteries of the Corpus Callosum: A Microsurgical Anatomic Study|journal=Neurosurgery|volume=39|issue=6|pages=1075–1084|doi=10.1097/00006123-199612000-00001|pmid=8938760|issn=0148-396X|doi-access=free}}{{Cite journal|last1=Kim|first1=D.J.|last2=Krings|first2=T.|date=2011-09-01|title=Whole-Brain Perfusion CT Patterns of Brain Arteriovenous Malformations: A Pilot Study in 18 Patients|journal=American Journal of Neuroradiology|volume=32|issue=11|pages=2061–2066|pmc=7964413| doi=10.3174/ajnr.a2659|pmid=21885720|issn=0195-6108|doi-access=free}}{{Cite book|last=Coyle|first=Peter|chapter=Collateral Pial Arteries|date=1994|work=The Human Brain Circulation: Functional Changes in Disease|pages=237–246|editor-last=Bevan|editor-first=Rosemary D.|series=Vascular Biomedicine|publisher=Humana Press|language=en|doi=10.1007/978-1-4612-0303-2_18|isbn=9781461203032|editor2-last=Bevan|editor2-first=John A.|title=The Human Brain Circulation}} Intra-territorial anastamoses connect adjacent arterial branches within the same arterial territory (between two branches of the same middle cerebral artery, for example).
Inter-territorial leptomeningeal anastamoses between the posterior cerebral artery and anterior cerebral artery have been observed between the parieto-occipital branch of the posterior cerebral artery, and the precuneal branch or the posterior pericallosal branch of the anterior cerebral artery.
Inter-territorial leptomeningeal anastamoses between the right and left anterior cerebral arteries have been observed between the right and left pericallosal arteries and the right and left callosal marginal arteries. Anastamoses have also been observed between precuneal branches originating from the middle portion of the pericallosal artery, or from the posterior portion of the callosal marginal branch of one side joining the opposite paracentral branch.
There is anatomical variation in collateral circulation from person to person, and as we age, collateral vessels decrease in diameter and number.
Function
Leptomeningeal collateral vessels allow limited cerebral blood flow and brain tissue perfusion when the brain receives insufficient blood supply through an artery, via a series of anastomotic connections between cerebral arteries.{{cite journal|vauthors=Tariq N, Khatri R|date=October 2008|title=Leptomeningeal collaterals in acute ischemic stroke|journal=Journal of Vascular and Interventional Neurology|volume=1|issue=4|pages=91–5|pmc=3317324|pmid=22518231}}
Clinical significance
= Stroke =
File:TOF MRI angiography of right middle cerebral artery stenosis.png
During an ischaemic stroke, blood flow through a cerebral artery is compromised. This frequently causes substantial injury to the area of the brain supplied by the artery, but not all of this territory is necessarily affected. A post mortem study of middle cerebral artery strokes demonstrated that the area of brain injury was often smaller than the total area supplied by the middle cerebral artery. Leptomeningeal collateral vessels from the anterior cerebral artery and posterior cerebral artery appeared to allow for perfusion of some brain tissue to persist, partially compensating for the loss of the major vessel.{{cite journal | vauthors = Vander Eecken HM, Adams RD | s2cid = 33711931 | title = The anatomy and functional significance of the meningeal arterial anastomoses of the human brain | journal = Journal of Neuropathology and Experimental Neurology | volume = 12 | issue = 2 | pages = 132–57 | date = April 1953 | pmid = 13053234 | doi = 10.1097/00005072-195304000-00002 }} This compensatory effect is however usually inadequate to maintain a normal blood supply.{{cite journal | vauthors = Derdeyn CP, Powers WJ, Grubb RL | title = Hemodynamic effects of middle cerebral artery stenosis and occlusion | journal = AJNR. American Journal of Neuroradiology | volume = 19 | issue = 8 | pages = 1463–9 | date = September 1998 | pmid = 9763379 | pmc = 8338700 | url = http://www.ajnr.org/content/ajnr/19/8/1463.full.pdf }}
Therapies that attempt to optimize leptomeningeal collateral circulation appear to improve outcomes following acute ischaemic stroke.{{Cite journal|last=Winship|first=Ian R.|date=April 2015|title=Cerebral collaterals and collateral therapeutics for acute ischemic stroke|journal=Microcirculation |volume=22|issue=3|pages=228–236|doi=10.1111/micc.12177|issn=1549-8719|pmid=25351102|s2cid=206189480 }}
MRI and CT brain imaging is used to determine the severity of a stroke, and help guide treatment. Fluid attenuated inversion recovery (FLAIR) vascular hyperintensity (FVH) is a radiographic marker seen on brain imaging in acute ischaemic stroke. FVH can be used as a proxy for slow leptomeningeal collateral blood flow, and may help reveal which areas of brain tissue are potentially salvageable.{{Cite journal|last1=Liu|first1=Dezhi|last2=Scalzo|first2=Fabien|last3=Rao|first3=Neal M|last4=Hinman|first4=Jason D.|last5=Kim|first5=Doojin|last6=Ali|first6=Latisha K|last7=Saver|first7=Jeffrey L.|last8=Sun|first8=Wen|last9=Dai|first9=Qiliang|date=2016|title=FLAIR Vascular Hyperintensity Topography, Novel Imaging Marker for Revascularization in Middle Cerebral Artery Occlusion|journal=Stroke: A Journal of Cerebral Circulation|volume=47|issue=11|pages=2763–2769|doi=10.1161/STROKEAHA.116.013953|issn=0039-2499|pmc=5079823|pmid=27659851}}
= Alzheimer’s disease =
The age-related changes that can be seen in leptomeningeal vessels over time appear to be accelerated by Alzheimer's disease, according to mouse models conducted in 2018.{{Cite journal|last1=Zhang|first1=Hua|last2=Jin|first2=Bo|last3=Faber|first3=James E.|date=2018-12-05|title=Mouse models of Alzheimer's disease cause rarefaction of pial collaterals and increased severity of ischemic stroke|journal=Angiogenesis|volume=22|issue=2|pages=263–279|doi=10.1007/s10456-018-9655-0|issn=1573-7209|pmid=30519973|pmc=6475514}}
= Intracranial haemorrhage =
A 2016 study compared patients awaiting carotid artery stenting for unilateral atherosclerotic plaques. Those with leptomeningeal collaterals evident on cranial angiography had a higher incidence of intracranial haemorrhage (ICH) after stenting. The authors argued that the presence of such collaterals on imaging should be considered a risk factor for ICH in patients where carotid stenting is otherwise indicated.{{Cite journal|last1=Lee|first1=Kang Ji|last2=Kwak|first2=Hyo Sung|last3=Chung|first3=Gyung Ho|last4=Song|first4=Ji Soo|last5=Hwang|first5=Seung Bae|s2cid=24415856|date=May 2016|title=Leptomeningeal collateral vessels are a major risk factor for intracranial hemorrhage after carotid stenting in patients with carotid atherosclerotic plaque|journal=Journal of NeuroInterventional Surgery|volume=8|issue=5|pages=512–516|doi=10.1136/neurintsurg-2014-011634|issn=1759-8486|pmid=25841168}}
History
The term 'leptomeningeal' derives from the Greek word leptos (λεπτός) meaning thin, in reference to the appearance of the pia mater and arachnoid mater.
Descriptions of leptomeningeal collateral vessels are found in Thomas Willis’ Cerebri Anatome (1664).{{Cite journal|last=Lega|first=Bradley C.|date=2006|title=An Essay Concerning Human Understanding: How the Cerebri Anatome of Thomas Willis Influenced John Locke|journal=Neurosurgery|volume=58|issue=3|pages=567–576|doi=10.1227/01.neu.0000197489.17675.c6|pmid=16528199|issn=0148-396X}}{{Cite book|url=https://searchworks.stanford.edu/view/6496675|title=Cerebri anatome : cui accessit Nervorum descriptio et usus /|last=Willis|first=Thomas|date=1664|publisher=Typis Tho. Roycroft, impensis Jo. Martyn & Ja. Allestry ...|location=Londini }} German physician Otto Heubner first demonstrated their presence in his 1874 work Die luetische Erkrankung Der Hirnaterien.{{Cite web|url=http://wellcomelibrary.org/item/b21780080|title=Die luetische Erkrankung der Hirnarterien |website=Wellcome Library|language=en|access-date=2019-03-10}} He injected the middle cerebral artery, anterior cerebral artery and posterior cerebral artery in turn, in an attempt to establish the territories these arteries supply. Even when other anastomoses from the circle of Willis were blocked off, the whole cerebral arterial tree could be filled. Later study in the 1950s and 60s by H.M. Vander Eecken and R.D. Adams provided a comprehensive review of the anatomy of the leptomeningeal collateral circulation.
The concept of the ischaemic penumbra, where brain tissue shows capacity to recover if perfusion is quickly restored, was defined in 1981 by Astrup et al. Persistent blood flow through leptomeningeal vessels is a key part of this recovery.{{Cite journal|last1=Paciaroni|first1=Maurizio|last2=Caso|first2=Valeria|last3=Agnelli|first3=Giancarlo|date=2009|title=The concept of ischemic penumbra in acute stroke and therapeutic opportunities|journal=European Neurology|volume=61|issue=6|pages=321–330|doi=10.1159/000210544|issn=1421-9913|pmid=19365124|doi-access=free}}
Other animals
Haemodynamic studies of leptomeningeal collaterals have been conducted in primates.{{Cite journal|last=Symon|first=L.|date=1968|title=Haemodynamic studies of the leptomeningeal circulation in primates|journal=Proceedings of the Royal Society of Medicine|volume=61|issue=6|pages=610–612|issn=0035-9157|pmc=1902586|pmid=4969977|doi=10.1177/003591576806100629}} Leptomeningeal circulation has been observed in mice and rats during experiments to assess changes associated with disease and ageing in these vessels.{{Cite journal|last1=Li|first1=Zhaojin|last2=Tremble|first2=Sarah M.|last3=Cipolla|first3=Marilyn J.|date=2018-12-01|title=Implications for understanding ischemic stroke as a sexually dimorphic disease: the role of pial collateral circulations|journal=American Journal of Physiology. Heart and Circulatory Physiology|volume=315|issue=6|pages=H1703–H1712|doi=10.1152/ajpheart.00402.2018|issn=1522-1539|pmc=6336971|pmid=30239233}}
References
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