Abstract
The existence of collateral circulation in patients with impaired intracranial circulation was studied. We analysed angiograms of 35 patients of the Neurology Clinic of Clinical Centre in Sarajevo with occlusion of internal carotid artery. In majority cases collateral circulation was not established. In patients with occlusion of internal carotid artery, extracranial-intracranial anastomoses were established in some cases, with results of surviving and patients recovery. Collateral circulation based on blood vessels which are formed in the early stages of fetal life. Some embryonal arteries undergo an involution process, while the other part of blood vessels stay unfunctional during life, until cerebrovascular disease appearence, when it comes to their activation. Establishing of the collateral circulation in post-occlusiv status depend on great number of factors: number of anastomoses, their calibre, velocity of occlusion and complete vascular status of patients.
Keywords: internal carotid artery, collateral circulation, extracranial-intracranial anastomoses
INTRODUCTION
Collateral brain arteries include the great number of anastomotic channels or plexus connections between brain arteries, as well as between brain arteries and head and neck arteries (8, 2, 7, 3, 1). Collateral circulation of brain has the great functional and clinical significance, and based on blood vessels which are formed in the early stages of fetal life. Common clinicians opinion are that patients have different ability for blood compensation in a case with changes in cerebral blood flow. Carotid artery occlusion in one persons can be followed only with tran-sitivé neurological deficit or without simptoms, while in other persons we can find infarction of the great part of one cerebral hemisphere. These differences are undoubted in connection with existence or non existence of adequately collateral circulation. Functional effect of collateral circulation in post-occlusive status depend on great number factors : number of anastomoses and their calibre, as well as status of cerebrovascular system, vascular variations and anomalies, velocity of occlusion (trombosis or embolism), on systemic arterial pressure, volume and blood viscosity.
Based on type and position of anastomotic arteries, anastomoses can divide into: cervical, extracranial - intracranial, extracerebral anastomoses, extracere-bral- cerebral anastomoses and cerebral anastomoses. According to some authors (11, 5), and others extracranial-intracranial anastomoses are connections between branches of the external carotid artery and internal carotid artery. There are in the field of the corresponding craniofacial cavities (orbit, nasal cavity, tympanic cavity). Anastomoses exists in orbit between branches of ophthalmic artery (branch of internal carotid artery) and corresponding branches of external carotid artery, are usually functional after occlusion of the internal carotid artery. In this group of anastomoses include and individual persistent embrional blood vessels The first idea for detail investigations of collateral circulation date from 1958. Modern radiology technics open possibility to precisely investigations of patients with cerebrovascular diseases, with possibility of visualization of collateral circulation through the existence of arterial anastomoses in the field of central nervous system.
MATERIAL AND METHODS
For this work we used angiograms of 35 patients of the Neurology Clinic of Clinical Centre in Sarajevo, suspected on occlusion of internal carotid artery, using direct carotid angiography. X-ray films were taken serially in two projections, with observation of all phases of circulation. Arteriograms were careful analysed.
RESULTS
In the pathology of hemodynamic diseases a frequent case is occlusion of internal carotid artery. Patients hospitalized at the Neurology Clinic in coma, who survived thanks to good development of the extracranial-intracranial anastomoses were analysed. Carotid angiography was applied after hospitalization. Carotid angiograms in the anteroposterior and the lateral projection show the external carotid artery and its collateral and terminal branches, facial artery, maxillary artery and superficial temporal artery. Except that we can observe blood vessels, branches of the ophthalmic artery, and anastomosis between good filled supraorbital artery and frontal branch of the superficial temporal artery (Fig. 1 and 2). Branches of the ophthalmic artery are filling retro-grade from the maxillary artery, with extracranial-intracranial anastomoses between sphenopalatine artery and ethmoidal arteries, as well as between deep temporalis arteries and lacrimal artery, and in the end through extracranial-intracranial anastomoses between infraorbital branches of the maxillary artery with inferior palpebral arteries of the ophthalmic artery. Supraorbital artery is filling by frontal branch of superficial temporal artery, so we can see many blood vessels in orbit. Althought occlusion of internal carotid artery is found, thankful extracranial-intracranial anastomoses, patients started recovery.
Figure 1.

Carotid angiogram. Anteroposterior projection
Figure 2.

Carotid angiogram. Lateral projection
Carotid angiography made again fifteen days later. Angiograms showed retrograde circulation through ophthalmic artery to supraclinoidal part of the internal carotid artery, and the biginning of the middle cerebral artery in anteroposterior and lateral projection is visible (Fig.3 and 4).
Figure 3.

Carotid angiogram. Anteroposterior projection. Establishing of the cerebral circulation with extracranial-intracranial anastomoses, in occlussion of carotid internal artery
Figure 4.

Carotid angiogram. Lateral projection. Establishing of the cerebral circulation with extracranial-intracranial anastomoses, in occlus-Sion of carotid internal artery.
DISCUSSION
Collateral circulation based on blood vessels which are formed in the early stages of fetal life. Some embryonal arteries undergo an involution process, while the other part of blood vessels stay for vascularization of stractures in development. Collateral blood vessels exist in the prenatal development, stay unfunctional during life, until cerebrovascular disease appearence, when it comes to their activation as describe Fields at al (3) in their study about collateral circulation.
Pitts (9) established atherosclerosis as the most frequent causa of stenosis in the big arteries usually on bifurcation of arterial channels. Before total occlusion the lumen of blood vessels is narrowing with subintima1 atherosclerotic plaque. In a case with compression on the lumen, the blood flow is slow, and the possibilities of tissue depend on collateral circulation. Although this process is more gradual than hasty, the body mechanisms are usually able for compensation of blood flow. This statement agree with our findings, in elder patients with occlusion of internal carotid artery and sclerotic blood vessels. Angiograms made when patients arrived in hospital, showed intracranial-extracranial anastomoses between ophthalmic artery and superficial temporal arterywith results of establishing of cerebral flow and the survival of an individual.
Krayenbuhl et Yasargil (6) et all. and Fisher (4) showed that the opening of the existing collaterals is the first body answer on occlusion of the large arteries. According to many authors this is possible because vasomotor reflex causing vasodilatation of the blood vessels. The differenees of the pressure can cause opening unfunctional collaterals and good blood flow through dilatable functional blood vessels.
Compensatory, hemodynamic, metabolic and nervous mechanisms are very important and their effect determine abilities of the ischemic tissue for life. The tissue recovery are not only depend on cells-life abilities, as well as on growth of blood flow, for an increase of metabolic changes.
In his study of collateral circulation Quiring (10) describe some factores which have influence on dinamic of collateral circulation:
-anatomical status of circulation schanel
-time of occlusion
-status of systematic circulation
According to many researches and their published papers, cerebral ischemia is not only in relation with physiological changes.
So, Lazorthes at all. (7), Duvernoy (2) and others consider the anatomical factors often neglected, but the same significant as was noted previously. We also agree that the anatomical variations in human development in the most percents are responsible for the variety of signs and symptoms of occlusion, have an effect on recovery from neulology deficit.
Based on type and position of anastomotic arteries, anastomoses can devide into: cervical, extracranial, extracranial - intracranial, extracerebral anastomoses, extracere-bral- cerebral anastomoses and cerebral anastomoses.
CONCLUSION
There is not a general model of the morphological changes of blood vessels in acute and chronic insufficiency, but there are an individual differences for the all man.
We can conclude that the functional activity of collateral circulation in post-occlusive status depend on great number factors : number of anastomoses and their calibre, as well as status of cerebrovascular system, vascular variations and anomalies, velocity of occlusion (trombosis or embolism), as well on systemic arterial pressure, volume and blood viscosity.
References
- 1.Coyle P. Diametar and length changes in cerebral collatérales after middle cerebral artery occlusion. Anat. Rec. 1984;210:357–364. doi: 10.1002/ar.1092100211. [DOI] [PubMed] [Google Scholar]
- 2.Duvernoy H.M, et al. Cortical blood vessels of the human brain. Brain. Res.Bull. 1981;7:519–579. doi: 10.1016/0361-9230(81)90007-1. [DOI] [PubMed] [Google Scholar]
- 3.Fields w.s. Collateral circulation in cerebrovascular disease. In: Vinken P.J, et Bruyan G.w, editors. Handbook of Clinical Neurology. Amsterdam: North - Holland Publishing Co; 1974. [Google Scholar]
- 4.Fisher CM. Lacunar strokes and infarcts, A. rewiew. Neurology. 1982;32:871–876. doi: 10.1212/wnl.32.8.871. [DOI] [PubMed] [Google Scholar]
- 5.Kaplan H.A. Anatomy and embriology of the arterial system of the forebrain. In: Vinken P.J, іBruyan G.w, editors. Handbook of Clinical Neurology. Amsterdam: North-Holland Publishing Co; 1975. [Google Scholar]
- 6.Krayenbuhl H, Yasargil M.G. Der cerebrale kollaterale, Blutkreislauf im angiographischen Bild. Acta Neurochir. 1978;6:30–80. doi: 10.1007/BF01577673. [DOI] [PubMed] [Google Scholar]
- 7.Lazorthes G, et al. La distribution centrale et corticale de l'artere cerebrale antérieure. Etude anatomique et incidence neurochirurgicales. Neurochirurgie. 1956;2:237. [PubMed] [Google Scholar]
- 8.Mount L.A, Taveras J.M. Artériographie demonstration of the collateral circulation of the cerebral hemispheres. Arch. Neurol. Psychiat. 1957;78:235–257. doi: 10.1001/archneurpsyc.1957.02330390017003. [DOI] [PubMed] [Google Scholar]
- 9.Pitts F.w. Variations of collateral circulation in internal carotid occlusion. Comparison of clinical and X-ray findings. Neurology. 1991;12:467–471. doi: 10.1212/wnl.12.7.467. [DOI] [PubMed] [Google Scholar]
- 10.Quiring D. Collateral circulation. Anatomic aspects. Philadelphia: Lia & Febiger; 1949. [Google Scholar]
- 11.Ring A.B, et al. The cerebral cortical arteries. In: Salamon G, editor. Advances in cerebral Angiography. Springer Verlag; 1975. [Google Scholar]
- 12.Tatelman M. Pathways of cerebral collateral circulation. Radiology. 1960;75:349–362. doi: 10.1148/75.3.349. [DOI] [PubMed] [Google Scholar]
