830 Journal ofNeurology, Neurosurgery, and Psychiatry 1991;54:830-831 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.54.9.830 on 1 September 1991. Downloaded from SHORT REPORT

Concepts of cerebral venous drainage and the aetiology of hydrocephalus

J Andeweg

Abstract there would be a connection through his Evidence is reviewed that an insufficient "veines medullaires"; any connection between venous flow from the brain can cause the ventricular veins and the basal vein was cerebral atrophy and ventricular dilata- apparently unknown to Duret. tion. The belief that hydrocephalus could In 1888, Hedon4 described three anasto- not be caused by venous obstruction is motic pathways from the ventricular veins to the result of erroneous or inadequate the basal vein: the striate veins, the vein of the concepts of venous anatomy. temporal horn (inferior ventricular vein) and the inferior choroidal vein. He also described drainage of the basal vein via the spheno- The anatomy of collateral venous pathways is parietal sinus into the cavernous sinus. He important in circumstances of venous insuffi- concluded that the paraventricular white mat- ciency under experimental or pathological ter drained to the ventricular subependymal conditions. In his 1956 Caldwell Lecture, the veins, not to the convexity via the medullary anatomist Batson' concluded that the large veins assumed by Duret, whose description of vertebral venous plexuses had become forgot- the venous part of the cerebral circulation he ten. These plexuses can serve as collateral found to be erroneous. Hedon did not find pathway for outflow of cranial blood when venous anastomoses passing through the cen- there is obstruction of the jugular veins or trum semiovale. superior vena cava. On this basis Bering and H&don's work was forgotten until it was Salibi2 produced experimental hydrocephalus confirmed by Padget5 in 1956. Padget added in dogs by simultaneous occlusion of the the lateral mesencephalic vein as an anasto- jugular veins and part of the vertebral venous mosis between the basal vein and lateral sinus, system. via the superior petrosal sinus. The result was still interpreted as an inter- In 1934, Bedford6 reported that ligation of ference with cerebrospinal fluid absorption, the great vein of Galen in dogs did not cause but this mechanism cannot explain the hydrocephalus, because there was collateral circulation through the striate, thalamic and occurrence of hydrocephalus when obstruc- http://jnnp.bmj.com/ tion affects only the deep cerebral venous inferior choroidal veins toward the basal vein. system. The anatomy of the deep (Galenic) He did not mention intracerebral anastomoses venots system, however, has been controver- through the centrum semiovale. Bedford sial for more than a century. found the basal vein drained mainly to the In 1874, Duret3 published his extensive lateral sinus in dogs, and he believed the basal investigation of the anatomy of the cerebral vein in humans drained only via the great vein arteries, related to necropsy findings and inter- of Galen. pretations communicated to him by Charcot. In his frequently cited paper, Schlesinger7 on September 27, 2021 by guest. Protected copyright. Charcot was very influential, and Duret's work claimed the existence of anastomoses through- became an important origin of developments out the centrum semiovale, so that separate in neuropathology; but little attention had obstruction of the deep venous system would been paid to veins. According to Duret, long be practically impossible. In three monkeys, so-called medullary arteries and veins straight Schlesinger coagulated the internal cerebral from the convexity would serve the white vein on one side. Instead of considering the matter of the centrum semiovale, with short resulting unilateral hyperaemia to be a mani- cortical arteries and veins serving only the festation of venous obstruction, he interpreted cortex. The corpus striatum would be sup- it as evidence of collateral flow. He called the plied by arteries from the base of the brain, congested radial venules "intracerebral anas- Heiloo, but the striate veins would only be directed tomotic veins", because according to his inter- The Netherlands toward the lateral ventricle. Together with pretation they connected ventricular with J Andeweg veins from the corpus callosum, Ammon's cortical veins. Correspondence to: horn and choroid plexus the striate veins Schlesinger also injected the straight sinus Dr Andeweg, Harrelaers 21, 1852 KT Heiloo, would form the internal cerebral veins termin- in two human brains, at high pressure, and The Netherlands ating in the great vein of Galen. Duret stated believed that this made the so called intra- Received 12 June 1990 that in one case he had succeeded in injecting cerebral anastomotic veins visible throughout and in final revised form 15 December 1990. the ventricular veins through one of the veins the hemispheres. An alternative interpretation Accepted 9 January 1991 of the convexity. He thought it probable that is that the high pressure caused retrograde Concepts of cerebral venous drainage and the aetiology ofhydrocephalus 831 J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.54.9.830 on 1 September 1991. Downloaded from filling ofthe thin medullary arteries descending these conditions retrograde filling of the very from the cortex into the paraventricular white thin arteries which descend from the cortex matter; passage through the capillaries is a into the white matter will also be obtained, via pitfall in anatomical injections, causing con- the capillaries. Hassler regarded the area of fusion between arteries and veins. capillary filling (in the radiographs whiter than Schlesinger considered his findings were the surroundings) as delineating the region of supported by the work of Pfeifer,' who claimed drainage by the deep cerebral veins. He con- to have demonstrated veins traversing the cen- sidered the eventual venous anastomoses too trum semiovale. It was, however, demon- small to be functional, and even maintained strated by a number of investigators that what that occlusion of the great vein of Galen will Pfeifer described as veins were really arteries generally lead to serious effects. His diagrams of and vice versa.9 Thus the "medullary veins" the maximum extent of the deep cerebral toward the cortex, described by Pfeifer, must venous system are clear illustrations ofFerner's have been arteries. "venous watershed". In her well-known monograph on hydro- cephalus, Dorothy Russell'0 briefly stated that venous congestion as a cause of hydrocephalus Conclusion became discredited when Bedford and When only the great vein of Galen is occluded, Schlesinger could not confirm that experi- collateral flow will take place toward cavernous mental occlusion of the great vein of Galen and lateral sinus, with the basal vein as resulted in hydrocephalus. The above account an intermediate channel. Anastomotic veins shows that this view is incorrect. The traversing the centrum semiovale are non- experiments by Bedford and Schlesinger existent or negligible. Instead, a "venous showed that obstruction of the great vein of watershed" exists between the paraventricular Galen alone leaves open many collateral venous white matter on one side, and the cortex and pathways. subcortical white matter on the other. This In 1958, Ferner" described a "venous water- makes it possible to explain ventricular dilata- shed" in the white matter of the cerebral tion as due to atrophy of the paraventricular hemispheres. He investigated the internal white matter, caused by insufficient blood per- cerebral veins and their tributaries by injection fusion from hindrance of venous outflow.'4 of 87 brains from adults. The veins serving the Cranial expansion in the infant can still be cortex and a layer of subcortical white matter regarded as a consequence of elevated intra- run toward the convexity. Venous flow from the cranial pressure. paraventricular white matter is directed toward this the ventricle. The great importance of 1 Batson OV. The vertebral vein system. Caldwell Lecture, separate paraventricular venous drainage is 1956. Am J Roentgenol 1957;78:195-212. 2 Bering EA, Salibi B. Production of hydrocephalus by that it can explain ventricular dilatation as an increased cephalic-venous pressure. Arch Neurol atrophy of the paraventricular white matter Psychiatry 1959;81:693-98. to venous 3 Duret H. Recherches anatomiques sur la circulation de from insufficient blood flow due l'encephale. Arch Physiol Norm Pathol 1874;6:60-91, obstruction. Thus in cases in which only the 316-53,664-93,919-57. will 4 Hedon E. Atude anatomique sur la circulation veineuse de deep venous system is involved, the cortex P'encephale. Bordeaux: Bellier, 1888. not be affected. In congenital hydrocephalus the 5 Padget DH. The cranial venous system in man in reference to development, adult configuration, and relation to the cortex is very often spared. arteries. Am J Anat 1956;98:307-55. http://jnnp.bmj.com/ Kaplan'2 made injection studies and 6 Bedford THB. The great vein of Galen and the syndrome of that anastomoses connect- increased intracranial pressure. Brain 1934;57:1-24. concluded directly 7 Schlesinger B. The venous drainage ofthe brain, with special ing the veins of the cerebral cortex with the reference to the Galenic system. Brain 1939;62:274-91. not been demonstrated 8 Pfeifer RA. Grundlegende Untersuchungen fu?r die Angio- Galenic system had architektonik des menschlichen Gehirns. Berlin: Springer, conclusively. Remarkably, he added that these 1930:209-14. be called "trans- 9 Wunscher W, Werner L. Zur Methodik angioarchitek- radiating channels should tonischer Untersuchungen. Psychiat Neurol Med Psychol cerebral veins". 1961;13:1-6. a contrast of low 10 Russell DS. Observations on the pathology of hydrocephalus. on September 27, 2021 by guest. Protected copyright. Hassler" injected agent London: HMSO, 1949:7. viscosity into the great vein of Galen of 35 11 Ferner H. Anatomische und phlebographische Studien der human brains. In of brain inneren Hirnvenen des Menschen. Z Anat Entwicklungs- radiographs slices, gesch 1958;120:481-91. very thin (approximately 0-1 mm) radiating 12 Kaplan HA. The transcerebral venous system. Arch Neurol channels could be several 1959;1:148-52. seen, totalling 13 Hassler 0. Deep cerebral venous system in man. Neurology thousands in a hemisphere. Low viscosity, high 1966;16:505-1 1. time were 14 Andeweg J. Intracranial venous pressures, hydrocephalus pressure and long injection designed and effects ofcerebrospinal fluid shunts. Child's Nerv Syst to reach even the smallest veins, but under 1989;5:318-23.