Age-dependent Changes of Cerebral Ventrieular Size Part I: Review of Intracranial Fluid Collections E. R. Cardoso, M. R. Del Bigio, and G. Schroeder Cerebral Hydrodynamics Laboratory, Department of Surgery, University of Manitoba, Winnipeg, Manitoba, Canada
Summary The age distributions of communicating hydrocephalus (CH), pseudotumour cerebri (PC) slit-ventricle syndrome (SVS), and chronic subdural haematomas (CSH) were reviewed in the medical literature. An age-related incidence was found: CH and CSH predominated in neonates less than 2 years and adults older than 55 years, while PC and SVS occurred mainly in older children and young adults. The latter two patient groups seem to show a greater resistance to ventricular dilatation in the presence of decreased CSF absorption. This may be related to larger volume and state of maturity of the cerebrum. On the other hand, neonates and the elderly more readily develop enlarged ventricles, in association with impairment of CSF absorption, or subdural fluid collections. Factors including status of cranial sutures, cerebral atrophy, cerebral water content, degree of cerebral myelination, and glial cell composition, may contribute to the age-related incidence of the four disorders investigated. Similarly, the development of ventriculomegaly may depend upon cerebral elastic properties besides the pri mary disturbance of CSF dynamics. The authors postulate that the size of cerebral ventricles in disorders of the ccrcbrospinal fluid (CSF) absorption is related to the elastic properties and volume of the brain. Furthermore, cerebral volume and elastic properties may also contribute to the age distribution of chronic subdural haematomas (CSH).
Introduction T h e b i o m e c h a n i c a l principles t h a t d e t e r m i n e the size o f the c e r e b r a l ventricles are n o t well u n d e r s t o o d . Dist u r b a n c e o f c e r e b r o s p i n a l fluid ( C S F ) c i r c u l a t i o n is the best studied m e c h a n i s m which alters the ventricle size. U n d o u b t e d l y , the p h y s i c a l p r o p e r t i e s o f the c e r e b r u m are also i m p o r t a n t in d e t e r m i n i n g v e n t r i c u l a r size. T h e r e are a v a r i e t y o f d i s o r d e r s t h a t affect fluid-filled c o m p a r t m e n t s in the c r a n i u m a n d s u b s e q u e n t l y affect the v o l u m e o f the b r a i n p a r e n c h y m a .
R a i s e d i n t r a c r a n i a l pressure resulting f r o m cerebrospinal fluid s h u n t m a l f u n c t i o n m a y occur w i t h o u t acc o m p a n y i n g d i l a t a t i o n in h y d r o c e p h a l i c children, a c o n d i t i o n t e r m e d "slit-ventricle s y n d r o m e " (SVS) 11' 45, 65. T h e r e has been n o satisfactory e x p l a n a t i o n w h y ventricles t h a t h a d been p r e v i o u s l y d i l a t e d in these p a tients s u b s e q u e n t l y fail to r e - e x p a n d , as the defect o f CSF absorption probably remains unchanged. Similarly, after o b s t r u c t i o n o f c e r e b r a l v e n o u s d r a i n a g e raised i n t r a c r a n i a l pressure w i t h o u t ventricu l a r d i l a t a t i o n , o r p s e u d o t u m o u r cerebri (PC), m a y result in a d u l t s 3' 7, 23,134. H o w e v e r , similar venous b l o c k age in n e o n a t e s causes h y d r o c e p h a l u s 2I' 23, 25, 84,108. N o t o n l y i n t r a v e n t r i c u l a r a c c u m u l a t i o n o f C S F seems to be r e l a t e d to age, b u t also the c h r o n i c collection o f subd u r a l fluid which is m u c h m o r e c 6 m m o n a m o n g neonates a n d the elderly despite a m u c h higher incidence o f h e a d injuries d u r i n g the second a n d t h i r d decades 83' 88, 105, 119
T h e p u r p o s e o f the p r e s e n t s t u d y is to c o m p a r e the age d i s t r i b u t i o n s o f r e p o r t e d cases o f C H , PC, SVS, a n d c h r o n i c s u b d u r a l h a e m a t o m a s (CSH). W e speculate t h a t a g e - r e l a t e d changes in b o t h cerebral a n d ext r a c e r e b r a l tissues m a y c o n t r i b u t e to the susceptibility to f o r m a t i o n o f i n t r a c r a n i a l fluid collections o f all types.
Methods The medical literature was searched for reports of patients with CH, PC, SVS, or CSH and whose ages were specified or categorized by age divisions of five or fewer years. Patients were then grouped into three intervals for the first decade and 10-year intervals thereafter. Many reported series could not be included in the study because of incomplete information on patient age. No distinction were made between different aetiologies of a particular disorder.
E. R. Cardoso el aL: Age-dependent Changes of Cerebral Ventricular Size. I 40"
Fig. 1. Age distribution of communicating hydrocephalus (CH) (349 patients), pseudotumour cerebri (PC) (289 cases), slit-ventricle syndrome (SVS) (77 cases), and chronic subdural haematoma (CSH) (590 cases). The vertical axis represents the percentage of each age group in relation to the total number of cases for each disorder
A total of 68 studies involving 1,327 patients were reviewed. These included 349 cases of CH t' 9, 26, 34, 49, 5l, 54, 66, 67, 69, 71, 74, 90, 91, 92. 95, 102, 117, 118, 125. 128, 137 289 cases of PC 3" 5, 10, 12, 20, 43, 47, 6,-, 72, 106, 122,124,126,127, 133 77 cases of SVS 4' 8, 16, 17, 24, 36, 38, 41, 45, 46, 58, 61, 68, 113, 1151 116, 130, 14I, and 590 cases of CSH TM 14, 48, 59, 78, 82, 83, 88, 89, 98, 105. 119, 132
The age distributions for the four disorders are displayed in Fig. 1. Well defined peaks of incidence exist for each of them. CH and CSH present a bimodal age distribution with peaks in the first and seventh decades. There is striking overlap between the age incidence for the two diseases. Within the first decade 93% of hydrocephalic patients and 82 % of subdural patients were younger than 4 years of age. Although the graph indicates a peak for PC in the second decade, most of the large series, in which ages are often not specified, indicate a peak in the third or fourth decade 7' 44, 104, 111, 134 In notable contrast to CH and CSH, only 1.1% of the total number of PC patients were younger than 2 years. The age distribution of SVS predominates in the first decade, with only 2.1% of the patients below age 2 years. The age distribution curve for PC paralleled that for SVS, with no patients under 2 years and only 5.2% of patients older than 50 years. Diseussion
CSF absorption is a dynamic process involving various anatomic sites 87' 103. Impaired CSF absorption is
believed to be the main pathophysiologic disturbance in CH and SVS 9' iv, 77, 93. There is controversy whether cerebral vascular engorgement is involved in the development of PC 2' 32,42. However, information obtained from isotope cisternography and dynamic CSF infusion techniques suggest that impaired CSF reabsorption is the most important mechanism involved 63~si, 85,109. Yet the cerebral ventricles remain normal or small in size23' 32, 104, 135
While the disturbance of CSF dynamics in CH is similar to that observed in PC and SVS, ventriculomegaly develops only in CH. The ages of 2 and 50 years represent the lower and upper thresholds involved in the development of ventriculomegaly in diseases caused by diminished CSF absorption. CSF overdrainage in shunted patients may cause cerebral ventricles that are "slit-like ''15' 39. Collapse of the ventricle walls onto the shunt may cause intermittent elevations of intracranial pressure TM 45, 65. Although radiological evidence of "slit-like" ventricles is a common finding following CSF shunting in children, symptomatic SVS, is much less frequent. The reasons for the persistence of small ventricles are not fully understood. Foltz postulated the development of periventricular gliosis which leads to "stiffness" of the ventricular wall 4~ Pathological confirmation of the phenomenon is only suggestive 94. There has been no comparison of shunted hydrocephalics with and without SVS to assess the pathology, SVS follows CH on the same patient. The impaired CSF absorption that caused the initial hydrocephalus
E.R. Cardoso et al.: Age-dependent Changes of Cerebrai Ventricular Size. I
persists throughout the course of SVS17. The ventricles in these patients are initially enlarged. Following shunting the ventricles decrease in size and appear to become resistant to subsequent dilatation. This suggests that cerebral or extra-cerebral factors change with age and lead hydrocephalus to evolve into SVS. SVS in shunted patients is, therefore, analogous to PC. Indeed, there are documented cases of patients who developed alternatively CH and PC, suggesting a common mechanism between the two diseases s7. CH, PC, and SVS have common pathophysiological features of impaired CSF absorption 6' 17, 60, 85, 101,120, reduced cerebral compliance 121, and favourable response to CSF shunting2' 79. Ventriculomegaly, however, develops in CH, but not in PC or SVS, and thus seems to spare the middle years of life. Such an age distribution suggests that other variables, besides decreased CSF absorption, are responsible for the development of ventriculomegaly in neonates and elderly. Elevation of intracranial pressure is likely the factor that precipitates the initial development of ventriculomegaly in C H 33' 50, 99. Furthermore, for ventriculomegaly or chronic subdural collections to develop, gradients of pressure within the cerebral tissue must exist, in order to displace the parenchyma outward is' 100.The displacement of cerebral tissue is probably facilitated by two conditions: 1) diminished resistance of cerebral tissue to deformity and 2) decreased resistance to expansion by structures surrounding the brain. Both conditions are present during neonatal and senile life and they may therefore explain the predisposition to the development of ventriculomegaly or subdural collections in those age groups.
may explain why cerebral venous hypertension, which frequently leads to PC in older age groups, causes CH in children less than 20 months in age21' 23, 25, 27, 84, 86, 97, 107, 108, 112. Rosman and Shands also hypothesized that some alteration of brain consistency is responsible for that differenceI~ In the elderly, the brain parenchyma may be subject to less external resistance to distortion because of larger CSF-filled spaces over the convexities, secondary to senile atrophy of the cerebrum 142.
Composition of Cerebral Tissue Besides impaired CSF absorption and age-related extra-parenchymal resistance, the development of ventriculomegaly and subdural collections may depend upon the physical properties of the cerebral paren-
LEGEND ........ Skull Neuron
1~ o 0"
NO VENTRICULAR DILATATION
Extra-parenehymal Resistance to Cerebral Expansion Patency of cranial sutures, which begin to close at 1 year, partly accounts for diminished resistance to centrifugal cerebral displacement in neonates21. Internal centrifugal forces generated by elevated intracranial pressure can separate the skull bones, thus allowing hydrocephalus and subdural collections to develop. Hochwald et al. described a technique of removal of skull and dura over the convexity prior to induction of obstruction of CSF flow for consistent production of gross ventriculomegaly in cats 37' 55, 56. When only half of the calvavium was removed, the cats showed a greater degree of ventriculomegaly on the craniectomized side 11~ In the clinical setting subtemporal craniectomy also leads to ipsilateral ventricular expansion in patients with impaired CSF absorption 37' 141. This
Fig. 2. Diagramatic representation of cerebral and extra-cerebral factors that may contribute to the development of ventriculomegaly in disorders of CSF absorption or subdural collection of blood. Top: The infant brain with complete number of neurons, but with relatively few glial cells, incompletely myelinated axons, and high water content. The open skull sutures fascilitates the centrifugal displacement of cerebral tissue. Middle: In older children and young adults, ventriculomegaly is prevented by dense glial mass, complete myelination, low water content and closed s~:ull sutures. Bottom: In the elderly, neuronal loss contributes to cerebral atrophy and increase in size of the subarachnoid spaces. Those factors may predispose the development of extra-cerebral fluid collections
E. R. Cardoso etal.: Age-dependent Changes of Cerebral Ventricular Size. I c h y m a itself. Indeed ventriculomegaly precedes head enlargement at the onset o f neonatal hydrocephalus 35' 53, 64, 70. The cyto-architecture o f cerebral tissue varies with age, and m a y alter the ability of the cerebrum to undergo structural deformity such as ventriculomegaly (Fig. 2). A l t h o u g h m o s t neurons are present at birth, the cerebrum contains a relatively sparse population o f glial cells, incompletely myelinated axons, and high water content 3~ 31, 96, 114. The rapid increase in cerebral volume during the first 18 24 m o n t h s o f life is due mainly to proliferation o f glial cells 19' 28, 29, ao. While there is increase in cell and myelin mass, the water content gradually decreases and reaches adult values by 2 to 21/2 years 8~ 129, 138. A x o n a l myelination in the cerebral hemispheres begins after birth and proceeds at a very rapid rate till age 229,129,136, leo. The increasing population o f cellular elements, increase in myelin, and decrease in extracellular water content during the first 2 years o f life are likely to after the elasticity o f the cerebrum and to decrease its capacity to undergo deformity, thus explaining the reduced incidence o f ventriculomegaly after that age. Indeed, the reduction in size o f cerebral ventricles that occurs after infancy has been attributed to myelination 52' 76. After age 55, progressive reduction in weight and volume o f the brain is c o m m o n 22' 75, 123, 139. The resulting a t r o p h y causes enlargement o f sulci and cerebral ventricles. Senile enlargement o f ventricular surface m a y facilitate the development o f hydrocephalus 49. Additionally, senile enlargement o f subarachnoid spaces m a y decrease the resistance to centrifugal displacement o f cerebral tissue and thus facilitate the development o f hydrocephalus and subdural collections in elderly persons.
Conclusions The population distribution o f CH, PC, SVS, and C S H suggests that age-related properties o f the brain and extra-cerebral tissue m a y play a role in the develo p m e n t o f extra-parenchymal fluid collections. A m o n g the entities involving disturbances o f C S F absorption, PC and SVS seem to be closely related. Lack o f ventricular dilatation in both conditions is p r o b a b l y related to the greater volume and stiffness o f the brain. This m a y also explain the rare incidence o f C S H in this age group. The elderly and neonates are m o r e prone to develop both C H and CSH. Lack o f cerebral maturity and opening o f cranial sutures in neonates, and smaller
brains in the elderly m a y predispose the development of extra-cerebral fluid collections in these age groups. The data also suggest that the development o f ventriculomegaly in conditions associated with defective C S F absorption m a y depend u p o n cerebral elasticity and extra-cerebral resistance, in addition to the primary disturbance o f C S F hydrodynamics.
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