Anaerobic glycolysis preceding white-matter destruction in experimental neonatal hydrocephalus

Paul D. Chumas F.R.C.S.(Edin)1, James M. Drake F.R.C.S.(C)1, Marc R. Del Bigio M.D., Ph.D.1, Marcia Da Silva M.D.1, and Ursula I. Tuor Ph.D.1
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  • 1 Departments of Surgery (Division of Neurosurgery), Pathology (Division of Neuropathology), and Paediatrics (Division of Neonatology), The Hospital for Sick Children and the University of Toronto, Toronto, Ontario, Canada
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✓ The metabolic changes in neonatal hydrocephalus that lead to permanent brain injury are not clearly defined, nor is the extent to which these changes can be prevented by a cerebrospinal fluid shunt. To clarify these processes, cerebral glucose utilization was examined using [14C]2-deoxyglucose autoradiography in 1-month-old kittens, kaolin-induced hydrocephalic littermates, and hydrocephalic kittens in which a ventriculoperitoneal shunt had been inserted 10 days after kaolin injection. The hydrocephalic kittens showed thinning of the cerebral mantle and an anterior-to-posterior gradient of enlargement of the ventricular system, with a ventricle:brain ratio of 24% for the frontal and 35% for the occipital horns compared with control (< 0.5%) and shunted (< 5%) animals. White matter in hydrocephalic animals was edematous. Myelination was delayed in the periventricular region and in the cores of the cerebral gyri.

Glucose utilization in hydrocephalic and shunted animals was unchanged from control animals in all gray-matter regions examined. However, in hydrocephalic animals, the frontal white matter exhibited a significant increase in glucose utilization (25 µmol • 100 gm−1 • min−1) in the cores of gyri compared with normal surrounding white-matter values (14.8 µmol • 100 gm−1 • min−1). Very low values (mean 4 µmol • 100 gm−1 • min−1) were found in areas corresponding to severe white-matter edema, and these areas were surrounded by a halo of increased activity (24 µmol • 100 gm−1 • min−1). In contrast, cytochrome oxidase activity in white matter was homogeneous. Shunting resulted in restoration of the cerebral mantle thickness, a return to normal levels of glucose utilization in the white matter, and an improvement in myelination.

It is suggested that the areas of increased glucose utilization seen in the white matter represent anaerobic glycolysis which, if untreated, progresses to infarction. The pattern of this increased glucose utilization matches that of expected myelination and, during this period of high energy demand, white matter may be susceptible to the hypoperfusion associated with hydrocephalus.

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  • 1.

    Azzarelli B, , Meade P, & Muller J: Hypoxic lesions in areas of primary myelination. A distinct pattern in cerebral palsy. Childs Brain 7:132145, 1980 Azzarelli B, Meade P, Muller J: Hypoxic lesions in areas of primary myelination. A distinct pattern in cerebral palsy. Childs Brain 7:132–145, 1980

    • Search Google Scholar
    • Export Citation
  • 2.

    Brooks DJ, , Beaney RP, & Powell M, et al: Studies on cerebral oxygen metabolism, blood flow, and blood volume, in patients with hydrocephalus before and after surgical decompression, using positron emission tomography. Brain 109:613628, 1986 Brooks DJ, Beaney RP, Powell M, et al: Studies on cerebral oxygen metabolism, blood flow, and blood volume, in patients with hydrocephalus before and after surgical decompression, using positron emission tomography. Brain 109:613–628, 1986

    • Search Google Scholar
    • Export Citation
  • 3.

    Burchfield DJ, , Abrams RM, & Hutchison AA: Local cerebral glucose utilization in normoxemic and hypoxemic newborn lambs. Brain Res Dev Brain Res 55:249253, 1990 Burchfield DJ, Abrams RM, Hutchison AA: Local cerebral glucose utilization in normoxemic and hypoxemic newborn lambs. Brain Res Dev Brain Res 55:249–253, 1990

    • Search Google Scholar
    • Export Citation
  • 4.

    Cavazzuti M, & Duffy TE: Regulation of local cerebral blood flow in normal and hypoxic newborn dogs. Ann Neurol 11:247257, 1982 Cavazzuti M, Duffy TE: Regulation of local cerebral blood flow in normal and hypoxic newborn dogs. Ann Neurol 11:247–257, 1982

    • Search Google Scholar
    • Export Citation
  • 5.

    Chugani HT, , Hovda DA, & Villablanca JR, et al: Metabolic maturation of the brain: a study of local cerebral glucose utilization in the developing cat. J Cereb Blood Flow Metab 11:3547, 1991 Chugani HT, Hovda DA, Villablanca JR, et al: Metabolic maturation of the brain: a study of local cerebral glucose utilization in the developing cat. J Cereb Blood Flow Metab 11:35–47, 1991

    • Search Google Scholar
    • Export Citation
  • 6.

    Chugani HT, & Phelps ME: Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. Science 231:840843, 1986 Chugani HT, Phelps ME: Maturational changes in cerebral function in infants determined by 18FDG positron emission tomography. Science 231:840–843, 1986

    • Search Google Scholar
    • Export Citation
  • 7.

    Chugani HT, , Phelps ME, & Mazziotta JC: Positron emission tomography study of human brain functional development. Ann Neurol 22:487497, 1987 Chugani HT, Phelps ME, Mazziotta JC: Positron emission tomography study of human brain functional development. Ann Neurol 22:487–497, 1987

    • Search Google Scholar
    • Export Citation
  • 8.

    Cremer JE, , Cunningham VJ, & Pardridge WM, et al: Kinetics of blood-brain barrier transport of pyruvate, lactate and glucose in suckling, weanling and adult rats. J Neurochem 33:439445, 1979 Cremer JE, Cunningham VJ, Pardridge WM, et al: Kinetics of blood-brain barrier transport of pyruvate, lactate and glucose in suckling, weanling and adult rats. J Neurochem 33:439–445, 1979

    • Search Google Scholar
    • Export Citation
  • 9.

    Darriet D, , Der T, & Collins RC: Distribution of cytochrome oxidase in rat brain: studies with diaminobenzidine histochemistry in vitro and [14C]cyanide tissue labeling in vivo. J Cereb Blood Flow Metab 6:814, 1986 Darriet D, Der T, Collins RC: Distribution of cytochrome oxidase in rat brain: studies with diaminobenzidine histochemistry in vitro and [14C]cyanide tissue labeling in vivo. J Cereb Blood Flow Metab 6:8–14, 1986

    • Search Google Scholar
    • Export Citation
  • 10.

    Del Bigio MR: Neuropathological changes caused by hydrocephalus. Acta Neuropathol 85:573585, 1993 Del Bigio MR: Neuropathological changes caused by hydrocephalus. Acta Neuropathol 85:573–585, 1993

    • Search Google Scholar
    • Export Citation
  • 11.

    Del Bigio MR, & Bruni JE: Changes in periventricular vasculature of rabbit brain following induction of hydrocephalus and after shunting. J Neurosurg 69:115120, 1988 Del Bigio MR, Bruni JE: Changes in periventricular vasculature of rabbit brain following induction of hydrocephalus and after shunting. J Neurosurg 69:115–120, 1988

    • Search Google Scholar
    • Export Citation
  • 12.

    Del Bigio MR, , Bruni JE, & Fewer HD: Human neonatal hydrocephalus. An electron microscopic study of the periventricular tissue. J Neurosurg 63:5663, 1985 Del Bigio MR, Bruni JE, Fewer HD: Human neonatal hydrocephalus. An electron microscopic study of the periventricular tissue. J Neurosurg 63:56–63, 1985

    • Search Google Scholar
    • Export Citation
  • 13.

    Drake JM, , Potts DG, & Lemaire C: Magnetic resonance imaging of silastic-induced canine hydrocephalus. Surg Neurol 31:2840, 1989 Drake JM, Potts DG, Lemaire C: Magnetic resonance imaging of silastic-induced canine hydrocephalus. Surg Neurol 31:28–40, 1989

    • Search Google Scholar
    • Export Citation
  • 14.

    Duffy TE, , Cavazzuti M, & Cruz NF, et al: Local cerebral glucose metabolism in newborn dogs: effects of hypoxia and halothane anesthesia. Ann Neurol 11:233246, 1982 Duffy TE, Cavazzuti M, Cruz NF, et al: Local cerebral glucose metabolism in newborn dogs: effects of hypoxia and halothane anesthesia. Ann Neurol 11:233–246, 1982

    • Search Google Scholar
    • Export Citation
  • 15.

    Fishman RA, & Greer M: Experimental obstructive hydrocephalus. Changes in the cerebrum. Arch Neurol 8:156161, 1963 Fishman RA, Greer M: Experimental obstructive hydrocephalus. Changes in the cerebrum. Arch Neurol 8:156–161, 1963

    • Search Google Scholar
    • Export Citation
  • 16.

    Friede RL: Hydrocephalus — basic concepts and general pathology, in Friede RL (ed): Developmental Neuropathology, ed 2. Berlin: Springer-Verlag, 1989, pp 220230 Friede RL: Hydrocephalus — basic concepts and general pathology, in Friede RL (ed): Developmental Neuropathology, ed 2. Berlin: Springer-Verlag, 1989, pp 220–230

    • Search Google Scholar
    • Export Citation
  • 17.

    Friede RL: A quantitative study of myelination in hydrocephalus. (Factors controlling glial proliferation in myelination.) J Neuropathol Exp Neurol 21:645648, 1962 Friede RL: A quantitative study of myelination in hydrocephalus. (Factors controlling glial proliferation in myelination.) J Neuropathol Exp Neurol 21:645–648, 1962

    • Search Google Scholar
    • Export Citation
  • 18.

    Fuglsang A, , Lomholt M, & Gjedde A: Blood-brain transfer of glucose and glucose analogs in newborn rats. J Neurochem 46:14171428, 1986 Fuglsang A, Lomholt M, Gjedde A: Blood-brain transfer of glucose and glucose analogs in newborn rats. J Neurochem 46:1417–1428, 1986

    • Search Google Scholar
    • Export Citation
  • 19.

    Gadson DR, , Variend S, & Emery JL: The effect of hydrocephalus upon the myelination of the corpus callosum. Z Kinderchir 25:311319, 1978 Gadson DR, Variend S, Emery JL: The effect of hydrocephalus upon the myelination of the corpus callosum. Z Kinderchir 25:311–319, 1978

    • Search Google Scholar
    • Export Citation
  • 20.

    Gibson GE, & Duffy TE: Impaired synthesis of acetylcholine by mild hypoxic hypoxia or nitrous oxide. J Neurochem 36:2833, 1981 Gibson GE, Duffy TE: Impaired synthesis of acetylcholine by mild hypoxic hypoxia or nitrous oxide. J Neurochem 36:28–33, 1981

    • Search Google Scholar
    • Export Citation
  • 21.

    Gilles FH: Perinatal neuropathology, in Davis RL, & Robertson DM (eds): Textbook of Neuropathology, ed 2. Baltimore: Williams & Wilkins, 1991, pp 281330 Gilles FH: Perinatal neuropathology, in Davis RL, Robertson DM (eds): Textbook of Neuropathology, ed 2. Baltimore: Williams & Wilkins, 1991, pp 281–330

    • Search Google Scholar
    • Export Citation
  • 22.

    Greenberg JH, , Hamar J, & Welsh FA, et al: Effect of ischemia and reperfusion on lambda of the lumped constant of the [14C]deoxyglucose technique. J Cereb Blood Flow Metab 12:7077, 1992 Greenberg JH, Hamar J, Welsh FA, et al: Effect of ischemia and reperfusion on lambda of the lumped constant of the [14C]deoxyglucose technique. J Cereb Blood Flow Metab 12:70–77, 1992

    • Search Google Scholar
    • Export Citation
  • 23.

    Higashi K, , Asahisa H, & Ueda N, et al: Cerebral blood flow and metabolism in experimental hydrocephalus. Neurol Res 8:169176, 1986 Higashi K, Asahisa H, Ueda N, et al: Cerebral blood flow and metabolism in experimental hydrocephalus. Neurol Res 8:169–176, 1986

    • Search Google Scholar
    • Export Citation
  • 24.

    Hill A, & Volpe JJ: Decrease in pulsatile flow in the anterior cerebral arteries in infantile hydrocephalus. Pediatrics 69:47, 1982 Hill A, Volpe JJ: Decrease in pulsatile flow in the anterior cerebral arteries in infantile hydrocephalus. Pediatrics 69:4–7, 1982

    • Search Google Scholar
    • Export Citation
  • 25.

    Hirayama A: Histopathological study of congenital and acquired experimental hydrocephalus. Brain Dev 2:171189, 1980 Hirayama A: Histopathological study of congenital and acquired experimental hydrocephalus. Brain Dev 2:171–189, 1980

    • Search Google Scholar
    • Export Citation
  • 26.

    Hochwald GM: Animal models of hydrocephalus: recent developments. Proc Soc Exp Biol Med 178:111, 1985 Hochwald GM: Animal models of hydrocephalus: recent developments. Proc Soc Exp Biol Med 178:1–11, 1985

    • Search Google Scholar
    • Export Citation
  • 27.

    Hochwald GM, , Boal RD, & Marlin AE, et al: Changes in regional blood-flow and water content of brain and spinal cord in acute and chronic experimental hydrocephalus. Dev Med Child Neurol 17 (Suppl 35): 4250, 1975 Hochwald GM, Boal RD, Marlin AE, et al: Changes in regional blood-flow and water content of brain and spinal cord in acute and chronic experimental hydrocephalus. Dev Med Child Neurol 17 (Suppl 35):42–50, 1975

    • Search Google Scholar
    • Export Citation
  • 28.

    Hochwald GM, , Epstein F, & Malhan C, et al: The relationship of compensated to decompensated hydrocephalus in the cat. J Neurosurg 39:694697, 1973 Hochwald GM, Epstein F, Malhan C, et al: The relationship of compensated to decompensated hydrocephalus in the cat. J Neurosurg 39:694–697, 1973

    • Search Google Scholar
    • Export Citation
  • 29.

    Hovda DA, , Yoshino A, & Kawamata T, et al: Diffuse prolonged depression of cerebral oxidative metabolism following concussive brain injury in the rat: a cytochrome oxidase histochemistry study. Brain Res 567:110, 1991 Hovda DA, Yoshino A, Kawamata T, et al: Diffuse prolonged depression of cerebral oxidative metabolism following concussive brain injury in the rat: a cytochrome oxidase histochemistry study. Brain Res 567:1–10, 1991

    • Search Google Scholar
    • Export Citation
  • 30.

    Ingvar M, , Abdul-Rahman A, & Siesjö BK: Local cerebral glucose consumption in the artificially ventilated rat: influence of nitrous oxide analgesia and of phenobarbital anesthesia. Acta Physiol Scand 109:177185, 1980 Ingvar M, Abdul-Rahman A, Siesjö BK: Local cerebral glucose consumption in the artificially ventilated rat: influence of nitrous oxide analgesia and of phenobarbital anesthesia. Acta Physiol Scand 109:177–185, 1980

    • Search Google Scholar
    • Export Citation
  • 31.

    Kennedy C, , Grave GD, & Jehle JW, et al: Blood flow to white matter during maturation of the brain. Neurology 20:613618, 1970 Kennedy C, Grave GD, Jehle JW, et al: Blood flow to white matter during maturation of the brain. Neurology 20:613–618, 1970

    • Search Google Scholar
    • Export Citation
  • 32.

    Kennedy C, , Grave GD, & Jehle JW, et al: Changes in blood flow in the component structures of the dog brain during postnatal maturation. J Neurochem 19:24232433, 1972 Kennedy C, Grave GD, Jehle JW, et al: Changes in blood flow in the component structures of the dog brain during postnatal maturation. J Neurochem 19:2423–2433, 1972

    • Search Google Scholar
    • Export Citation
  • 33.

    Kennedy C, , Sakurada O, & Shinohara M, et al: Local cerebral glucose utilization in the newborn Macaque monkey. Ann Neurol 12:333340, 1982 Kennedy C, Sakurada O, Shinohara M, et al: Local cerebral glucose utilization in the newborn Macaque monkey. Ann Neurol 12:333–340, 1982

    • Search Google Scholar
    • Export Citation
  • 34.

    Kim SC, , Tompkins P, & Pollay M, et al: Cerebrovascular flow and glucose transport in the hydrocephalic rat, in Matsumoto S, & Tamaki N (eds): Hydrocephalus, Pathogenesis and Treatment. Tokyo: Springer-Verlag, 1991, pp 102106 Kim SC, Tompkins P, Pollay M, et al: Cerebrovascular flow and glucose transport in the hydrocephalic rat, in Matsumoto S, Tamaki N (eds): Hydrocephalus, Pathogenesis and Treatment. Tokyo: Springer-Verlag, 1991, pp 102–106

    • Search Google Scholar
    • Export Citation
  • 35.

    Kim SC, , Tompkins P, & Roberts PA, et al: Cerebral hemodynamics in the chronic hydrocephalic rat. Neurosci Abstr 17:1991 (Abstract No. 190.11) Kim SC, Tompkins P, Roberts PA, et al: Cerebral hemodynamics in the chronic hydrocephalic rat. Neurosci Abstr 17:1991 (Abstract No. 190.11)

    • Search Google Scholar
    • Export Citation
  • 36.

    Lovely TJ, , McAllister JP II, & Miller DW, et al: Effects of hydrocephalus and surgical decompression on cortical norepinephrine levels in neonatal cats. Neurosurgery 24:4352, 1989 Lovely TJ, McAllister JP II, Miller DW, et al: Effects of hydrocephalus and surgical decompression on cortical norepinephrine levels in neonatal cats. Neurosurgery 24:43–52, 1989

    • Search Google Scholar
    • Export Citation
  • 37.

    Lumsden CE: Multiple cystic softening of the brain in the newborn. J Neuropathol Exp Neurol 9:119138, 1950 Lumsden CE: Multiple cystic softening of the brain in the newborn. J Neuropathol Exp Neurol 9:119–138, 1950

    • Search Google Scholar
    • Export Citation
  • 38.

    Lux WE Jr, , Hochwald GM, & Sahar A, et al: Periventricular water content. Effect of pressure in experimental chronic hydrocephalus. Arch Neurol 23:475479, 1970 Lux WE Jr, Hochwald GM, Sahar A, et al: Periventricular water content. Effect of pressure in experimental chronic hydrocephalus. Arch Neurol 23:475–479, 1970

    • Search Google Scholar
    • Export Citation
  • 39.

    Matsumae M, , Sogabe T, & Miura I, et al: Energy metabolism in kaolin-induced hydrocephalic rat brain. Assessed by phosphorus (31P) magnetic resonance spectroscopy and the diversity of lactate-dehydrogenase and its isoenzyme patterns. Childs Nerv Syst 6:392396, 1990 Matsumae M, Sogabe T, Miura I, et al: Energy metabolism in kaolin-induced hydrocephalic rat brain. Assessed by phosphorus (31P) magnetic resonance spectroscopy and the diversity of lactate-dehydrogenase and its isoenzyme patterns. Childs Nerv Syst 6:392–396, 1990

    • Search Google Scholar
    • Export Citation
  • 40.

    McAllister JP III, , Cohen MI, & O'Mara KA, et al: Progression of experimental infantile hydrocephalus and effects of ventriculoperitoneal shunts: an analysis correlating magnetic resonance imaging with gross morphology. Neurosurgery 29:329340, 1991 McAllister JP III, Cohen MI, O'Mara KA, et al: Progression of experimental infantile hydrocephalus and effects of ventriculoperitoneal shunts: an analysis correlating magnetic resonance imaging with gross morphology. Neurosurgery 29:329–340, 1991

    • Search Google Scholar
    • Export Citation
  • 41.

    McCulloch J: Mapping functional alterations in the CNS with [14C]deoxyglucose, in Iverson LL, , Iverson SD, & Snyder SH (eds): Handbook of Psychopharmacology. New York: Plenum Press, 1982, Vol 15, pp 321410 McCulloch J: Mapping functional alterations in the CNS with [14C]deoxyglucose, in Iverson LL, Iverson SD, Snyder SH (eds): Handbook of Psychopharmacology. New York: Plenum Press, 1982, Vol 15, pp 321–410

    • Search Google Scholar
    • Export Citation
  • 42.

    Miyaoka M, , Ito M, & Wada M, et al: Measurement of local cerebral glucose utilization before and after V-P shunt in congenital hydrocephalus in rats. Metab Brain Dis 3:125132, 1988 Miyaoka M, Ito M, Wada M, et al: Measurement of local cerebral glucose utilization before and after V-P shunt in congenital hydrocephalus in rats. Metab Brain Dis 3:125–132, 1988

    • Search Google Scholar
    • Export Citation
  • 43.

    Myers RE: Experimental models of perinatal brain damage: relevance to human pathology, in Gluck L (ed): Intrauterine Asphyxia and the Developing Fetal Brain. Chicago: Year Book Medical, 1977, pp 3798 Myers RE: Experimental models of perinatal brain damage: relevance to human pathology, in Gluck L (ed): Intrauterine Asphyxia and the Developing Fetal Brain. Chicago: Year Book Medical, 1977, pp 37–98

    • Search Google Scholar
    • Export Citation
  • 44.

    Nehlig A, , Pereira de Vasconcelos A, & Boyet S: Relationship between local cerebral blood flow and local cerebral glucose utilization in the rat during postnatal maturation. J Cereb Blood Flow Metab 9 (Suppl 1): S29, 1989 (Abstract) Nehlig A, Pereira de Vasconcelos A, Boyet S: Relationship between local cerebral blood flow and local cerebral glucose utilization in the rat during postnatal maturation. J Cereb Blood Flow Metab 9 (Suppl 1):S29, 1989 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 45.

    Okuyama T, , Hashi K, & Sasaki S, et al: Changes in cerebral microvasculature in congenital hydrocephalus of the inbred rat LEW/Jms: light and electron microscopic examination. Surg Neurol 27:338342, 1987 Okuyama T, Hashi K, Sasaki S, et al: Changes in cerebral microvasculature in congenital hydrocephalus of the inbred rat LEW/Jms: light and electron microscopic examination. Surg Neurol 27:338–342, 1987

    • Search Google Scholar
    • Export Citation
  • 46.

    Pulsinelli WA, & Duffy TE: Local cerebral glucose metabolism during controlled hypoxemia in rats. Science 204:626629, 1979 Pulsinelli WA, Duffy TE: Local cerebral glucose metabolism during controlled hypoxemia in rats. Science 204:626–629, 1979

    • Search Google Scholar
    • Export Citation
  • 47.

    Ransohoff J, , Dimattio J, & Hochwald G, et al: Cerebral fluid dynamics and brain regional blood flow in experimental hydrocephalus. Childs Brain 1:183186, 1975 Ransohoff J, Dimattio J, Hochwald G, et al: Cerebral fluid dynamics and brain regional blood flow in experimental hydrocephalus. Childs Brain 1:183–186, 1975

    • Search Google Scholar
    • Export Citation
  • 48.

    Richards HK, , Bucknall RM, & Jones HC, et al: Cortical glucose metabolism is depressed in symptomatic but not in asymptomatic hydrocephalus in the rat. J Cereb Blood Flow Metab 7 (Suppl 1): S90, 1987 (Abstract) Richards HK, Bucknall RM, Jones HC, et al: Cortical glucose metabolism is depressed in symptomatic but not in asymptomatic hydrocephalus in the rat. J Cereb Blood Flow Metab 7 (Suppl 1):S90, 1987 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 49.

    Richards HK, , Bucknall RM, & Jones HC, et al: The uptake of [14C]deoxyglucose into brain of young rats with inherited hydrocephalus. Exp Neurol 103:194198, 1989 Richards HK, Bucknall RM, Jones HC, et al: The uptake of [14C]deoxyglucose into brain of young rats with inherited hydrocephalus. Exp Neurol 103:194–198, 1989

    • Search Google Scholar
    • Export Citation
  • 50.

    Richards HK, , Pickard JD, & Punt J: Local cerebral glucose utilization in experimental chronic hydrocephalus in the rat. Z Kinderchir 40 (Suppl 1): 9, 1985 (Abstract) Richards HK, Pickard JD, Punt J: Local cerebral glucose utilization in experimental chronic hydrocephalus in the rat. Z Kinderchir 40 (Suppl 1):9, 1985 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 51.

    Rosenberg GA, , Kyner WT, & Estrada E: Bulk flow of brain interstitial fluid under normal and hyperosmolar conditions. Am J Physiol 238:F42F49, 1980 Rosenberg GA, Kyner WT, Estrada E: Bulk flow of brain interstitial fluid under normal and hyperosmolar conditions. Am J Physiol 238:F42–F49, 1980

    • Search Google Scholar
    • Export Citation
  • 52.

    Rosenberg GA, , Saland L, & Kyner WT: Pathophysiology of periventricular tissue changes with raised CSF pressure in cats. J Neurosurg 59:606611, 1983 Rosenberg GA, Saland L, Kyner WT: Pathophysiology of periventricular tissue changes with raised CSF pressure in cats. J Neurosurg 59:606–611, 1983

    • Search Google Scholar
    • Export Citation
  • 53.

    Rowlatt U: The microscopic effects of ventricular dilatation without increase in head size. J Neurosurg 48:957961, 1978 Rowlatt U: The microscopic effects of ventricular dilatation without increase in head size. J Neurosurg 48:957–961, 1978

    • Search Google Scholar
    • Export Citation
  • 54.

    Rubin RC, , Hochwald GM, & Tiell M, et al: Hydrocephalus: I. Histological and ultrastructural changes in the pre-shunted cortical mantle. Surg Neurol 5:109114, 1976 Rubin RC, Hochwald GM, Tiell M, et al: Hydrocephalus: I. Histological and ultrastructural changes in the pre-shunted cortical mantle. Surg Neurol 5:109–114, 1976

    • Search Google Scholar
    • Export Citation
  • 55.

    Rubin RC, , Hochwald GM, & Tiell M, et al: Hydrocephalus: II. Cell number and size, and myelin content of the preshunted cerebral cortical mantle. Surg Neurol 5:115118, 1976 Rubin RC, Hochwald GM, Tiell M, et al: Hydrocephalus: II. Cell number and size, and myelin content of the preshunted cerebral cortical mantle. Surg Neurol 5:115–118, 1976

    • Search Google Scholar
    • Export Citation
  • 56.

    Russell DS: Observations on the pathology of hydrocephalus. Med Res Council Special Rep Ser 265:1138, 1949 Russell DS: Observations on the pathology of hydrocephalus. Med Res Council Special Rep Ser 265:1–138, 1949

    • Search Google Scholar
    • Export Citation
  • 57.

    Sakabe T, , Kuramoto T, & Inoue S, et al: Cerebral effects of nitrous oxide in the dog. Anesthesiology 48:195200, 1978 Sakabe T, Kuramoto T, Inoue S, et al: Cerebral effects of nitrous oxide in the dog. Anesthesiology 48:195–200, 1978

    • Search Google Scholar
    • Export Citation
  • 58.

    Sato O, , Ohya M, & Nojiri K, et al: Microcirculatory changes in experimental hydrocephalus: morphological and physiological studies, in Shapiro K, , Marmarou A, & Portnoy H (eds): Hydrocephalus. New York: Raven Press, 1984, pp 215230 Sato O, Ohya M, Nojiri K, et al: Microcirculatory changes in experimental hydrocephalus: morphological and physiological studies, in Shapiro K, Marmarou A, Portnoy H (eds): Hydrocephalus. New York: Raven Press, 1984, pp 215–230

    • Search Google Scholar
    • Export Citation
  • 59.

    Savaki HE, , Davidsen L, & Smith C, et al: Measurement of free glucose turnover in brain. J Neurochem 35:495502, 1980 Savaki HE, Davidsen L, Smith C, et al: Measurement of free glucose turnover in brain. J Neurochem 35:495–502, 1980

    • Search Google Scholar
    • Export Citation
  • 60.

    Shapiro HM, , Greenberg JH, & Reivich M, et al: Local cerebral glucose uptake in awake and halothane-anesthetized primates. Anesthesiology 48:97103, 1978 Shapiro HM, Greenberg JH, Reivich M, et al: Local cerebral glucose uptake in awake and halothane-anesthetized primates. Anesthesiology 48:97–103, 1978

    • Search Google Scholar
    • Export Citation
  • 61.

    Shirane R, , Sato S, & Kameyama A, et al: Cerebral blood flow and oxygen metabolism in infants with hydrocephalus measured with positron emission tomography. J Cereb Blood Flow Metab 11 ( Suppl 2): S199, 1991 (Abstract) Shirane R, Sato S, Kameyama A, et al: Cerebral blood flow and oxygen metabolism in infants with hydrocephalus measured with positron emission tomography. J Cereb Blood Flow Metab 11 (Suppl 2):S199, 1991 (Abstract)

    • Search Google Scholar
    • Export Citation
  • 62.

    Silverman MS, & Tootell RBH: Modified technique for cytochrome oxidase histochemistry: increased staining intensity and compatibility with 2-deoxyglucose autoradiography. J Neurosci Methods 19:110, 1987 Silverman MS, Tootell RBH: Modified technique for cytochrome oxidase histochemistry: increased staining intensity and compatibility with 2-deoxyglucose autoradiography. J Neurosci Methods 19:1–10, 1987

    • Search Google Scholar
    • Export Citation
  • 63.

    Sogabe T, , Matsumae M, & Sato O, et al: Change in glucose metabolism with time in hydrocephalic rats. Biochem Int 19:513518, 1989 Sogabe T, Matsumae M, Sato O, et al: Change in glucose metabolism with time in hydrocephalic rats. Biochem Int 19:513–518, 1989

    • Search Google Scholar
    • Export Citation
  • 64.

    Sokoloff L, , Reivich M, & Kennedy C, et al: The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem 28:897916, 1977 Sokoloff L, Reivich M, Kennedy C, et al: The [14C]deoxyglucose method for the measurement of local cerebral glucose utilization: theory, procedure, and normal values in the conscious and anesthetized albino rat. J Neurochem 28:897–916, 1977

    • Search Google Scholar
    • Export Citation
  • 65.

    Sutton LN, , Barranco D, & Greenberg J, et al: Cerebral blood flow and glucose metabolism in experimental brain edema. J Neurosurg 71:868874, 1989 Sutton LN, Barranco D, Greenberg J, et al: Cerebral blood flow and glucose metabolism in experimental brain edema. J Neurosurg 71:868–874, 1989

    • Search Google Scholar
    • Export Citation
  • 66.

    Sutton LN, , Welsh F, & Bruce DA: Bioenergetics of acute vasogenic edema. J Neurosurg 53:470476, 1980 Sutton LN, Welsh F, Bruce DA: Bioenergetics of acute vasogenic edema. J Neurosurg 53:470–476, 1980

    • Search Google Scholar
    • Export Citation
  • 67.

    Sutton LN, , Wood JH, & Brooks BR, et al: Cerebrospinal fluid myelin basic protein in hydrocephalus. J Neurosurg 59:467470, 1983 Sutton LN, Wood JH, Brooks BR, et al: Cerebrospinal fluid myelin basic protein in hydrocephalus. J Neurosurg 59:467–470, 1983

    • Search Google Scholar
    • Export Citation
  • 68.

    Takei F, , Shapiro K, & Kohn I: Influence of the rate of ventricular enlargement on the white matter water content in progressive feline hydrocephalus. J Neurosurg 66:577583, 1987 Takei F, Shapiro K, Kohn I: Influence of the rate of ventricular enlargement on the white matter water content in progressive feline hydrocephalus. J Neurosurg 66:577–583, 1987

    • Search Google Scholar
    • Export Citation
  • 69.

    Tamaki N, , Yamashita H, & Kimura M, et al: Changes in the components and content of biological water in the brain of experimental hydrocephalic rabbits. J Neurosurg 73:274278, 1990 Tamaki N, Yamashita H, Kimura M, et al: Changes in the components and content of biological water in the brain of experimental hydrocephalic rabbits. J Neurosurg 73:274–278, 1990

    • Search Google Scholar
    • Export Citation
  • 70.

    Tamaki N, , Yasuda M, & Matsumoto S, et al: Cerebral energy metabolism in experimental canine hydrocephalus. Childs Nerv Syst 6:172178, 1990 Tamaki N, Yasuda M, Matsumoto S, et al: Cerebral energy metabolism in experimental canine hydrocephalus. Childs Nerv Syst 6:172–178, 1990

    • Search Google Scholar
    • Export Citation
  • 71.

    Tuor UI, , Edvinsson L, & McCulloch J: Catecholamines and the relationship between cerebral blood flow and glucose use. Am J Physiol 251:H824H833, 1986 Tuor UI, Edvinsson L, McCulloch J: Catecholamines and the relationship between cerebral blood flow and glucose use. Am J Physiol 251:H824–H833, 1986

    • Search Google Scholar
    • Export Citation
  • 72.

    Villablanca JR, & Olmstead CE: Neurological development of kittens. Dev Psychobiol 12:101127, 1979 Villablanca JR, Olmstead CE: Neurological development of kittens. Dev Psychobiol 12:101–127, 1979

    • Search Google Scholar
    • Export Citation
  • 73.

    Wako N: [Cerebral glucose metabolism studied with (14C)-deoxyglucose method in experimental hydrocephalus.] No To Shinkei 35:693701, 1983 (Jpn) Wako N: [Cerebral glucose metabolism studied with (14C)-deoxyglucose method in experimental hydrocephalus.] No To Shinkei 35:693–701, 1983 (Jpn)

    • Search Google Scholar
    • Export Citation
  • 74.

    Weller RO, & Shulman K: Infantile hydrocephalus: clinical, histological, and ultrastructural study of brain damage. J Neurosurg 36:255265, 1972 Weller RO, Shulman K: Infantile hydrocephalus: clinical, histological, and ultrastructural study of brain damage. J Neurosurg 36:255–265, 1972

    • Search Google Scholar
    • Export Citation
  • 75.

    Weller RO, & Williams BN: Cerebral biopsy and assessment of brain damage in hydrocephalus. Arch Dis Child 50:763768, 1975 Weller RO, Williams BN: Cerebral biopsy and assessment of brain damage in hydrocephalus. Arch Dis Child 50:763–768, 1975

    • Search Google Scholar
    • Export Citation
  • 76.

    Welsh FA, , O'Connor MJ, & Marcy VR: Effect of oligemia on regional metabolite levels in cat brain. J Neurochem 31:311319, 1978 Welsh FA, O'Connor MJ, Marcy VR: Effect of oligemia on regional metabolite levels in cat brain. J Neurochem 31:311–319, 1978

    • Search Google Scholar
    • Export Citation
  • 77.

    Wong-Riley MTT: Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12:94101, 1989 Wong-Riley MTT: Cytochrome oxidase: an endogenous metabolic marker for neuronal activity. Trends Neurosci 12:94–101, 1989

    • Search Google Scholar
    • Export Citation
  • 78.

    Wozniak M, , McLone DG, & Raimondi AJ: Micro- and macrovascular changes as the direct cause of parenchymal destruction in congenital murine hydrocephalus. J Neurosurg 43:535545, 1975 Wozniak M, McLone DG, Raimondi AJ: Micro- and macrovascular changes as the direct cause of parenchymal destruction in congenital murine hydrocephalus. J Neurosurg 43:535–545, 1975

    • Search Google Scholar
    • Export Citation
  • 79.

    Yoshida Y, , Koya G, & Tamayama K, et al: [Histopathology of cystic cavities in the cerebral white matter of HTX rats with inherited hydrocephalus.] Neurol Med Chir 30:229233, 1990 (Jpn) Yoshida Y, Koya G, Tamayama K, et al: [Histopathology of cystic cavities in the cerebral white matter of HTX rats with inherited hydrocephalus.] Neurol Med Chir 30:229–233, 1990 (Jpn)

    • Search Google Scholar
    • Export Citation

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