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Perinatal Cerebellar Injury in Human and Animal Models

DOI: 10.1155/2012/858929

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Abstract:

Cerebellar injury is increasingly recognized through advanced neonatal brain imaging as a complication of premature birth. Survivors of preterm birth demonstrate a constellation of long-term neurodevelopmental deficits, many of which are potentially referable to cerebellar injury, including impaired motor functions such as fine motor incoordination, impaired motor sequencing and also cognitive, behavioral dysfunction among older patients. This paper reviews the morphogenesis and histogenesis of the human and rodent developing cerebellum, and its more frequent injuries in preterm. Most cerebellar lesions are cerebellar hemorrhage and infarction usually leading to cerebellar abnormalities and/or atrophy, but the exact pathogenesis of lesions of the cerebellum is unknown. The different mechanisms involved have been investigated with animal models and are primarily hypoxia, ischemia, infection, and inflammation Exposure to drugs and undernutrition can also induce cerebellar abnormalities. Different models are detailed to analyze these various disturbances of cerebellar development around birth. 1. Introduction Premature birth is a significant risk factor for adverse motor, coordination, cognitive, and behavioral outcomes in survivors [1]. The prevailing brain pathology in very preterm infants is diffuse white matter injury in the cerebral hemispheres [2]. In addition, a consistent pattern of regionally specific long-term volume reduction and abnormalities in cortical and deep grey matter structures in ex-preterm infants is now recognized [3, 4]. Injury and impaired development of the cerebellum, involving both white matter and grey matter components as a complication of premature birth, are also becoming increasingly recognized with advanced neonatal brain imaging [5–11]. Survivors of preterm birth demonstrate a constellation of long-term neurodevelopmental deficits, many of which are potentially related to cerebellar injury, including impaired motor functions such as hypotonia, fine motor incoordination, ataxia, and impaired motor sequencing [12, 13]. Cerebellar injury has also been implicated in cognitive, social, and behavioral dysfunction among older patients [14, 15] and may contribute to the long-term cognitive, language, and behavioral dysfunction seen among 25% to 50% formerly preterm infants [16–19]. The cerebellum is considered particularly vulnerable in the newborn human because of its very rapid growth at that time, a period comparable in the developing animal. The concept of a particular vulnerability of the cerebellum during its phase of rapid

References

[1]  S. Saigal and L. W. Doyle, “An overview of mortality and sequelae of preterm birth from infancy to adulthood,” The Lancet, vol. 371, no. 9608, pp. 261–269, 2008.
[2]  J. J. Volpe, “Cerebral white matter injury of the premature infant—more common than you think,” Pediatrics, vol. 112, no. 1, pp. 176–180, 2003.
[3]  C. Limperopoulos, J. S. Soul, H. Haidar et al., “Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants,” Pediatrics, vol. 116, no. 4, pp. 844–850, 2005.
[4]  E. W. Y. Tam, S. P. Miller, C. Studholme et al., “Differential effects of intraventricular hemorrhage and white matter injury on preterm cerebellar growth,” Journal of Pediatrics, vol. 158, no. 3, pp. 366–371, 2011.
[5]  A. Messerschmidt, P. C. Brugger, E. Boltshauser et al., “Disruption of cerebellar development: potential complication of extreme prematurity,” American Journal of Neuroradiology, vol. 26, no. 7, pp. 1659–1667, 2005.
[6]  C. R. Pierson, R. D. Folkerth, S. S. Billiards et al., “Gray matter injury associated with periventricular leukomalacia in the premature infant,” Acta Neuropathologica, vol. 114, no. 6, pp. 619–631, 2007.
[7]  C. Nosarti, E. Giouroukou, E. Healy et al., “Grey and white matter distribution in very preterm adolescents mediates neurodevelopmental outcome,” Brain, vol. 131, no. 1, pp. 205–217, 2008.
[8]  J. Parker, A. Mitchell, A. Kalpakidou et al., “Cerebellar growth and behavioural & neuropsychological outcome in preterm adolescents,” Brain, vol. 131, no. 5, pp. 1344–1351, 2008.
[9]  E. W. Y. Tam, D. M. Ferriero, D. Xu et al., “Cerebellar development in the preterm neonate: effect of supratentorial brain injury,” Pediatric Research, vol. 66, no. 1, pp. 102–106, 2009.
[10]  E. W. Y. Tam, G. Rosenbluth, E. E. Rogers et al., “Cerebellar hemorrhage on magnetic resonance imaging in preterm newborns associated with abnormal neurologic outcome,” Journal of Pediatrics, vol. 158, no. 2, pp. 245–250, 2011.
[11]  E. W. Y. Tam, V. Chau, D. M. Ferriero et al., “Preterm birth: preterm cerebellar growth impairment after postnatal exposure to glucocorticoids,” Science Translational Medicine, vol. 3, no. 105, Article ID 105ra105, 2011.
[12]  A. Powls, N. Botting, R. W. I. Cooke, and N. Marlow, “Motor impairment in children 12 to 13 years old with a birthweight of less than 1250?g,” Archives of Disease in Childhood, vol. 73, no. 2, pp. F62–F66, 1995.
[13]  T. A. Goyen, K. Lui, and R. Woods, “Visual-motor, visual-perceptual, and fine motor outcomes in very-low-birthweight children at 5 years,” Developmental Medicine and Child Neurology, vol. 40, no. 2, pp. 76–81, 1998.
[14]  P. C. Berquin, J. N. Giedd, L. K. Jacobsen et al., “Cerebellum in attention-deficit hyperactivity disorder: a morphometric MRI study,” Neurology, vol. 50, no. 4, pp. 1087–1093, 1998.
[15]  L. Levisohn, A. Cronin-Golomb, and J. D. Schmahmann, “Neuropsychological consequences of cerebellar tumour resection in children. Cerebellar cognitive affective syndrome in a paediatric population,” Brain, vol. 123, part 5, pp. 1041–1050, 2000.
[16]  M. Allin, H. Matsumoto, A. M. Santhouse et al., “Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term,” Brain, vol. 124, no. 1, pp. 60–66, 2001.
[17]  C. Limperopoulos, C. B. Benson, H. Bassan et al., “Cerebellar hemorrhage in the preterm infant: ultrasonographic findings and risk factors,” Pediatrics, vol. 116, no. 3, pp. 717–724, 2005.
[18]  C. Limperopoulos, H. Bassan, K. Gauvreau et al., “Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors?” Pediatrics, vol. 120, no. 3, pp. 584–593, 2007.
[19]  A. Messerschmidt, R. Fuiko, D. Prayer et al., “Disrupted cerebellar development in preterm infants is associated with impaired neurodevelopmental outcome,” European Journal of Pediatrics, vol. 167, no. 10, pp. 1141–1147, 2008.
[20]  J. Dobbing, J. W. Hopewell, A. Lynch, and J. Sands, “Vulnerability of developing brain: I. Some lasting effects of X-irradiation,” Experimental Neurology, vol. 28, no. 3, pp. 442–449, 1970.
[21]  J. Dobbing and J. Sands, “Quantitative growth and development of human brain,” Archives of Disease in Childhood, vol. 48, no. 10, pp. 757–767, 1973.
[22]  J. Dobbing, “The later growth of the brain and its vulnerability,” Pediatrics, vol. 53, no. 1, pp. 2–6, 1974.
[23]  C. Sotelo, “Cellular and genetic regulation of the development of the cerebellar system,” Progress in Neurobiology, vol. 72, no. 5, pp. 295–339, 2004.
[24]  M. Ito, “The modifiable neuronal network of the cerebellum,” Japanese Journal of Physiology, vol. 34, no. 5, pp. 781–792, 1984.
[25]  R. J. T. Wingate, “The rhombic lip and early cerebellar development,” Current Opinion in Neurobiology, vol. 11, no. 1, pp. 82–88, 2001.
[26]  J. Altman and S. A. Bayer, “Embryonic development of the rat cerebellum. III. Regional differences in the time of origin, migration, and settling of Purkinje cells,” Journal of Comparative Neurology, vol. 231, no. 1, pp. 42–65, 1985.
[27]  J. D. Loeser, R. J. Lemire, and E. C. Alvord, “The development of the folia in the human cerebellar vermis,” Anatomical Record, vol. 173, no. 1, pp. 109–113, 1972.
[28]  R. L. Sidman and P. Rakic, “Neuronal migration, with special reference to developing human brain: a review,” Brain Research, vol. 62, no. 1, pp. 1–35, 1973.
[29]  C. H. Chang, F. M. Chang, C. H. Yu, H. C. Ko, and H. Y. Chen, “Assessment of fetal cerebellar volume using three-dimensional ultrasound,” Ultrasound in Medicine and Biology, vol. 26, no. 6, pp. 981–988, 2000.
[30]  C. Limperopoulos, J. S. Soul, K. Gauvreau et al., “Late gestation cerebellar growth is rapid and impeded by premature birth,” Pediatrics, vol. 115, no. 3, pp. 688–695, 2005.
[31]  J. D. Merrill, R. E. Piecuch, S. C. Fell, A. J. Barkovich, and R. B. Goldstein, “A new pattern of cerebellar hemorrhages in preterm infants,” Pediatrics, vol. 102, no. 6, p. E62, 1998.
[32]  E. Mercuri, J. He, W. L. Curati, L. M. S. Dubowitz, F. M. Cowan, and G. M. Bydder, “Cerebellar infarction and atrophy in infants and children with a history of premature birth,” Pediatric Radiology, vol. 27, no. 2, pp. 139–143, 1997.
[33]  J. J. Volpe, “Cerebellum of the premature infant: rapidly developing, vulnerable, clinically important,” Journal of Child Neurology, vol. 24, no. 9, pp. 1085–1104, 2009.
[34]  K. E. Pape, D. L. Armstrong, and P. M. Fitzhardinge, “Central nervous system pathology associated with mask ventilation in the very low birthweight infant: a new etiology for intracerebellar hemorrhages,” Pediatrics, vol. 58, no. 4, pp. 473–483, 1976.
[35]  P. Haldipur, U. Bharti, C. Alberti et al., “Preterm delivery disrupts the developmental program of the cerebellum,” PLoS One, vol. 6, no. 8, Article ID e23449, 2011.
[36]  V. Biran, V. M. Heine, C. Verney et al., “Cerebellar abnormalities following hypoxia alone compared to hypoxic-ischemic forebrain injury in the developing rat brain,” Neurobiology of Disease, vol. 41, no. 1, pp. 138–146, 2011.
[37]  J. Towfighi, D. Mauger, R. C. Vannucci, and S. J. Vannucci, “Influence of age on the cerebral lesions in an immature rat model of cerebral hypoxia-ischemia: a light microscopic study,” Developmental Brain Research, vol. 100, no. 2, pp. 149–160, 1997.
[38]  R. Geddes, R. C. Vannucci, and S. J. Vannucci, “Delayed cerebral atrophy following moderate hypoxia-ischemia in the immature rat,” Developmental Neuroscience, vol. 23, no. 3, pp. 180–185, 2001.
[39]  F. J. Northington, D. M. Ferriero, E. M. Graham, R. J. Traystman, and L. J. Martin, “Early neurodegeneration after hypoxia-ischemia in neonatal rat is necrosis while delayed neuronal death is apoptosis,” Neurobiology of Disease, vol. 8, no. 2, pp. 207–219, 2001.
[40]  R. C. Vannucci and S. J. Vannucci, “Perinatal hypoxic-ischemic brain damage: evolution of an animal model,” Developmental Neuroscience, vol. 27, no. 2–4, pp. 81–86, 2005.
[41]  J. S. Meyer, K. Obara, and K. Muramatsu, “Diaschisis,” Neurological Research, vol. 15, no. 6, pp. 362–366, 1993.
[42]  C. Young, T. Tenkova, K. Dikranian, and J. W. Olney, “Excitotoxic versus apoptotic mechanisms of neuronal cell death in perinatal Hypoxia/Ischemia,” Current Molecular Medicine, vol. 4, no. 2, pp. 77–85, 2004.
[43]  B. Infeld, S. M. Davis, M. Lichtenstein, P. J. Mitchell, and J. L. Hopper, “Crossed cerebellar diaschisis and brain recovery after stroke,” Stroke, vol. 26, no. 1, pp. 90–95, 1995.
[44]  J. J. Volpe, “Postnatal sepsis, necrotizing entercolitis, and the critical role of systemic inflammation in white matter injury in premature infants,” Journal of Pediatrics, vol. 153, no. 2, pp. 160–163, 2008.
[45]  D. K. Shah, L. W. Doyle, P. J. Anderson et al., “Adverse neurodevelopment in preterm infants with postnatal sepsis or necrotizing enterocolitis is mediated by white matter abnormalities on magnetic resonance imaging at term,” Journal of Pediatrics, vol. 153, no. 2, pp. 170–175, 2008.
[46]  T. Debillon, C. Gras-Leguen, V. Vérielle et al., “Intrauterine infection induces programmed cell death in rabbit periventricular white matter,” Pediatric Research, vol. 47, no. 6, pp. 736–742, 2000.
[47]  Z. Cai, Z. L. Pan, Y. Pang, O. B. Evans, and P. G. Rhodes, “Cytokine induction in fetal rat brains and brain injury in neonatal rats after maternal lipopolysaccharide administration,” Pediatric Research, vol. 47, no. 1, pp. 64–72, 2000.
[48]  K. Wallace, S. Veerisetty, I. Paul, W. May, J. J. Miguel-Hidalgo, and W. Bennett, “Prenatal infection decreases calbindin, decreases purkinje cell volume and density and produces long-term motor deficits in Sprague-Dawley rats,” Developmental Neuroscience, vol. 32, no. 4, pp. 302–312, 2010.
[49]  K. Nguon, M. G. Baxter, and E. M. Sajdel-Sulkowska, “Perinatal exposure to polychlorinated biphenyls differentially affects cerebellar development and motor functions in male and female rat neonates,” Cerebellum, vol. 4, no. 2, pp. 112–122, 2005.
[50]  J. M. Dean, D. Farrag, S. A. M. Zahkouk et al., “Cerebellar white matter injury following systemic endotoxemia in preterm fetal sheep,” Neuroscience, vol. 160, no. 3, pp. 606–615, 2009.
[51]  L. C. Hutton, E. Yan, T. Yawno, M. Castillo-Melendez, J. J. Hirst, and D. W. Walker, “Injury of the developing cerebellum: a brief review of the effects of endotoxin and asphyxial challenges in the late gestation sheep fetus,” Cerebellum, vol. 3, pp. 1–10, 2007.
[52]  H. Hagberg, D. Peebles, and C. Mallard, “Models of white matter injury: comparison of infectious, hypoxic-Ischemic, and excitotoxic insults,” Mental Retardation and Developmental Disabilities Research Reviews, vol. 8, no. 1, pp. 30–38, 2002.
[53]  J. R. O'Kusky, B. E. Boyes, D. G. Walker, and E. G. McGeer, “Cytomegalovirus infection of the developing brain alters catecholamine and indoleamine metabolism,” Brain Research, vol. 559, no. 2, pp. 322–330, 1991.
[54]  T. Koontz, M. Bralic, J. Tomac et al., “Altered development of the brain after focal herpesvirus infection of the central nervous system,” Journal of Experimental Medicine, vol. 205, no. 2, pp. 423–435, 2008.
[55]  A. N. van den Pol, J. D. Reuter, and J. G. Santarelli, “Enhanced cytomegalovirus infection of developing brain independent of the adaptive immune system,” Journal of Virology, vol. 76, no. 17, pp. 8842–8854, 2002.
[56]  D. J. Bonthius, J. Mahoney, M. J. Buchmeier, B. Karacay, and D. Taggard, “Critical role for glial cells in the propagation and spread of lymphocytic choriomeningitis virus in the developing rat brain,” Journal of Virology, vol. 76, no. 13, pp. 6618–6635, 2002.
[57]  R. L. Naeye, “Cognitive and behavioral abnormalities in children whose mothers smoked cigarettes during pregnancy,” Journal of Developmental and Behavioral Pediatrics, vol. 13, no. 6, pp. 425–428, 1992.
[58]  A. Abdel-Rahman, A. M. Dechkovskaia, J. M. Sutton et al., “Maternal exposure of rats to nicotine via infusion during gestation produces neurobehavioral deficits and elevated expression of glial fibrillary acidic protein in the cerebellum and CA1 subfield in the offspring at puberty,” Toxicology, vol. 209, no. 3, pp. 245–261, 2005.
[59]  T. S. Roy, F. J. Seidler, and T. A. Slotkin, “Prenatal nicotine exposure evokes alterations of cell structure in hippocampus and somatosensory cortex,” Journal of Pharmacology and Experimental Therapeutics, vol. 300, no. 1, pp. 124–133, 2002.
[60]  D. J. Bonthius, N. E. Bonthius, R. M. Napper, S. J. Astley, S. K. Clarren, and J. R. West, “Purkinje cell deficits in nonhuman primates following weekly exposure to ethanol during gestation,” Teratology, vol. 53, pp. 230–236, 1996.
[61]  A. Pavlik and M. Buresova, “The neonatal cerebellum: the highest level of glucocorticoid receptors in the brain,” Developmental Brain Research, vol. 12, no. 1, pp. 13–20, 1984.
[62]  K. K. Noguchi, K. C. Walls, D. F. Wozniak, J. W. Olney, K. A. Roth, and N. B. Farber, “Acute neonatal glucocorticoid exposure produces selective and rapid cerebellar neural progenitor cell apoptotic death,” Cell Death and Differentiation, vol. 15, no. 10, pp. 1582–1592, 2008.
[63]  N. A. Parikh, R. E. Lasky, K. A. Kennedy et al., “Postnatal dexamethasone therapy and cerebral tissue volumes in extremely low birth weight infants,” Pediatrics, vol. 119, no. 2, pp. 265–272, 2007.
[64]  M. J. N. L. Benders, F. Groenendaal, F. van Bel et al., “Brain development of the preterm neonate after neonatal hydrocortisone treatment for chronic lung disease,” Pediatric Research, vol. 66, no. 5, pp. 555–559, 2009.
[65]  C. M. Jacobs, M. D. Trinh, T. Rootwelt, J. L?mo, and R. E. Paulsen, “Dexamethasone induces cell death which may be blocked by NMDA receptor antagonists but is insensitive to Mg2+ in cerebellar granule neurons,” Brain Research, vol. 1070, no. 1, pp. 116–123, 2006.
[66]  P. Aden, I. Goverud, K. Liest?l et al., “Low-potency glucocorticoid hydrocortisone has similar neurotoxic effects as high-potency glucocorticoid dexamethasone on neurons in the immature chicken cerebellum,” Brain Research, vol. 1236, pp. 39–48, 2008.
[67]  V. M. Heine and D. H. Rowitch, “Hedgehog signaling has a protective effect in glucocorticoid-induced mouse neonatal brain injury through an 11βHSD2-dependent mechanism,” The Journal of Clinical Investigation, vol. 119, no. 2, pp. 267–277, 2009.
[68]  V. M. Heine, A. Griveau, C. Chapin, P. L. Ballard, J. K. Chen, and D. H. Rowitch, “Preterm birth: a small-molecule smoothened agonist prevents glucocorticoid-induced neonatal cerebellar injury,” Science Translational Medicine, vol. 3, no. 105, 2011.
[69]  I. K. Sung, B. Vohr, and W. Oh, “Growth and neurodevelopmental outcome of very low birth weight infants with intrauterine growth retardation: comparison with control subjects matched by birth weight and gestational age,” Journal of Pediatrics, vol. 123, no. 4, pp. 618–624, 1993.
[70]  B. Latal-Hajnal, K. Von Siebenthal, H. Kovari, H. U. Bucher, and R. H. Largo, “Postnatal growth in VLBW infants: significant association with neurodevelopmental outcome,” Journal of Pediatrics, vol. 143, no. 2, pp. 163–170, 2003.
[71]  A. Lucas, R. Morley, and T. J. Cole, “Randomised trial of early diet in preterm babies and later intelligence quotient,” British Medical Journal, vol. 317, no. 7171, pp. 1481–1487, 1998.
[72]  M. Hayakawa, A. Okumura, F. Hayakawa et al., “Nutritional state and growth and functional maturation of the brain in extremely low birth weight infants,” Pediatrics, vol. 111, no. 5, pp. 991–995, 2003.
[73]  J. Dobbing, “The effects of early growth retardation on the human brain: the usefulness of animal experiments,” Journal of Pathology, vol. 101, no. 4, article P13, 1970.
[74]  S. Rees, C. Mallard, S. Breen, M. Stringer, M. Cock, and R. Harding, “Fetal brain injury following prolonged hypoxemia and placental insufficiency: a review,” Comparative Biochemistry and Physiology, vol. 119, no. 3, pp. 653–660, 1998.
[75]  S. Rees, M. Stringer, Y. Just, S. B. Hooper, and R. Harding, “The vulnerability of the fetal sheep brain to hypoxemia at mid-gestation,” Developmental Brain Research, vol. 103, no. 2, pp. 103–118, 1997.
[76]  C. Mallard, M. Loeliger, D. Copolov, and S. Rees, “Reduced number of neurons in the hippocampus and the cerebellum in the postnatal guinea-pig following intrauterine growth-restriction,” Neuroscience, vol. 100, no. 2, pp. 327–333, 2000.
[77]  M. Bisignano and S. Rees, “The effects of intrauterine growth retardation on synaptogenesis and mitochondrial formation in the cerebral and cerebellar cortices of fetal sheep,” International Journal of Developmental Neuroscience, vol. 6, no. 5, pp. 453–460, 1988.
[78]  S. Rees and R. Harding, “The effects of intrauterine growth retardation on the development of the Purkinje cell dendritic tree in the cerebellar cortex of fetal sheep: a note on the ontogeny of the Purkinje cell,” International Journal of Developmental Neuroscience, vol. 6, no. 5, pp. 461–469, 1988.
[79]  J. A. Schulman and F. E. Bloom, “Golgi cells of the cerebellum are inhibited by inferior olive activity,” Brain Research, vol. 210, no. 1-2, pp. 350–355, 1981.

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