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Published in: Neuroradiology 2/2013

01-09-2013 | Invited Review

Potential mechanisms of cerebellar hypoplasia in prematurity

Author: Emily W. Y. Tam

Published in: Neuroradiology | Special Issue 2/2013

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Abstract

Introduction

The cerebellum undergoes dramatic growth and maturation over the neonatal period after preterm birth and is thus particularly sensitive to impaired development due to various clinical factors.

Methods

Impairments in growth can occur independent of cerebellar parenchymal damage, such as from local hemorrhage, resulting from reduced expression of sonic hedgehog signaling to trigger the appropriate expansion of the granule precursor cells.

Results

The primary risk factors for impaired cerebellar development include postnatal glucocorticoid exposure, which has direct effects on the sonic hedgehog pathway, and supratentorial brain injury, including intraventricular hemorrhage and white matter injury, which may result in crossed cerebellar diaschisis and local toxic effects of blood products on the external granular layer. Other cardiorespiratory and nutritional factors may also exist. Impaired cerebellar development is associated with adverse outcomes in motor and cognitive development.

Conclusion

New approaches to care to counteract these risk factors may help improve long-term outcome after preterm birth.
Literature
1.
go back to reference Tommiska V, Heinonen K, Lehtonen L, Renlund M, Saarela T, Tammela O, Virtanen M, Fellman V (2007) No improvement in outcome of nationwide extremely low birth weight infant populations between 1996–1997 and 1999–2000. Pediatrics 119(1):29–36PubMedCrossRef Tommiska V, Heinonen K, Lehtonen L, Renlund M, Saarela T, Tammela O, Virtanen M, Fellman V (2007) No improvement in outcome of nationwide extremely low birth weight infant populations between 1996–1997 and 1999–2000. Pediatrics 119(1):29–36PubMedCrossRef
2.
go back to reference Arnaud C, Daubisse-Marliac L, White-Koning M, Pierrat V, Larroque B, Grandjean H, Alberge C, Marret S, Burguet A, Ancel PY, Supernant K, Kaminski M (2007) Prevalence and associated factors of minor neuromotor dysfunctions at age 5 years in prematurely born children: the EPIPAGE study. Arch Pediatr Adolesc Med 161(11):1053–1061PubMedCrossRef Arnaud C, Daubisse-Marliac L, White-Koning M, Pierrat V, Larroque B, Grandjean H, Alberge C, Marret S, Burguet A, Ancel PY, Supernant K, Kaminski M (2007) Prevalence and associated factors of minor neuromotor dysfunctions at age 5 years in prematurely born children: the EPIPAGE study. Arch Pediatr Adolesc Med 161(11):1053–1061PubMedCrossRef
3.
go back to reference Roussounis SH, Hubley PA, Dear PR (1993) Five-year-follow-up of very low birthweight infants: neurological and psychological outcome. Child Care Health Dev 19(1):45–59PubMedCrossRef Roussounis SH, Hubley PA, Dear PR (1993) Five-year-follow-up of very low birthweight infants: neurological and psychological outcome. Child Care Health Dev 19(1):45–59PubMedCrossRef
4.
go back to reference Wood NS, Marlow N, Costeloe K, Gibson AT, Wilkinson AR (2000) Neurologic and developmental disability after extremely preterm birth. EPICure study group. N Engl J Med 343(6):378–384PubMedCrossRef Wood NS, Marlow N, Costeloe K, Gibson AT, Wilkinson AR (2000) Neurologic and developmental disability after extremely preterm birth. EPICure study group. N Engl J Med 343(6):378–384PubMedCrossRef
5.
go back to reference Hack M, Taylor G, Breslau N et al (1994) School-age outcomes in children with birth weights under 750 g. N Eng J Med 331:753–759CrossRef Hack M, Taylor G, Breslau N et al (1994) School-age outcomes in children with birth weights under 750 g. N Eng J Med 331:753–759CrossRef
6.
go back to reference Hack M, Taylor HG (2000) Perinatal brain injury in preterm infants and later neurobehavioral function. JAMA 284(15):1973–1974PubMedCrossRef Hack M, Taylor HG (2000) Perinatal brain injury in preterm infants and later neurobehavioral function. JAMA 284(15):1973–1974PubMedCrossRef
7.
go back to reference Hack M, Flannery D, Schluchter M, Cartar L, Borawski E, Klein N (2002) Outcomes in young adulthood for very-low-birth-weight infants. N Engl J Med 346:149–157PubMedCrossRef Hack M, Flannery D, Schluchter M, Cartar L, Borawski E, Klein N (2002) Outcomes in young adulthood for very-low-birth-weight infants. N Engl J Med 346:149–157PubMedCrossRef
8.
go back to reference Bhutta A, Cleves M, Casey P, Cradock M, Anand K (2002) Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. JAMA 288:728–737PubMedCrossRef Bhutta A, Cleves M, Casey P, Cradock M, Anand K (2002) Cognitive and behavioral outcomes of school-aged children who were born preterm: a meta-analysis. JAMA 288:728–737PubMedCrossRef
9.
go back to reference Dyet LE, Kennea N, Counsell SJ, Maalouf EF, Ajayi-Obe M, Duggan PJ, Harrison M, Allsop JM, Hajnal J, Herlihy AH, Edwards B, Laroche S, Cowan FM, Rutherford MA, Edwards AD (2006) Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 118(2):536–548PubMedCrossRef Dyet LE, Kennea N, Counsell SJ, Maalouf EF, Ajayi-Obe M, Duggan PJ, Harrison M, Allsop JM, Hajnal J, Herlihy AH, Edwards B, Laroche S, Cowan FM, Rutherford MA, Edwards AD (2006) Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 118(2):536–548PubMedCrossRef
10.
go back to reference Northam GB, Liegeois F, Chong WK, Wyatt JS, Baldeweg T (2011) Total brain white matter is a major determinant of IQ in adolescents born preterm. Ann Neurol 69(4):702–711PubMedCrossRef Northam GB, Liegeois F, Chong WK, Wyatt JS, Baldeweg T (2011) Total brain white matter is a major determinant of IQ in adolescents born preterm. Ann Neurol 69(4):702–711PubMedCrossRef
11.
go back to reference Brouwer A, Groenendaal F, van Haastert IL, Rademaker K, Hanlo P, de Vries L (2008) Neurodevelopmental outcome of preterm infants with severe intraventricular hemorrhage and therapy for post-hemorrhagic ventricular dilatation. J Pediatr 152(5):648–654PubMedCrossRef Brouwer A, Groenendaal F, van Haastert IL, Rademaker K, Hanlo P, de Vries L (2008) Neurodevelopmental outcome of preterm infants with severe intraventricular hemorrhage and therapy for post-hemorrhagic ventricular dilatation. J Pediatr 152(5):648–654PubMedCrossRef
12.
go back to reference Miller SP, Ferriero DM, Leonard C, Piecuch R, Glidden DV, Partridge JC, Perez M, Mukherjee P, Vigneron DB, Barkovich AJ (2005) Early brain injury in premature newborns detected with magnetic resonance imaging is associated with adverse early neurodevelopmental outcome. J Pediatr 147(5):609–616PubMedCrossRef Miller SP, Ferriero DM, Leonard C, Piecuch R, Glidden DV, Partridge JC, Perez M, Mukherjee P, Vigneron DB, Barkovich AJ (2005) Early brain injury in premature newborns detected with magnetic resonance imaging is associated with adverse early neurodevelopmental outcome. J Pediatr 147(5):609–616PubMedCrossRef
13.
go back to reference Haldipur P, Bharti U, Govindan S, Sarkar C, Iyengar S, Gressens P, Mani S (2012) Expression of sonic hedgehog during cell proliferation in the human cerebellum. Stem Cells Dev 21(7):1059–1068PubMedCrossRef Haldipur P, Bharti U, Govindan S, Sarkar C, Iyengar S, Gressens P, Mani S (2012) Expression of sonic hedgehog during cell proliferation in the human cerebellum. Stem Cells Dev 21(7):1059–1068PubMedCrossRef
14.
go back to reference Kiessling MC, Buttner A, Butti C, Muller-Starck J, Milz S, Hof PR, Frank HG, Schmitz C (2013) Cerebellar granule cells are generated postnatally in humans. Brain Struct Funct. doi:10.1007/s00429-013-0565-z PubMed Kiessling MC, Buttner A, Butti C, Muller-Starck J, Milz S, Hof PR, Frank HG, Schmitz C (2013) Cerebellar granule cells are generated postnatally in humans. Brain Struct Funct. doi:10.​1007/​s00429-013-0565-z PubMed
15.
go back to reference Tam EW, Miller SP, Studholme C, Chau V, Glidden D, Poskitt KJ, Ferriero DM, Barkovich AJ (2011) Differential effects of intraventricular hemorrhage and white matter injury on preterm cerebellar growth. J Pediatr 158(3):366–371PubMedCrossRef Tam EW, Miller SP, Studholme C, Chau V, Glidden D, Poskitt KJ, Ferriero DM, Barkovich AJ (2011) Differential effects of intraventricular hemorrhage and white matter injury on preterm cerebellar growth. J Pediatr 158(3):366–371PubMedCrossRef
16.
go back to reference Lemire R, Loeser J, Leech R, Alvord EJ (1975) Normal and abnormal development of the human nervous system. Harper & Row, Hagerstown Lemire R, Loeser J, Leech R, Alvord EJ (1975) Normal and abnormal development of the human nervous system. Harper & Row, Hagerstown
17.
go back to reference Allin M, Matsumoto H, Santhouse AM, Nosarti C, AlAsady MH, Stewart AL, Rifkin L, Murray RM (2001) Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain 124(Pt 1):60–66PubMedCrossRef Allin M, Matsumoto H, Santhouse AM, Nosarti C, AlAsady MH, Stewart AL, Rifkin L, Murray RM (2001) Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain 124(Pt 1):60–66PubMedCrossRef
18.
go back to reference Messerschmidt A, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Birnbacher R, Prayer D (2005) Disruption of cerebellar development: potential complication of extreme prematurity. AJNR Am J Neuroradiol 26(7):1659–1667PubMed Messerschmidt A, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Birnbacher R, Prayer D (2005) Disruption of cerebellar development: potential complication of extreme prematurity. AJNR Am J Neuroradiol 26(7):1659–1667PubMed
19.
go back to reference Hart AR, Whitby EH, Clark SJ, Paley MN, Smith MF (2010) Diffusion-weighted imaging of cerebral white matter and the cerebellum following preterm birth. Dev Med Child Neurol 52(7):652–659PubMedCrossRef Hart AR, Whitby EH, Clark SJ, Paley MN, Smith MF (2010) Diffusion-weighted imaging of cerebral white matter and the cerebellum following preterm birth. Dev Med Child Neurol 52(7):652–659PubMedCrossRef
20.
go back to reference Haldipur P, Bharti U, Alberti C, Sarkar C, Gulati G, Iyengar S, Gressens P, Mani S (2011) Preterm delivery disrupts the developmental program of the cerebellum. PLoS One 6(8):e23449PubMedCrossRef Haldipur P, Bharti U, Alberti C, Sarkar C, Gulati G, Iyengar S, Gressens P, Mani S (2011) Preterm delivery disrupts the developmental program of the cerebellum. PLoS One 6(8):e23449PubMedCrossRef
21.
go back to reference Limperopoulos C, Bassan H, Gauvreau K, Robertson RL Jr, Sullivan NR, Benson CB, Avery L, Stewart J, Soul JS, Ringer SA, Volpe JJ, du Plessis AJ (2007) Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics 120(3):584–593PubMedCrossRef Limperopoulos C, Bassan H, Gauvreau K, Robertson RL Jr, Sullivan NR, Benson CB, Avery L, Stewart J, Soul JS, Ringer SA, Volpe JJ, du Plessis AJ (2007) Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics 120(3):584–593PubMedCrossRef
23.
go back to reference Tam EW, Rosenbluth G, Rogers EE, Ferriero DM, Glidden D, Goldstein RB, Glass HC, Piecuch RE, Barkovich AJ (2011) Cerebellar hemorrhage on magnetic resonance imaging in preterm newborns associated with abnormal neurologic outcome. J Pediatr 158(2):245–250PubMedCrossRef Tam EW, Rosenbluth G, Rogers EE, Ferriero DM, Glidden D, Goldstein RB, Glass HC, Piecuch RE, Barkovich AJ (2011) Cerebellar hemorrhage on magnetic resonance imaging in preterm newborns associated with abnormal neurologic outcome. J Pediatr 158(2):245–250PubMedCrossRef
24.
go back to reference Spittle AJ, Doyle LW, Anderson PJ, Inder TE, Lee KJ, Boyd RN, Cheong JL (2010) Reduced cerebellar diameter in very preterm infants with abnormal general movements. Early Hum Dev 86(1):1–5PubMedCrossRef Spittle AJ, Doyle LW, Anderson PJ, Inder TE, Lee KJ, Boyd RN, Cheong JL (2010) Reduced cerebellar diameter in very preterm infants with abnormal general movements. Early Hum Dev 86(1):1–5PubMedCrossRef
25.
go back to reference Messerschmidt A, Fuiko R, Prayer D, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Weber M, Birnbacher R (2008) Disrupted cerebellar development in preterm infants is associated with impaired neurodevelopmental outcome. Eur J Pediatr 167(10):1141–1147PubMedCrossRef Messerschmidt A, Fuiko R, Prayer D, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Weber M, Birnbacher R (2008) Disrupted cerebellar development in preterm infants is associated with impaired neurodevelopmental outcome. Eur J Pediatr 167(10):1141–1147PubMedCrossRef
26.
go back to reference Lind A, Parkkola R, Lehtonen L, Munck P, Maunu J, Lapinleimu H, Haataja L (2011) Associations between regional brain volumes at term-equivalent age and development at 2 years of age in preterm children. Pediatr Radiol 41(8):953–961PubMedCrossRef Lind A, Parkkola R, Lehtonen L, Munck P, Maunu J, Lapinleimu H, Haataja L (2011) Associations between regional brain volumes at term-equivalent age and development at 2 years of age in preterm children. Pediatr Radiol 41(8):953–961PubMedCrossRef
27.
go back to reference Van Kooij BJ, Benders MJ, Anbeek P, Van Haastert IC, De Vries LS, Groenendaal F (2012) Cerebellar volume and proton magnetic resonance spectroscopy at term, and neurodevelopment at 2 years of age in preterm infants. Dev Med Child Neurol 54(3):260–266PubMedCrossRef Van Kooij BJ, Benders MJ, Anbeek P, Van Haastert IC, De Vries LS, Groenendaal F (2012) Cerebellar volume and proton magnetic resonance spectroscopy at term, and neurodevelopment at 2 years of age in preterm infants. Dev Med Child Neurol 54(3):260–266PubMedCrossRef
28.
go back to reference Parker J, Mitchell A, Kalpakidou A, Walshe M, Jung H-Y, Nosarti C, Santosh P, Rifkin L, Wyatt J, Murray RM, Allin M (2008) Cerebellar growth and behavioural & neuropsychological outcome in preterm adolescents. Brain 131(Pt 5):1344–1351PubMed Parker J, Mitchell A, Kalpakidou A, Walshe M, Jung H-Y, Nosarti C, Santosh P, Rifkin L, Wyatt J, Murray RM, Allin M (2008) Cerebellar growth and behavioural & neuropsychological outcome in preterm adolescents. Brain 131(Pt 5):1344–1351PubMed
29.
go back to reference Allin MP, Salaria S, Nosarti C, Wyatt J, Rifkin L, Murray RM (2005) Vermis and lateral lobes of the cerebellum in adolescents born very preterm. Neuroreport 16(16):1821–1824PubMedCrossRef Allin MP, Salaria S, Nosarti C, Wyatt J, Rifkin L, Murray RM (2005) Vermis and lateral lobes of the cerebellum in adolescents born very preterm. Neuroreport 16(16):1821–1824PubMedCrossRef
30.
go back to reference Pavlik A, Buresova M (1984) The neonatal cerebellum: the highest level of glucocorticoid receptors in the brain. Brain Res 314(1):13–20PubMed Pavlik A, Buresova M (1984) The neonatal cerebellum: the highest level of glucocorticoid receptors in the brain. Brain Res 314(1):13–20PubMed
31.
go back to reference Noguchi KK, Walls KC, Wozniak DF, Olney JW, Roth KA, Farber NB (2008) Acute neonatal glucocorticoid exposure produces selective and rapid cerebellar neural progenitor cell apoptotic death. Cell Death Differ 15(10):1582–1592PubMedCrossRef Noguchi KK, Walls KC, Wozniak DF, Olney JW, Roth KA, Farber NB (2008) Acute neonatal glucocorticoid exposure produces selective and rapid cerebellar neural progenitor cell apoptotic death. Cell Death Differ 15(10):1582–1592PubMedCrossRef
32.
go back to reference Bohn MC, Lauder JM (1978) The effects of neonatal hydrocortisone on rat cerebellar development. Dev Neurosci 1:250–266CrossRef Bohn MC, Lauder JM (1978) The effects of neonatal hydrocortisone on rat cerebellar development. Dev Neurosci 1:250–266CrossRef
33.
go back to reference Jacobs CM, Trinh MD, Rootwelt T, Lomo J, Paulsen RE (2006) Dexamethasone induces cell death which may be blocked by NMDA receptor antagonists but is insensitive to Mg2+ in cerebellar granule neurons. Brain Res 1070(1):116–123PubMedCrossRef Jacobs CM, Trinh MD, Rootwelt T, Lomo J, Paulsen RE (2006) Dexamethasone induces cell death which may be blocked by NMDA receptor antagonists but is insensitive to Mg2+ in cerebellar granule neurons. Brain Res 1070(1):116–123PubMedCrossRef
34.
go back to reference Aden P, Goverud I, Liestol K, Loberg EM, Paulsen RE, Maehlen J, Lomo J (2008) Low-potency glucocorticoid hydrocortisone has similar neurotoxic effects as high-potency glucocorticoid dexamethasone on neurons in the immature chicken cerebellum. Brain Res 1236:39–48PubMedCrossRef Aden P, Goverud I, Liestol K, Loberg EM, Paulsen RE, Maehlen J, Lomo J (2008) Low-potency glucocorticoid hydrocortisone has similar neurotoxic effects as high-potency glucocorticoid dexamethasone on neurons in the immature chicken cerebellum. Brain Res 1236:39–48PubMedCrossRef
35.
go back to reference Heine VM, Rowitch DH (2009) Hedgehog signaling has a protective effect in glucocorticoid-induced mouse neonatal brain injury through an 11betaHSD2-dependent mechanism. J Clin Invest 119(2):267–277PubMed Heine VM, Rowitch DH (2009) Hedgehog signaling has a protective effect in glucocorticoid-induced mouse neonatal brain injury through an 11betaHSD2-dependent mechanism. J Clin Invest 119(2):267–277PubMed
36.
go back to reference Tam EW, Chau V, Ferriero DM, Barkovich AJ, Poskitt KJ, Studholme C, Fok ED, Grunau RE, Glidden DV, Miller SP (2011) Preterm cerebellar growth impairment after postnatal exposure to glucocorticoids. Sci Transl Med 3(105):105ra105PubMedCrossRef Tam EW, Chau V, Ferriero DM, Barkovich AJ, Poskitt KJ, Studholme C, Fok ED, Grunau RE, Glidden DV, Miller SP (2011) Preterm cerebellar growth impairment after postnatal exposure to glucocorticoids. Sci Transl Med 3(105):105ra105PubMedCrossRef
37.
go back to reference Parikh NA, Lasky RE, Kennedy KA, Moya FR, Hochhauser L, Romo S, Tyson JE (2007) Postnatal dexamethasone therapy and cerebral tissue volumes in extremely low birth weight infants. Pediatrics 119(2):265–272PubMedCrossRef Parikh NA, Lasky RE, Kennedy KA, Moya FR, Hochhauser L, Romo S, Tyson JE (2007) Postnatal dexamethasone therapy and cerebral tissue volumes in extremely low birth weight infants. Pediatrics 119(2):265–272PubMedCrossRef
38.
go back to reference Benders MJ, Groenendaal F, van Bel F, Ha Vinh R, Dubois J, Lazeyras F, Warfield SK, Huppi PS, de Vries LS (2009) Brain development of the preterm neonate after neonatal hydrocortisone treatment for chronic lung disease. Pediatr Res 66(5):555–559PubMedCrossRef Benders MJ, Groenendaal F, van Bel F, Ha Vinh R, Dubois J, Lazeyras F, Warfield SK, Huppi PS, de Vries LS (2009) Brain development of the preterm neonate after neonatal hydrocortisone treatment for chronic lung disease. Pediatr Res 66(5):555–559PubMedCrossRef
40.
go back to reference Srinivasan L, Allsop J, Counsell SJ, Boardman JP, Edwards AD, Rutherford M (2006) Smaller cerebellar volumes in very preterm infants at term-equivalent age are associated with the presence of supratentorial lesions. AJNR Am J Neuroradiol 27(3):573–579PubMed Srinivasan L, Allsop J, Counsell SJ, Boardman JP, Edwards AD, Rutherford M (2006) Smaller cerebellar volumes in very preterm infants at term-equivalent age are associated with the presence of supratentorial lesions. AJNR Am J Neuroradiol 27(3):573–579PubMed
41.
go back to reference Limperopoulos C, Soul JS, Gauvreau K, Huppi PS, Warfield SK, Bassan H, Robertson RL, Volpe JJ, du Plessis AJ (2005) Late gestation cerebellar growth is rapid and impeded by premature birth. Pediatrics 115(3):688–695PubMedCrossRef Limperopoulos C, Soul JS, Gauvreau K, Huppi PS, Warfield SK, Bassan H, Robertson RL, Volpe JJ, du Plessis AJ (2005) Late gestation cerebellar growth is rapid and impeded by premature birth. Pediatrics 115(3):688–695PubMedCrossRef
42.
go back to reference Shah DK, Anderson PJ, Carlin JB, Pavlovic M, Howard K, Thompson DK, Warfield SK, Inder TE (2006) Reduction in cerebellar volumes in preterm infants: relationship to white matter injury and neurodevelopment at two years of age. Pediatr Res 60(1):97–102PubMedCrossRef Shah DK, Anderson PJ, Carlin JB, Pavlovic M, Howard K, Thompson DK, Warfield SK, Inder TE (2006) Reduction in cerebellar volumes in preterm infants: relationship to white matter injury and neurodevelopment at two years of age. Pediatr Res 60(1):97–102PubMedCrossRef
43.
go back to reference Limperopoulos C, Soul JS, Haidar H, Huppi PS, Bassan H, Warfield SK, Robertson RL, Moore M, Akins P, Volpe JJ, du Plessis AJ (2005) Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics 116(4):844–850PubMedCrossRef Limperopoulos C, Soul JS, Haidar H, Huppi PS, Bassan H, Warfield SK, Robertson RL, Moore M, Akins P, Volpe JJ, du Plessis AJ (2005) Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics 116(4):844–850PubMedCrossRef
44.
go back to reference Limperopoulos C, Chilingaryan G, Guizard N, Robertson RL, Du Plessis AJ (2010) Cerebellar injury in the premature infant is associated with impaired growth of specific cerebral regions. Pediatr Res 68(2):145–150PubMedCrossRef Limperopoulos C, Chilingaryan G, Guizard N, Robertson RL, Du Plessis AJ (2010) Cerebellar injury in the premature infant is associated with impaired growth of specific cerebral regions. Pediatr Res 68(2):145–150PubMedCrossRef
45.
go back to reference Limperopoulos C, Chilingaryan G, Sullivan N, Guizard N, Robertson RL, du Plessis AJ (2012) Injury to the premature cerebellum: outcome is related to remote cortical development. Cereb Cortex. doi:10.1093/cercor/bhs354 Limperopoulos C, Chilingaryan G, Sullivan N, Guizard N, Robertson RL, du Plessis AJ (2012) Injury to the premature cerebellum: outcome is related to remote cortical development. Cereb Cortex. doi:10.​1093/​cercor/​bhs354
46.
go back to reference Yan J, Chen C, Hu Q, Yang X, Lei J, Yang L, Wang K, Qin L, Huang H, Zhou C (2008) The role of p53 in brain edema after 24 h of experimental subarachnoid hemorrhage in a rat model. Exp Neurol 214(1):37–46PubMedCrossRef Yan J, Chen C, Hu Q, Yang X, Lei J, Yang L, Wang K, Qin L, Huang H, Zhou C (2008) The role of p53 in brain edema after 24 h of experimental subarachnoid hemorrhage in a rat model. Exp Neurol 214(1):37–46PubMedCrossRef
47.
go back to reference Nakamura T, Keep RF, Hua Y, Schallert T, Hoff JT, Xi G (2004) Deferoxamine-induced attenuation of brain edema and neurological deficits in a rat model of intracerebral hemorrhage. J Neurosurg 100(4):672–678PubMedCrossRef Nakamura T, Keep RF, Hua Y, Schallert T, Hoff JT, Xi G (2004) Deferoxamine-induced attenuation of brain edema and neurological deficits in a rat model of intracerebral hemorrhage. J Neurosurg 100(4):672–678PubMedCrossRef
48.
go back to reference Grojean S, Koziel V, Vert P, Daval JL (2000) Bilirubin induces apoptosis via activation of NMDA receptors in developing rat brain neurons. Exp Neurol 166(2):334–341PubMedCrossRef Grojean S, Koziel V, Vert P, Daval JL (2000) Bilirubin induces apoptosis via activation of NMDA receptors in developing rat brain neurons. Exp Neurol 166(2):334–341PubMedCrossRef
49.
go back to reference Tam EW, Ferriero DM, Xu D, Berman JI, Vigneron DB, Barkovich AJ, Miller SP (2009) Cerebellar development in the preterm neonate: effect of supratentorial brain injury. Pediatr Res 66(1):102–106PubMedCrossRef Tam EW, Ferriero DM, Xu D, Berman JI, Vigneron DB, Barkovich AJ, Miller SP (2009) Cerebellar development in the preterm neonate: effect of supratentorial brain injury. Pediatr Res 66(1):102–106PubMedCrossRef
50.
go back to reference Messerschmidt A, Prayer D, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Pollak A, Weber M, Birnbacher R (2008) Preterm birth and disruptive cerebellar development: assessment of perinatal risk factors. Eur J Paediatr Neurol 12(6):455–460PubMedCrossRef Messerschmidt A, Prayer D, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Pollak A, Weber M, Birnbacher R (2008) Preterm birth and disruptive cerebellar development: assessment of perinatal risk factors. Eur J Paediatr Neurol 12(6):455–460PubMedCrossRef
51.
go back to reference Padilla N, Falcon C, Sanz-Cortes M, Figueras F, Bargallo N, Crispi F, Eixarch E, Arranz A, Botet F, Gratacos E (2011) Differential effects of intrauterine growth restriction on brain structure and development in preterm infants: a magnetic resonance imaging study. Brain Res 1382:98–108PubMedCrossRef Padilla N, Falcon C, Sanz-Cortes M, Figueras F, Bargallo N, Crispi F, Eixarch E, Arranz A, Botet F, Gratacos E (2011) Differential effects of intrauterine growth restriction on brain structure and development in preterm infants: a magnetic resonance imaging study. Brain Res 1382:98–108PubMedCrossRef
52.
go back to reference Ekblad M, Korkeila J, Parkkola R, Lapinleimu H, Haataja L, Lehtonen L (2010) Maternal smoking during pregnancy and regional brain volumes in preterm infants. J Pediatr 156(2):185–190.e1PubMedCrossRef Ekblad M, Korkeila J, Parkkola R, Lapinleimu H, Haataja L, Lehtonen L (2010) Maternal smoking during pregnancy and regional brain volumes in preterm infants. J Pediatr 156(2):185–190.e1PubMedCrossRef
Metadata
Title
Potential mechanisms of cerebellar hypoplasia in prematurity
Author
Emily W. Y. Tam
Publication date
01-09-2013
Publisher
Springer Berlin Heidelberg
Published in
Neuroradiology / Issue Special Issue 2/2013
Print ISSN: 0028-3940
Electronic ISSN: 1432-1920
DOI
https://doi.org/10.1007/s00234-013-1230-1

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