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Published in: Acta Neuropathologica Communications 1/2013

Open Access 01-12-2013 | Research

Cerebellar hemorrhagic injury in premature infants occurs during a vulnerable developmental period and is associated with wider neuropathology

Authors: Krista M Haines, Wei Wang, Christopher R Pierson

Published in: Acta Neuropathologica Communications | Issue 1/2013

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Abstract

Background

Cerebellar hemorrhagic injury (CHI) is being recognized more frequently in premature infants. However, much of what we know about CHI neuropathology is from autopsy studies that date back to a prior era of neonatal intensive care. To update and expand our knowledge of CHI we reviewed autopsy materials and medical records of all live-born preterm infants (<37 weeks gestation) autopsied at our institution from 1999–2010 who had destructive hemorrhagic injury to cerebellar parenchyma (n = 19) and compared them to matched non-CHI controls (n = 26).

Results

CHI occurred at a mean gestational age of 25 weeks and involved the ventral aspect of the posterior lobe in almost all cases. CHI arose as a large hemorrhage or as multiple smaller hemorrhages in the emerging internal granule cell layer of the developing cortex or in the nearby white matter. Supratentorial germinal matrix hemorrhage occurred in 95% (18/19) of CHI cases compared to 54% (14/26) of control cases (p = 0.003). The cerebellar cortex frequently showed focal neuronal loss and gliosis (both 15/19, 79%) in CHI cases compared to control cases (both 1/26, 4% p < 0.0001). The cerebellar dentate had more neuronal loss (8/15, 53%) and gliosis (9/15, 60%) in CHI cases than controls (both 0/23, 0%; p < 0.0001). The inferior olivary nuclei showed significantly more neuronal loss in CHI (10/17, 59%) than in control cases (5/26, 19%) (p = 0.0077). All other gray matter sites examined showed no significant difference in the incidence of neuronal loss or gliosis between CHI and controls.

Conclusions

We favor the possibility that CHI represents a primary hemorrhage arising due to the effects of impaired autoregulation in a delicate vascular bed. The incidences of neuronal loss and gliosis in the inferior olivary and dentate nuclei, critical cerebellar input and output structures, respectively were higher in CHI compared to control cases and may represent a transsynpatic degenerative process. CHI occurs during a critical developmental period and may render the cerebellum vulnerable to additional deficits if cerebellar growth and neuronal connectivity are not established as expected. Therefore, CHI has the potential to significantly impact neurodevelopmental outcome in survivors.
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Literature
1.
go back to reference Di Salvo DN: A new view of the neonatal brain: clinical utility of supplemental neurologic US imaging windows. Radiographics 2001,21(4):943–955.PubMed Di Salvo DN: A new view of the neonatal brain: clinical utility of supplemental neurologic US imaging windows. Radiographics 2001,21(4):943–955.PubMed
2.
go back to reference Johnsen SD, Tarby TJ, Lewis KS, Bird R, Prenger E: Cerebellar infarction: an unrecognized complication of very low birthweight. J Child Neurol 2002,17(5):320–324. 10.1177/088307380201700502PubMed Johnsen SD, Tarby TJ, Lewis KS, Bird R, Prenger E: Cerebellar infarction: an unrecognized complication of very low birthweight. J Child Neurol 2002,17(5):320–324. 10.1177/088307380201700502PubMed
3.
go back to reference Merrill JD, Piecuch RE, Fell SC, Barkovich AJ, Goldstein RB: A new pattern of cerebellar hemorrhages in preterm infants. Pediatrics 1998,102(6):E62. 10.1542/peds.102.6.e62PubMed Merrill JD, Piecuch RE, Fell SC, Barkovich AJ, Goldstein RB: A new pattern of cerebellar hemorrhages in preterm infants. Pediatrics 1998,102(6):E62. 10.1542/peds.102.6.e62PubMed
4.
go back to reference Limperopoulos C, Benson CB, Bassan H, Disalvo DN, Kinnamon DD, Moore M, Ringer SA, Volpe JJ, du Plessis AJ: Cerebellar hemorrhage in the preterm infant: ultrasonographic findings and risk factors. Pediatrics 2005,116(3):717–724. 10.1542/peds.2005-0556PubMed Limperopoulos C, Benson CB, Bassan H, Disalvo DN, Kinnamon DD, Moore M, Ringer SA, Volpe JJ, du Plessis AJ: Cerebellar hemorrhage in the preterm infant: ultrasonographic findings and risk factors. Pediatrics 2005,116(3):717–724. 10.1542/peds.2005-0556PubMed
5.
go back to reference Volpe JJ: Intracranial hemorrhage: subdural, primary subarachnoid, intracerebellar, intraventricular (term infnat) and miscellaneous. In Neurology of the newborn. 4th edition. Edited by: Volpe JJ. Philadelphia: Elsevier; 2004:408–413. Volpe JJ: Intracranial hemorrhage: subdural, primary subarachnoid, intracerebellar, intraventricular (term infnat) and miscellaneous. In Neurology of the newborn. 4th edition. Edited by: Volpe JJ. Philadelphia: Elsevier; 2004:408–413.
6.
go back to reference Martin R, Roessmann U, Fanaroff A: Massive intracerebellar hemorrhage in low-birth-weight infants. J Pediatr 1976,89(2):290–293. 10.1016/S0022-3476(76)80470-2PubMed Martin R, Roessmann U, Fanaroff A: Massive intracerebellar hemorrhage in low-birth-weight infants. J Pediatr 1976,89(2):290–293. 10.1016/S0022-3476(76)80470-2PubMed
7.
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: Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 2006,118(2):536–548. 10.1542/peds.2005-1866PubMed 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: Natural history of brain lesions in extremely preterm infants studied with serial magnetic resonance imaging from birth and neurodevelopmental assessment. Pediatrics 2006,118(2):536–548. 10.1542/peds.2005-1866PubMed
8.
go back to reference Hou D, Shetty U, Phillips M, Gray PH: Cerebellar haemorrhage in the extremely preterm infant. J Paediatr Child Health 2012,48(4):350–355. 10.1111/j.1440-1754.2011.02232.xPubMed Hou D, Shetty U, Phillips M, Gray PH: Cerebellar haemorrhage in the extremely preterm infant. J Paediatr Child Health 2012,48(4):350–355. 10.1111/j.1440-1754.2011.02232.xPubMed
9.
go back to reference Muller H, Beedgen B, Schenk JP, Troger J, Linderkamp O: Intracerebellar hemorrhage in premature infants: sonographic detection and outcome. J Perinat Med 2007,35(1):67–70.PubMed Muller H, Beedgen B, Schenk JP, Troger J, Linderkamp O: Intracerebellar hemorrhage in premature infants: sonographic detection and outcome. J Perinat Med 2007,35(1):67–70.PubMed
10.
go back to reference O’Shea TM, Kuban KC, Allred EN, Paneth N, Pagano M, Dammann O, Bostic L, Brooklier K, Butler S, Goldstein DJ, Hounshell G, Keller C, McQuiston S, Miller A, Pasternak S, Plesha-Troyke S, Price J, Romano E, Solomon KM, Jacobson A, Westra S, Leviton A, Extremely Low Gestational Age Newborns Study I: Neonatal cranial ultrasound lesions and developmental delays at 2 years of age among extremely low gestational age children. Pediatrics 2008,122(3):e662-e669. 10.1542/peds.2008-0594PubMedCentralPubMed O’Shea TM, Kuban KC, Allred EN, Paneth N, Pagano M, Dammann O, Bostic L, Brooklier K, Butler S, Goldstein DJ, Hounshell G, Keller C, McQuiston S, Miller A, Pasternak S, Plesha-Troyke S, Price J, Romano E, Solomon KM, Jacobson A, Westra S, Leviton A, Extremely Low Gestational Age Newborns Study I: Neonatal cranial ultrasound lesions and developmental delays at 2 years of age among extremely low gestational age children. Pediatrics 2008,122(3):e662-e669. 10.1542/peds.2008-0594PubMedCentralPubMed
11.
go back to reference Sehgal A, El-Naggar W, Glanc P, Asztalos E: Risk factors and ultrasonographic profile of posterior fossa haemorrhages in preterm infants. J Paediatr Child Health 2009,45(4):215–218. 10.1111/j.1440-1754.2008.01456.xPubMed Sehgal A, El-Naggar W, Glanc P, Asztalos E: Risk factors and ultrasonographic profile of posterior fossa haemorrhages in preterm infants. J Paediatr Child Health 2009,45(4):215–218. 10.1111/j.1440-1754.2008.01456.xPubMed
12.
go back to reference Steggerda SJ, Leijser LM, Wiggers-de Bruine FT, van der Grond J, Walther FJ, van Wezel-Meijler G: Cerebellar injury in preterm infants: incidence and findings on US and MR images. Radiology 2009,252(1):190–199. 10.1148/radiol.2521081525PubMed Steggerda SJ, Leijser LM, Wiggers-de Bruine FT, van der Grond J, Walther FJ, van Wezel-Meijler G: Cerebellar injury in preterm infants: incidence and findings on US and MR images. Radiology 2009,252(1):190–199. 10.1148/radiol.2521081525PubMed
13.
go back to reference Zayek MM, Benjamin JT, Maertens P, Trimm RF, Lal CV, Eyal FG: Cerebellar hemorrhage: a major morbidity in extremely preterm infants. J Perinatol 2012,32(9):699–704. 10.1038/jp.2011.185PubMed Zayek MM, Benjamin JT, Maertens P, Trimm RF, Lal CV, Eyal FG: Cerebellar hemorrhage: a major morbidity in extremely preterm infants. J Perinatol 2012,32(9):699–704. 10.1038/jp.2011.185PubMed
14.
go back to reference Volpe JJ: Cerebellum of the premature infant: rapidly developing, vulnerable, clinically important. J Child Neurol 2009,24(9):1085–1104. 10.1177/0883073809338067PubMedCentralPubMed Volpe JJ: Cerebellum of the premature infant: rapidly developing, vulnerable, clinically important. J Child Neurol 2009,24(9):1085–1104. 10.1177/0883073809338067PubMedCentralPubMed
15.
go back to reference Flodmark O, Becker LE, Harwood-Nash DC, Fitzhardinge PM, Fitz CR, Chuang SH: Correlation between computed tomography and autopsy in premature and full-term neonates that have suffered perinatal asphyxia. Radiology 1980,137(1 Pt 1):93–103.PubMed Flodmark O, Becker LE, Harwood-Nash DC, Fitzhardinge PM, Fitz CR, Chuang SH: Correlation between computed tomography and autopsy in premature and full-term neonates that have suffered perinatal asphyxia. Radiology 1980,137(1 Pt 1):93–103.PubMed
16.
go back to reference Grunnet ML, Shields WD: Cerebellar hemorrhage in the premature infant. J Pediatr 1976, 88: 605–608. 4 Pt. 1 10.1016/S0022-3476(76)80019-4PubMed Grunnet ML, Shields WD: Cerebellar hemorrhage in the premature infant. J Pediatr 1976, 88: 605–608. 4 Pt. 1 10.1016/S0022-3476(76)80019-4PubMed
17.
go back to reference Pape KE, Armstrong DL, Fitzhardinge PM: Central nervous system pathology associated with mask ventilation in the very low birthweight infant: a new etiology for intracerebellar hemorrhages. Pediatrics 1976,58(4):473–483.PubMed Pape KE, Armstrong DL, Fitzhardinge PM: Central nervous system pathology associated with mask ventilation in the very low birthweight infant: a new etiology for intracerebellar hemorrhages. Pediatrics 1976,58(4):473–483.PubMed
18.
go back to reference Perlman JM, Nelson JS, McAlister WH, Volpe JJ: Intracerebellar hemorrhage in a premature newborn: diagnosis by real-time ultrasound and correlation with autopsy findings. Pediatrics 1983,71(2):159–162.PubMed Perlman JM, Nelson JS, McAlister WH, Volpe JJ: Intracerebellar hemorrhage in a premature newborn: diagnosis by real-time ultrasound and correlation with autopsy findings. Pediatrics 1983,71(2):159–162.PubMed
19.
go back to reference Takashima S: Olivocerebellar lesions in infants born prematurely. Brain Dev 1982,4(5):361–366. 10.1016/S0387-7604(82)80020-XPubMed Takashima S: Olivocerebellar lesions in infants born prematurely. Brain Dev 1982,4(5):361–366. 10.1016/S0387-7604(82)80020-XPubMed
20.
go back to reference Pierson CR, Folkerth RD, Billiards SS, Trachtenberg FL, Drinkwater ME, Volpe JJ, Kinney HC: Gray matter injury associated with periventricular leukomalacia in the premature infant. Acta Neuropathol 2007,114(6):619–631. 10.1007/s00401-007-0295-5PubMedCentralPubMed Pierson CR, Folkerth RD, Billiards SS, Trachtenberg FL, Drinkwater ME, Volpe JJ, Kinney HC: Gray matter injury associated with periventricular leukomalacia in the premature infant. Acta Neuropathol 2007,114(6):619–631. 10.1007/s00401-007-0295-5PubMedCentralPubMed
21.
go back to reference Allin M, Matsumoto H, Santhouse AM, Nosarti C, AlAsady MH, Stewart AL, Rifkin L, Murray RM: Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain 2001,124(Pt 1):60–66.PubMed Allin M, Matsumoto H, Santhouse AM, Nosarti C, AlAsady MH, Stewart AL, Rifkin L, Murray RM: Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain 2001,124(Pt 1):60–66.PubMed
22.
go back to reference Gottwald B, Wilde B, Mihajlovic Z, Mehdorn HM: Evidence for distinct cognitive deficits after focal cerebellar lesions. J Neurol Neurosurg Psychiatry 2004,75(11):1524–1531. 10.1136/jnnp.2003.018093PubMedCentralPubMed Gottwald B, Wilde B, Mihajlovic Z, Mehdorn HM: Evidence for distinct cognitive deficits after focal cerebellar lesions. J Neurol Neurosurg Psychiatry 2004,75(11):1524–1531. 10.1136/jnnp.2003.018093PubMedCentralPubMed
23.
go back to reference Levisohn L, Cronin-Golomb A, Schmahmann JD: Neuropsychological consequences of cerebellar tumour resection in children: cerebellar cognitive affective syndrome in a paediatric population. Brain 2000,123(Pt 5):1041–1050.PubMed Levisohn L, Cronin-Golomb A, Schmahmann JD: Neuropsychological consequences of cerebellar tumour resection in children: cerebellar cognitive affective syndrome in a paediatric population. Brain 2000,123(Pt 5):1041–1050.PubMed
24.
go back to reference Riva D, Giorgi C: The cerebellum contributes to higher functions during development: evidence from a series of children surgically treated for posterior fossa tumours. Brain 2000,123(Pt 5):1051–1061.PubMed Riva D, Giorgi C: The cerebellum contributes to higher functions during development: evidence from a series of children surgically treated for posterior fossa tumours. Brain 2000,123(Pt 5):1051–1061.PubMed
25.
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: Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics 2007,120(3):584–593. 10.1542/peds.2007-1041PubMed 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: Does cerebellar injury in premature infants contribute to the high prevalence of long-term cognitive, learning, and behavioral disability in survivors? Pediatrics 2007,120(3):584–593. 10.1542/peds.2007-1041PubMed
26.
go back to reference Auer RN Dunn JS, Sutherland GR: Hypoxia and related conditions. In Greenfield’s Neuropathology. Vol1. 8th edition. Edited by: Love S, Louis DN, Ellison D. London: Arnold; 2008:63–105. Auer RN Dunn JS, Sutherland GR: Hypoxia and related conditions. In Greenfield’s Neuropathology. Vol1. 8th edition. Edited by: Love S, Louis DN, Ellison D. London: Arnold; 2008:63–105.
27.
go back to reference Kinney HC, Haynes RL, Folkerth RD: White matter lesions in the perinatal period. In Developmental neuropathology. Edited by: Golden JA, Harding BN. Basel: ISN Neuropathology; 2004:156–170. Kinney HC, Haynes RL, Folkerth RD: White matter lesions in the perinatal period. In Developmental neuropathology. Edited by: Golden JA, Harding BN. Basel: ISN Neuropathology; 2004:156–170.
28.
go back to reference Aziz A, Ohlsson A: Surfactant for pulmonary hemorrhage in neonates. Cochrane Database Syst Rev 2008., 2: doi:10.1002/14651858 CD005254 Aziz A, Ohlsson A: Surfactant for pulmonary hemorrhage in neonates. Cochrane Database Syst Rev 2008., 2: doi:10.1002/14651858 CD005254
29.
go back to reference Papile LA, Burstein J, Burstein R, Koffler H: Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. J Pediatr 1978,92(4):529–534. 10.1016/S0022-3476(78)80282-0PubMed Papile LA, Burstein J, Burstein R, Koffler H: Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. J Pediatr 1978,92(4):529–534. 10.1016/S0022-3476(78)80282-0PubMed
30.
go back to reference Johnsen SD, Bodensteiner JB, Lotze TE: Frequency and nature of cerebellar injury in the extremely premature survivor with cerebral palsy. J Child Neurol 2005,20(1):60–64. 10.1177/08830738050200011001PubMed Johnsen SD, Bodensteiner JB, Lotze TE: Frequency and nature of cerebellar injury in the extremely premature survivor with cerebral palsy. J Child Neurol 2005,20(1):60–64. 10.1177/08830738050200011001PubMed
31.
go back to reference Messerschmidt A, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Birnbacher R, Prayer D: Disruption of cerebellar development: potential complication of extreme prematurity. AJNR Am J Neuroradiol 2005,26(7):1659–1667.PubMed Messerschmidt A, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Birnbacher R, Prayer D: Disruption of cerebellar development: potential complication of extreme prematurity. AJNR Am J Neuroradiol 2005,26(7):1659–1667.PubMed
32.
go back to reference Weir FJ, Ohlsson A, Myhr TL, Fong K, Ryan ML: A patent ductus arteriosus is associated with reduced middle cerebral artery blood flow velocity. Eur J Pediatr 1999,158(6):484–487. 10.1007/s004310051125PubMed Weir FJ, Ohlsson A, Myhr TL, Fong K, Ryan ML: A patent ductus arteriosus is associated with reduced middle cerebral artery blood flow velocity. Eur J Pediatr 1999,158(6):484–487. 10.1007/s004310051125PubMed
33.
go back to reference Argyropoulou MI, Xydis V, Drougia A, Argyropoulou PI, Tzoufi M, Bassounas A, Andronikou S, Efremidis SC: MRI measurements of the pons and cerebellum in children born preterm; associations with the severity of periventricular leukomalacia and perinatal risk factors. Neuroradiology 2003,45(10):730–734. 10.1007/s00234-003-1067-0PubMed Argyropoulou MI, Xydis V, Drougia A, Argyropoulou PI, Tzoufi M, Bassounas A, Andronikou S, Efremidis SC: MRI measurements of the pons and cerebellum in children born preterm; associations with the severity of periventricular leukomalacia and perinatal risk factors. Neuroradiology 2003,45(10):730–734. 10.1007/s00234-003-1067-0PubMed
34.
go back to reference Bassan H: Intracranial hemorrhage in the preterm infant: understanding it, preventing it. Clin Perinatol 2009,36(4):737–762. 10.1016/j.clp.2009.07.014PubMed Bassan H: Intracranial hemorrhage in the preterm infant: understanding it, preventing it. Clin Perinatol 2009,36(4):737–762. 10.1016/j.clp.2009.07.014PubMed
35.
go back to reference Clyman RI, Chorne N: Patent ductus arteriosus: evidence for and against treatment. J Pediatr 2007,150(3):216–219. 10.1016/j.jpeds.2006.12.048PubMedCentralPubMed Clyman RI, Chorne N: Patent ductus arteriosus: evidence for and against treatment. J Pediatr 2007,150(3):216–219. 10.1016/j.jpeds.2006.12.048PubMedCentralPubMed
36.
go back to reference Donat JF, Okazaki H, Kleinberg F: Cerebellar hemorrhages in newborn infants. Amer J Dis Child 1979,133(4):441.PubMed Donat JF, Okazaki H, Kleinberg F: Cerebellar hemorrhages in newborn infants. Amer J Dis Child 1979,133(4):441.PubMed
37.
go back to reference Duvernoy H, Delon S, Vannson JL: The vascularization of the human cerebellar cortex. Brain Res Bull 1983,11(4):419–480. 10.1016/0361-9230(83)90116-8PubMed Duvernoy H, Delon S, Vannson JL: The vascularization of the human cerebellar cortex. Brain Res Bull 1983,11(4):419–480. 10.1016/0361-9230(83)90116-8PubMed
38.
go back to reference Calkins H, Seifert M, Morady F: Clinical presentation and long-term follow-up of athletes with exercise-induced vasodepressor syncope. Am Heart J 1995,129(6):1159–1164. 10.1016/0002-8703(95)90398-4PubMed Calkins H, Seifert M, Morady F: Clinical presentation and long-term follow-up of athletes with exercise-induced vasodepressor syncope. Am Heart J 1995,129(6):1159–1164. 10.1016/0002-8703(95)90398-4PubMed
39.
go back to reference Gillilan LA: The arterial and venous blood supplies to the cerebellum of primates. J Neuropathol Exp Neurol 1969,28(2):295–297. 10.1097/00005072-196904000-00008PubMed Gillilan LA: The arterial and venous blood supplies to the cerebellum of primates. J Neuropathol Exp Neurol 1969,28(2):295–297. 10.1097/00005072-196904000-00008PubMed
40.
go back to reference Limperopoulos C, Soul JS, Gauvreau K, Huppi PS, Warfield SK, Bassan H, Robertson RL, Volpe JJ, du Plessis AJ: Late gestation cerebellar growth is rapid and impeded by premature birth. Pediatrics 2005,115(3):688–695. 10.1542/peds.2004-1169PubMed Limperopoulos C, Soul JS, Gauvreau K, Huppi PS, Warfield SK, Bassan H, Robertson RL, Volpe JJ, du Plessis AJ: Late gestation cerebellar growth is rapid and impeded by premature birth. Pediatrics 2005,115(3):688–695. 10.1542/peds.2004-1169PubMed
41.
go back to reference Chang CH, Chang FM, Yu CH, Ko HC, Chen HY: Assessment of fetal cerebellar volume using three-dimensional ultrasound. Ultrasound Med Biol 2000,26(6):981–988. 10.1016/S0301-5629(00)00225-8PubMed Chang CH, Chang FM, Yu CH, Ko HC, Chen HY: Assessment of fetal cerebellar volume using three-dimensional ultrasound. Ultrasound Med Biol 2000,26(6):981–988. 10.1016/S0301-5629(00)00225-8PubMed
42.
go back to reference Inder T, Mocatta T, Darlow B, Spencer C, Volpe JJ, Winterbourn C: Elevated free radical products in the cerebrospinal fluid of VLBW infants with cerebral white matter injury. Pediatr Res 2002,52(2):213–218. 10.1203/00006450-200208000-00013PubMed Inder T, Mocatta T, Darlow B, Spencer C, Volpe JJ, Winterbourn C: Elevated free radical products in the cerebrospinal fluid of VLBW infants with cerebral white matter injury. Pediatr Res 2002,52(2):213–218. 10.1203/00006450-200208000-00013PubMed
43.
go back to reference Juliet PA, Mao X, Del Bigio MR: Proinflammatory cytokine production by cultured neonatal rat microglia after exposure to blood products. Brain Res 2008, 1210: 230–239.PubMed Juliet PA, Mao X, Del Bigio MR: Proinflammatory cytokine production by cultured neonatal rat microglia after exposure to blood products. Brain Res 2008, 1210: 230–239.PubMed
44.
go back to reference Messerschmidt A, Prayer D, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Pollak A, Weber M, Birnbacher R: Preterm birth and disruptive cerebellar development: assessment of perinatal risk factors. Eur J Paediatr Neurol 2008,12(6):455–460. 10.1016/j.ejpn.2007.11.003PubMed Messerschmidt A, Prayer D, Brugger PC, Boltshauser E, Zoder G, Sterniste W, Pollak A, Weber M, Birnbacher R: Preterm birth and disruptive cerebellar development: assessment of perinatal risk factors. Eur J Paediatr Neurol 2008,12(6):455–460. 10.1016/j.ejpn.2007.11.003PubMed
45.
go back to reference Savman K, Nilsson UA, Blennow M, Kjellmer I, Whitelaw A: Non-protein-bound iron is elevated in cerebrospinal fluid from preterm infants with posthemorrhagic ventricular dilatation. Pediatr Res 2001,49(2):208–212. 10.1203/00006450-200102000-00013PubMed Savman K, Nilsson UA, Blennow M, Kjellmer I, Whitelaw A: Non-protein-bound iron is elevated in cerebrospinal fluid from preterm infants with posthemorrhagic ventricular dilatation. Pediatr Res 2001,49(2):208–212. 10.1203/00006450-200102000-00013PubMed
46.
go back to reference Yakubu MA, Leffler CW: 5-Hydroxytryptamine-induced vasoconstriction after cerebral hematoma in piglets. Pediatr Res 1997,41(3):317–320. 10.1203/00006450-199703000-00002PubMed Yakubu MA, Leffler CW: 5-Hydroxytryptamine-induced vasoconstriction after cerebral hematoma in piglets. Pediatr Res 1997,41(3):317–320. 10.1203/00006450-199703000-00002PubMed
47.
go back to reference Inage YW, Itoh M, Wada K, Hoshika A, Takashima S: Glutamate transporters in neonatal cerebellar subarachnoid hemorrhage. Pediatr Neurol 2000,23(1):42–48. 10.1016/S0887-8994(00)00142-9PubMed Inage YW, Itoh M, Wada K, Hoshika A, Takashima S: Glutamate transporters in neonatal cerebellar subarachnoid hemorrhage. Pediatr Neurol 2000,23(1):42–48. 10.1016/S0887-8994(00)00142-9PubMed
48.
go back to reference Pehlemann FW, Sievers J, Berry M: Meningeal cells are involved in foliation, lamination, and neurogenesis of the cerebellum: evidence from 6-hydroxydopamine-induced destruction of meningeal cells. Dev Biol 1985,110(1):136–146. 10.1016/0012-1606(85)90071-5PubMed Pehlemann FW, Sievers J, Berry M: Meningeal cells are involved in foliation, lamination, and neurogenesis of the cerebellum: evidence from 6-hydroxydopamine-induced destruction of meningeal cells. Dev Biol 1985,110(1):136–146. 10.1016/0012-1606(85)90071-5PubMed
49.
go back to reference Sievers J, von Knebel DC, Pehlemann FW, Berry M: Meningeal cells influence cerebellar development over a critical period. Anat Embryol (Berl) 1986,175(1):91–100. 10.1007/BF00315459 Sievers J, von Knebel DC, Pehlemann FW, Berry M: Meningeal cells influence cerebellar development over a critical period. Anat Embryol (Berl) 1986,175(1):91–100. 10.1007/BF00315459
50.
go back to reference von Knebel DC, Sievers J, Sadler M, Pehlemann FW, Berry M, Halliwell P: Destruction of meningeal cells over the newborn hamster cerebellum with 6-hydroxydopamine prevents foliation and lamination in the rostral cerebellum. Neuroscience 1986,17(2):409–426. 10.1016/0306-4522(86)90256-3 von Knebel DC, Sievers J, Sadler M, Pehlemann FW, Berry M, Halliwell P: Destruction of meningeal cells over the newborn hamster cerebellum with 6-hydroxydopamine prevents foliation and lamination in the rostral cerebellum. Neuroscience 1986,17(2):409–426. 10.1016/0306-4522(86)90256-3
51.
go back to reference Hayaran A, Bijlani V: Polyacrylamide as an infiltrating and embedding medium for vibratome sectioning of human fetal cerebellum containing DiI-filled axons. J Neurosci Methods 1992,42(1–2):65–68.PubMed Hayaran A, Bijlani V: Polyacrylamide as an infiltrating and embedding medium for vibratome sectioning of human fetal cerebellum containing DiI-filled axons. J Neurosci Methods 1992,42(1–2):65–68.PubMed
52.
go back to reference Marin-Padilla M: Neurogenesis of the climbing fibers in the human cerebellum: a Golgi study. J Comp Neurol 1985,235(1):82–96. 10.1002/cne.902350107PubMed Marin-Padilla M: Neurogenesis of the climbing fibers in the human cerebellum: a Golgi study. J Comp Neurol 1985,235(1):82–96. 10.1002/cne.902350107PubMed
53.
go back to reference Mihajlovic P, Zecevic N: Development of the human dentate nucleus. Hum Neurobiol 1986,5(3):189–197.PubMed Mihajlovic P, Zecevic N: Development of the human dentate nucleus. Hum Neurobiol 1986,5(3):189–197.PubMed
54.
go back to reference Yamaguchi K, Goto N, Yamamoto TY: Development of human cerebellar nuclei. Morphometric study. Acta Anat 1989,136(1):61–68. 10.1159/000146799PubMed Yamaguchi K, Goto N, Yamamoto TY: Development of human cerebellar nuclei. Morphometric study. Acta Anat 1989,136(1):61–68. 10.1159/000146799PubMed
55.
go back to reference Zecevic N, Rakic P: Differentiation of Purkinje cells and their relationship to other components of developing cerebellar cortex in man. J Comp Neurol 1976,167(1):27–47. 10.1002/cne.901670103PubMed Zecevic N, Rakic P: Differentiation of Purkinje cells and their relationship to other components of developing cerebellar cortex in man. J Comp Neurol 1976,167(1):27–47. 10.1002/cne.901670103PubMed
56.
go back to reference Peterson BS, Vohr B, Staib LH, Cannistraci CJ, Dolberg A, Schneider KC, Katz KH, Westerveld M, Sparrow S, Anderson AW, Duncan CC, Makuch RW, Gore JC, Ment LR: Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 2000,284(15):1939–1947. 10.1001/jama.284.15.1939PubMed Peterson BS, Vohr B, Staib LH, Cannistraci CJ, Dolberg A, Schneider KC, Katz KH, Westerveld M, Sparrow S, Anderson AW, Duncan CC, Makuch RW, Gore JC, Ment LR: Regional brain volume abnormalities and long-term cognitive outcome in preterm infants. JAMA 2000,284(15):1939–1947. 10.1001/jama.284.15.1939PubMed
57.
go back to reference Srinivasan L, Allsop J, Counsell SJ, Boardman JP, Edwards AD, Rutherford M: Smaller cerebellar volumes in very preterm infants at term-equivalent age are associated with the presence of supratentorial lesions. AJNR Am J Neuroradiol 2006,27(3):573–579.PubMed Srinivasan L, Allsop J, Counsell SJ, Boardman JP, Edwards AD, Rutherford M: Smaller cerebellar volumes in very preterm infants at term-equivalent age are associated with the presence of supratentorial lesions. AJNR Am J Neuroradiol 2006,27(3):573–579.PubMed
58.
go back to reference Tam EW, Rosenbluth G, Rogers EE, Ferriero DM, Glidden D, Goldstein RB, Glass HC, Piecuch RE, Barkovich AJ: Cerebellar hemorrhage on magnetic resonance imaging in preterm newborns associated with abnormal neurologic outcome. J Pediatr 2011,158(2):245–250. 10.1016/j.jpeds.2010.07.049PubMedCentralPubMed Tam EW, Rosenbluth G, Rogers EE, Ferriero DM, Glidden D, Goldstein RB, Glass HC, Piecuch RE, Barkovich AJ: Cerebellar hemorrhage on magnetic resonance imaging in preterm newborns associated with abnormal neurologic outcome. J Pediatr 2011,158(2):245–250. 10.1016/j.jpeds.2010.07.049PubMedCentralPubMed
59.
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: Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics 2005,116(4):844–850. 10.1542/peds.2004-2282PubMed Limperopoulos C, Soul JS, Haidar H, Huppi PS, Bassan H, Warfield SK, Robertson RL, Moore M, Akins P, Volpe JJ, du Plessis AJ: Impaired trophic interactions between the cerebellum and the cerebrum among preterm infants. Pediatrics 2005,116(4):844–850. 10.1542/peds.2004-2282PubMed
Metadata
Title
Cerebellar hemorrhagic injury in premature infants occurs during a vulnerable developmental period and is associated with wider neuropathology
Authors
Krista M Haines
Wei Wang
Christopher R Pierson
Publication date
01-12-2013
Publisher
BioMed Central
Published in
Acta Neuropathologica Communications / Issue 1/2013
Electronic ISSN: 2051-5960
DOI
https://doi.org/10.1186/2051-5960-1-69

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