Disruptions / Hypoxic-Ischemic Injury

Mirna Lechpammer; Marc Del Bigio; Rebecca Folkerth

Section 4 - Disruptions / Hypoxic-Ischemic Injury

Published online by Cambridge University Press: 07 August 2021

Mirna Lechpammer ,

Marc Del Bigio and

Rebecca Folkerth

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Mirna Lechpammer: Affiliation:
New York University School of Medicine
Marc Del Bigio: Affiliation:
University of Manitoba, Canada
Rebecca Folkerth: Affiliation:
New York University School of Medicine

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Type: Chapter
Information: Perinatal Neuropathology , pp. 145 - 210

DOI: https://doi.org/10.1017/9781316671863 [Opens in a new window]

Publisher: Cambridge University Press

Print publication year: 2021

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References

Lockshin, RA, Williams, CM. Programmed cell death–I. Cytology of degeneration in the intersegmental muscles of the pernyi silkmoth. J Insect Physiol. 1965;11:123–33.Google Scholar PubMed

Kerr, JF, Wyllie, AH, Currie, AR. Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer. 1972;26(4):239–57.CrossRef Google Scholar PubMed

Schweichel, JU, Merker, HJ. The morphology of various types of cell death in prenatal tissues. Teratology. 1973;7(3):253–66.CrossRef Google Scholar PubMed

Tsujimoto, Y. Multiple ways to die: non-apoptotic forms of cell death. Acta Oncol. 2012;51(3):293–300.Google Scholar

Denaxa, M, Neves, G, Rabinowitz, A, Kemlo, S, Liodis, P, Burrone, J, et al. Modulation of apoptosis controls inhibitory interneuron number in the cortex. Cell Rep. 2018;22(7):1710–21.CrossRef Google Scholar PubMed

Orrenius, S, McConkey, DJ, Jones, DP, Nicotera, P. Ca2+-activated mechanisms in toxicity and programmed cell death. ISI Atlas Sci: Pharmacol. 1988;2(4):319–24.Google Scholar

Burke, RE, Kholodilov, NG. Programmed cell death: does it play a role in Parkinson’s disease? Ann Neurol. 1998;44(3 Suppl 1):S126–33.CrossRef Google Scholar PubMed

Zhang, L, Kokkonen, G, Roth, GS. Identification of neuronal programmed cell death in situ in the striatum of normal adult rat brain and its relationship to neuronal death during aging. Brain Res. 1995;677(1):177–9.CrossRef Google Scholar PubMed

Bursch, W, Kleine, L, Tenniswood, M. The biochemistry of cell death by apoptosis. Biochem Cell Biol. 1990;68(9):1071–4.Google Scholar

Goya, RG. Role of programmed cell death in the aging process: an unexplored possibility. Gerontology. 1986;32(1):37–42.Google Scholar

Krantic, S, Mechawar, N, Reix, S, Quirion, R. Molecular basis of programmed cell death involved in neurodegeneration. Trends Neurosci. 2005;28(12):670–6.Google Scholar

Galluzzi, L, Vitale, I, Aaronson, SA, Abrams, JM, Adam, D, Agostinis, P, et al. Molecular mechanisms of cell death: recommendations of the Nomenclature Committee on Cell Death 2018. Cell Death Differ. 2018;25(3):486–541.Google Scholar

Napoletano, F, Baron, O, Vandenabeele, P, Mollereau, B, Fanto, M. Intersections between regulated cell death and autophagy. Trends Cell Biol. 2019;29(4):323–38.Google Scholar

Virchow, R. Die Cellularpathologie in ihrer Begründung auf physiologische und pathologische Gewebelehre. 1st ed. Berlin: August Hirschwald; 1858.Google Scholar

King, LS. Studies on eastern equine encephalomyelitis. I. Histopathology of the nervous system in the guinea pig. J Exp Med. 1938;68(5):677–92.Google Scholar

Weller, SD, Norman, RM. Epilepsy due to birth injury in one of identical twins. Arch Dis Child. 1955;30(153):453–6.Google Scholar

Meriwether, LS, Hager, H, Scholz, W. Kernicterus; hypoxemia, significant pathogenic factor. AMA Arch Neurol Psychiatry. 1955;73(3):293–301.CrossRef Google Scholar PubMed

Levine, S. Anoxic-ischemic encephalopathy in rats. Am J Pathol. 1960;36:1–17.Google Scholar PubMed

Claireaux, A. Haemolytic disease of the newborn: Part I. A clinical-pathological study of 157 cases. Arch Dis Child. 1950;25(121):61–80.CrossRef Google Scholar

Lossi, L, Castagna, C, Merighi, A. Neuronal cell death: an overview of its different forms in central and peripheral neurons. Methods Mol Biol. 2015;1254:1–18.Google Scholar

Fricker, M, Tolkovsky, AM, Borutaite, V, Coleman, M, Brown, GC. Neuronal cell death. Physiol Rev. 2018;98(2):813–80.CrossRef Google Scholar PubMed

Unal-Cevik, I, Kilinc, M, Can, A, Gursoy-Ozdemir, Y, Dalkara, T. Apoptotic and necrotic death mechanisms are concomitantly activated in the same cell after cerebral ischemia. Stroke. 2004;35(9):2189–94.Google Scholar

Elmore, SA, Dixon, D, Hailey, JR, Harada, T, Herbert, RA, Maronpot, RR, et al. Recommendations from the INHAND Apoptosis/Necrosis Working Group. Toxicol Pathol. 2016;44(2):173–88.CrossRef Google Scholar PubMed

Kroemer, G, Galluzzi, L, Vandenabeele, P, Abrams, J, Alnemri, ES, Baehrecke, EH, et al. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ. 2009;16(1):3–11.CrossRef Google Scholar

Galluzzi, L, Bravo-San Pedro, JM, Vitale, I, Aaronson, SA, Abrams, JM, Adam, D, et al. Essential versus accessory aspects of cell death: recommendations of the NCCD 2015. Cell Death Differ. 2015;22(1):58–73.Google Scholar

Galluzzi, L, Vitale, I, Abrams, JM, Alnemri, ES, Baehrecke, EH, Blagosklonny, MV, et al. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ. 2012;19(1):107–20.CrossRef Google Scholar PubMed

Martin, LJ, Chang, Q. DNA damage response and repair, DNA methylation, and cell death in human neurons and experimental animal neurons are different. J Neuropathol Exp Neurol. 2018;77(7):636–55.CrossRef Google Scholar PubMed

Tagaya, M, Liu, KF, Copeland, B, Seiffert, D, Engler, R, Garcia, JH, et al. DNA scission after focal brain ischemia. Temporal differences in two species. Stroke. 1997;28(6):1245–54.CrossRef Google Scholar PubMed

Elmore, S. Apoptosis: a review of programmed cell death. Toxicol Pathol. 2007;35(4):495–516.CrossRef Google Scholar PubMed

Mnatsakanyan, N, Beutner, G, Porter, GA, Alavian, KN, Jonas, EA. Physiological roles of the mitochondrial permeability transition pore. J Bioenerg Biomembr. 2017;49(1):13–25.Google Scholar

Lossi, L, Castagna, C, Merighi, A. Caspase-3 mediated cell death in the normal development of the mammalian cerebellum. Int J Mol Sci. 2018;19(12):ii:E3999.Google Scholar

Srinivasan, A, Roth, KA, Sayers, RO, Shindler, KS, Wong, AM, Fritz, LC, et al. In situ immunodetection of activated caspase-3 in apoptotic neurons in the developing nervous system. Cell Death Differ. 1998;5(12):1004–16.Google Scholar

Love, S, Barber, R, Srinivasan, A, Wilcock, GK. Activation of caspase-3 in permanent and transient brain ischaemia in man. Neuroreport. 2000;11(11):2495–9.Google Scholar

Stadelman, C, Mews, I, Srinivasan, A, Deckwerth, TL, Lassmann, H, Bruck, W. Expression of cell death-associated proteins in neuronal apoptosis associated with pontosubicular neuron necrosis. Brain Pathol. 2001;11(3):273–81.Google Scholar

Machaalani, R, Radford, JL, Waters, KA. Tissue fixation effects on immunohistochemical staining of caspase-3 in brain tissue. Appl Immunohistochem Mol Morphol. 2007;15(4):463–70.Google Scholar

Rossiter, JP, Anderson, LL, Yang, F, Cole, GM. Caspase-3 activation and caspase-like proteolytic activity in human perinatal hypoxic-ischemic brain injury. Acta Neuropathol. 2002;103(1):66–73.CrossRef Google Scholar PubMed

Schafer, MK, Pfeiffer, A, Jaeckel, M, Pouya, A, Dolga, AM, Methner, A. Regulators of mitochondrial Ca(2+) homeostasis in cerebral ischemia. Cell Tissue Res. 2014;357(2):395–405.CrossRef Google Scholar PubMed

Nagley, P, Higgins, GC, Atkin, JD, Beart, PM. Multifaceted deaths orchestrated by mitochondria in neurones. Biochim Biophys Acta. 2010;1802(1):167–85.Google Scholar

Samejima, K, Earnshaw, WC. Trashing the genome: the role of nucleases during apoptosis. Nat Rev Mol Cell Biol. 2005;6(9):677–88.Google Scholar

Larsen, BD, Sorensen, CS. The caspase-activated DNase: apoptosis and beyond. FEBS J. 2017;284(8):1160–70.Google Scholar

Ruchaud, S, Korfali, N, Villa, P, Kottke, TJ, Dingwall, C, Kaufmann, SH, et al. Caspase-6 gene disruption reveals a requirement for lamin A cleavage in apoptotic chromatin condensation. EMBO J. 2002;21(8):1967–77.Google Scholar

Miller, JA, Ding, SL, Sunkin, SM, Smith, KA, Ng, L, Szafer, A, et al. Transcriptional landscape of the prenatal human brain. Nature. 2014;508(7495):199–206.Google Scholar

Hyman, BT, Yuan, J. Apoptotic and non-apoptotic roles of caspases in neuronal physiology and pathophysiology. Nat Rev Neurosci. 2012;13(6):395–406.CrossRef Google Scholar PubMed

Hooker, DJ, Mobarok, M, Anderson, JL, Rajasuriar, R, Gray, LR, Ellett, AM, et al. A new way of measuring apoptosis by absolute quantitation of inter-nucleosomally fragmented genomic DNA. Nucleic Acids Res. 2012;40(15):e113.Google Scholar

Lesauskaite, V, Epistolato, MC, Ivanoviene, L, Tanganelli, P. Apoptosis of cardiomyocytes in explanted and transplanted hearts. Comparison of results from in situ TUNEL, ISEL, and ISOL reactions. Am J Clin Pathol. 2004;121(1):108–16.Google Scholar

Charriaut-Marlangue, C, Ben-Ari, Y. A cautionary note on the use of the TUNEL stain to determine apoptosis. Neuroreport. 1995;7(1):61–4.Google Scholar

Burke, C, Gobe, G. Pontosubicular apoptosis (“necrosis”) in human neonates with intrauterine growth retardation and placental infarction. Virchows Arch. 2005;446(6):640–5.Google Scholar

Zille, M, Farr, TD, Przesdzing, I, Muller, J, Sommer, C, Dirnagl, U, et al. Visualizing cell death in experimental focal cerebral ischemia: promises, problems, and perspectives. J Cereb Blood Flow Metab. 2012;32(2):213–31.Google Scholar

Didenko, VV, Ngo, H, Minchew, CL, Boudreaux, DJ, Widmayer, MA, Baskin, DS. Visualization of irreparable ischemic damage in brain by selective labeling of double strand blunt-ended DNA breaks. Mol Med. 2002;8(12):818–23.Google Scholar

Hornsby, PJ, Didenko, VV. In situ ligation: a decade and a half of experience. Methods Mol Biol. 2011;682:49–63.Google Scholar

Nakajima, YI, Kuranaga, E. Caspase-dependent non-apoptotic processes in development. Cell Death Differ. 2017;24(8):1422–30.CrossRef Google Scholar PubMed

Kumar, A, Rothman, JH. Cell death: hook, line and linker. Curr Biol. 2007;17(8):R286-9.CrossRef Google Scholar PubMed

Kutscher, LM, Shaham, S. Non-apoptotic cell death in animal development. Cell Death Differ. 2017;24(8):1326–36.Google Scholar

Gudipaty, SA, Conner, CM, Rosenblatt, J, Montell, DJ. Unconventional ways to live and die: cell death and survival in development, homeostasis, and disease. Annu Rev Cell Dev Biol. 2018;34:311–32.Google Scholar

Loh, KY, Wang, Z, Liao, P. Oncotic cell death in stroke. Rev Physiol Biochem Pharmacol. 2019;176:37–64.CrossRef Google Scholar PubMed

Yagami, T, Yamamoto, Y, Koma, H. Pathophysiological roles of intracellular proteases in neuronal development and neurological diseases. Mol Neurobiol. 2019;56(5):3090–112.Google Scholar

Czogalla, A, Sikorski, AF. Spectrin and calpain: a ‘target’ and a ‘sniper’ in the pathology of neuronal cells. Cell Mol Life Sci. 2005;62(17):1913–24.CrossRef Google Scholar

Vanderklish, PW, Bahr, BA. The pathogenic activation of calpain: a marker and mediator of cellular toxicity and disease states. Int J Exp Pathol. 2000;81(5):323–39.Google Scholar

McCracken, E, Hunter, AJ, Patel, S, Graham, DI, Dewar, D. Calpain activation and cytoskeletal protein breakdown in the corpus callosum of head-injured patients. J Neurotrauma. 1999;16(9):749–61.Google Scholar

Fujikawa, DG. The role of excitotoxic programmed necrosis in acute brain injury. Comput Struct Biotechnol J. 2015;13:212–21.Google Scholar

Varela-Ramirez, A, Abendroth, J, Mejia, AA, Phan, IQ, Lorimer, DD, Edwards, TE, et al. Structure of acid deoxyribonuclease. Nucleic Acids Res. 2017;45(10):6217–27.CrossRef Google Scholar PubMed

Minchew, CL, Didenko, VV. Dual detection of nucleolytic and proteolytic markers of lysosomal cell death: DNase ii-type breaks and cathepsin d. Methods Mol Biol. 2017;1554:229–36.CrossRef Google Scholar PubMed

Uhlen, M, Fagerberg, L, Hallstrom, BM, Lindskog, C, Oksvold, P, Mardinoglu, A, et al. Proteomics. Tissue-based map of the human proteome. Science. 2015;347(6220):1260419.Google Scholar

Grassi Zucconi, G, Cosi, C, Palmieri, M, Furia, A, Bassetti, MA, Carsana, A. A pancreatic-like ribonuclease is synthesized in rat brain. Brain Res Mol Brain Res. 1992;14(1–2):1–6.Google Scholar

Morita, T, Sanda, A, Takizawa, Y, Ohgi, K, Irie, M. Distribution of a kidney acid-ribonuclease-like enzyme and the other ribonucleases in bovine organs and body fluids. Agric Biol Chem. 1987;51(10):2751–61.Google Scholar

Albrecht, J, Yanagihara, T. Effect of anoxia and ischemia on ribonuclease activity in brain. J Neurochem. 1979;32(3):1131–3.Google Scholar

Thornton, C, Hagberg, H. Role of mitochondria in apoptotic and necroptotic cell death in the developing brain. Clin Chim Acta. 2015;451(PartA):35–8.CrossRef Google Scholar PubMed

Grootjans, S, Vanden Berghe, T, Vandenabeele, P. Initiation and execution mechanisms of necroptosis: an overview. Cell Death Differ. 2017;24(7):1184–95.Google Scholar

Hribljan, V, Lisjak, D, Petrovic, DJ, Mitrecic, D. Necroptosis is one of the modalities of cell death accompanying ischemic brain stroke: from pathogenesis to therapeutic possibilities. Croat Med J. 2019;60(2):121–6.Google Scholar

Liu, T, Bao, YH, Wang, Y, Jiang, JY. The role of necroptosis in neurosurgical diseases. Braz J Med Biol Res. 2015;48(4):292–8.CrossRef Google Scholar PubMed

Dunai, Z, Bauer, PI, Mihalik, R. Necroptosis: biochemical, physiological and pathological aspects. Pathol Oncol Res. 2011;17(4):791–800.Google Scholar

Jouan-Lanhouet, S, Riquet, F, Duprez, L, Vanden Berghe, T, Takahashi, N, Vandenabeele, P. Necroptosis, in vivo detection in experimental disease models. Semin Cell Dev Biol. 2014;35:2–13.CrossRef Google Scholar PubMed

Degterev, A, Zhou, W, Maki, JL, Yuan, J. Assays for necroptosis and activity of RIP kinases. Methods Enzymol. 2014;545:1–33.Google Scholar

Ofengeim, D, Ito, Y, Najafov, A, Zhang, Y, Shan, B, DeWitt, JP, et al. Activation of necroptosis in multiple sclerosis. Cell Rep. 2015;10(11):1836–49.CrossRef Google Scholar PubMed

Fan, H, Tang, HB, Kang, J, Shan, L, Song, H, Zhu, K, et al. Involvement of endoplasmic reticulum stress in the necroptosis of microglia/macrophages after spinal cord injury. Neuroscience. 2015;311:362–73.Google Scholar

Wang, Y, An, R, Umanah, GK, Park, H, Nambiar, K, Eacker, SM, et al. A nuclease that mediates cell death induced by DNA damage and poly(ADP-ribose) polymerase-1. Science. 2016;354(6308):pii:aad6872.CrossRef Google Scholar PubMed

Sairanen, T, Szepesi, R, Karjalainen-Lindsberg, ML, Saksi, J, Paetau, A, Lindsberg, PJ. Neuronal caspase-3 and PARP-1 correlate differentially with apoptosis and necrosis in ischemic human stroke. Acta Neuropathol. 2009;118(4):541–52.CrossRef Google Scholar PubMed

Stockwell, BR, Friedmann Angeli, JP, Bayir, H, Bush, AI, Conrad, M, Dixon, SJ, et al. Ferroptosis: a regulated cell death nexus linking metabolism, redox biology, and disease. Cell. 2017;171(2):273–85.Google Scholar

Li, Q, Weiland, A, Chen, X, Lan, X, Han, X, Durham, F, et al. Ultrastructural characteristics of neuronal death and white matter injury in mouse brain tissues after intracerebral hemorrhage: coexistence of ferroptosis, autophagy, and necrosis. Front Neurol. 2018;9:581.CrossRef Google Scholar PubMed

Wenzel, SE, Tyurina, YY, Zhao, J, St Croix, CM, Dar, HH, Mao, G, et al. PEBP1 wardens ferroptosis by enabling lipoxygenase generation of lipid death signals. Cell. 2017;171(3):628–41.CrossRef Google Scholar PubMed

Cui, D, Sun, D, Wang, X, Yi, L, Kulikowicz, E, Reyes, M, et al. Impaired autophagosome clearance contributes to neuronal death in a piglet model of neonatal hypoxic-ischemic encephalopathy. Cell Death Dis. 2017;8(7):e2919.Google Scholar

Galluzzi, L, Pedro, JM, Blomgren, K, Kroemer, G. Autophagy in acute brain injury. Nat Rev Neurosci. 2016;17(8):467–84.Google Scholar

Descloux, C, Ginet, V, Clarke, PG, Puyal, J, Truttmann, AC. Neuronal death after perinatal cerebral hypoxia-ischemia: Focus on autophagy-mediated cell death. Int J Dev Neurosci. 2015;45:75–85.CrossRef Google Scholar PubMed

Button, RW, Luo, S, Rubinsztein, DC. Autophagic activity in neuronal cell death. Neurosci Bull. 2015;31(4):382–94.Google Scholar

Uchiyama, Y, Koike, M, Shibata, M, Sasaki, M. Autophagic neuron death. Methods Enzymol. 2009;453:33–51.Google Scholar

Tang, D, Kang, R, Berghe, TV, Vandenabeele, P, Kroemer, G. The molecular machinery of regulated cell death. Cell Res. 2019;29(5):347–64.Google Scholar

Weilinger, NL, Maslieieva, V, Bialecki, J, Sridharan, SS, Tang, PL, Thompson, RJ. Ionotropic receptors and ion channels in ischemic neuronal death and dysfunction. Acta Pharmacol Sin. 2013;34(1):39–48.Google Scholar

Serwach, K, Gruszczynska-Biegala, J. STIM proteins and glutamate receptors in neurons: role in neuronal physiology and neurodegenerative diseases. Int J Mol Sci. 2019;20(9):E2289.Google Scholar

Back, SA, Rosenberg, PA. Pathophysiology of glia in perinatal white matter injury. Glia. 2014;62(11):1790–815.CrossRef Google Scholar PubMed

Back, SA. White matter injury in the preterm infant: pathology and mechanisms. Acta Neuropathol. 2017;134(3):331–49.CrossRef Google Scholar PubMed

Fujikawa, DG. Activation of caspase-independent programmed pathways in seizure-induced neuronal necrosis. In: Fujikawa, DG, editor. Acute Neuronal Injury. New York: Springer; 2018. pp. 191–211.CrossRef Google Scholar

Olney, JW, Rhee, V, Ho, OL. Kainic acid: a powerful neurotoxic analogue of glutamate. Brain Res. 1974;77(3):507–12.Google Scholar

Olney, JW. Glutamate-induced neuronal necrosis in the infant mouse hypothalamus. An electron microscopic study. J Neuropathol Exp Neurol. 1971;30(1):75–90.Google Scholar

Bano, D, Ankarcrona, M. Beyond the critical point: An overview of excitotoxicity, calcium overload and the downstream consequences. Neurosci Lett. 2018;663:79–85.Google Scholar

Curcio, M, Salazar, IL, Mele, M, Canzoniero, LM, Duarte, CB. Calpains and neuronal damage in the ischemic brain: The swiss knife in synaptic injury. Prog Neurobiol. 2016;143:1–35.Google Scholar

Bonfoco, E, Krainc, D, Ankarcrona, M, Nicotera, P, Lipton, SA. Apoptosis and necrosis: two distinct events induced, respectively, by mild and intense insults with N-methyl-D-aspartate or nitric oxide/superoxide in cortical cell cultures. Proc Natl Acad Sci U S A. 1995;92(16):7162–6.Google Scholar

Petito, CK, Pulsinelli, WA. Sequential development of reversible and irreversible neuronal damage following cerebral ischemia. J Neuropathol Exp Neurol. 1984;43(2):141–53.Google Scholar

Garcia, JH, Liu, KF, Ho, KL. Neuronal necrosis after middle cerebral artery occlusion in Wistar rats progresses at different time intervals in the caudoputamen and the cortex. Stroke. 1995;26:636–43.CrossRef Google Scholar PubMed

Pulsinelli, WA, Brierley, JB, Plum, F. Temporal profile of neuronal damage in a model of transient forebrain ischemia. Ann Neurol. 1982;11(5):491–8.CrossRef Google Scholar

Schmued, LC, Stowers, CC, Scallet, AC, Xu, L. Fluoro-Jade C results in ultra high resolution and contrast labeling of degenerating neurons. Brain Res. 2005;1035(1):24–31.CrossRef Google Scholar PubMed

Xu, X, Lai, Y, Hua, ZC. Apoptosis and apoptotic body: disease message and therapeutic target potentials. Biosci Rep. 2019;39(1):BSR20180992.Google Scholar

Shen, Y, Wang, Z, Li, F, Sun, L. Morphological characteristics of eosinophilic neuronal death after transient unilateral forebrain ischemia in Mongolian gerbils. Neuropathology. 2016;36(3):227–36.Google Scholar

Nitatori, T, Sato, N, Waguri, S, Karasawa, Y, Araki, H, Shibanai, K, et al. Delayed neuronal death in the CA1 pyramidal cell layer of the gerbil hippocampus following transient ischemia is apoptosis. J Neurosci. 1995;15(2):1001–11.CrossRef Google Scholar PubMed

Bartus, RT, Dean, RL, Mennerick, S, Eveleth, D, Lynch, G. Temporal ordering of pathogenic events following transient global ischemia. Brain Res. 1998;790(1–2):1–13.Google Scholar

Sun, L, Kuroiwa, T, Ishibashi, S, Katsumata, N, Endo, S, Mizusawa, H. Transition of areas of eosinophilic neurons and reactive astrocytes to delayed cortical infarcts after transient unilateral forebrain ischemia in Mongolian gerbils. Acta Neuropathol. 2006;111(1):21–8.Google Scholar

Garcia, JH, Liu, KF, Ye, ZR, Gutierrez, JA. Incomplete infarct and delayed neuronal death after transient middle cerebral artery occlusion in rats. Stroke. 1997;28(11):2303–9.Google Scholar

Colbourne, F, Li, H, Buchan, AM, Clemens, JA. Continuing postischemic neuronal death in CA1: influence of ischemia duration and cytoprotective doses of NBQX and SNX-111 in rats. Stroke. 1999;30(3):662–8.CrossRef Google Scholar PubMed

Friede, RL. Developmental Neuropathology. 2nd edition. Berlin: Springer Verlag; 1989.Google Scholar

Marin-Padilla, M. Developmental neuropathology and impact of perinatal brain damage. III: Gray matter lesions of the neocortex. J Neuropathol Exp Neurol. 1999;58(5):407–29.CrossRef Google Scholar PubMed

Mito, T, Becker, LE, Takashima, S. Neuropathology of central respiratory dysfunction in infancy. Pediatr Neurosurg. 1991;17(2):80–7.Google Scholar

DiMario, FJ, Jr., Clancy, R. Symmetrical thalamic degeneration with calcifications of infancy. Am J Dis Child. 1989;143(9):1056–60.Google Scholar

Rosales, RK, Riggs, HE. Symmetrical thalamic degeneration in infants. J Neuropathol Exp Neurol. 1962;21:372–6.Google Scholar

Parisi, JE, Collins, GH, Kim, RC, Crosley, CJ. Prenatal symmetrical thalamic degeneration with flexion spasticity at birth. Ann Neurol. 1983;13(1):94–7.Google Scholar

Leestma, JE, Martin, E. An electron probe and histochemical study of the “ferruginated” neuron. Arch Pathol. 1968;86(6):597–605.Google Scholar

Gayoso, MJ, Al-Majdalawi, A, Garrosa, M, Calvo, B, Diaz-Flores, L. Selective calcification of rat brain lesions caused by systemic administration of kainic acid. Histol Histopathol. 2003;18(3):855–69.Google Scholar

Oehmichen, M. Vitality and time course of wounds. Forensic Sci Int. 2004;144(2–3):221–31.Google Scholar

Portera-Cailliau, C, Price, DL, Martin, LJ. Excitotoxic neuronal death in the immature brain is an apoptosis-necrosis morphological continuum. J Comp Neurol. 1997;378(1):70–87.Google Scholar

Thornton, C, Leaw, B, Mallard, C, Nair, S, Jinnai, M, Hagberg, H. Cell death in the developing brain after hypoxia-ischemia. Front Cell Neurosci. 2017;11:248.Google Scholar

Kuan, CY, Roth, KA, Flavell, RA, Rakic, P. Mechanisms of programmed cell death in the developing brain. Trends Neurosci. 2000;23(7):291–7.Google Scholar

Krajewska, M, Mai, JK, Zapata, JM, Ashwell, KW, Schendel, SL, Reed, JC, et al. Dynamics of expression of apoptosis-regulatory proteins Bid, Bcl-2, Bcl-X, Bax and Bak during development of murine nervous system. Cell Death Differ. 2002;9(2):145–57.Google Scholar

Ludwig-Galezowska, AH, Flanagan, L, Rehm, M. Apoptosis repressor with caspase recruitment domain, a multifunctional modulator of cell death. J Cell Mol Med. 2011;15(5):1044–53.Google Scholar

Yuan, J, Amin, P, Ofengeim D. Necroptosis and RIPK1-mediated neuroinflammation in CNS diseases. Nat Rev Neurosci. 2019;20(1):19–33.Google Scholar

Hill, CS, Coleman, MP, Menon, DK. Traumatic axonal injury: mechanisms and translational opportunities. Trends Neurosci. 2016;39(5):311–24.Google Scholar

Cornejo, VH, Luarte, A, Couve, A. Global and local mechanisms sustain axonal proteostasis of transmembrane proteins. Traffic. 2017;18(5):255–66.Google Scholar

Iwata, A, Stys, PK, Wolf, JA, Chen, XH, Taylor, AG, Meaney, DF, et al. Traumatic axonal injury induces proteolytic cleavage of the voltage-gated sodium channels modulated by tetrodotoxin and protease inhibitors. J Neurosci. 2004;24(19):4605–13.Google Scholar

Simon, DJ, Weimer, RM, McLaughlin, T, Kallop, D, Stanger, K, Yang, J, et al. A caspase cascade regulating developmental axon degeneration. J Neurosci. 2012;32(49):17540–53.CrossRef Google Scholar PubMed

Arrazola, MS, Saquel, C, Catalan, RJ, Barrientos, SA, Hernandez, DE, Martinez, NW, et al. Axonal degeneration is mediated by necroptosis activation. J Neurosci. 2019;39(20):3832–44.Google Scholar

Arrazola, MS, Court, FA. Compartmentalized necroptosis activation in excitotoxicity-induced axonal degeneration: a novel mechanism implicated in neurodegenerative disease pathology. Neural Regen Res. 2019;14(8):1385–6.Google Scholar

Hernandez, DE, Salvadores, NA, Moya-Alvarado, G, Catalan, RJ, Bronfman, FC, Court, FA. Axonal degeneration induced by glutamate excitotoxicity is mediated by necroptosis. J Cell Sci. 2018;131(22):jcs214684.Google Scholar

Ding, C, Hammarlund, M. Mechanisms of injury-induced axon degeneration. Curr Opin Neurobiol. 2019;57:171–8.CrossRef Google Scholar PubMed

Sherriff, FE, Bridges, LR, Gentleman, SM, Sivaloganathan, S, Wilson, S. Markers of axonal injury in post mortem human brain. Acta Neuropathol. 1994;88(5):433–9.Google Scholar

Baiden Amissah, K, Joashi, U, Blumberg, R, Mehmet, H, Edwards, AD, Cox, PM. Expression of amyloid precursor protein (beta-APP) in the neonatal brain following hypoxic ischaemic injury. Neuropathol Appl Neurobiol. 1998;24(5):346–52.Google Scholar

Bell, JE, Becher, JC, Wyatt, B, Keeling, JW, McIntosh, N. Brain damage and axonal injury in a Scottish cohort of neonatal deaths. Brain. 2005;128(Pt. 5):1070–81.CrossRef Google Scholar

Johnson, VE, Stewart, W, Weber, MT, Cullen, DK, Siman, R, Smith, DH. SNTF immunostaining reveals previously undetected axonal pathology in traumatic brain injury. Acta Neuropathol. 2016;131(1):115–35.Google Scholar

Liu, CH, Rasband, MN. Axonal spectrins: nanoscale organization, functional domains and spectrinopathies. Front Cell Neurosci. 2019;13:234.CrossRef Google Scholar PubMed

Siman, R, Baudry, M, Lynch, G. Brain fodrin: substrate for calpain I, an endogenous calcium-activated protease. Proc Natl Acad Sci U S A. 1984;81(11):3572–6.CrossRef Google Scholar PubMed

Sokolowski, JD, Gamage, KK, Heffron, DS, Leblanc, AC, Deppmann, CD, Mandell, JW. Caspase-mediated cleavage of actin and tubulin is a common feature and sensitive marker of axonal degeneration in neural development and injury. Acta Neuropathol Commun. 2014;2:16.CrossRef Google Scholar PubMed

Maor-Nof, M, Yaron, A. Neurite pruning and neuronal cell death: spatial regulation of shared destruction programs. Curr Opin Neurobiol. 2013;23(6):990–6.Google Scholar

References

Sofroniew, MV, Vinters, HV. Astrocytes: biology and pathology. Acta Neuropathol. 2010;119(1):7–35.CrossRef Google Scholar PubMed

Verkhratsky, A, Steardo, L, Parpura, V, Montana, V. Translational potential of astrocytes in brain disorders. Prog Neurobiol. 2016;144:188–205.Google Scholar

Bayraktar, OA, Fuentealba, LC, Alvarez-Buylla, A, Rowitch, DH. Astrocyte development and heterogeneity. Cold Spring Harb Perspect Biol. 2015;7(1):a020362.Google Scholar

Namihira, M, Nakashima, K. Mechanisms of astrocytogenesis in the mammalian brain. Curr Opin Neurobiol. 2013;23(6):921–7.Google Scholar

Thrane, AS, Rangroo Thrane, V, Nedergaard, M. Drowning stars: reassessing the role of astrocytes in brain edema. Trends Neurosci. 2014;37(11):620–8.Google Scholar

Bazargani, N, Attwell, D. Astrocyte calcium signaling: the third wave. Nat Neurosci. 2016;19(2):182–9.Google Scholar

Matyash, V, Kettenmann, H. Heterogeneity in astrocyte morphology and physiology. Brain Res Rev. 2010;63(1–2):2–10.Google Scholar

Sun, W, Cornwell, A, Li, J, Peng, S, Osorio, MJ, Su Wanga, NA, et al. SOX9 is an astrocyte-specific nuclear marker in the adult brain outside the neurogenic regions. J Neurosci. 2017;37(17):4493–507.Google Scholar

Lafrenaye, AD, Simard, JM. Bursting at the seams: molecular mechanisms mediating astrocyte swelling. Int J Mol Sci. 2019;20(2):pii:E330.Google Scholar

Del Bigio, MR, Deck, JHN, Davidson, GS. Glial swelling with eosinophilia in human post-mortem brains: a change indicative of plasma extravasation. Acta Neuropathol. 2000;100:688–94.Google Scholar

Pekny, M, Nilsson, M. Astrocyte activation and reactive gliosis. Glia. 2005;50(4):427–34.Google Scholar

Pekny, M, Pekna, M. Astrocyte reactivity and reactive astrogliosis: costs and benefits. Physiol Rev. 2014;94(4):1077–98.Google Scholar

Rosenstein, JM, Krum, JM, Ruhrberg, C. VEGF in the nervous system. Organogenesis. 2010;6(2):107–14.Google Scholar

Liberto, CM, Albrecht, PJ, Herx, LM, Yong, VW, Levison, SW. Pro-regenerative properties of cytokine-activated astrocytes. J Neurochem. 2004;89(5):1092–100.Google Scholar

Liddelow, SA, Barres, BA. Reactive astrocytes: production, function, and therapeutic potential. Immunity. 2017;46(6):957–67.Google Scholar

Ge, WP, Jia, JM. Local production of astrocytes in the cerebral cortex. Neuroscience. 2016;323:3–9.Google Scholar

Kanski, R, van Strien, ME, van Tijn, P, Hol, EM. A star is born: new insights into the mechanism of astrogenesis. Cell Mol Life Sci. 2014;71(3):433–47.Google Scholar

Manlow, A, Munoz, DG. A non-toxic method for the demonstration of gliosis. J Neuropathol Exp Neurol. 1992;51:298–302.CrossRef Google Scholar PubMed

Fernandez-Klett, F, Priller, J. The fibrotic scar in neurological disorders. Brain Pathol. 2014;24(4):404–13.Google Scholar

Nave, KA. Myelination and the trophic support of long axons. Nat Rev Neurosci. 2010;11(4):275–83.Google Scholar

van Tilborg, E, CGM, de Theije, van Hal, M, Wagenaar, N, de Vries, LS, Benders, MJ, et al. Origin and dynamics of oligodendrocytes in the developing brain: Implications for perinatal white matter injury. Glia. 2018;66(2):221–38.Google Scholar

Chang, A, Nishiyama, A, Peterson, J, Prineas, J, Trapp, BD. NG2-positive oligodendrocyte progenitor cells in adult human brain and multiple sclerosis lesions. J Neurosci. 2000;20(17):6404–12.Google Scholar

Levine, JM, Reynolds, R, Fawcett, JW. The oligodendrocyte precursor cell in health and disease. Trends Neurosci. 2001;24(1):39–47.Google Scholar

Foerster, S, Hill, MFE, Franklin, RJM. Diversity in the oligodendrocyte lineage: Plasticity or heterogeneity? Glia. 2019;67(10):1797–1805.Google Scholar

Elbaz, B, Popko, B. Molecular control of oligodendrocyte development. Trends Neurosci. 2019;42(4):263–77.Google Scholar

Takase, H, Washida, K, Hayakawa, K, Arai, K, Wang, X, Lo, EH, et al. Oligodendrogenesis after traumatic brain injury. Behav Brain Res. 2018;340:205–11.Google Scholar

Flygt, J, Gumucio, A, Ingelsson, M, Skoglund, K, Holm, J, Alafuzoff, I, et al. Human traumatic brain injury results in oligodendrocyte death and increases the number of oligodendrocyte progenitor cells. J Neuropathol Exp Neurol. 2016;75(6):503–15.Google Scholar

Bruni, JE. Ependymal development, proliferation, and functions: a review. Microsc Res Tech. 1998;41(1):2–13.Google Scholar

Sarnat, HB. Role of the human fetal ependyma. Pediatr Neurol. 1992;8:163–78.Google Scholar

Del Bigio, MR. Cell proliferation in human ganglionic eminence and suppression after prematurity-associated haemorrhage. Brain. 2011;134(Pt 5):1344–61.Google Scholar

Shah, PT, Stratton, JA, Stykel, MG, Abbasi, S, Sharma, S, Mayr, KA, et al. Single-cell transcriptomics and fate mapping of ependymal cells reveals an absence of neural stem cell function. Cell. 2018;173(4):1045–57.e9.Google Scholar

Coletti, AM, Singh, D, Kumar, S, Shafin, TN, Briody, PJ, Babbitt, BF, et al. Characterization of the ventricular-subventricular stem cell niche during human brain development. Development. 2018;145(20):pii:dev170100.Google Scholar

Sarnat, HB. Histochemistry and immunocytochemistry of the developing ependyma and choroid plexus. Microsc Res Tech. 1998;41(1):14–28.Google Scholar

Kawanishi, R, Mizutani, T, Yamada, H, Minami, M, Kakimi, S, Yamada, T, et al. Ubiquitin-positive inclusions in ependymal cells. Acta Neuropathol. 2003;106(2):129–36.Google Scholar

Abdi, K, Lai, CH, Paez-Gonzalez, P, Lay, M, Pyun, J, Kuo, CT. Uncovering inherent cellular plasticity of multiciliated ependyma leading to ventricular wall transformation and hydrocephalus. Nat Commun. 2018;9(1):1655.Google Scholar

Del Bigio, MR. Ependymal cells: biology and pathology. Acta Neuropathol. 2010;119(1):55–73.Google Scholar

Sarnat, HB. Ependymal reactions to injury. A review. J Neuropathol Exp Neurol. 1995;54(1):1–15.Google Scholar

Bruni, JE, Del Bigio, MR, Clattenburg, RE. Ependyma: normal and pathological. A review of the literature. Brain Res. 1985;356(1):1–19.Google Scholar

Munoz, RI, Kahne, T, Herrera, H, Rodriguez, S, Guerra, MM, Vio, K, et al. The subcommissural organ and the Reissner fiber: old friends revisited. Cell Tissue Res. 2019;375(2):507–29.Google Scholar

Wohlsein, P, Deschl, U, Baumgartner, W. Nonlesions, unusual cell types, and postmortem artifacts in the central nervous system of domestic animals. Vet Pathol. 2013;50(1):122–43.Google Scholar

Keene, MF, Hewer, EE. The subcommissural organ and the mesocoelic recess in the human brain, together with a note on reissner’s fibre. J Anat. 1935;69(4):501–7.Google Scholar

Galarza, M. Evidence of the subcommissural organ in humans and its association with hydrocephalus. Neurosurg Rev. 2002;25(4):205–15.Google Scholar

Cantaut-Belarif, Y, Sternberg, JR, Thouvenin, O, Wyart, C, Bardet, PL. The Reissner fiber in the cerebrospinal fluid controls morphogenesis of the body axis. Curr Biol. 2018;28(15):2479–86 e4.Google Scholar

Grondona, JM, Hoyo-Becerra, C, Visser, R, Fernandez-Llebrez, P, Lopez-Avalos, MD. The subcommissural organ and the development of the posterior commissure. Int Rev Cell Mol Biol. 2012;296:63–137.CrossRef Google Scholar PubMed

Milhorat, TH, Kotzen, RM, Anzil, AP. Stenosis of central canal of spinal cord in man: incidence and pathological findings in 232 autopsy cases. J Neurosurg. 1994;80(4):716–22.Google Scholar

References

Kuper, CF, van Bilsen, J, Cnossen, H, Houben, G, Garthoff, J, Wolterbeek, A. Development of immune organs and functioning in humans and test animals: Implications for immune intervention studies. Reprod Toxicol. 2016;64:180–90.Google Scholar

Yockey, LJ, Iwasaki, A. Interferons and proinflammatory cytokines in pregnancy and fetal development. Immunity. 2018;49(3):397–412.Google Scholar

Simon, AK, Hollander, GA, McMichael, A. Evolution of the immune system in humans from infancy to old age. Proc Biol Sci. 2015;282(1821):20143085.Google Scholar

Thapa, P, Farber, DL. The role of the thymus in the immune response. Thorac Surg Clin. 2019;29(2):123–31.Google Scholar

Kinder, JM, Stelzer, IA, Arck, PC, Way, SS. Immunological implications of pregnancy-induced microchimerism. Nat Rev Immunol. 2017;17(8):483–94.Google Scholar

Rijnink, EC, Penning, ME, Wolterbeek, R, Wilhelmus, S, Zandbergen, M, van Duinen, SG, et al. Tissue microchimerism is increased during pregnancy: a human autopsy study. Mol Hum Reprod. 2015;21(11):857–64.Google Scholar

Visser, GHA, Di Renzo, GC, Spitalnik, SL, Motherhood, FCS, Newborn, H. The continuing burden of Rh disease 50 years after the introduction of anti-Rh(D) immunoglobin prophylaxis: call to action. Am J Obstet Gynecol. 2019;Epub:pii: S0002-9378(19)30677–5.Google Scholar

Maddux, AB, Douglas, IS. Is the developmentally immature immune response in paediatric sepsis a recapitulation of immune tolerance? Immunology. 2015;145(1):1–10.Google Scholar

Graeber, MB, Streit, WJ. Microglia: biology and pathology. Acta Neuropathol. 2010;119:89–105.Google Scholar

Menassa, DA, Gomez-Nicola, D. Microglial dynamics during human brain development. Front Immunol. 2018;9:1014.CrossRef Google Scholar PubMed

Askew, K, Gomez-Nicola, D. A story of birth and death: Insights into the formation and dynamics of the microglial population. Brain Behav Immun. 2018;69:9–17.Google Scholar

Smolders, SM, Kessels, S, Vangansewinkel, T, Rigo, JM, Legendre, P, Brone, B. Microglia: brain cells on the move. Prog Neurobiol. 2019;178:101612.CrossRef Google Scholar PubMed

Askew, K, Li, K, Olmos-Alonso, A, Garcia-Moreno, F, Liang, Y, Richardson, P, et al. Coupled proliferation and apoptosis maintain the rapid turnover of microglia in the adult brain. Cell Rep. 2017;18(2):391–405.Google Scholar

Dennis, CV, Suh, LS, Rodriguez, ML, Kril, JJ, Sutherland, GT. Human adult neurogenesis across the ages: An immunohistochemical study. Neuropathol Appl Neurobiol. 2016;42(7):621–38.CrossRef Google Scholar PubMed

Reu, P, Khosravi, A, Bernard, S, Mold, JE, Salehpour, M, Alkass, K, et al. The lifespan and turnover of microglia in the human brain. Cell Rep. 2017;20(4):779–84.Google Scholar

Billiards, SS, Haynes, RL, Folkerth, RD, Trachtenberg, FL, Liu, LG, Volpe, JJ, et al. Development of microglia in the cerebral white matter of the human fetus and infant. J Comp Neurol. 2006;497(2):199–208.Google Scholar

Joost, E, Jordao, MJC, Mages, B, Prinz, M, Bechmann, I, Krueger, M. Microglia contribute to the glia limitans around arteries, capillaries and veins under physiological conditions, in a model of neuroinflammation and in human brain tissue. Brain Struct Funct. 2019;224(3):1301–14.Google Scholar

Blakemore, WF. The ultrastructure of normal and reactive microglia. Acta Neuropathol Suppl. 1975;Suppl 6:273–8.Google Scholar

Zhao, X, Eyo, UB, Murugan, M, Wu, LJ. Microglial interactions with the neurovascular system in physiology and pathology. Dev Neurobiol. 2018;78(6):604–17.Google Scholar

Arnold, T, Betsholtz, C. The importance of microglia in the development of the vasculature in the central nervous system. Vasc Cell. 2013;5(1):12.Google Scholar

Konishi, H, Kiyama, H, Ueno, M. Dual functions of microglia in the formation and refinement of neural circuits during development. Int J Dev Neurosci. 2019 77:18–25.CrossRef Google Scholar

Thion, MS, Ginhoux, F, Garel, S. Microglia and early brain development: An intimate journey. Science. 2018;362(6411):185–9.Google Scholar

Pierre, WC, Smith, PLP, Londono, I, Chemtob, S, Mallard, C, Lodygensky, GA. Neonatal microglia: The cornerstone of brain fate. Brain Behav Immun. 2017;59:333–45.Google Scholar

Kierdorf, K, Prinz, M. Microglia in steady state. J Clin Invest. 2017;127(9):3201–9.Google Scholar

Mosser, CA, Baptista, S, Arnoux, I, Audinat, E. Microglia in CNS development: shaping the brain for the future. Prog Neurobiol. 2017;149–150:1–20.Google Scholar

Eyo, UB, Wu, LJ. Microglia: lifelong patrolling immune cells of the brain. Prog Neurobiol. 2019;179:101614.Google Scholar

Goldmann, T, Wieghofer, P, Jordao, MJ, Prutek, F, Hagemeyer, N, Frenzel, K, et al. Origin, fate and dynamics of macrophages at central nervous system interfaces. Nat Immunol. 2016;17(7):797–805.Google Scholar

Lopez-Atalaya, JP, Askew, KE, Sierra, A, Gomez-Nicola, D. Development and maintenance of the brain’s immune toolkit: Microglia and non-parenchymal brain macrophages. Dev Neurobiol. 2018;78(6):561–79.Google Scholar

Bechmann, I, Kwidzinski, E, Kovac, AD, Simburger, E, Horvath, T, Gimsa, U, et al. Turnover of rat brain perivascular cells. Exp Neurol. 2001;168(2):242–9.Google Scholar

Owens, T, Bechmann, I, Engelhardt, B. Perivascular spaces and the two steps to neuroinflammation. J Neuropathol Exp Neurol. 2008;67(12):1113–21.Google Scholar

Krueger, M, Bechmann, I. CNS pericytes: concepts, misconceptions, and a way out. Glia. 2010;58(1):1–10.CrossRef Google Scholar

Muramatsu, R, Yamashita, T. Pericyte function in the physiological central nervous system. Neurosci Res. 2014;81–82:38–41.Google Scholar

Berthiaume, AA, Hartmann, DA, Majesky, MW, Bhat, NR, Shih, AY. Pericyte structural remodeling in cerebrovascular health and homeostasis. Front Aging Neurosci. 2018;10:210.Google Scholar

Giannoni, P, Badaut, J, Dargazanli, C, De Maudave, AF, Klement, W, Costalat, V, et al. The pericyte-glia interface at the blood-brain barrier. Clin Sci (Lond). 2018;132(3):361–74.Google Scholar

Lambracht-Hall, M, Dimitriadou, V, Theoharides, TC. Migration of mast cells in the developing rat brain. Brain Res Dev Brain Res. 1990;56(2):151–9.Google Scholar

Dropp, JJ. Mast cells in the human brain. Acta Anat (Basel). 1979;105(4):505–13.Google Scholar

Forsythe, P. Mast cells in neuroimmune interactions. Trends Neurosci. 2019;42(1):43–55.Google Scholar

Hendriksen, E, van Bergeijk, D, Oosting, RS, Redegeld, FA. Mast cells in neuroinflammation and brain disorders. Neurosci Biobehav Rev. 2017;79:119–33.Google Scholar

Silver, R, Silverman, AJ, Vitkovic, L, Lederhendler, II. Mast cells in the brain: evidence and functional significance. Trends Neurosci. 1996;19(1):25–31.Google Scholar

Strecker, JK, Schmidt, A, Schabitz, WR, Minnerup, J. Neutrophil granulocytes in cerebral ischemia – Evolution from killers to key players. Neurochem Int. 2017;107:117–26.Google Scholar

Hickey, WF. Migration of hematogenous cells through the blood-brain barrier and the initiation of CNS inflammation. Brain Pathol. 1991;1:97–105.Google Scholar

Hickey, WF. Leukocyte traffic in the central nervous system: the participants and their roles. Semin Immunol. 1999;11(2):125–37.Google Scholar

Williams, KC, Hickey, WF. Traffic of hematogenous cells through the central nervous system. Curr Top Microbiol Immunol. 1995;202:221–45.Google Scholar

Liu, F, McCullough, LD. Inflammatory responses in hypoxic ischemic encephalopathy. Acta Pharmacol Sin. 2013;34(9):1121–30.Google Scholar

Izquierdo, P, Attwell, D, Madry, C. Ion channels and receptors as determinants of microglial function. Trends Neurosci. 2019;42(4):278–92.Google Scholar

Alderliesten, T, Nikkels, PG, Benders, MJ, de Vries, LS, Groenendaal, F. Antemortem cranial MRI compared with postmortem histopathologic examination of the brain in term infants with neonatal encephalopathy following perinatal asphyxia. Arch Dis Child Fetal Neonatal Ed. 2013;98(4):F304–F9.Google Scholar

Boche, D, Perry, VH, Nicoll, JA. Activation patterns of microglia and their identification in the human brain. Neuropathol Appl Neurobiol. 2013;39:3–18.Google Scholar

Smith, AM, Dragunow, M. The human side of microglia. Trends Neurosci. 2014;37(3):125–35.Google Scholar

Walker, DG, Lue, LF. Immune phenotypes of microglia in human neurodegenerative disease: challenges to detecting microglial polarization in human brains. Alzheimer’s Res Ther. 2015;7(1):56.Google Scholar

Schetters, STT, Gomez-Nicola, D, Garcia-Vallejo, JJ, Van Kooyk, Y. Neuroinflammation: microglia and T cells get ready to tango. Front Immunol. 2017;8:1905.Google Scholar

Torres-Platas, SG, Comeau, S, Rachalski, A, Bo, GD, Cruceanu, C, Turecki, G, et al. Morphometric characterization of microglial phenotypes in human cerebral cortex. J Neuroinflammation. 2014;11:12.Google Scholar

Brooks, SA. Lectin histochemistry: historical perspectives, state of the art, and the future. Methods Mol Biol. 2017;1560:93–107.Google Scholar

Del Bigio, MR, Becker, LE. Microglial aggregation in the dentate gyrus: a marker of mild hypoxic-ischaemic brain insult in human infants. Neuropathol Appl Neurobiol. 1994;20:144–51.Google Scholar

Fujimoto, E, Miki, A, Mizoguti, H. Histochemical study of the differentiation of microglial cells in the developing human cerebral hemispheres. J Anat. 1989;166:253–64.Google Scholar

Zrzavy, T, Hoftberger, R, Berger, T, Rauschka, H, Butovsky, O, Weiner, H, et al. Pro-inflammatory activation of microglia in the brain of patients with sepsis. Neuropathol Appl Neurobiol. 2019;45(3):278–90.Google Scholar

Sarkar, T, Patro, N, Patro, IK. Cumulative multiple early life hits- a potent threat leading to neurological disorders. Brain Res Bull. 2019;147:58–68.Google Scholar

Hantsoo, L, Kornfield, S, Anguera, MC, Epperson, CN. Inflammation: A Proposed Intermediary Between Maternal Stress and Offspring Neuropsychiatric Risk. Biol Psychiatry. 2019;85(2):97–106.Google Scholar

Jiang, NM, Cowan, M, Moonah, SN, Petri, WA, Jr. The impact of systemic inflammation on neurodevelopment. Trends Mol Med. 2018;24(9):794–804.Google Scholar

Hung, TH, Chen, VC, Yang, YH, Tsai, CS, Lu, ML, McIntyre, RS, et al. Association between enterovirus infection and speech and language impairments: a nationwide population-based study. Res Dev Disabil. 2018;77:76–86.Google Scholar

Instanes, JT, Halmoy, A, Engeland, A, Haavik, J, Furu, K, Klungsoyr, K. Attention-deficit / hyperactivity disorder in offspring of mothers with inflammatory and immune system diseases. Biol Psychiatry. 2017;81(5):452–9.Google Scholar

Strunk, T, Inder, T, Wang, X, Burgner, D, Mallard, C, Levy, O. Infection-induced inflammation and cerebral injury in preterm infants. Lancet Infect Dis. 2014;14(8):751–62.Google Scholar

Mallard, C, Tremblay, ME, Vexler, ZS. Microglia and neonatal brain injury. Neuroscience. 2019;405:68–76.Google Scholar

Ikegami, A, Haruwaka, K, Wake, H. Microglia: lifelong modulator of neural circuits. Neuropathology. 2019;39(3):173–80.Google Scholar

Wohleb, ES. Neuron-microglia interactions in mental health disorders: “for better, and for worse.” Front Immunol. 2016;7:544.Google Scholar

Galloway, DA, Phillips, AEM, Owen, DRJ, Moore, CS. Phagocytosis in the brain: homeostasis and disease. Front Immunol. 2019;10:790.Google Scholar

Giraud, A, Guiraut, C, Chevin, M, Chabrier, S, Sebire, G. Role of perinatal inflammation in neonatal arterial ischemic stroke. Front Neurol. 2017;8:612.Google Scholar

Parrella, E, Porrini, V, Benarese, M, Pizzi, M. The role of mast cells in stroke. Cells. 2019;8(5):E437.Google Scholar

Bhalala, US, Koehler, RC, Kannan, S. Neuroinflammation and neuroimmune dysregulation after acute hypoxic-ischemic injury of developing brain. Front Pediatr. 2014;2:144.Google Scholar

McDonough, A, Lee, RV, Weinstein, JR. Microglial interferon signaling and white matter. Neurochem Res. 2017;42(9):2625–38.Google Scholar

Aggarwal, S, Bahal, A, Dalal, A. Renal dysfunction in sibs with band like calcification with simplified gyration and polymicrogyria: report of a new mutation and review of literature. Eur J Med Genet. 2016;59(1):5–10.Google Scholar

Biber, K, Owens, T, Boddeke, E. What is microglia neurotoxicity (Not)? Glia. 2014;62(6):841–54.Google Scholar

Hendrickx, DAE, van Eden, CG, Schuurman, KG, Hamann, J, Huitinga, I. Staining of HLA-DR, Iba1 and CD68 in human microglia reveals partially overlapping expression depending on cellular morphology and pathology. J Neuroimmunol. 2017;309:12–22.Google Scholar

Ito, D, Imai, Y, Ohsawa, K, Nakajima, K, Fukuuchi, Y, Kohsaka, S. Microglia-specific localisation of a novel calcium binding protein, Iba1. Brain Res Mol Brain Res. 1998;57(1):1–9.Google Scholar

Monier, A, Evrard, P, Gressens, P, Verney, C. Distribution and differentiation of microglia in the human encephalon during the first two trimesters of gestation. J Comp Neurol. 2006;499(4):565–82.Google Scholar

Monier, A, Adle-Biassette, H, Delezoide, AL, Evrard, P, Gressens, P, Verney, C. Entry and distribution of microglial cells in human embryonic and fetal cerebral cortex. J Neuropathol Exp Neurol. 2007;66(5):372–82.Google Scholar

Micklem, K, Rigney, E, Cordell, J, Simmons, D, Stross, P, Turley, H, et al. A human macrophage-associated antigen (CD68) detected by six different monoclonal antibodies. Br J Haematol. 1989;73(1):6–11.Google Scholar

Gehrmann, J, Banati, RB, Kreutzberg, GW. Microglia in the immune surveillance of the brain: human microglia constitutively express HLA-DR molecules. J Neuroimmunol. 1993;48(2):189–98.Google Scholar

Mildner, A, Huang, H, Radke, J, Stenzel, W, Priller, J. P2Y12 receptor is expressed on human microglia under physiological conditions throughout development and is sensitive to neuroinflammatory diseases. Glia. 2017;65(2):375–87.Google Scholar

Bennett, ML, Bennett, FC, Liddelow, SA, Ajami, B, Zamanian, JL, Fernhoff, NB, et al. New tools for studying microglia in the mouse and human CNS. Proc Natl Acad Sci U S A. 2016;113(12):E1738–E46.CrossRef Google Scholar PubMed

Satoh, JI, Kino, Y, Asahina, N, Takitani, M, Miyoshi, J, Ishida, T, et al. TMEM119 marks a subset of microglia in the human brain. Neuropathology. 2015;36(1):39–49.Google Scholar

Zrzavy, T, Machado-Santos, J, Christine, S, Baumgartner, C, Weiner, HL, Butovsky, O, et al. Dominant role of microglial and macrophage innate immune responses in human ischemic infarcts. Brain Pathol. 2018;28(6):791–805.Google Scholar

Haage, V, Semtner, M, Vidal, RO, Hernandez, DP, Pong, WW, Chen, Z, et al. Comprehensive gene expression meta-analysis identifies signature genes that distinguish microglia from peripheral monocytes/macrophages in health and glioma. Acta Neuropathol Commun. 2019;7(1):20.Google Scholar

References

Courville, CB. Antenatal and paranatal circulatory disorders as a cause of cerebral damage in early life. J Neuropathol Exp Neurol. 1959;18(1):115–40.Google Scholar

Courville, CB. Paranatal anoxia and its residual encephalic lesions. Can Anaesth Soc J. 1961;8:3–13.Google Scholar

Marin-Padilla, M. Developmental neuropathology and impact of perinatal brain damage. II: white matter lesions of the neocortex. J Neuropathol Exp Neurol. 1997;56(3):219–35.Google Scholar

Marin-Padilla, M. Developmental neuropathology and impact of perinatal brain damage. III: Gray matter lesions of the neocortex. J Neuropathol Exp Neurol. 1999;58(5):407–29.Google Scholar

Millar, LJ, Shi, L, Hoerder-Suabedissen, A, Molnar, Z. Neonatal hypoxia ischaemia: mechanisms, models, and therapeutic challenges. Front Cell Neurosci. 2017;11:78.Google Scholar

Little, WJ. On the influence of parturition, difficult labours, premature birth, and asphyxia neonatorum on the mental and physical condition of the child, especially in relation to deformities. Trans Obstet Soc Lond. 1862;3:293–344.Google Scholar

Courville, CB. Palsy, Cerebral. A Brief Introduction to Its History, Etiology, and Pathology, with Some Notes on the Resultant Clinical Syndromes and Their Treatment. Los Angeles: San Lucas Press; 1954. p. 80.Google Scholar

Towbin, A. Pathology of cerebral palsy. II. Cerebral palsy due to encephaloclastic processes. AMA Arch Pathol. 1955;59:529–52.Google Scholar

Crome, L. Some morbid-anatomical aspects of mental deficiency. J Ment Sci. 1954;100(421):894–912.Google Scholar

Crome, LL. Cortical lesions in cerebral palsy. Dev Med Chil Neurol. 1959;1(6):22–8.Google Scholar

Crome, L. The brain and mental retardation. Br Med J. 1960;1(5177):897–904.Google Scholar

Southard, EE. General aspects of the brain anatomy of the feeble-minded. Mem Am Acad Arts Sci. 1918;14(2):25–58.Google Scholar

Schreiber, F. Apnea of the newborn and associated cerebral injury. A clinical and statistical study. JAMA. 1938;111(14):1263–9.Google Scholar

Brandenburg, JE, Fogarty, MJ, Sieck, GC. A critical evaluation of current concepts in cerebral palsy. Physiology (Bethesda). 2019;34(3):216–29.Google Scholar

Leviton, A. Why the term neonatal encephalopathy should be preferred over neonatal hypoxic-ischemic encephalopathy. Am J Obstet Gynecol. 2013;208(3):176–80.Google Scholar

Volpe, JJ. Neonatal encephalopathy: an inadequate term for hypoxic-ischemic encephalopathy. Ann Neurol. 2012;72(2):156–66.Google Scholar

Becher, JC, Bell, JE, Keeling, JW, Liston, WA, McIntosh, N, Wyatt, B. The Scottish Perinatal Neuropathology Study–clinicopathological correlation in stillbirths. BJOG. 2006;113(3):310–7.Google Scholar

Zhang, X, Kramer, MS. Temporal trends in stillbirth in the United States, 1992–2004: a population-based cohort study. BJOG. 2014;121(10):1229–36.Google Scholar

Platts, J, Mitchell, EA, Stacey, T, Martin, BL, Roberts, D, McCowan, L, et al. The Midland and North of England Stillbirth Study (MiNESS). BMC Pregnancy Childbirth. 2014;14:171.Google Scholar

Salihu, HM. Epidemiology of stillbirth and fetal central nervous system injury. Semin Perinatol. 2008;32(4):232–8.Google Scholar

McCormick, MC, Litt, JS, Smith, VC, Zupancic, JA. Prematurity: an overview and public health implications. Annu Rev Public Health. 2011;32:367–79.Google Scholar

Volpe, JJ. The encephalopathy of prematurity – brain injury and impaired brain development inextricably intertwined. Semin Pediatr Neurol. 2009;16(4):167–78.Google Scholar

Lee, AC, Kozuki, N, Blencowe, H, Vos, T, Bahalim, A, Darmstadt, GL, et al. Intrapartum-related neonatal encephalopathy incidence and impairment at regional and global levels for 2010 with trends from 1990. Pediatr Res. 2013;74 Suppl 1:50–72.Google Scholar

American College of Obstetricians and Gynecologists’ Task Force on Neonatal Encephalopathy. Executive summary: Neonatal Encephalopathy and Neurologic Outcome, 2nd edition. Obstet Gynecol. 2014;123(4):896–901.Google Scholar

Smith, J, Wells, L, Dodd, K. The continuing fall in incidence of hypoxic-ischaemic encephalopathy in term infants. BJOG. 2000;107(4):461–6.Google Scholar

Kurinczuk, JJ, White-Koning, M, Badawi, N. Epidemiology of neonatal encephalopathy and hypoxic-ischaemic encephalopathy. Early Hum Dev. 2010;86(6):329–38.Google Scholar

Martinez-Biarge, M, Diez-Sebastian, J, Wusthoff, CJ, Mercuri, E, Cowan, FM. Antepartum and intrapartum factors preceding neonatal hypoxic-ischemic encephalopathy. Pediatrics. 2013;132(4):e952–e9.Google Scholar

McIntyre, S, Blair, E, Badawi, N, Keogh, J, Nelson, KB. Antecedents of cerebral palsy and perinatal death in term and late preterm singletons. Obstet Gynecol. 2013;122(4):869–77.Google Scholar

Rutherford, M, Malamateniou, C, McGuinness, A, Allsop, J, Biarge, MM, Counsell, S. Magnetic resonance imaging in hypoxic-ischaemic encephalopathy. Early Hum Dev. 2010;86(6):351–60.Google Scholar

Nikas, I, Dermentzoglou, V, Theofanopoulou, M, Theodoropoulos, V. Parasagittal lesions and ulegyria in hypoxic-ischemic encephalopathy: neuroimaging findings and review of the pathogenesis. J Child Neurol. 2008;23(1):51–8.Google Scholar

Thayyil, S, Chandrasekaran, M, Taylor, A, Bainbridge, A, Cady, EB, Chong, WK, et al. Cerebral magnetic resonance biomarkers in neonatal encephalopathy: a meta-analysis. Pediatrics. 2010;125(2):e382–e95.Google Scholar

Montaldo, P, Chaban, B, Lally, PJ, Sebire, NJ, Taylor, AM, Thayyil, S. Quantification of ante-mortem hypoxic ischemic brain injury by post-mortem cerebral magnetic resonance imaging in neonatal encephalopathy. Eur J Paediatr Neurol. 2015;19(6):665–71.Google Scholar

Squier, W, Cowan, FM. The value of autopsy in determining the cause of failure to respond to resuscitation at birth. Semin Neonatol. 2004;9(4):331–45.Google Scholar

Elder, DE, Zuccollo, JM. Autopsy after death due to extreme prematurity. Arch Dis Child Fetal Neonatal Ed. 2005;90(3):F270–F2.Google Scholar

Jacques, SM, Kupsky, WJ, Qureshi, F. Antenatal brain injury in third trimester neonates with severe congenital anomalies: an autopsy study. J Matern Fetal Neonatal Med. 2015;28(12):1414–20.Google Scholar

Swinton, CH, Weiner, J, Okah, FA. The neonatal autopsy: can it be revived? Am J Perinatol. 2013;30(9):739–44.Google Scholar

Brown, AW. Structural abnormalities in neurons. J Clin Pathol Suppl. 1977;11:155–69.Google Scholar

Brody, BA, Kinney, HC, Kloman, AS, Gilles, FH. Sequence of central nervous system myelination in human infancy. I. An autopsy study of myelination. J Neuropathol Exp Neurol. 1987;46:283–301.Google Scholar

Yakovlev, PI, Lecours, AR. The myelogenetic cycles of regional maturation of the brain. In: Minkowski, A, editor. Regional Development of the Brain in Early Life. Oxford: Blackwell Scientific Publications; 1967. pp. 3–70.Google Scholar

Kramer, W. Multilocular encephalomalacia. J Neurol Neurosurg Psychiatry. 1956;19(3):209–16.Google Scholar

Ahdab-Barmada, M, Moossy, J, Painter, M. Pontosubicular necrosis and hyperoxemia. Pediatrics. 1980;66(6):840–7.Google Scholar

Friede, RL. Ponto-subicular lesions in perinatal anoxia. Arch Pathol. 1972;94(4):343–54.Google Scholar

Sohma, O, Mito, T, Mizuguchi, M, Takashima, S. The prenatal age critical for the development of the pontosubicular necrosis. Acta Neuropathol. 1995;90(1):7–10.Google Scholar

Bruck, Y, Bruck, W, Kretzschmar, HA, Lassmann, H. Evidence for neuronal apoptosis in pontosubicular neuron necrosis. Neuropathol Appl Neurobiol. 1996;22(1):23–9.Google Scholar

Burke, C, Gobe, G. Pontosubicular apoptosis (“necrosis”) in human neonates with intrauterine growth retardation and placental infarction. Virchows Arch. 2005;446(6):640–5.Google Scholar

Hernandez-Jimenez, M, Sacristan, S, Morales, C, Garcia-Villanueva, M, Garcia-Fernandez, E, Alcazar, A, et al. Apoptosis-related proteins are potential markers of neonatal hypoxic-ischemic encephalopathy (HIE) injury. Neurosci Lett. 2014;558:143–8.Google Scholar

Del Bigio, MR, Becker, LE. Microglial aggregation in the dentate gyrus: a marker of mild hypoxic-ischaemic brain insult in human infants. Neuropathol Appl Neurobiol. 1994;20:144–51.Google Scholar

Squier, W, Salisbury, H, Sisodiya, S. Stroke in the developing brain and intractable epilepsy: effect of timing on hippocampal sclerosis. Dev Med Child Neurol. 2003;45(9):580–5.Google Scholar

Heschl, R. Gehirndefect und Hydrocephalus. Vierteljahrsschr prakt Heilk (Prager). 1859;61(1):59–74.Google Scholar

de la Croix, NJ. Ein Fall von ausgebreiteter Porencephalie an der medialen Fläche der rechten Grosshirnhemisphäre. Virchows Archiv. 1884;97(2):307–29.Google Scholar

Lyon, G, Robain, O. Etude comparative des encephalopathies circulatories prenatales et para-natales (hydranencephalies, porencephalies et encephalomalacies kystiques de la substance blanche). Acta Neuropathol. 1967;9(1):79–98.Google Scholar

Gilles, FH. Classification of cerebral palsy: neuropathologist’s perspective. Dev Med Child Neurol. 2007;49 Suppl 2:19–21.Google Scholar

Norman, RM, Urich, H, Woods, GE. The relationship between prenatal porencephaly and the encephalomalacias of early life. J Ment Sci. 1958;104(436):758–71.Google Scholar

Yakovlev, PI, Wadsworth, RC. Schizencephalies. A study of the congenital clefts in the cerebral mantle. I. Clefts with fused lips. J Neuropathol Exp Neurol. 1946;5:116–30.Google Scholar

Yakovlev, PI, Wadsworth, RC. Schizencephalies. A study of the congenital clefts in the cerebral mantle. II. Clefts with hydrocephalus and lips separated. J Neuropathol Exp Neurol. 1946;5(3):169–206.Google Scholar

Curry, CJ, Lammer, EJ, Nelson, V, Shaw, GM. Schizencephaly: heterogeneous etiologies in a population of 4 million California births. Am J Med Genet A. 2005;137(2):181–9.Google Scholar

Fernandez-Bouzas, A, Harmony, T, Santiago-Rodriguez, E, Ricardo-Garcell, J, Fernandez, T, Avila-Acosta, D. Schizencephaly with occlusion or absence of middle cerebral artery. Neuroradiology. 2006;48(3):171–5.Google Scholar

Merello, E, Swanson, E, De Marco, P, Akhter, M, Striano, P, Rossi, A, et al. No major role for the EMX2 gene in schizencephaly. Am J Med Genet A. 2008;146A(9):1142–50.Google Scholar

Yoneda, Y, Haginoya, K, Kato, M, Osaka, H, Yokochi, K, Arai, H, et al. Phenotypic spectrum of COL4A1 mutations: porencephaly to schizencephaly. Ann Neurol. 2013;73(1):48–57.Google Scholar

Norman, RM. Atrophic sclerosis of the cerebral cortex associated with birth injury. Arch Dis Child. 1944;19(99):111–21.Google Scholar

Bresler, J. Klinische und pathologisch-anatomische Beiträge zur Mikrogyrie. Arch Psychiatr Nervenkr. 1899;31(3):566–73.Google Scholar

Morys, J, Narkiewicz, O, Wisniewski, HM. Neuronal loss in the human claustrum following ulegyria. Brain Res. 1993;616(1–2):176–80.Google Scholar

Norman, MG. On the morphogenesis of ulegyria. Acta Neuropathol. 1981;53(4):331–2.Google Scholar

Atapattu, N, Ainsworth, J, Willshaw, H, Parulekar, M, MacPherson, L, Miller, C, et al. Septo-optic dysplasia: antenatal risk factors and clinical features in a regional study. Horm Res Paediatr. 2012;78(2):81–7.Google Scholar

Maeda, T, Akaishi, M, Shimizu, M, Sekiguchi, K, Anan, A, Takano, T, et al. The subclassification of schizencephaly and its clinical characterization. Brain Dev. 2009;31(9):694–701.Google Scholar

Bonasoni, MP, Reyes, J, Cromwell, S, Halliday, W, Taylor, GP, Chiasson, DA. Sudden death in the septo-optic dysplasia spectrum. Acad Forensic Pathol. 2014;4(3):400–8.Google Scholar

Bhatnagar, S, Kuber, R, Shah, D, Kulkarni, V. Unilateral closed lip schizencephaly with septo-optic dysplasia. Ann Med Health Sci Res. 2014;4(2):283–5.Google Scholar

Labate, A, Gambardella, A, Quattrone, A. Septo-optic dysplasia plus bilateral perisylvian polymicrogyria: a case report. Neurol Sci. 2013;34(8):1479–80.Google Scholar

Lubinsky, MS. Hypothesis: septo-optic dysplasia is a vascular disruption sequence. Am J Med Genet. 1997;69(3):235–6.Google Scholar

Borchert, M. Reappraisal of the optic nerve hypoplasia syndrome. J Neuroophthalmol. 2012;32(1):58–67.Google Scholar

Clinch, TA. A case of imperfect porencephaly. J Mental Sci. 1899;45(189):246–57.Google Scholar

Andriezen, WL. The pathogenesis of epileptic idiocy and epileptic imbecility. Brit Med J. 1897;1:1081–3.Google Scholar

Mickle, WJ. Atypical and unusual brain-forms, especially in relation to mental status: a study on brain-surface morphology. J Mental Sci. 1896;42(178):541–83.Google Scholar

Binswanger, O. Ueber eine Missbildung des Gehirns. Virchows Archiv. 1882;87(3):427–76.Google Scholar

Jacob, H. Die feinere Oberflächengestaltung der Hirnwindungen, die Hirnwarzenbildung und die Mikropolygyrie. Z gesamte Neurol Psychiatrie. 1940;170(1):64–84.Google Scholar

Warner, FJ. The histogenic principle of microgyria and related cerebral malformations. J Nerv Ment Dis. 1953;118(1):1–18.Google Scholar

Heffner, RR. Syndrome of absent abdominal muscles: two cases with microcephaly, polymicrogyria, and cerebellar malformations. J Neurol Neurosurg Psychiatry. 1970;33(6):844–50.Google Scholar

Pitner, SE, Edwards, JE, McCormick, WF. Observations on the pathology of the Moebius syndrome. J Neurol Neurosurg Psychiatry. 1965;28:362–74.Google Scholar

Squier, W, Jansen, A. Polymicrogyria: pathology, fetal origins and mechanisms. Acta Neuropathol Commun. 2014;2:80.Google Scholar

Jansen, AC, Robitaille, Y, Honavar, M, Mullatti, N, Leventer, RJ, Andermann, E, et al. The histopathology of polymicrogyria: a series of 71 brain autopsy studies. Dev Med Child Neurol. 2016;58(1):39–48.Google Scholar

Friede, RL, Mikolasek, J. Postencephalitic porencephaly, hydranencephaly or polymicrogyria. A review. Acta Neuropathol. 1978;43(1–2):161–8.Google Scholar

Judkins, AR, Martinez, D, Ferreira, P, Dobyns, WB, Golden, JA. Polymicrogyria includes fusion of the molecular layer and decreased neuronal populations but normal cortical laminar organization. J Neuropathol Exp Neurol. 2011;70(6):438–43.Google Scholar

Ferrer, I, Catala, I. Unlayered polymicrogyria: structural and developmental aspects. Anat Embryol. 1991;184:517–28.Google Scholar

Diamandis, P, Chitayat, D, Toi, A, Blaser, S, Shannon, P. The pathology of incipient polymicrogyria. Brain Dev. 2017;39(1):23–39.Google Scholar

Stutterd, CA, Leventer, RJ. Polymicrogyria: a common and heterogeneous malformation of cortical development. Am J Med Genet C Semin Med Genet. 2014;166C(2):227–39.Google Scholar

Pagnamenta, AT, Howard, MF, Wisniewski, E, Popitsch, N, Knight, SJ, Keays, DA, et al. Germline recessive mutations in PI4 KA are associated with perisylvian polymicrogyria, cerebellar hypoplasia and arthrogryposis. Hum Mol Genet. 2015;24(13):3732–41.Google Scholar

Poirier, K, Saillour, Y, Fourniol, F, Francis, F, Souville, I, Valence, S, et al. Expanding the spectrum of TUBA1A-related cortical dysgenesis to polymicrogyria. Eur J Hum Genet. 2013;21(4):381–5.Google Scholar

Fry, AE, Fawcett, KA, Zelnik, N, Yuan, H, Thompson, BAN, Shemer-Meiri, L, et al. De novo mutations in GRIN1 cause extensive bilateral polymicrogyria. Brain. 2018;141(3):698–712.Google Scholar

Chabrier, S, Husson, B, Dinomais, M, Landrieu, P, Nguyen The Tich S. New insights (and new interrogations) in perinatal arterial ischemic stroke. Thromb Res. 2011;127(1):13–22.Google Scholar

Martinez-Biarge, M, Cheong, JL, Diez-Sebastian, J, Mercuri, E, Dubowitz, LM, Cowan, FM. Risk factors for neonatal arterial ischemic stroke: the importance of the intrapartum period. J Pediatr. 2016;173:62–8.Google Scholar

van der Aa, NE, Benders, MJ, Groenendaal, F, de Vries, LS. Neonatal stroke: a review of the current evidence on epidemiology, pathogenesis, diagnostics and therapeutic options. Acta Paediatr. 2014;103(4):356–64.Google Scholar

Fernandez-Lopez, D, Natarajan, N, Ashwal, S, Vexler, ZS. Mechanisms of perinatal arterial ischemic stroke. J Cereb Blood Flow Metab. 2014;34(6):921–32.Google Scholar

Lehman, LL, Rivkin, MJ. Perinatal arterial ischemic stroke: presentation, risk factors, evaluation, and outcome. Pediatr Neurol. 2014;51(6):760–8.Google Scholar

Barmada, MA, Moossy, J, Shuman, RM. Cerebral infarcts with arterial occlusion in neonates. Ann Neurol. 1979;6(6):495–502.Google Scholar

Benders, MJ, Groenendaal, F, De Vries, LS. Preterm arterial ischemic stroke. Semin Fetal Neonatal Med. 2009;14(5):272–7.Google Scholar

deVeber, G, Andrew, M, Adams, C, Bjornson, B, Booth, F, Buckley, DJ, et al. Cerebral sinovenous thrombosis in children. N Engl J Med. 2001;345(6):417–23.Google Scholar

Tan, M, Deveber, G, Shroff, M, Moharir, M, Pontigon, AM, Widjaja, E, et al. Sagittal sinus compression is associated with neonatal cerebral sinovenous thrombosis. Pediatrics. 2011;128(2):e429-35.Google Scholar

Kirton, A, Shroff, M, Pontigon, AM, deVeber, G. Risk factors and presentations of periventricular venous infarction vs arterial presumed perinatal ischemic stroke. Arch Neurol. 2010;67(7):842–8.Google Scholar

Grunt, S, Wingeier, K, Wehrli, E, Boltshauser, E, Capone, A, Fluss, J, et al. Cerebral sinus venous thrombosis in Swiss children. Dev Med Child Neurol. 2010;52(12):1145–50.Google Scholar

Lahutte, M, Bordarier, C, Hornoy, P, Fallet-Bianco, C, Adamsbaum, C. L’infarctus veineux hémorragique du nouveau-né. J Radiol. 2010;91(7–8):787–96.Google Scholar

Davies, RP, Slavotinek, JP, James, SL, Morphett, AD. Calcified cerebral sinus thrombosis in infancy–CT appearances with pathological correlation. Pediatr Radiol. 1989;20(1–2):101–3.Google Scholar

Halsey, JH, Jr., Allen, N, Chamberlin, HR. The morphogenesis of hydranencephaly. J Neurol Sci. 1971;12(2):187–217.Google Scholar

Muir, CS. Hydranencephaly and allied disorders: a study of cerebral defect in Chinese children. Arch Dis Child. 1959;34:231–46.Google Scholar

Naidich, TP, Griffiths, PD, Rosenbloom, L. Central nervous system injury in utero: selected entities. Pediatr Radiol. 2015;45 Suppl 3:S454-S62.Google Scholar

Weiss, MH, Young, HF, McFarland, DE. Hydranencephaly of postnatal origin. Case report. J Neurosurg. 1970;32(6):715–20.Google Scholar

Fowler, M, Dow, R, White, TA, Greer, CH. Congenital hydrocephalus-hydrencephaly in five siblings, with autopsy studies: a new disease. Dev Med Child Neurol. 1972;14(2):173–88.Google Scholar

Harding, BN, Ramani, P, Thurley, P. The familial syndrome of proliferative vasculopathy and hydranencephaly-hydrocephaly: immunocytochemical and ultrastructural evidence for endothelial proliferation. Neuropathol Appl Neurobiol. 1995;21(1):61–7.Google Scholar

Williams, D, Patel, C, Fallet-Bianco, C, Kalyanasundaram, K, Yacoubi, M, Dechelotte, P, et al. Fowler syndrome-a clinical, radiological, and pathological study of 14 cases. Am J Med Genet A. 2010;152A(1):153–60.Google Scholar

Bessieres-Grattagliano, B, Foliguet, B, Devisme, L, Loeuillet, L, Marcorelles, P, Bonniere, M, et al. Refining the clinicopathological pattern of cerebral proliferative glomeruloid vasculopathy (Fowler syndrome): report of 16 fetal cases. Eur J Med Genet. 2009;52(6):386–92.Google Scholar

Meyer, E, Ricketts, C, Morgan, NV, Morris, MR, Pasha, S, Tee, LJ, et al. Mutations in FLVCR2 are associated with proliferative vasculopathy and hydranencephaly-hydrocephaly syndrome (Fowler syndrome). Am J Hum Genet. 2010;86(3):471–8.Google Scholar

Radio, FC, Di Meglio, L, Agolini, E, Bellacchio, E, Rinelli, M, Toscano, P, et al. Proliferative vasculopathy and hydranencephaly-hydrocephaly syndrome or Fowler syndrome: report of a family and insight into the disease’s mechanism. Mol Genet Genomic Med. 2018;6(3):446–51.Google Scholar

Frosk, P, Arts, HH, Philippe, J, Gunn, CS, Brown, EL, Chodirker, B, et al. A truncating mutation in CEP55 is the likely cause of MARCH, a novel syndrome affecting neuronal mitosis. J Med Genet. 2017;54(7):490–501.Google Scholar

Ligam, P, Haynes, RL, Folkerth, RD, Liu, L, Yang, M, Volpe, JJ, et al. Thalamic damage in periventricular leukomalacia: novel pathologic observations relevant to cognitive deficits in survivors of prematurity. Pediatr Res. 2009;65(5):524–9.Google Scholar

Parisi, JE, Collins, GH, Kim, RC, Crosley, CJ. Prenatal symmetrical thalamic degeneration with flexion spasticity at birth. Ann Neurol. 1983;13(1):94–7.Google Scholar

Peters, B, Walka, MM, Friedmann, W, Stoltenburg-Didinger, G, Obladen, M. Hypoxic-ischemic encephalopathy with cystic brain stem necroses and thalamic calcifications in a preterm twin. Brain Dev. 2000;22(4):265–71.Google Scholar

Pols, T, de Vries, LS, Salamon, AS, Nikkels, PGJ, Lichtenbelt, KD, Mulder-de Tollenaer, SM, et al. Symmetrical thalamic lesions in the newborn: a case series. Neuropediatrics. 2019;50(3):152–9.Google Scholar

Rodriguez, MJ, Ursu, G, Bernal, F, Cusi, V, Mahy, N. Perinatal human hypoxia-ischemia vulnerability correlates with brain calcification. Neurobiol Dis. 2001;8(1):59–68.Google Scholar

Rosales, RK, Riggs, HE. Symmetrical thalamic degeneration in infants. J Neuropathol Exp Neurol. 1962;21:372–6.Google Scholar

Malamud, N. Status marmoratus; a form of cerebral palsy following either birth injury or inflammation of the central nervous system. J Pediatr. 1950;37(4):610–19.Google Scholar

Norman, RM. An example of status marmoratus of the cerebral cortex. J Neurol Psychiatry. 1938;1(1):7–16.Google Scholar

Löwenburg, K, Malamud, W. Status marmoratus: etiology and manner of development. Arch Neurol Psychiatr. 1933;29(1):104–24.Google Scholar

Norman, RM. Etat marbre of the corpus striatum following birth injury. J Neurol Neurosurg Psychiatry. 1947;10(1):12–25.Google Scholar

Norman, RM. Etat marbre of the thalamus following birth injury. Brain. 1949;72:83–8.Google Scholar

Friede, RL, Schachenmayr, W. Early stages of status marmoratus. Acta Neuropathol. 1977;38(2):123–7.Google Scholar

Aravamuthan, BR, Waugh, JL. Localization of basal ganglia and thalamic damage in dyskinetic cerebral palsy. Pediatr Neurol. 2016;54:11–21.Google Scholar

Yagishita, A, Nakano, I, Ushioda, T, Otsuki, N, Hasegawa, A. Acute encephalopathy with bilateral thalamotegmental involvement in infants and children: imaging and pathology findings. AJNR Am J Neuroradiol. 1995;16(3):439–47.Google Scholar

Miller, SP, McQuillen, PS, Hamrick, S, Xu, D, Glidden, DV, Charlton, N, et al. Abnormal brain development in newborns with congenital heart disease. N Engl J Med. 2007;357(19):1928–38.Google Scholar

Berman, JI, Hamrick, SE, McQuillen, PS, Studholme, C, Xu, D, Henry, RG, et al. Diffusion-weighted imaging in fetuses with severe congenital heart defects. AJNR Am J Neuroradiol. 2011;32(2):E21–2.Google Scholar

Schneider, H, Ballowitz, L, Schachinger, H, Hanefeld, F, Droszus, JU. Anoxic encephalopathy with predominant involvement of basal ganglia, brain stem and spinal cord in the perinatal period. Report on seven newborns. Acta Neuropathol. 1975;32(4):287–98.Google Scholar

Kwan, S, Boudes, E, Gilbert, G, Saint-Martin, C, Albrecht, S, Shevell, M, et al. Injury to the cerebellum in term asphyxiated newborns treated with hypothermia. AJNR Am J Neuroradiol. 2015;36(8):1542–9.Google Scholar

Pierson, CR, Al Sufiani, F. Preterm birth and cerebellar neuropathology. Semin Fetal Neonatal Med. 2016;21(5):305–11.Google Scholar

Biran, V, Verney, C, Ferriero, DM. Perinatal cerebellar injury in human and animal models. Neurol Res Int. 2012;2012:858929.Google Scholar

Sargent, MA, Poskitt, KJ, Roland, EH, Hill, A, Hendson, G. Cerebellar vermian atrophy after neonatal hypoxic-ischemic encephalopathy. AJNR Am J Neuroradiol. 2004;25(6):1008–15.Google Scholar

Poretti, A, Prayer, D, Boltshauser, E. Morphological spectrum of prenatal cerebellar disruptions. Eur J Paediatr Neurol. 2009;13(5):397–407.Google Scholar

Poretti, A, Boltshauser, E, Huisman, TA. Prenatal cerebellar disruptions: neuroimaging spectrum of findings in correlation with likely mechanisms and etiologies of injury. Neuroimaging Clin N Am. 2016;26(3):359–72.Google Scholar

Sarnat, HB, Nochlin, D, Born, DE. Neuronal nuclear antigen (NeuN): a marker of neuronal maturation in early human fetal nervous system. Brain Dev. 1998;20(2):88–94.Google Scholar

Leech, RW, Alvord, EC. Anoxic-ischemic encephalopathy in the human neonatal period. The significance of brain stem involvement. Arch Neurol. 1977;34:109–13.Google Scholar

Leong, S, Ashwell, KW. Is there a zone of vascular vulnerability in the fetal brain stem? Neurotoxicol Teratol. 1997;19(4):265–75.Google Scholar

Shioda, M, Hayashi, M, Takanashi, J, Osawa, M. Lesions in the central tegmental tract in autopsy cases of developmental brain disorders. Brain Dev. 2011;33(7):541–7.Google Scholar

Leech, RW, Brumback, RA. Massive brain stem necrosis in the human neonate: presentation of three cases with review of the literature. J Child Neurol. 1988;3(4):258–62.Google Scholar

Pindur, J, Capin, DM, Johnson, MI, Rance, NE. Cystic brain stem necrosis in a premature infant after prolonged bradycardia. Acta Neuropathol. 1992;83(6):667–9.Google Scholar

Cortez, SC, Kinney, HC. Brainstem tegmental necrosis and olivary hypoplasia: a lethal entity associated with congenital apnea. J Neuropathol Exp Neurol. 1996;55(7):841–9.Google Scholar

D’Cruz, OF, Swisher, CN, Jaradeh, S, Tang, T, Konkol, RJ. Mobius syndrome: evidence for a vascular etiology. J Child Neurol. 1993;8(3):260–5.Google Scholar

Borlot, F, da Paz, JA, Gonzalez, CH, Lucato, LT, Marques-Dias, MJ. Mobius sequence in a girl and arthrogryposis in her half-brother: distinct phenotypes caused by prenatal injuries. Fetal Pediatr Pathol. 2011;30(4):260–5.Google Scholar

Katsetos, CD, Anderson, CE, Guzman, MA, Pascasio, JM, de Chadarevian, JP, Legido, A. Brainstem tegmental necrosis and olivary hypoplasia: raising awareness of a rare neuropathologic correlate of congenital apnea. Semin Pediatr Neurol. 2014;21(2):177–83.Google Scholar

Marques-Dias, MJ, Gonzalez, CH, Rosemberg, S. Mobius sequence in children exposed in utero to misoprostol: neuropathological study of three cases. Birth Defects Res A Clin Mol Teratol. 2003;67(12):1002–7.Google Scholar

Mito, T, Becker, LE, Takashima, S. Neuropathology of central respiratory dysfunction in infancy. Pediatr Neurosurg. 1991;17(2):80–7.Google Scholar

Moya, MP, Delong, GR, Barboriak, D, Cummings, TJ. A lethal association of congenital apnea with brainstem tegmental necrosis. Pediatr Neurol. 2004;30(3):219–21.Google Scholar

Thakkar, N, O’Neil, W, Duvally, J, Liu, C, Ambler, M. Mobius syndrome due to brain stem tegmental necrosis. Arch Neurol. 1977;34(2):124–6.Google Scholar

Towfighi, J, Marks, K, Palmer, E, Vannucci, R. Mobius syndrome. Neuropathologic observations. Acta Neuropathol. 1979;48(1):11–17.CrossRef Google Scholar PubMed

Verloes, A, Bitoun, P, Heuskin, A, Amrom, D, van de Broeck, H, Nikkel, SM, et al. Mobius sequence, Robin complex, and hypotonia: severe expression of brainstem disruption spectrum versus Carey-Fineman-Ziter syndrome. Am J Med Genet A. 2004;127A(3):277–87.Google Scholar

Wilson, ER, Mirra, SS, Schwartz, JF. Congenital diencephalic and brain stem damage: neuropathologic study of three cases. Acta Neuropathol. 1982;57(1):70–4.Google Scholar

Gerards, M, Sallevelt, SC, Smeets, HJ. Leigh syndrome: resolving the clinical and genetic heterogeneity paves the way for treatment options. Mol Genet Metab. 2016;117(3):300–12.Google Scholar

Rudzinski, ER, Kapur, RP, Hevner, RF. Fetal akinesia deformation sequence with delayed skeletal muscle maturation and polymicrogyria: evidence for a hypoxic/ischemic pathogenesis. Pediatr Dev Pathol. 2010;13(3):192–201.Google Scholar

Quinn, CM, Wigglesworth, JS, Heckmatt, J. Lethal arthrogryposis multiplex congenita: a pathological study of 21 cases. Histopathology. 1991;19(2):155–62.Google Scholar

Johnson, MW, Stoll, L, Rubio, A, Troncoso, J, Pletnikova, O, Fowler, DR, et al. Axonal injury in young pediatric head trauma: a comparison study of beta-amyloid precursor protein (beta-APP) immunohistochemical staining in traumatic and nontraumatic deaths. J Forensic Sci. 2011;56(5):1198–205.CrossRef Google Scholar PubMed

McKenzie, KJ, McLellan, DR, Gentleman, SM, Maxwell, WL, Gennarelli, TA, Graham, DI. Is beta-APP a marker of axonal damage in short-surviving head injury? Acta Neuropathol (Berl). 1996;92(6):608–13.Google Scholar

Rahaman, P, Del Bigio, MR. Histology of brain trauma and hypoxia-ischemia. Acad Forensic Pathol. 2018;8(3):539–54.Google Scholar

Riezzo, I, Neri, M, De Stefano, F, Fulcheri, E, Ventura, F, Pomara, C, et al. The timing of perinatal hypoxia/ischemia events in term neonates: a retrospective autopsy study. HSPs, ORP-150 and COX2 are reliable markers to classify acute, perinatal events. Diagn Pathol. 2010;5:49.Google Scholar

Dies, KA, Bodell, A, Hisama, FM, Guo, CY, Barry, B, Chang, BS, et al. Schizencephaly: association with young maternal age, alcohol use, and lack of prenatal care. J Child Neurol. 2013;28(2):198–203.Google Scholar

Kuchukhidze, G, Unterberger, I, Dobesberger, J, Embacher, N, Walser, G, Haberlandt, E, et al. Electroclinical and imaging findings in ulegyria and epilepsy: a study on 25 patients. J Neurol Neurosurg Psychiatry. 2008;79(5):547–52.Google Scholar

References

Munell, F, Tormos, MA, Roig-Quilis, M. Brainstem dysgenesis: beyond Moebius syndrome. Rev Neurol 2018;66:241–50.Google Scholar

Webb, BD, Shaaban, S, Gaspar, H, Cunh, LF, Schubert, CR, Hao, K, Robson, CD, Chan, WM, Andrews C, , MacKinnon, S, Oystreck, DT, Hunter, DG, Iacovelli, AJ, Ye, X, Camminady, A, Engle, EC, Jabs, EW. HOXB1 founder mutation in humans recapitulates the phenotype of Hoxb1-/- mice. Am J Hum Genet 2012;91:171–9.Google Scholar

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;114:619–31.Google Scholar

Sladky, JT, Rorke, LB. Perinatal hypoxic-ischemic spinal cord injury. Pediatr Pathol 1986;6:87–101.Google Scholar

Singer, R, Joseph, K, Gilai, AN, Meyer, S. Nontraumatic, acute neonatal paraplegia. J Pediatr Orthop 1991;11:588–93.CrossRef Google Scholar PubMed

Sheikh, A, Warren, D, Childs, A-M, Russell, J, Liddington, M, Guruswamy, V, Chumas, P. Paediatric spinal cord infarction – a review of the literature and two case reports. Childs Nerv Syst 2017;33:671–6.Google Scholar

Di Gioia, SA, Connors, S, Matsunami, N, Cannavino, J, Rose, MF, Gilette, NM, Artoni, P, de Macena Sobreira, NL, Chan, WM, Webb, BD, Robson, CD, Cheng, L, Van Ryzin, C, Ramirez-Martinez, A, Mohassel, P, Leppert, M, Scholand, MB, Grunseich, C, Ferreira, CR, Hartman, T, Hayes, IM, Morgan, T, Markie, DM, Fagiolini, M, Swift, A, Chines, PS, Speck-Martins, CE, Collins, FS, Jabs, EW, Bönnemann, CG, Olson, EN; Moebius Syndrome Research Consortium, Carey, JC, Robertson, SP, Manoli, I, Engle, EC. A defect in myoblast fusion underlies Carey-Fineman-Ziter syndrome. Nat Commun 2017;8:16077–93.CrossRef Google Scholar PubMed

Quattrocchi, CC, Longo, D, Delfino, LN, Cilio, MR, Piersigilli, F, Capua, MD, Seganti, G, Danhaive, O, Fariello, G. Dorsal brain stem syndrome: MR imaging location of brain stem tegmental lesions in neonates with oral motor dysfunction. AJNR Am J Neuroradiol 2010;31:1438–42.Google Scholar

de Léon, GA, Radkowski, MA, Crawford, SE, Swisher, CN, Uzoaru, I, de Léon, W. Persistent respiratory failure due to low cervical cord infarction in newborn babies. J Child Neurol 1995;10:200–4.Google Scholar

Clancy, RR, Sladky, JT, Rorke, LB. Hypoxic-ischemic spinal cord injury following perinatal asphyxia. Ann Neurol 1989;25:185–9.Google Scholar

Poretti, A, Boltshauser, E, Huisman, TA. Prenatal cerebellar disruptions: Neuroimaging spectrum of findings in correlation with likely mechanisms and etiologies of injury. Neuroimaging Clin N Am 2016;26:359–72.CrossRef Google Scholar PubMed

Mahieu-Caputo, D, Salomon, LJ, Dommergues, M, Aubry, MC, Sonigo, P, Martinovic, Y, Le Merrer, M, Dumez, Y, Encha-Razavi, F. Arthrogryposis multiplex congenita and cerebellopontine ischemic lesions in sibs: recurrence of prenatal disruptive brain lesions with different patterns of expression? Fetal Diagn Ther 2002;17:153–6.Google Scholar

Folkerth, RD, McLaughlin, ME, Levine, D. Organizing posterior fossa hematomas simulating developmental cysts on prenatal imaging: report of 3 cases. J Ultrasound Med 2001;20:1233–40.Google Scholar

Ebinger, F, Boor, R, Bruhl, K, Reitter, B. Cervical spinal cord atrophy in the atrumatically born neonate: one form of prenatal or perinatal ischaemic insult? Neuropediatrics 2003;34:45–51.Google Scholar

Jiang, ZD, Xu, X, Yin, R, Shao, XM, Wilkinson, AR. Differential changes in peripheral and central components of the brain stem auditory evoked potentials during the neonatal period in term infants after perinatal hypoxia-ischemia. Ann Otol Rhinol Laryngol 2004;113:571–6.Google Scholar

Groenendaal, F, Vles, J, Lammers, H, De Vente, J, Smit, D, Nikkels, PG. Nitrotyrosine in human neonatal spinal cord after perinatal asphyxia. Neonatology 2008;93:1–6.Google Scholar

van Bel, F, Groenendaal, F. Drugs for neuroprotection after birth asphyxia: Pharmacologic adjuncts to hypothermia. Semin Perinatl 2016;40:152–9.Google Scholar

References

Haynes, RL, Folkerth, RD. White matter lesions in the perinatal period. In: Developmental Neuropathology, 2nd ed., Adle-Biassette, H, Harding, BN, Golden, JA, eds. Boston: Wiley; 2018, pp. 213–27.Google Scholar

Hefti, MM, Trachtenberg, FL, Haynes, RL, Hassett, C, Volpe, JJ, Kinney, HC. A century of germinal matrix intraventricular hemorrhage in autopsied premature infants: A historical account. Pediatr Dev Pathol 2016;19:108–14.Google Scholar

Volpe, JJ. The encephalopathy of prematurity–brain injury and impaired brain development inextricably intertwined. Semin Pediatr Neurol 2009;16:167–78.Google Scholar

Benders, MJ, Kersbergen, KJ, de Vries, LS. Neuroimaging of white matter injury, intraventricular and cerebellar hemorrhage. Clin Perinatol 2014;41:69–82.Google Scholar

Buser, JR, Maire, J, Riddle, A, Gong, X, Nguyen, T, Nelson, K, Luo, NL, Ren, J, Struve, J, Sherman, LS, Miller, SP, Chau, V, Hendson, G, Ballabh, P, Grafe, MR, Back, SA. Arrested preoligodendrocyte maturation contributes to myelination failure in premature infants. Ann Neurol 2012;71:93–109.Google Scholar

Haynes, RL, Sleeper, LA, Volpe, JJ, Kinney, HC. Neuropathologic studies of the encephalopathy of prematurity in the late preterm infant. Clin Perinatol 2013;40:707–22.Google Scholar

Zupan, V, Gonzalez, P, Lacaze-Masmonteil, T, Boithias, C, d’Allest AM, Dehan M, Gabilan JC. Periventricular leukomalacia: risk factors revisited.Dev Med Child Neurol 1996;38:1061–7.Google Scholar

Huang, J, Zhang, L, Kang, B, Zhu, T, Li, Y, Zhao, F, Qu, Y, Mu, D. Association between perinatal hypoxia-ischemia and periventricular leukomalacia in preterm infants: A systematic review and meta-analysis. PLoS One. 2017;12(9):e0184993.Google Scholar

Volpe, JJ (2008) Neurology of the Newborn, 5th ed. Philadelphia: Saunders Elsevier.Google Scholar

Panigrahy, A, Wisnowski, JL, Furtado, A, Lepore, N, Paquette, L, Bluml, S. Neuroimaging biomarkers of preterm brain injury: toward developing the preterm connectome. Pediatr Radiol 2012 42 Suppl 1:S33–S61.Google Scholar

Ceschin, R, Lee, VK, Schmithorst, V, Panigrahy, A. Regional vulnerability of longitudinal cortical association connectivity: Associated with structural network topology alterations in preterm children with cerebral palsy. Neuroimage Clin 2015 9:322–37.Google Scholar

Inder, TE, Huppi, PS, Warfield, S, Kikinis, R, Zientara, GP, Barnes, PD, Jolesz, F, Volpe, JJ. Periventricular white matter injury in the premature infant is followed by reduced cerebral cortical gray matter volume at term. Ann Neurol 1999 46(5):755–60.Google Scholar

Jin, C, Londono, I, Mallard, C, Lodygensky, GA. New means to assess neonatal inflammatory brain injury. J Neuroinflammation 205;(12):180–95.Google Scholar

O’Shea, TM, Joseph, RM, Kuban, KCK, Allred, EN, Ware, J, Coster, T, Fichorova, R, Dammann, O, Leviton, A, for the ELGAN Study Investigators.Elevated blood levels of inflammation-related proteins are associated with an attention problem at age 24 months in extremely preterm infants. Pediatr Res 2014;75:781–7.Google Scholar

Leviton, A, Gilles, FH. Acquired perinatal leukoencephalopathy. Ann Neurol 1984;6:1–8.Google Scholar

Haynes, RL, Billiards, SS, Borenstein, NS, Volpe, JJ, Kinney, HC. Diffuse axonal injury in periventricular leukomalacia as determined by apoptotic marker fractin. Pediatr Res 2008;63:656–61.Google Scholar

References

Rorke, LB. Pathology of Perinatal Brain Injury. New York: Raven Press; 1982. p. 146.Google Scholar

Friede, RL. Hemorrhages in Asphyxiated Premature Infants: Developmental Neuropathology, 2nd rev. ed. Berlin: Springer-Verlag; 1989. pp. 44–58.Google Scholar

Leviton, A, Gilles, FH, Dooling, EC. The epidemiology of ganglionic eminence hemorrhage. In: Gilles, FH, Leviton, A, Dooling, EC, editors. The Developing Human Brain Growth and Epidemiologic Neuropathology. Boston: John Wright; 1983. pp. 204–16.Google Scholar

Leech, RW, Kohnen, P. Subependymal and intraventricular hemorrhages in the newborn. Am J Pathol. 1974;77(3):465–75.Google Scholar

Kutuk, MS, Yikilmaz, A, Ozgun, MT, Dolanbay, M, Canpolat, M, Uludag, S, et al. Prenatal diagnosis and postnatal outcome of fetal intracranial hemorrhage. Childs Nerv Syst. 2014;30(3):411–8.Google Scholar

Kirkinen, P, Partanen, K, Ryynanen, M, Orden, MR. Fetal intracranial hemorrhage. Imaging by ultrasound and magnetic resonance imaging. J Reprod Med. 1997;42(8):467–72.Google Scholar

Sanapo, L, Whitehead, MT, Bulas, DI, Ahmadzia, HK, Pesacreta, L, Chang, T, et al. Fetal intracranial hemorrhage: role of fetal MRI. Prenat Diagn. 2017;37(8):827–36.Google Scholar

Goto, T, Kakita, H, Takasu, M, Takeshita, S, Ueda, H, Muto, D, et al. A rare case of fetal extensive intracranial hemorrhage and whole-cerebral hypoplasia due to latent maternal vitamin K deficiency. J Neonatal Perinatal Med. 2018;11(2):191–4.Google Scholar

Burrows, RF, Caco, CC, Kelton, JG. Neonatal alloimmune thrombocytopenia: spontaneous in utero intracranial hemorrhage. Am J Hematol. 1988;28(2):98–102.CrossRef Google Scholar PubMed

Gherman, RB, Chauhan, SP. Placental abruption and fetal intraventricular hemorrhage after airbag deployment: a case report. J Reprod Med. 2014;59(9–10):501–3.Google Scholar

Kapur, RP, Shaw, CM, Shepard, TH. Brain hemorrhages in cocaine-exposed human fetuses. Teratology. 1991;44(1):11–18.Google Scholar

Tongsong, T, Sukpan, K, Wanapirak, C, Phadungkiatwattna, P. Fetal cytomegalovirus infection associated with cerebral hemorrhage, hydrops fetalis, and echogenic bowel: case report. Fetal Diagn Ther. 2008;23(3):169–72.Google Scholar

Matsumoto, T, Miyakoshi, K, Fukutake, M, Ochiai, D, Minegishi, K, Tanaka, M. Intracranial sonographic features demonstrating in utero development of hemorrhagic brain damage leading to schizencephaly-associated COL4A1 mutation. J Med Ultrason. (2001) 2015;42(3):445–6.Google Scholar

Kutuk, MS, Balta, B, Kodera, H, Matsumoto, N, Saitsu, H, Doganay, S, et al. Is there a relation between COL4A1/A2 mutations and antenatally detected fetal intraventricular hemorrhage? Childs Nerv Syst. 2014;30(3):419–24.Google Scholar

Huang, YF, Chen, WC, Tseng, JJ, Ho, ES, Chou, MM. Fetal intracranial hemorrhage (fetal stroke): report of four antenatally diagnosed cases and review of the literature. Taiwan J Obstet Gynecol. 2006;45(2):135–41.Google Scholar

Morioka, T, Hashiguchi, K, Nagata, S, Miyagi, Y, Mihara, F, Hikino, S, et al. Fetal germinal matrix and intraventricular hemorrhage. Pediatr Neurosurg. 2006;42(6):354–61.Google Scholar

Kim, KR, Jung, SW, Kim, DW. Risk factors associated with germinal matrix-intraventricular hemorrhage in preterm neonates. J Korean Neurosurg Soc. 2014;56(4):334–7.Google Scholar

Chevallier, M, Debillon, T, Pierrat, V, Delorme, P, Kayem, G, Durox, M, et al. Leading causes of preterm delivery as risk factors for intraventricular hemorrhage in very preterm infants: results of the EPIPAGE 2 cohort study. Am J Obstet Gynecol. 2017;216(5):518.e1–e12.Google Scholar

Lim, J, Hagen, E. Reducing germinal matrix-intraventricular hemorrhage: perinatal and delivery room factors. Neoreviews. 2019;20(8):e452–e63.Google Scholar

Poryo, M, Boeckh, JC, Gortner, L, Zemlin, M, Duppre, P, Ebrahimi-Fakhari, D, et al. Ante-, peri- and postnatal factors associated with intraventricular hemorrhage in very premature infants. Early Hum Dev. 2018;116:1–8.Google Scholar

Ment, LR, Aden, U, Lin, A, Kwon, SH, Choi, M, Hallman, M, et al. Gene-environment interactions in severe intraventricular hemorrhage of preterm neonates. Pediatr Res. 2014;75(1–2):241–50.Google Scholar

Rong, Z, Liu, H, Xia, S, Chang, L. Risk and protective factors of intraventricular hemorrhage in preterm babies in Wuhan, China. Childs Nerv Syst. 2012;28(12):2077–84.Google Scholar

Shalak, L, Perlman, JM. Hemorrhagic-ischemic cerebral injury in the preterm infant: current concepts. Clin Perinatol. 2002;29(4):745–63.Google Scholar

Ment, LR, Bada, HS, Barnes, P, Grant, PE, Hirtz, D, Papile, LA, et al. Practice parameter: neuroimaging of the neonate: report of the Quality Standards Subcommittee of the American Academy of Neurology and the Practice Committee of the Child Neurology Society. Neurology. 2002;58(12):1726–38.Google Scholar

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):529–34.Google Scholar

Intrapiromkul, J, Northington, F, Huisman, TA, Izbudak, I, Meoded, A, Tekes, A. Accuracy of head ultrasound for the detection of intracranial hemorrhage in preterm neonates: comparison with brain MRI and susceptibility-weighted imaging. J Neuroradiol. 2013;40(2):81–8.Google Scholar

Parodi, A, Morana, G, Severino, MS, Malova, M, Natalizia, AR, Sannia, A, et al. Low-grade intraventricular hemorrhage: is ultrasound good enough? J Matern Fetal Neonatal Med. 2015;28 Suppl 1:2261–4.Google Scholar

McCormick, MC, Litt, JS, Smith, VC, Zupancic, JA. Prematurity: an overview and public health implications. Annu Rev Public Health. 2011;32:367–79.Google Scholar

De Noronha, L, Medeiros, F, Nones, RB, Martins, VD, Sepulcri R de, P, Sampaio, GA, et al. Injúria hipóxico-isquêmica de padrao hemorrágico em encéfalos de neomortos do Hospital de Clínicas de Curitiba. Análise de 1028 casos de necrópsia entre 1960 e 1995. Arq Neuropsiquiatr. 1999;57(4):950–8.Google Scholar

Jammes, JL, Gilles, FH. Telencephalic development: matrix volume and isocortex and allocortex surface areas. In: Gilles, FH, Leviton, A, Dooling, EC, editors. The Developing Human Brain Growth and Epidemiologic Neuropathology. Boston: John Wright; 1983. pp. 87–93.Google Scholar

Terplan, KL. Histopathologic brain changes in 1152 cases of the perinatal and early infancy period. Biol Neonat. 1967;11:348–66.Google Scholar

Chen, HJ, Wei, KL, Zhou, CL, Yao, YJ, Yang, YJ, Fan, XF, et al. Incidence of brain injuries in premature infants with gestational age </= 34 weeks in ten urban hospitals in China. World J Pediatr. 2013;9(1):17–24.Google Scholar

Del Bigio, MR. Hemorrhagic lesions. In: Adle-Biassette, H, Harding, BN, Golden, JA, editors. Developmental Neuropathology, 2nd ed. Hoboken: John Wiley and Sons; 2018. p. 203–11.Google Scholar

Berger, R, Bender, S, Sefkow, S, Klingmuller, V, Kunzel, W, Jensen, A. Peri/intraventricular haemorrhage: a cranial ultrasound study on 5286 neonates. Eur J Obstet Gynecol Reprod Biol. 1997;75(2):191–203.Google Scholar

Ancel, PY, Goffinet, F, Kuhn, P, Langer, B, Matis, J, Hernandorena, X, et al. Survival and morbidity of preterm children born at 22 through 34 weeks’ gestation in France in 2011: results of the EPIPAGE-2 cohort study. JAMA Pediatr. 2015;169(3):230–8.Google Scholar

Sheth, RD. Trends in incidence and severity of intraventricular hemorrhage. J Child Neurol. 1998;13(6):261–4.Google Scholar

Groenendaal, F, Termote, J, van der Heide-Jalving, M, van Haastert, I, de Vries, L. Complications affecting preterm neonates from 1991 to 2006: what have we gained? Acta Paediatr. 2010;99(3):354–8.Google Scholar

Kuban, KC, Allred, EN, Dammann, O, Pagano, M, Leviton, A, Share, J, et al. Topography of cerebral white-matter disease of prematurity studied prospectively in 1607 very-low-birthweight infants. J Child Neurol. 2001;16(6):401–8.Google Scholar

Larroche, JC. Hémorragies cérébrales intra-ventriculaires chez le prématuré. Ie partie: anatomie at physiopathologie. Biol Neonat. 1964;91:26–56.Google Scholar

Shankaran, S. Hemorrhagic lesions of the central nervous system. In: Stevenson, DK, Benitz, WE, Sunshine, P, editors. Fetal and Neonatal Brain Injury, 3rd ed. Cambridge: Cambridge University Press; 2003. pp. 175–88.Google Scholar

Darrow, VC, Alvord, ECJ, Mack, LA, Hodson, WA. Histologic evaluation of the reactions to hemorrhage in the premature human infant’s brain. A combined ultrasound and autopsy study and a comparison with the reaction in adults. Am J Pathol. 1988;130:44–58.Google Scholar

Xue, M, Balasubramaniam, J, Del Bigio, MR. Brain inflammation following intracerebral hemorrhage. Current Neuropharmacol. 2003;1(4):325–32.Google Scholar

Towbin, A. Cerebral intraventricular hemorrhage and subependymal matrix infarction in the fetus and premature newborn. Am J Pathol. 1968;52(1):121–40.Google Scholar

Lategan, B, Chodirker, BN, Del Bigio, MR. Fetal hydrocephalus caused by cryptic intraventricular hemorrhage. Brain Pathol. 2010;20(2):391–8.Google Scholar

Dolfin, T, Skidmore, MB, Fong, KW, Hoskins, EM, Shennan, AT. Incidence, severity, and timing of subependymal and intraventricular hemorrhages in preterm infants born in a perinatal unit as detected by serial real-time ultrasound. Pediatrics. 1983;71(4):541–6.Google Scholar

Paneth, N, Pinto-Martin, J, Gardiner, J, Wallenstein, S, Katsikiotis, V, Hegyi, T, et al. Incidence and timing of germinal matrix/intraventricular hemorrhage in low birth weight infants. Am J Epidemiol. 1993;137(11):1167–76.Google Scholar

Ballabh, P. Pathogenesis and prevention of intraventricular hemorrhage. Clin Perinatol. 2014;41(1):47–67.CrossRef Google Scholar PubMed

Tortora, D, Severino, M, Malova, M, Parodi, A, Morana, G, Sedlacik, J, et al. Differences in subependymal vein anatomy may predispose preterm infants to GMH-IVH. Arch Dis Child Fetal Neonatal Ed. 2018;103:F59–F65.Google Scholar

Ghazi-Birry, HS, Brown, WR, Moody, DM, Challa, VR, Block, SM, Reboussin, DM. Human germinal matrix: venous origin of hemorrhage and vascular characteristics. AJNR Am J Neuroradiol. 1997;18(2):219–29.Google Scholar

Nakamura, Y, Okudera, T, Hashimoto, T. Microvasculature in germinal matrix layer: its relationship to germinal matrix hemorrhage. Mod Pathol. 1991;4(4):475–80.Google Scholar

Nakamura, Y, Okudera, T, Fukuda, S, Hashimoto, T. Germinal matrix hemorrhage of venous origin in preterm neonates. Hum Pathol. 1990;21(10):1059–62.Google Scholar

Ment, LR, Stewart, WB, Ardito, TA, Madri, JA. Germinal matrix microvascular maturation correlates inversely with the risk period for neonatal intraventricular hemorrhage. Dev Brain Res. 1995;84(1):142–9.Google Scholar

Del Bigio, MR. Cell proliferation in human ganglionic eminence and suppression after prematurity-associated haemorrhage. Brain. 2011;134(Pt 5):1344–61.Google Scholar

Alderliesten, T, Lemmers, PM, Smarius, JJ, van de Vosse, RE, Baerts, W, van Bel, F. Cerebral oxygenation, extraction, and autoregulation in very preterm infants who develop peri-intraventricular hemorrhage. J Pediatr. 2013;162(4):698–704.Google Scholar

McAllister, JP, Guerra, MM, Ruiz, LC, Jimenez, AJ, Dominguez-Pinos, D, Sival, D, et al. Ventricular zone disruption in human neonates with intraventricular hemorrhage. J Neuropathol Exp Neurol. 2017;76(5):358–75.Google Scholar

Folkerth, RD. Germinal matrix haemorrhage: destroying the brain’s building blocks. Brain. 2011;134(Pt 5):1261–3.Google Scholar

Bruschettini, M, Romantsik, O, Zappettini, S, Banzi, R, Ramenghi, LA, Calevo, MG. Antithrombin for the prevention of intraventricular hemorrhage in very preterm infants. Cochrane Database Syst Rev. 2016;3:CD011636.Google Scholar

Whitelaw, A, Lee-Kelland, R. Repeated lumbar or ventricular punctures in newborns with intraventricular haemorrhage. Cochrane Database Syst Rev. 2017;4:Cd000216.Google Scholar

Lekic, T, Klebe, D, Pichon, P, Brankov, K, Sultan, S, McBride, D, et al. Aligning animal models of clinical germinal matrix hemorrhage, from basic correlation to therapeutic approach. Curr Drug Targets. 2017;18(12):1316–28.Google Scholar

Flores, JJ, Klebe, D, Tang, J, Zhang, JH. A comprehensive review of therapeutic targets that induce microglia/macrophage-mediated hematoma resolution after germinal matrix hemorrhage. J Neurosci Res. 2020 98(1):121–128.Google Scholar

Klebe, D, McBride, D, Krafft, PR, Flores, JJ, Tang, J, Zhang, JH. Posthemorrhagic hydrocephalus development after germinal matrix hemorrhage: established mechanisms and proposed pathways. J Neurosci Res. 2020 98(1):105–120.Google Scholar

Larroque, B, Marret, S, Ancel, PY, Arnaud, C, Marpeau, L, Supernant, K, et al. White matter damage and intraventricular hemorrhage in very preterm infants: the EPIPAGE study. J Pediatr. 2003;143(4):477–83.Google Scholar

Gilles, FH, Leviton, A, Golden, JA, Paneth, N, Rudelli, RD. Groups of histopathologic abnormalities in brains of very low birthweight infants. J Neuropathol Exp Neurol. 1998;57(11):1026–34.Google Scholar

Wang, LW, Lin, YC, Tu, YF, Wang, ST, Huang, CC. Isolated cystic periventricular leukomalacia differs from cystic periventricular leukomalacia with intraventricular hemorrhage in prevalence, risk factors and outcomes in preterm infants. Neonatology. 2017;111(1):86–92.Google Scholar

Mito, T, Becker, LE, Perlman, M, Takashima, S. A neuropathologic analysis of neonatal deaths occurring in a single neonatal unit over a 20-year period. Pediatr Pathol. 1993;13(6):773–85.Google Scholar

Golden, JA, Gilles, FH, Rudelli, R, Leviton, A. Frequency of neuropathological abnormalities in very low birth weight infants. J Neuropathol Exp Neurol. 1997;56(5):472–8.Google Scholar

Armstrong, DL, Sauls, CD, Goddard-Finegold, J. Neuropathologic findings in short-term survivors of intraventricular hemorrhage. Am J Dis Child. 1987;141(6):617–21.Google Scholar

Babcock, DS, Bove, KE, Han, BK. Intracranial hemorrhage in premature infants: sonographic-pathologic correlation. AJNR Am J Neuroradiol. 1982;3(3):309–17.Google Scholar

Lun, MP, Monuki, ES, Lehtinen, MK. Development and functions of the choroid plexus-cerebrospinal fluid system. Nat Rev Neurosci. 2015;16(8):445–57.Google Scholar

Xiang, J, Routhe, LJ, Andrew Wilkinson, D, Hua, Y, Moos, T, Xi, G, et al. The choroid plexus as a site of damage in hemorrhagic and ischemic stroke and its role in responding to injury. Fluids Barriers CNS. 2017;14(1):8.Google Scholar

Haines, KM, Wang, W, Pierson, CR. Cerebellar hemorrhagic injury in premature infants occurs during a vulnerable developmental period and is associated with wider neuropathology. Acta Neuropathol Commun. 2013;1(1):69.Google Scholar

Pierson, CR, Al Sufiani, F. Preterm birth and cerebellar neuropathology. Semin Fetal Neonatal Med. 2016;21(5):305–11.Google Scholar

Kusters, CD, Chen, ML, Follett, PL, Dammann, O. “Intraventricular” hemorrhage and cystic periventricular leukomalacia in preterm infants: how are they related? J Child Neurol. 2009;24(9):1158–70.Google Scholar

Lin, PY, Hagan, K, Fenoglio, A, Grant, PE, Franceschini, MA. Reduced cerebral blood flow and oxygen metabolism in extremely preterm neonates with low-grade germinal matrix- intraventricular hemorrhage. Sci Rep. 2016;6:25903.Google Scholar

Goldstein, RF, Cotten, CM, Shankaran, S, Gantz, MG, Poole, WK. Influence of gestational age on death and neurodevelopmental outcome in premature infants with severe intracranial hemorrhage. J Perinatol. 2013;33(1):25–32.Google Scholar

Bolisetty, S, Dhawan, A, Abdel-Latif, M, Bajuk, B, Stack, J, Lui, K. Intraventricular hemorrhage and neurodevelopmental outcomes in extreme preterm infants. Pediatrics. 2014;133(1):55–62.Google Scholar

Fumagalli, M, Bassi, L, Sirgiovanni, I, Mosca, F, Sannia, A, Ramenghi, LA. From germinal matrix to cerebellar haemorrhage. J Matern Fetal Neonatal Med. 2015;28 Suppl 1:2280–5.Google Scholar

Reubsaet, P, Brouwer, AJ, van Haastert, IC, Brouwer, MJ, Koopman, C, Groenendaal, F, et al. The impact of low-grade germinal matrix-intraventricular hemorrhage on neurodevelopmental outcome of very preterm infants. Neonatology. 2017;112(3):203–10.Google Scholar

Ou, X, Glasier, CM, Ramakrishnaiah, RH, Mulkey, SB, Ding, Z, Angtuaco, TL, et al. Impaired white matter development in extremely low-birth-weight infants with previous brain hemorrhage. AJNR Am J Neuroradiol. 2014;35(10):1983–9.Google Scholar

Jeong, HJ, Shim, SY, Cho, HJ, Cho, SJ, Son, DW, Park, EA. Cerebellar development in preterm infants at term-equivalent age is impaired after low-grade intraventricular hemorrhage. J Pediatr. 2016;175:86–92 e2.Google Scholar

Sancak, S, Gursoy, T, Karatekin, G, Ovali, F. Effect of intraventricular hemorrhage on cerebellar growth in preterm neonates. Cerebellum. 2017;16(1):89–94.Google Scholar

Young, JM, Vandewouw, MM, Mossad, SI, Morgan, BR, Lee, W, Smith, ML, et al. White matter microstructural differences identified using multi-shell diffusion imaging in six-year-old children born very preterm. Neuroimage Clin. 2019;23:101855.Google Scholar

Dewan, MC, Rattani, A, Mekary, R, Glancz, LJ, Yunusa, I, Baticulon, RE, et al. Global hydrocephalus epidemiology and incidence: systematic review and meta-analysis. J Neurosurg. 2019; 130:1065–1079.Google Scholar

Nagra, G, Del Bigio, MR. Pathology of pediatric hydrocephalus. In: Cinalli, G, Özek, MM, Sainte-Rose, C, editors. Pediatric Hydrocephalus, 2nd ed. New York: Springer; 2019. pp. 359–77.Google Scholar

References

Volpe, JJ. Cerebellum of the premature infant – Rapidly developing, vulnerable, clinically important. J Child Neurol 2009; 24:1085–104.Google Scholar

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;116:717–24.Google Scholar

Pierson, CR, Folkerth, RD, Billards, SS, Trachtenberg, FL, et al. Gray matter injury associated with periventricular leukomalacia in the premature infant. Acta Neuropathol 2007;114:619–31.Google Scholar

Brouwer, AJ, Groenendaal, , Koopman, C, Nievelstein, R-JA, Han, SK, de Vries, LS. Intracranial hemorrhage in full-term newborns: a hospital-based cohort study. Neuroradiology 2010;52:567–76.Google Scholar

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;116:844–50.Google Scholar

Folkerth, RD, McLaughlin, ME, Levine, D. Organizing posterior fossa hematomas simulating developmental cysts on prenatal imaging: report of 3 cases. J Ultrasound Med 2001 20(11):1233–40.Google Scholar

Limperopoulos, C, Folkerth, R, Barnewolt, CE, Connolly, S, Du Plessis, AJ. Posthemorrhagic cerebellar disruption mimicking Dandy-Walker malformation: fetal imaging and neuropathology findings. Semin Pediatr Neurol 2010 17(1):75–81.Google Scholar

Book contents

Section 4 - Disruptions / Hypoxic-Ischemic Injury

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