{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,26]],"date-time":"2026-02-26T15:33:36Z","timestamp":1772120016410,"version":"3.50.1"},"reference-count":40,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2024,12,19]],"date-time":"2024-12-19T00:00:00Z","timestamp":1734566400000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"},{"start":{"date-parts":[[2024,12,19]],"date-time":"2024-12-19T00:00:00Z","timestamp":1734566400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/www.springernature.com\/gp\/researchers\/text-and-data-mining"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Cerebellum"],"DOI":"10.1007\/s12311-024-01765-z","type":"journal-article","created":{"date-parts":[[2024,12,19]],"date-time":"2024-12-19T03:53:09Z","timestamp":1734580389000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Uneven Distribution of Purkinje Cell Injury in the Cerebellar Vermis of Term Neonates with Hypoxic-Ischemic Encephalopathy"],"prefix":"10.1007","volume":"24","author":[{"given":"Kim V.","family":"Annink","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Ilona C. E.","family":"van Leeuwen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Nina A.","family":"Smeets","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Lianne A. J.","family":"Peeters","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Niek E.","family":"van der Aa","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Thomas","family":"Alderliesten","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Floris","family":"Groenendaal","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Reint K.","family":"Jellema","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Cora H. A.","family":"Nijboer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Peter G. J.","family":"Nikkels","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Martin","family":"Lammens","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Manon J. N. L.","family":"Benders","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Freek E.","family":"Hoebeek","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jeroen","family":"Dudink","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2024,12,19]]},"reference":[{"issue":"5","key":"1765_CR1","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1080\/14737175.2017.1259567","volume":"17","author":"EP Y\u0131ld\u0131z","year":"2017","unstructured":"Y\u0131ld\u0131z EP, Ekici B, Tatl\u0131 B. Neonatal hypoxic ischemic encephalopathy: an update on disease pathogenesis and treatment. Expert Rev Neurother. 2017;17(5):449\u201359.","journal-title":"Expert Rev Neurother"},{"issue":"2","key":"1765_CR2","doi-asserted-by":"publisher","first-page":"140","DOI":"10.1056\/NEJMoa1315788","volume":"371","author":"D Azzopardi","year":"2014","unstructured":"Azzopardi D, Strohm B, Marlow N, et al. Effects of hypothermia for perinatal asphyxia on childhood outcomes. N Engl J Med. 2014;371(2):140\u20139.","journal-title":"N Engl J Med"},{"issue":"1","key":"1765_CR3","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1186\/1471-2431-8-17","volume":"8","author":"D Azzopardi","year":"2008","unstructured":"Azzopardi D, Brocklehurst P, Edwards D, et al. The TOBY study. Whole body hypothermia for the treatment of perinatal asphyxial encephalopathy: a randomised controlled trial. BMC Pediatr. 2008;8(1):1\u201312.","journal-title":"BMC Pediatr."},{"issue":"1","key":"1765_CR4","doi-asserted-by":"publisher","first-page":"39","DOI":"10.1016\/S1474-4422(09)70295-9","volume":"9","author":"M Rutherford","year":"2010","unstructured":"Rutherford M, Ramenghi LA, Edwards AD, et al. Assessment of brain tissue injury after moderate hypothermia in neonates with hypoxic-ischaemic encephalopathy: a nested substudy of a randomised controlled trial. Lancet Neurol. 2010;9(1):39\u201345.","journal-title":"Lancet Neurol"},{"issue":"SUP","key":"1765_CR5","first-page":"163216","volume":"6","author":"JO Davidson","year":"2015","unstructured":"Davidson JO, Wassink G, van den Heuij LG, Bennet L, Gunn AJ. Therapeutic hypothermia for neonatal hypoxic-ischemic encephalopathy - where to from here? Front Neurol. 2015;6(SUP):163216.","journal-title":"Front Neurol"},{"key":"1765_CR6","doi-asserted-by":"crossref","unstructured":"Jacobs SE, Berg M, Hunt R, Tarnow-Mordi WO, Inder TE, Davis PG. Cooling for newborns with hypoxic ischaemic encephalopathy. Cochrane Database Syst Rev. 2013;2013(1):CD003311.","DOI":"10.1002\/14651858.CD003311.pub3"},{"issue":"7","key":"1765_CR7","doi-asserted-by":"publisher","first-page":"645","DOI":"10.1007\/s00431-007-0437-8","volume":"166","author":"HM Van","year":"2007","unstructured":"Van Handel M, Swaab H, De Vries LS, Jongmans MJ. Long-term cognitive and behavioral consequences of neonatal encephalopathy following perinatal asphyxia: a review. Eur J Pediatr. 2007;166(7):645\u201354.","journal-title":"Eur J Pediatr"},{"issue":"6","key":"1765_CR8","doi-asserted-by":"publisher","first-page":"555","DOI":"10.1007\/s00234-010-0674-9","volume":"52","author":"VLS De","year":"2010","unstructured":"De Vries LS, Groenendaal F. Patterns of neonatal hypoxic-ischaemic brain injury. Neuroradiology. 2010;52(6):555\u201366.","journal-title":"Neuroradiology"},{"key":"1765_CR9","first-page":"463","volume":"25","author":"E Le Strange","year":"2004","unstructured":"Le Strange E, Saeed N, Cowan F, Edwards A, Rutherford M. MR imaging quantification of cerebellar growth following hypoxic-ischemic injury to the neonatal brain. AJNR Am J Neuroradiol. 2004;25:463\u20138.","journal-title":"AJNR Am J Neuroradiol"},{"issue":"1","key":"1765_CR10","doi-asserted-by":"publisher","first-page":"60","DOI":"10.1093\/brain\/124.1.60","volume":"124","author":"M Allin","year":"2001","unstructured":"Allin M, Matsumoto H, Santhouse AM, et al. Cognitive and motor function and the size of the cerebellum in adolescents born very pre-term. Brain. 2001;124(1):60\u20136.","journal-title":"Brain"},{"issue":"2","key":"1765_CR11","doi-asserted-by":"publisher","first-page":"552","DOI":"10.1007\/s12311-016-0815-8","volume":"16","author":"M Adamaszek","year":"2016","unstructured":"Adamaszek M, D\u2019Agata F, Ferrucci R, et al. Consensus Paper: Cerebellum and Emotion. Cerebellum. 2016;16(2):552\u201376.","journal-title":"Cerebellum"},{"issue":"3","key":"1765_CR12","doi-asserted-by":"publisher","first-page":"518","DOI":"10.1016\/j.neuron.2014.07.016","volume":"83","author":"SSH Wang","year":"2014","unstructured":"Wang SSH, Kloth AD, Badura A. The cerebellum, sensitive periods, and autism. Neuron. 2014;83(3):518\u201332.","journal-title":"Neuron"},{"key":"1765_CR13","doi-asserted-by":"crossref","unstructured":"Hortensius LM, Dijkshoorn ABC, Ecury-Goossen GM, et al. Neurodevelopmental consequences of preterm isolated cerebellar hemorrhage: a systematic review. Pediatrics. 2018;142(5):e20180609.","DOI":"10.1542\/peds.2018-0609"},{"issue":"1","key":"1765_CR14","first-page":"858929","volume":"2012","author":"V Biran","year":"2012","unstructured":"Biran V, Verney C, Ferriero DM. Perinatal cerebellar injury in human and animal models. Neurol Res Int. 2012;2012(1):858929.","journal-title":"Neurol Res Int"},{"issue":"9","key":"1765_CR15","doi-asserted-by":"publisher","first-page":"1085","DOI":"10.1177\/0883073809338067","volume":"24","author":"JJ Volpe","year":"2009","unstructured":"Volpe JJ. Cerebellum of the premature infant: rapidly developing, vulnerable, clinically important. J Child Neurol. 2009;24(9):1085\u2013104.","journal-title":"J Child Neurol"},{"issue":"2","key":"1765_CR16","doi-asserted-by":"publisher","first-page":"72","DOI":"10.1055\/s-2003-39599","volume":"34","author":"RJ Vermeulen","year":"2003","unstructured":"Vermeulen RJ, Fetter WPF, Hendrikx L, Van Schie PEM, van der Knaap MS, Berkhof F. Diffusion-weighted MRI in severe neonatal hypoxic ischaemia: the white cerebrum. Neuropediatrics. 2003;34(2):72\u20136.","journal-title":"Neuropediatrics"},{"issue":"2","key":"1765_CR17","doi-asserted-by":"publisher","first-page":"264","DOI":"10.3174\/ajnr.A1318","volume":"30","author":"L Liauw","year":"2009","unstructured":"Liauw L, Van Wezel-Meijer G, Veen S, Van Buchem MA, Van Der Grond J. Do apparent diffusion coefficient measurements predict outcome in children with neonatal hypoxic-ischemic encephalopathy? Am J Neuroradiol. 2009;30(2):264\u201370.","journal-title":"Am J Neuroradiol"},{"issue":"5","key":"1765_CR18","doi-asserted-by":"publisher","first-page":"1171","DOI":"10.1038\/s41390-020-01173-z","volume":"89","author":"KV Annink","year":"2020","unstructured":"Annink KV, Meerts L, van der Aa NE, et al. Cerebellar injury in term neonates with hypoxic\u2013ischemic encephalopathy is underestimated. Pediatr Res. 2020;89(5):1171\u20138.","journal-title":"Pediatr Res"},{"issue":"3","key":"1765_CR19","doi-asserted-by":"publisher","first-page":"175","DOI":"10.1007\/s00414-006-0122-x","volume":"121","author":"R Hausmann","year":"2007","unstructured":"Hausmann R, Seidl S, Betz P. Hypoxic changes in Purkinje cells of the human cerebellum. Int J Legal Med. 2007;121(3):175\u201383.","journal-title":"Int J Legal Med"},{"issue":"2","key":"1765_CR20","doi-asserted-by":"publisher","first-page":"312","DOI":"10.1016\/j.neuron.2016.05.037","volume":"91","author":"L Witter","year":"2016","unstructured":"Witter L, Rudolph S, Pressler RT, Lahlaf SI, Regehr WG. Purkinje cell collaterals enable output signals from the cerebellar cortex to feed back to Purkinje cells and interneurons. Neuron. 2016;91(2):312\u20139.","journal-title":"Neuron"},{"issue":"3","key":"1765_CR21","doi-asserted-by":"publisher","first-page":"245","DOI":"10.1016\/S0168-0102(01)00234-6","volume":"40","author":"P Barenberg","year":"2001","unstructured":"Barenberg P, Strahlendorf H, Strahlendorf J. Hypoxia induces an excitotoxic-type of dark cell degeneration in cerebellar Purkinje neurons. Neurosci Res. 2001;40(3):245\u201354.","journal-title":"Neurosci Res"},{"key":"1765_CR22","doi-asserted-by":"publisher","first-page":"106901","DOI":"10.1016\/j.nlm.2018.07.005","volume":"165","author":"Z Zhang","year":"2019","unstructured":"Zhang Z, Narayan S, Su L, Al-Alawyat H, Liu J, Kannan S. Cerebellar injury and impaired function in a rabbit model of maternal inflammation induced neonatal brain injury. Neurobiol Learn Mem. 2019;165:106901.","journal-title":"Neurobiol Learn Mem"},{"issue":"1","key":"1765_CR23","doi-asserted-by":"publisher","first-page":"29","DOI":"10.1006\/exnr.2001.7855","volume":"174","author":"BWDJ Van De","year":"2002","unstructured":"Van de Berg WDJ, Schmitz C, Steinbusch HWM, Blanco CE. Perinatal asphyxia induced neuronal loss by apoptosis in the neonatal rat striatum: a combined TUNEL and stereological study. Exp Neurol. 2002;174(1):29\u201336.","journal-title":"Exp Neurol"},{"issue":"1","key":"1765_CR24","doi-asserted-by":"publisher","first-page":"87","DOI":"10.1016\/j.devbrainres.2005.02.002","volume":"156","author":"JHF Peng","year":"2005","unstructured":"Peng JHF, Feng Y, LeBlanc MH, Rhodes PG, Parker JC. Apoptosis and necrosis in developing cerebellum and brainstem induced after focal cerebral hypoxic\u2013ischemic injury. Dev Brain Res. 2005;156(1):87\u201392.","journal-title":"Dev Brain Res"},{"issue":"2","key":"1765_CR25","doi-asserted-by":"publisher","first-page":"79","DOI":"10.1038\/nrn3886","volume":"16","author":"NL Cerminara","year":"2015","unstructured":"Cerminara NL, Lang EJ, Sillitoe RV, Apps R. Redefining the cerebellar cortex as an assembly of non-uniform Purkinje cell microcircuits. Nat Rev Neurosci. 2015;16(2):79\u201393.","journal-title":"Nat Rev Neurosci"},{"issue":"1","key":"1765_CR26","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1002\/cne.901090102","volume":"109","author":"V Braitenberg","year":"1958","unstructured":"Braitenberg V, Atwood RP. Morphological observations on the cerebellar cortex. J Comp Neurol. 1958;109(1):1\u201333.","journal-title":"J Comp Neurol"},{"issue":"4","key":"1765_CR27","doi-asserted-by":"publisher","first-page":"F304","DOI":"10.1136\/archdischild-2012-301768","volume":"98","author":"T Alderliesten","year":"2013","unstructured":"Alderliesten T, Nikkels PGJ, Benders MJNL, 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\u20139.","journal-title":"Arch Dis Child Fetal Neonatal Ed"},{"issue":"4","key":"1765_CR28","doi-asserted-by":"publisher","first-page":"449","DOI":"10.1002\/cne.901390405","volume":"139","author":"DM Armstrong","year":"1970","unstructured":"Armstrong DM, Schild RF. A quantitative study of the Purkinje cells in the cerebellum of the albino rat. J Comp Neurol. 1970;139(4):449\u201356.","journal-title":"J Comp Neurol"},{"issue":"2","key":"1765_CR29","doi-asserted-by":"publisher","first-page":"99","DOI":"10.1111\/j.1440-1789.1993.tb00219.x","volume":"13","author":"M Akima","year":"1993","unstructured":"Akima M. A morphological study on the microcirculation of the central nervous system. Selective vulnerability to hypoxia. Neuropathology. 1993;13(2):99\u2013112.","journal-title":"Neuropathology"},{"issue":"1","key":"1765_CR30","doi-asserted-by":"publisher","first-page":"69","DOI":"10.1007\/BF00686795","volume":"75","author":"M Akima","year":"1987","unstructured":"Akima M, Nonaka H, Kagesawa M, Tanaka K. A study on the microvasculature of the cerebellar cortex - the fundamental architecture and its senile change in the cerebellar hemisphere. Acta Neuropathol. 1987;75(1):69\u201376.","journal-title":"Acta Neuropathol"},{"issue":"6","key":"1765_CR31","doi-asserted-by":"publisher","first-page":"608","DOI":"10.1007\/s00401-002-0592-y","volume":"104","author":"H Nonaka","year":"2002","unstructured":"Nonaka H, Akima M, Hatori T, Nagayama T, Zhang Z, Ihara F. The microvasculature of the human cerebellar meninges. Acta Neuropathol. 2002;104(6):608\u201314.","journal-title":"Acta Neuropathol"},{"issue":"3","key":"1765_CR32","doi-asserted-by":"publisher","first-page":"566","DOI":"10.1007\/BF02047152","volume":"31","author":"Bresler","year":"1899","unstructured":"Bresler. Klinische und pathologisch-anatomische Beitr\u00e4ge zur Mikrogyrie. Arch Psychiatr Nervenkr. 1899;31(3):566\u201373.","journal-title":"Arch Psychiatr Nervenkr"},{"issue":"3","key":"1765_CR33","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1016\/S0920-1211(03)00121-9","volume":"55","author":"F Villani","year":"2003","unstructured":"Villani F, D\u2019Incerti L, Granata T, et al. Epileptic and imaging findings in perinatal hypoxic-ischemic encephalopathy with ulegyria. Epilepsy Res. 2003;55(3):235\u201343.","journal-title":"Epilepsy Res"},{"issue":"1","key":"1765_CR34","doi-asserted-by":"publisher","first-page":"51","DOI":"10.1177\/0883073807308694","volume":"23","author":"I Nikas","year":"2007","unstructured":"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. 2007;23(1):51\u20138.","journal-title":"J Child Neurol"},{"issue":"4","key":"1765_CR35","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1007\/BF00690375","volume":"53","author":"MG Norman","year":"1981","unstructured":"Norman MG. On the morphogenesis of ulegyria. Acta Neuropathol. 1981;53(4):331\u20132.","journal-title":"Acta Neuropathol"},{"issue":"3","key":"1765_CR36","doi-asserted-by":"publisher","first-page":"472","DOI":"10.1016\/S0022-3476(77)81328-0","volume":"91","author":"JJ Volpe","year":"1977","unstructured":"Volpe JJ, Pasternak JF. Parasagittal cerebral injury in neonatal hypoxic-ischemic encephalopathy: clinical and neuroradiologic features. J Pediatr. 1977;91(3):472\u20136.","journal-title":"J Pediatr"},{"key":"1765_CR37","first-page":"82","volume-title":"Developmental Neuropathology","author":"R Friede","year":"2012","unstructured":"Friede R. Developmental Neuropathology. New York: Springer Verlag. Published online; 2012. p. 82\u201397."},{"issue":"4","key":"1765_CR38","doi-asserted-by":"publisher","first-page":"209","DOI":"10.4103\/2349-0977.191041","volume":"2","author":"M Kumar","year":"2016","unstructured":"Kumar M, Gupta R, Kaul B, Agarwal Y. Recognizing ulegyria\u2014the lesser known form of hypoxic ischemic encephalopathy. Astrocyte. 2016;2(4):209.","journal-title":"Astrocyte"},{"issue":"5","key":"1765_CR39","doi-asserted-by":"publisher","first-page":"547","DOI":"10.1136\/jnnp.2007.118216","volume":"79","author":"G Kuchukhidze","year":"2008","unstructured":"Kuchukhidze G, Unterberger I, Dobesberger J, et al. Electroclinical and imaging findings in ulegyria and epilepsy: a study on 25 patients. J Neurol Neurosurg Psychiatry. 2008;79(5):547\u201352.","journal-title":"J Neurol Neurosurg Psychiatry"},{"issue":"1","key":"1765_CR40","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1038\/s41598-023-49211-0","volume":"13","author":"CQ Wu","year":"2023","unstructured":"Wu CQ, Cowan FM, Jary S, Thoresen M, Chakkarapani E, Spencer APC. Cerebellar growth, volume and diffusivity in children cooled for neonatal encephalopathy without cerebral palsy. Sci Rep. 2023;13(1):1\u201311.","journal-title":"Sci Rep"}],"container-title":["The Cerebellum"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12311-024-01765-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s12311-024-01765-z\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12311-024-01765-z.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,1,22]],"date-time":"2025-01-22T13:08:31Z","timestamp":1737551311000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s12311-024-01765-z"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,12,19]]},"references-count":40,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2025,2]]}},"alternative-id":["1765"],"URL":"https:\/\/doi.org\/10.1007\/s12311-024-01765-z","relation":{"has-preprint":[{"id-type":"doi","id":"10.1101\/2020.04.15.043018","asserted-by":"object"}]},"ISSN":["1473-4230"],"issn-type":[{"value":"1473-4230","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,12,19]]},"assertion":[{"value":"25 October 2024","order":1,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"19 December 2024","order":2,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The Medical Ethical Committee (MEC) of UMC Utrecht confirmed that the \u2018Medical Research Involving Human Subjects Act\u2019 did not apply to this study and therefore an official approval of the MEC and informed consent was not required (MEC # 18\u2013167). The UMC Utrecht biobank approved the use of the residual tissue (biobank # 18\u2013284). This study was conducted in accordance with the Declaration of Helsinki.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethical Approval"}},{"value":"The authors declare no competing interests.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing Interests"}}],"article-number":"17"}}