{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,26]],"date-time":"2026-02-26T19:59:57Z","timestamp":1772135997607,"version":"3.50.1"},"reference-count":36,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2022,1,7]],"date-time":"2022-01-07T00:00:00Z","timestamp":1641513600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,1,7]],"date-time":"2022-01-07T00:00:00Z","timestamp":1641513600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Sci Rep"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>\n                    We investigated the characteristics of midbrain injuries in patients with spontaneous subarachnoid hemorrhage (SAH) by using diffusion tensor imaging (DTI). Twenty-seven patients with SAH and 25 healthy control subjects were recruited for this study. Fractional anisotropy (FA) and mean diffusivity (MD) data were obtained for four regions of the midbrain (the anterior ventral midbrain, posterior ventral midbrain, tegmentum area, and tectum) in 27 hemispheres that did not show any pathology other than SAH. The mean FA and MD values of the four regions of the midbrain (anterior ventral midbrain, posterior ventral midbrain, tegmentum, and tectum) of the patient group were significantly lower and higher than those of the control group, respectively (\n                    <jats:italic>p<\/jats:italic>\n                    \u2009&lt;\u20090.05). The mean FA values of the patient group were significantly different among the anterior ventral midbrain, posterior ventral midbrain, tegmentum, and tectum regions (ANOVA; F\u2009=\u20093.22,\n                    <jats:italic>p<\/jats:italic>\n                    \u2009&lt;\u20090.05). Post hoc testing showed that the mean FA value of the anterior ventral midbrain was significantly lower than those of the posterior ventral midbrain, tegmentum, and tectum (\n                    <jats:italic>p<\/jats:italic>\n                    \u2009&lt;\u20090.05); in contrast, there were no differences in mean FA values of the posterior ventral midbrain, tegmentum, and tectum (\n                    <jats:italic>p<\/jats:italic>\n                    \u2009&gt;\u20090.05). However, differences were not observed among four regions of the midbrain (anterior ventral midbrain, posterior ventral midbrain, tegmentum, and tectum) in the mean MD values. We detected evidence of neural injury in all four regions of the midbrain of patients with SAH, and the anterior ventral midbrain was the most severely injured among four regions of the midbrain. Our results suggest that a pathophysiological mechanism of these neural injuries might be related to the occurrence of a subarachnoid hematoma.\n                  <\/jats:p>","DOI":"10.1038\/s41598-021-03747-1","type":"journal-article","created":{"date-parts":[[2022,1,7]],"date-time":"2022-01-07T06:03:21Z","timestamp":1641535401000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":2,"title":["Midbrain injury in patients with subarachnoid hemorrhage: a diffusion tensor imaging study"],"prefix":"10.1038","volume":"12","author":[{"given":"Sung Ho","family":"Jang","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Young Hyeon","family":"Kwon","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2022,1,7]]},"reference":[{"key":"3747_CR1","doi-asserted-by":"publisher","first-page":"355","DOI":"10.1016\/S1474-4422(09)70025-0","volume":"8","author":"VL Feigin","year":"2009","unstructured":"Feigin, V. L., Lawes, C. M., Bennett, D. A., Barker-Collo, S. L. & Parag, V. Worldwide stroke incidence and early case fatality reported in 56 population-based studies: A systematic review. Lancet Neurol. 8, 355\u2013369 (2009).","journal-title":"Lancet Neurol."},{"key":"3747_CR2","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1016\/S0140-6736(16)30668-7","volume":"389","author":"RL Macdonald","year":"2017","unstructured":"Macdonald, R. L. & Schweizer, T. A. Spontaneous subarachnoid haemorrhage. Lancet 389, 655\u2013666 (2017).","journal-title":"Lancet"},{"key":"3747_CR3","doi-asserted-by":"publisher","first-page":"387","DOI":"10.1056\/NEJMra052732","volume":"354","author":"JI Suarez","year":"2006","unstructured":"Suarez, J. I., Tarr, R. W. & Selman, W. R. Aneurysmal subarachnoid hemorrhage. N. Engl. J. Med. 354, 387\u2013396 (2006).","journal-title":"N. Engl. J. Med."},{"key":"3747_CR4","doi-asserted-by":"publisher","first-page":"306","DOI":"10.1016\/S0140-6736(07)60153-6","volume":"369","author":"J van Gijn","year":"2007","unstructured":"van Gijn, J., Kerr, R. S. & Rinkel, G. J. Subarachnoid haemorrhage. Lancet 369, 306\u2013318 (2007).","journal-title":"Lancet"},{"key":"3747_CR5","doi-asserted-by":"publisher","first-page":"819","DOI":"10.1227\/NEU.0b013e3182367124","volume":"70","author":"JH Hong","year":"2012","unstructured":"Hong, J. H. et al. Injuries of the cingulum and fornix after rupture of an anterior communicating artery aneurysm: A diffusion tensor tractography study. Neurosurgery 70, 819\u2013823 (2012).","journal-title":"Neurosurgery"},{"key":"3747_CR6","doi-asserted-by":"publisher","first-page":"798","DOI":"10.1016\/j.clineuro.2011.12.045","volume":"114","author":"TA Schweizer","year":"2012","unstructured":"Schweizer, T. A., Al-Khindi, T. & Loch, M. R. Diffusion tensor imaging as a surrogate marker for outcome after perimesencephalic subarachnoid hemorrhage. Clin. Neurol. Neurosurg. 114, 798\u2013800 (2012).","journal-title":"Clin. Neurol. Neurosurg."},{"key":"3747_CR7","doi-asserted-by":"publisher","first-page":"2239","DOI":"10.1161\/STROKEAHA.112.661116","volume":"43","author":"SS Yeo","year":"2012","unstructured":"Yeo, S. S. et al. Evidence of corticospinal tract injury at midbrain in patients with subarachnoid hemorrhage. Stroke 43, 2239\u20132241 (2012).","journal-title":"Stroke"},{"key":"3747_CR8","doi-asserted-by":"publisher","first-page":"e005613","DOI":"10.1136\/bmjopen-2014-005613","volume":"4","author":"SH Jang","year":"2014","unstructured":"Jang, S. H. et al. Injury of the mammillothalamic tract in patients with subarachnoid haemorrhage: A retrospective diffusion tensor imaging study. BMJ Open 4, e005613 (2014).","journal-title":"BMJ Open"},{"key":"3747_CR9","doi-asserted-by":"publisher","first-page":"133","DOI":"10.2340\/16501977-1896","volume":"47","author":"SH Jang","year":"2015","unstructured":"Jang, S. H. et al. Injury of the corticoreticular pathway in subarachnoid haemorrhage after rupture of a cerebral artery aneurysm. J. Rehabil. Med. 47, 133\u2013137 (2015).","journal-title":"J. Rehabil. Med."},{"key":"3747_CR10","doi-asserted-by":"publisher","first-page":"667","DOI":"10.3174\/ajnr.A4203","volume":"36","author":"SH Jang","year":"2015","unstructured":"Jang, S. H. & Kim, H. S. Aneurysmal subarachnoid hemorrhage causes injury of the ascending reticular activating system: Relation to consciousness. AJNR Am. J. Neuroradiol. 36, 667\u2013671 (2015).","journal-title":"AJNR Am. J. Neuroradiol."},{"key":"3747_CR11","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1007\/s13760-016-0602-9","volume":"116","author":"SH Jang","year":"2016","unstructured":"Jang, S. H. & Yeo, S. S. Injury of the Papez circuit in a patient with provoked confabulation following subarachnoid hemorrhage: A diffusion tensor tractography study. Acta Neurol. Belg. 116, 655\u2013658 (2016).","journal-title":"Acta Neurol. Belg."},{"key":"3747_CR12","doi-asserted-by":"publisher","first-page":"e7356","DOI":"10.1097\/MD.0000000000007356","volume":"96","author":"SH Jang","year":"2017","unstructured":"Jang, S. H. & Seo, J. P. Injury of optic radiation and visual field defect in a patient with aneurysmal subarachnoid hemorrhage: A case report. Medicine 96, e7356 (2017).","journal-title":"Medicine"},{"key":"3747_CR13","doi-asserted-by":"publisher","first-page":"e624","DOI":"10.1016\/j.wneu.2018.03.042","volume":"114","author":"R Darwazeh","year":"2018","unstructured":"Darwazeh, R. et al. Significant injury of the mammillothalamic tract without injury of the corticospinal tract after aneurysmal subarachnoid hemorrhage: A retrospective diffusion tensor imaging study. World Neurosurg. 114, e624\u2013e630 (2018).","journal-title":"World Neurosurg."},{"key":"3747_CR14","doi-asserted-by":"publisher","first-page":"563","DOI":"10.4103\/1673-5374.228763","volume":"13","author":"SH Jang","year":"2018","unstructured":"Jang, S. H., Chang, C. H., Jung, Y. J., Kim, S. H. & Seo, J. P. Optic radiation injury in patients with aneurismal subarachnoid hemorrhage: A preliminary diffusion tensor imaging report. Neural Regen. Res. 13, 563\u2013566 (2018).","journal-title":"Neural Regen. Res."},{"key":"3747_CR15","doi-asserted-by":"publisher","first-page":"e98","DOI":"10.1016\/j.jstrokecerebrovasdis.2017.12.045","volume":"27","author":"SH Jang","year":"2018","unstructured":"Jang, S. H. & Yeo, S. S. Injury of the precommissural fornix in a patient with subarachnoid hemorrhage: A case report. J. Stroke Cerebrovasc. Dis. 27, e98\u2013e101 (2018).","journal-title":"J. Stroke Cerebrovasc. Dis."},{"key":"3747_CR16","doi-asserted-by":"publisher","first-page":"2040","DOI":"10.1161\/STROKEAHA.118.021622","volume":"49","author":"YD Reijmer","year":"2018","unstructured":"Reijmer, Y. D. et al. Microstructural white matter abnormalities and cognitive impairment after aneurysmal subarachnoid hemorrhage. Stroke 49, 2040\u20132045 (2018).","journal-title":"Stroke"},{"key":"3747_CR17","doi-asserted-by":"publisher","first-page":"1117","DOI":"10.1007\/s007010070039","volume":"142","author":"S Kawamura","year":"2000","unstructured":"Kawamura, S., Suzuki, A., Hadeishi, H., Yasui, N. & Hatazawa, J. Cerebral blood flow and oxygen metabolism during mild hypothermia in patients with subarachnoid haemorrhage. Acta Neurochir. 142, 1117\u20131121 (2000) (discussion 1121\u20131112).","journal-title":"Acta Neurochir."},{"key":"3747_CR18","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1046\/j.0001-6314.2003.00189.x","volume":"109","author":"L Brandt","year":"2004","unstructured":"Brandt, L., Saveland, H., Valdemarsson, S., Sjoholm, H. & Reinstrup, P. Fatigue after aneurysmal subarachnoid hemorrhage evaluated by pituitary function and 3D-CBF. Acta Neurol. Scand. 109, 91\u201396 (2004).","journal-title":"Acta Neurol. Scand."},{"key":"3747_CR19","doi-asserted-by":"publisher","first-page":"15","DOI":"10.3109\/02699052.2013.847209","volume":"28","author":"K Uchikawa","year":"2014","unstructured":"Uchikawa, K. et al. Executive dysfunction is related with decreased frontal lobe blood flow in patients with subarachnoid haemorrhage. Brain Inj. 28, 15\u201319 (2014).","journal-title":"Brain Inj."},{"key":"3747_CR20","doi-asserted-by":"publisher","first-page":"1538","DOI":"10.1007\/s11682-016-9609-3","volume":"11","author":"J Plata-Bello","year":"2017","unstructured":"Plata-Bello, J. et al. Subarachnoid hemorrhage and visuospatial and visuoperceptive impairment: Disruption of the mirror neuron system. Brain Imaging Behav. 11, 1538\u20131547 (2017).","journal-title":"Brain Imaging Behav."},{"key":"3747_CR21","doi-asserted-by":"publisher","first-page":"247","DOI":"10.1006\/jmrb.1994.1037","volume":"103","author":"PJ Basser","year":"1994","unstructured":"Basser, P. J., Mattiello, J. & LeBihan, D. Estimation of the effective self-diffusion tensor from the NMR spin echo. J. Magn. Reson. B. 103, 247\u2013254 (1994).","journal-title":"J. Magn. Reson. B."},{"key":"3747_CR22","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1002\/1531-8249(199902)45:2<265::AID-ANA21>3.0.CO;2-3","volume":"45","author":"S Mori","year":"1999","unstructured":"Mori, S., Crain, B. J., Chacko, V. P. & van Zijl, P. C. Three-dimensional tracking of axonal projections in the brain by magnetic resonance imaging. Ann. Neurol. 45, 265\u2013269 (1999).","journal-title":"Ann. Neurol."},{"key":"3747_CR23","doi-asserted-by":"publisher","first-page":"316","DOI":"10.1016\/j.nurt.2007.05.011","volume":"4","author":"AL Alexander","year":"2007","unstructured":"Alexander, A. L., Lee, J. E., Lazar, M. & Field, A. S. Diffusion tensor imaging of the brain. Neurotherapeutics 4, 316\u2013329 (2007).","journal-title":"Neurotherapeutics"},{"key":"3747_CR24","doi-asserted-by":"publisher","first-page":"130","DOI":"10.1007\/s00330-007-0733-8","volume":"18","author":"A Stadlbauer","year":"2008","unstructured":"Stadlbauer, A., Salomonowitz, E., Strunk, G., Hammen, T. & Ganslandt, O. Quantitative diffusion tensorfiber tracking of age-related changes in the limbic system. Eur. Radiol. 18, 130\u2013137 (2008).","journal-title":"Eur. Radiol."},{"key":"3747_CR25","doi-asserted-by":"publisher","first-page":"493","DOI":"10.1212\/WNL.35.4.493","volume":"35","author":"J van Gijn","year":"1985","unstructured":"van Gijn, J., Van Dongen, K. J., Vermeulen, M. & Hijdra, A. Perimesencephalic hemorrhage: A nonaneurysmal and benign form of subarachnoid hemorrhage. Neurology 35, 493\u2013497 (1985).","journal-title":"Neurology"},{"key":"3747_CR26","first-page":"129","volume-title":"The Human Central Nervous System","author":"R Nieuwenhuys","year":"2007","unstructured":"Nieuwenhuys, R., Voogd, J. & Huijzen, C. V. The Human Central Nervous System 4th edn, 129 (Springer, 2007).","edition":"4"},{"key":"3747_CR27","first-page":"258524","volume":"2012","author":"K Ruchalski","year":"2012","unstructured":"Ruchalski, K. & Hathout, G. M. A medley of midbrain maladies: A brief review of midbrain anatomy and syndromology for radiologists. Radiol. Res. Pract. 2012, 258524 (2012).","journal-title":"Radiol. Res. Pract."},{"key":"3747_CR28","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/B978-0-443-10321-6.00003-5","volume-title":"Clinical Neuroscience, 1st","author":"P Johns","year":"2014","unstructured":"Johns, P. Clinical Neuroscience, 1st 27 (Churchill Livingstone, 2014)."},{"key":"3747_CR29","doi-asserted-by":"publisher","first-page":"45","DOI":"10.1212\/WNL.45.1.45","volume":"45","author":"KA Greene","year":"1995","unstructured":"Greene, K. A. et al. Anterior communicating artery aneurysm paraparesis syndrome: Clinical manifestations and pathologic correlates. Neurology 45, 45\u201350 (1995).","journal-title":"Neurology"},{"key":"3747_CR30","doi-asserted-by":"publisher","first-page":"518","DOI":"10.1148\/radiol.2422051698","volume":"242","author":"Y Liu","year":"2007","unstructured":"Liu, Y. et al. Subarachnoid hemorrhage in the subacute stage: Elevated apparent diffusion coefficient in normal-appearing brain tissue after treatment. Radiology 242, 518\u2013525 (2007).","journal-title":"Radiology"},{"key":"3747_CR31","doi-asserted-by":"publisher","first-page":"3369","DOI":"10.1161\/STROKEAHA.109.549212","volume":"40","author":"CO Chua","year":"2009","unstructured":"Chua, C. O. et al. Consequences of intraventricular hemorrhage in a rabbit pup model. Stroke 40, 3369\u20133377 (2009).","journal-title":"Stroke"},{"key":"3747_CR32","doi-asserted-by":"publisher","first-page":"235","DOI":"10.1159\/000330942","volume":"66","author":"SS Yeo","year":"2011","unstructured":"Yeo, S. S. et al. Periventricular white matter injury by primary intraventricular hemorrhage: A diffusion tensor imaging study. Eur. Neurol. 66, 235\u2013241 (2011).","journal-title":"Eur. Neurol."},{"key":"3747_CR33","doi-asserted-by":"publisher","first-page":"2608","DOI":"10.1093\/brain\/awv180","volume":"138","author":"TT Kummer","year":"2015","unstructured":"Kummer, T. T. et al. Experimental subarachnoid haemorrhage results in multifocal axonal injury. Brain 138, 2608\u20132618 (2015).","journal-title":"Brain"},{"key":"3747_CR34","doi-asserted-by":"publisher","first-page":"553","DOI":"10.3349\/ymj.2011.52.4.553","volume":"5","author":"SH Jang","year":"2011","unstructured":"Jang, S. H. Somatotopic arrangement and location of the corticospinal tract in the brainstem of the human brain. Yonsei Med. J. 5, 553\u2013557 (2011).","journal-title":"Yonsei Med. J."},{"key":"3747_CR35","doi-asserted-by":"publisher","first-page":"53","DOI":"10.1148\/rg.251045085","volume":"25","author":"SK Lee","year":"2005","unstructured":"Lee, S. K. et al. Diffusion-tensor MR imaging and fiber tractography: A new method of describing aberrant fiber connections in developmental CNS anomalies. Radiographics 25, 53\u201365 (2005) (discussion 66\u201358).","journal-title":"Radiographics"},{"key":"3747_CR36","doi-asserted-by":"publisher","first-page":"527","DOI":"10.1016\/j.neuron.2006.08.012","volume":"51","author":"S Mori","year":"2006","unstructured":"Mori, S. & Zhang, J. Principles of diffusion tensor imaging and its applications to basic neuroscience research. Neuron 51, 527\u2013539 (2006).","journal-title":"Neuron"}],"container-title":["Scientific Reports"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-03747-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-03747-1","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-03747-1.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,11,24]],"date-time":"2022-11-24T15:01:34Z","timestamp":1669302094000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s41598-021-03747-1"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,1,7]]},"references-count":36,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2022,12]]}},"alternative-id":["3747"],"URL":"https:\/\/doi.org\/10.1038\/s41598-021-03747-1","relation":{"has-preprint":[{"id-type":"doi","id":"10.21203\/rs.3.rs-514929\/v1","asserted-by":"object"}]},"ISSN":["2045-2322"],"issn-type":[{"value":"2045-2322","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,1,7]]},"assertion":[{"value":"11 May 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"8 December 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"7 January 2022","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"187"}}