{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,2,23]],"date-time":"2026-02-23T23:00:55Z","timestamp":1771887655439,"version":"3.50.1"},"reference-count":24,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2026,2,23]],"date-time":"2026-02-23T00:00:00Z","timestamp":1771804800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2026,2,23]],"date-time":"2026-02-23T00:00:00Z","timestamp":1771804800000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"funder":[{"name":"Berufsgenossenschaftliches Klinikum Bergmannsheil gGmbH"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Eur J Trauma Emerg Surg"],"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:sec>\n                    <jats:title>Aims<\/jats:title>\n                    <jats:p>Traumatic brain injuries (TBI) and spinal cord injuries (SCI) are associated with an increased risk to develop heterotopic ossifications (HO). Aim of the study was to analyze biochemical markers and osteogenic differentiation capacity of patients\u2019 plasma during the early posttraumatic period to assess the risk for HO.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Methods<\/jats:title>\n                    <jats:p>\n                      To evaluate predictive markers of HO in response to TBI\/SCI, comparative cytokine array analyses of plasma obtained from patients with TBI\/SCI were performed to identify expressed proteins. The expression of 105 proteins in plasma of patients with TBI (\n                      <jats:italic>n<\/jats:italic>\n                      \u2009=\u20099) and SCI (\n                      <jats:italic>n<\/jats:italic>\n                      \u2009=\u20099) was compared to patients with multiple trauma (MT;\n                      <jats:italic>n<\/jats:italic>\n                      \u2009=\u20099) and controls (norm). Additionally, the effect of patients\u2019 plasma on osteogenic differentiation of bone marrow-derived human mesenchymal stem cells (MSC) was tested by in vitro cell assay.\n                    <\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Results<\/jats:title>\n                    <jats:p>Cytokine array analyses showed that plasma of TBI-group had a different protein expression profile compared to SCI-, MT- or norm-group. TBI-group exhibited the greatest number of up-regulated proteins and the greatest magnitude of alterations. Conversely, MT-group showed the greatest number of down-regulated proteins. In vitro cell assay showed that MSC exhibited a stronger capacity for osteogenic differentiation after treatment with plasma of TBI-\/SCI-group with clinical signs of HO, than TBI-\/SCI-group without HO or MT- and norm-group.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Conclusion<\/jats:title>\n                    <jats:p>This pilot study demonstrates distinct plasma factors in SCI\/TBI patients and suggests a possible correlation between HO development and enhanced in-vitro osteogenesis of MSCs. The applied osteogenic differentiation assay could therefore represent a simple and reproducible tool to predict early stages of HO and to identify patients at risk. However, these findings do not allow causal conclusions, and further studies are required to clarify the underlying mechanisms and the predictive value of the assay.<\/jats:p>\n                  <\/jats:sec>\n                  <jats:sec>\n                    <jats:title>Level of evidence<\/jats:title>\n                    <jats:p>III.<\/jats:p>\n                  <\/jats:sec>","DOI":"10.1007\/s00068-026-03123-6","type":"journal-article","created":{"date-parts":[[2026,2,23]],"date-time":"2026-02-23T10:00:42Z","timestamp":1771840842000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":0,"title":["Cytokine array analyses and osteogenic potential of plasma from patients with traumatic brain-\/spinal cord injury: predictive markers of heterotopic ossification?"],"prefix":"10.1007","volume":"52","author":[{"given":"Ole","family":"Somberg","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Jan","family":"Gessmann","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Elvira","family":"Peter","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Marina","family":"Breisch","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Matthias","family":"K\u00f6nigshausen","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Thomas","family":"Schildhauer","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Manfred","family":"K\u00f6ller","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Thomas","family":"Rosteius","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2026,2,23]]},"reference":[{"key":"3123_CR1","doi-asserted-by":"publisher","first-page":"1629","DOI":"10.2106\/00004623-197355080-00006","volume":"55","author":"AF Brooker","year":"1973","unstructured":"Brooker AF, Bowerman JW, Robinson RA, Riley LH Jr. Ectopic ossification following total hip replacement. Incidence and a method of classification. J Bone Joint Surg Am. 1973;55:1629\u201332.","journal-title":"J Bone Joint Surg Am"},{"key":"3123_CR2","doi-asserted-by":"publisher","first-page":"666","DOI":"10.1007\/s11914-020-00636-w","volume":"18","author":"KA Alexander","year":"2020","unstructured":"Alexander KA, Tseng HW, Salga M, Gen\u00eat F, Levesque JP. When the nervous system turns skeletal muscles into bones: how to solve the conundrum of neurogenic heterotopic ossification. Curr Osteoporos Rep. 2020;18:666\u201376.","journal-title":"Curr Osteoporos Rep"},{"key":"3123_CR3","doi-asserted-by":"publisher","first-page":"1519","DOI":"10.1016\/j.spinee.2017.04.021","volume":"17","author":"M Ohlmeier","year":"2017","unstructured":"Ohlmeier M, Suero EM, Aach M, Meindl R, Schildhauer TA, Citak M. Muscle localization of heterotopic ossification following spinal cord injury. Spine J. 2017;17:1519\u201322.","journal-title":"Spine J"},{"key":"3123_CR4","doi-asserted-by":"publisher","first-page":"78","DOI":"10.1038\/sj.sc.3100561","volume":"36","author":"B Schurch","year":"1998","unstructured":"Schurch B, Dollfus P. The \u2018Dejerines\u2019: an historical review and homage to two pioneers in the field of neurology and their contribution to the Understanding of spinal cord pathology. Spinal Cord. 1998;36:78\u201386.","journal-title":"Spinal Cord"},{"key":"3123_CR5","first-page":"19","volume":"14","author":"JE Reznik","year":"2014","unstructured":"Reznik JE, Biros E, Marshall R, Jelbart M, Milanese S, Gordon S, Galea MP. Prevalence and risk-factors of neurogenic heterotopic ossification in traumatic spinal cord and traumatic brain injured patients admitted to specialised units in Australia. J Musculoskelet Neuronal Interact. 2014;14:19\u201328.","journal-title":"J Musculoskelet Neuronal Interact"},{"key":"3123_CR6","doi-asserted-by":"publisher","first-page":"1146","DOI":"10.1016\/j.injury.2007.03.019","volume":"38","author":"LL Simonsen","year":"2007","unstructured":"Simonsen LL, Sonne-Holm S, Krasheninnikoff M, Engberg AW. Symptomatic heterotopic ossification after very severe traumatic brain injury in 114 patients: incidence and risk factors. Injury. 2007;38:1146\u201350.","journal-title":"Injury"},{"key":"3123_CR7","doi-asserted-by":"publisher","first-page":"229","DOI":"10.1002\/path.4519","volume":"236","author":"F Gen\u00eat","year":"2015","unstructured":"Gen\u00eat F, Kulina I, Vaquette C, Torossian F, Millard S, Pettit AR, Sims NA, Anginot A, Guerton B, Winkler IG, Barbier V, Lataillade JJ, et al. Neurological heterotopic ossification following spinal cord injury is triggered by macrophage-mediated inflammation in muscle. J Pathol. 2015;236:229\u201340.","journal-title":"J Pathol"},{"key":"3123_CR8","doi-asserted-by":"publisher","first-page":"313","DOI":"10.1038\/sj.sc.3101309","volume":"40","author":"AA van Kuijk","year":"2002","unstructured":"van Kuijk AA, Geurts AC, van Kuppevelt HJ. Neurogenic heterotopic ossification in spinal cord injury. Spinal Cord. 2002;40:313\u201326.","journal-title":"Spinal Cord"},{"key":"3123_CR9","first-page":"230","volume":"12","author":"VI Sakellariou","year":"2012","unstructured":"Sakellariou VI, Grigoriou E, Mavrogenis AF, Soucacos PN, Papagelopoulos PJ. Heterotopic ossification following traumatic brain injury and spinal cord injury: insight into the etiology and pathophysiology. J Musculoskelet Neuronal Interact. 2012;12:230\u201340.","journal-title":"J Musculoskelet Neuronal Interact"},{"key":"3123_CR10","doi-asserted-by":"publisher","first-page":"e10172","DOI":"10.1002\/jbm4.10172","volume":"3","author":"C Meyers","year":"2019","unstructured":"Meyers C, Lisiecki J, Miller S, Levin A, Fayad L, Ding C, Sono T, McCarthy E, Levi B, James AW. Heterotopic ossification: A comprehensive review. JBMR Plus. 2019;3:e10172.","journal-title":"JBMR Plus"},{"key":"3123_CR11","doi-asserted-by":"publisher","first-page":"1101","DOI":"10.2106\/JBJS.N.01056","volume":"97","author":"K Ranganathan","year":"2015","unstructured":"Ranganathan K, Loder S, Agarwal S, Wong VW, Forsberg J, Davis TA, Wang S, James AW, Levi B. Heterotopic ossification: Basic-Science principles and clinical correlates. J Bone Joint Surg Am. 2015;97:1101\u201311.","journal-title":"J Bone Joint Surg Am"},{"key":"3123_CR12","doi-asserted-by":"publisher","first-page":"932","DOI":"10.1038\/s42003-023-05316-w","volume":"6","author":"J Gueguen","year":"2023","unstructured":"Gueguen J, Girard D, Rival B, Fernandez J, Goriot ME, Banzet S. Spinal cord injury dysregulates fibro-adipogenic progenitors MiRNAs signaling to promote neurogenic heterotopic ossifications. Commun Biol. 2023;6:932.","journal-title":"Commun Biol"},{"key":"3123_CR13","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1016\/j.bone.2017.05.015","volume":"109","author":"RD Brady","year":"2018","unstructured":"Brady RD, Shultz SR, McDonald SJ, O\u2019Brien TJ. Neurological heterotopic ossification: current Understanding and future directions. Bone. 2018;109:35\u201342.","journal-title":"Bone"},{"key":"3123_CR14","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1038\/s41393-025-01070-4","volume":"63","author":"E Ulrich","year":"2025","unstructured":"Ulrich E, Brinkemper A, K\u00f6ller M, Stricker I, Gisevius A, Schildhauer TA, Meindl R, Grasm\u00fccke D, Buche-Lyding S, Nicolas V, Aach M. Histology of neurogenic heterotopic ossification and comparison with its radiological expression in acute spinal cord injured patients. Spinal Cord. 2025;63:227\u201332.","journal-title":"Spinal Cord"},{"key":"3123_CR15","first-page":"S317","volume":"8","author":"TB Schildhauer","year":"1993","unstructured":"Schildhauer TB, Lane MPG, Berberian JM, Tomin WS, Missri E, Weiland AAE, Rosen A, Doty VM, S. Immunolocalization of bone morphogenetic proteins 2\/4 in the embryological development of the rat. J Bone Miner Res. 1993;8:S317.","journal-title":"J Bone Miner Res"},{"key":"3123_CR16","doi-asserted-by":"publisher","first-page":"1558","DOI":"10.1002\/cam4.502","volume":"4","author":"T Uchiyama","year":"2015","unstructured":"Uchiyama T, Kawabata H, Miura Y, Yoshioka S, Iwasa M, Yao H, Sakamoto S, Fujimoto M, Haga H, Kadowaki N, Maekawa T, Takaori-Kondo A. The role of growth differentiation factor 15 in the pathogenesis of primary myelofibrosis. Cancer Med. 2015;4:1558\u201372.","journal-title":"Cancer Med"},{"key":"3123_CR17","doi-asserted-by":"publisher","first-page":"411","DOI":"10.3181\/00379727-163-40788","volume":"163","author":"GT Syftestad","year":"1980","unstructured":"Syftestad GT, Urist MR. Growth hormone dependent matrix-induced heterotopic bone formation. Proc Soc Exp Biol Med. 1980;163:411\u20135.","journal-title":"Proc Soc Exp Biol Med"},{"key":"3123_CR18","first-page":"119","volume":"113","author":"R Wildburger","year":"2001","unstructured":"Wildburger R, Zarkovic N, Leb G, Borovic S, Zarkovic K, Tatzber F. Post-traumatic changes in insulin-like growth factor type 1 and growth hormone in patients with bone fractures and traumatic brain injury. Wien Klin Wochenschr. 2001;113:119\u201326.","journal-title":"Wien Klin Wochenschr"},{"key":"3123_CR19","doi-asserted-by":"publisher","first-page":"1630","DOI":"10.1210\/endo.140.4.6637","volume":"140","author":"T Thomas","year":"1999","unstructured":"Thomas T, Gori F, Khosla S, Jensen MD, Burguera B, Riggs BL. Leptin acts on human marrow stromal cells to enhance differentiation to osteoblasts and to inhibit differentiation to adipocytes. Endocrinology. 1999;140:1630\u20138.","journal-title":"Endocrinology"},{"key":"3123_CR20","doi-asserted-by":"publisher","first-page":"1017","DOI":"10.1002\/jcp.25955","volume":"233","author":"H Jiang","year":"2018","unstructured":"Jiang H, Chen Y, Chen G, Tian X, Tang J, Luo L, Huang M, Yan B, Ao X, Zhou W, Wang L, Bai X, et al. Leptin accelerates the pathogenesis of heterotopic ossification in rat tendon tissues via mTORC1 signaling. J Cell Physiol. 2018;233:1017\u201328.","journal-title":"J Cell Physiol"},{"key":"3123_CR21","first-page":"7","volume":"14","author":"L Wang","year":"2011","unstructured":"Wang L, Yuan JS, Zhang HX, Ding H, Tang XG, Wei YZ. Effect of leptin on bone metabolism in rat model of traumatic brain injury and femoral fracture. Chin J Traumatol. 2011;14:7\u201313.","journal-title":"Chin J Traumatol"},{"key":"3123_CR22","doi-asserted-by":"crossref","unstructured":"Cannav\u00f2 SP, Bertino L, Di Salvo E, Papaianni V, Ventura-Spagnolo E, Gangemi S. (2019) Possible Roles of IL-33 in the Innate-Adaptive Immune Crosstalk of Psoriasis Pathogenesis. Mediators Inflamm. 2019:7158014.","DOI":"10.1155\/2019\/7158014"},{"key":"3123_CR23","doi-asserted-by":"publisher","first-page":"902","DOI":"10.1186\/s12967-023-04782-4","volume":"21","author":"Y Zhou","year":"2023","unstructured":"Zhou Y, Xu Z, Liu Z. Role of IL-33-ST2 pathway in regulating inflammation: current evidence and future perspectives. J Transl Med. 2023;21:902.","journal-title":"J Transl Med"},{"key":"3123_CR24","doi-asserted-by":"publisher","first-page":"8511","DOI":"10.1002\/jcb.27080","volume":"119","author":"S Macari","year":"2018","unstructured":"Macari S, Madeira MFM, Lima ILA, Pereira TSF, Dias GJ, Cirelli JA, de Molon RS, Fukada SY, Szawka RE, Garlet GP, Teixeira MM, Silva TA. ST2 regulates bone loss in a site-dependent and estrogen-dependent manner. J Cell Biochem. 2018;119:8511\u201321.","journal-title":"J Cell Biochem"}],"container-title":["European Journal of Trauma and Emergency Surgery"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00068-026-03123-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s00068-026-03123-6","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s00068-026-03123-6.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2026,2,23]],"date-time":"2026-02-23T22:04:19Z","timestamp":1771884259000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s00068-026-03123-6"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2026,2,23]]},"references-count":24,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2026,12]]}},"alternative-id":["3123"],"URL":"https:\/\/doi.org\/10.1007\/s00068-026-03123-6","relation":{},"ISSN":["1863-9941"],"issn-type":[{"value":"1863-9941","type":"electronic"}],"subject":[],"published":{"date-parts":[[2026,2,23]]},"assertion":[{"value":"28 November 2025","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 February 2026","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"23 February 2026","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The study was reviewed and approved by the local ethics committee of the medical faculty of Ruhr University Bochum, Germany (registered number: 18-6509-BR).","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":"64"}}