{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,10,26]],"date-time":"2025-10-26T21:39:26Z","timestamp":1761514766512},"reference-count":23,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2021,5,20]],"date-time":"2021-05-20T00:00:00Z","timestamp":1621468800000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2021,5,20]],"date-time":"2021-05-20T00:00:00Z","timestamp":1621468800000},"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":["J Orthop Surg Res"],"published-print":{"date-parts":[[2021,12]]},"abstract":"<jats:title>Abstract<\/jats:title><jats:sec>\n                <jats:title>Background and objective<\/jats:title>\n                <jats:p>The neuropeptide vasoactive intestinal peptide is a 28-amino acid neuropeptide that has been shown to stimulate bone repair and angiogenesis. The purpose of this study was to explore the potential role of serum VIP concentration in osteonecrosis of femoral trauma (ONFH).<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>One hundred five patients diagnosed with non-traumatic ONFH and 103 healthy individuals were enrolled in our study. Serum VIP, tumor necrosis factor-\u03b1 (TNF-\u03b1), interluekin-1 beta (IL-1\u03b2), and macrophage colony-stimulating factor (M-CSF) levels also were detected using the commercial ELISA kit. Radiographic progression was evaluated using FICAT classification. The clinical severity of ONFH was assessed by visual analog score (VAS) and Harris Hip Score (HHS). Receiver-operating characteristic (ROC) curve was performed to test the potential diagnostic value of VIP in radiographic progression.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>The serum VIP level of patients with non-traumatic ONFH was significantly lower than that of healthy controls. There was no significant difference between the alcohol group, the steroid-induction group, and the idiopathic group. Serum VIP levels were significantly higher in ONFH patients with femoral head pre-collapse stage than collapse stage. Serum VIP levels were significantly lower. FICAT 4 non-traumatic ONFH patients had significantly lower serum concentrations of VIP when compared with FICAT 3 and FICAT 2. Moreover, serum VIP levels were significantly lower in ONFH patients with FICAT 3 than FICAT 2. Serum VIP levels were negatively related to FICAT stage. In addition, serum VIP levels were negatively associated with VAS score and positively associated with HHS score. Last, we found serum VIP levels were negatively associated with serum TNF-\u03b1 and IL-1\u03b2 levels. ROC curve analysis indicated that decreased serum VIP could serve as a decent biomarker with regard to the diagnosis of radiographic progression.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusion<\/jats:title>\n                <jats:p>Attenuated serum VIP concentrations are correlated with disease severity of non-traumatic ONFH. Decreased serum VIP may serve as a potential indicator of non-traumatic ONFH.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s13018-021-02486-3","type":"journal-article","created":{"date-parts":[[2021,5,20]],"date-time":"2021-05-20T07:18:57Z","timestamp":1621495137000},"update-policy":"http:\/\/dx.doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":6,"title":["Attenuated serum vasoactive intestinal peptide concentrations are correlated with disease severity of non-traumatic osteonecrosis of femoral head"],"prefix":"10.1186","volume":"16","author":[{"given":"Ming","family":"Liu","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Gan","family":"Zhao","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"Biao-Fang","family":"Wei","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"297","published-online":{"date-parts":[[2021,5,20]]},"reference":[{"key":"2486_CR1","doi-asserted-by":"publisher","first-page":"407","DOI":"10.1016\/j.jos.2016.03.008","volume":"21","author":"T Kubo","year":"2016","unstructured":"Kubo T, Ueshima K, Saito M, et al. Clinical and basic research on steroid-induced osteonecrosis of the femoral head in Japan. J Orthop Sci. 2016;21:407\u201313.","journal-title":"J Orthop Sci"},{"key":"2486_CR2","doi-asserted-by":"publisher","first-page":"267","DOI":"10.1007\/s00264-015-3061-7","volume":"40","author":"L Cui","year":"2016","unstructured":"Cui L, Zhuang Q, Lin J, et al. Multicentric epidemiologic study on six thousand three hundred and ninety five cases of femoral head osteonecrosis in China. Int Orthop. 2016;40:267\u201376.","journal-title":"Int Orthop"},{"key":"2486_CR3","first-page":"1117","volume":"88","author":"MA Mont","year":"2006","unstructured":"Mont MA, Jones LC, Hungerford DS. Nontraumatic osteonecrosis of the femoral head: ten years later. J Bone Joint Surg Am. 2006;88:1117\u201332.","journal-title":"J Bone Joint Surg Am"},{"key":"2486_CR4","doi-asserted-by":"publisher","first-page":"100","DOI":"10.1016\/j.jot.2019.12.004","volume":"21","author":"D Zhao","year":"2020","unstructured":"Zhao D, Zhang F, Wang B, et al. Guidelines for clinical diagnosis and treatment of osteonecrosis of the femoral head in adults (2019 version). J Orthop Translat. 2020;21:100\u201310.","journal-title":"J Orthop Translat"},{"key":"2486_CR5","doi-asserted-by":"publisher","first-page":"3","DOI":"10.1111\/os.12302","volume":"9","author":"Association MDotOBotCMD","year":"2017","unstructured":"Association MDotOBotCMD. Chinese guideline for the diagnosis and treatment of osteonecrosis of the femoral head in adults. Orthop Surg. 2017;9:3.","journal-title":"Orthop Surg"},{"key":"2486_CR6","doi-asserted-by":"publisher","first-page":"2165","DOI":"10.2106\/JBJS.I.00575","volume":"92","author":"MA Mont","year":"2010","unstructured":"Mont MA, Zywiel MG, Marker DR, et al. The natural history of untreated asymptomatic osteonecrosis of the femoral head: a systematic literature review. J Bone Joint Surg Am. 2010;92:2165\u201370.","journal-title":"J Bone Joint Surg Am"},{"key":"2486_CR7","doi-asserted-by":"publisher","first-page":"590","DOI":"10.5312\/wjo.v6.i8.590","volume":"6","author":"J Moya-Angeler","year":"2015","unstructured":"Moya-Angeler J, Gianakos AL, Villa JC, Ni A, et al. Current concepts on osteonecrosis of the femoral head. World J Orthop. 2015;6:590\u2013601.","journal-title":"World J Orthop"},{"key":"2486_CR8","doi-asserted-by":"publisher","first-page":"1604","DOI":"10.2106\/JBJS.O.00071","volume":"97","author":"MA Mont","year":"2015","unstructured":"Mont MA, Cherian JJ, Sierra RJ, et al. Nontraumatic osteonecrosis of the femoral head: where do we stand today? A ten-year update. J Bone Joint Surg Am. 2015;97:1604\u201327.","journal-title":"J Bone Joint Surg Am"},{"key":"2486_CR9","doi-asserted-by":"publisher","first-page":"1607e12","DOI":"10.1016\/j.clinbiochem.2012.08.020","volume":"45","author":"W Jiang","year":"2012","unstructured":"Jiang W, Gao SG, Chen XG, et al. Expression of synovial fluid and articular cartilage VIP in human osteoarthritic knee: a new indicator of disease severity? Clin Biochem. 2012;45:1607e12.","journal-title":"Clin Biochem"},{"key":"2486_CR10","doi-asserted-by":"publisher","first-page":"63","DOI":"10.1186\/s12929-016-0280-1","volume":"23","author":"W Jiang","year":"2016","unstructured":"Jiang W, Wang H, Li YS, et al. Role of vasoactive intestinal peptide in osteoarthritis. J Biomed Sci. 2016;23:63.","journal-title":"J Biomed Sci"},{"key":"2486_CR11","doi-asserted-by":"publisher","first-page":"3732e41","DOI":"10.1002\/jcb.23304","volume":"112","author":"E Persson","year":"2011","unstructured":"Persson E, Lerner UH. The neuropeptide VIP regulates the expression of osteoclastogenic factors in osteoblasts. J Cell Biochem. 2011;112:3732e41.","journal-title":"J Cell Biochem"},{"key":"2486_CR12","doi-asserted-by":"publisher","first-page":"158e63","DOI":"10.1006\/bbrc.2000.2599","volume":"271","author":"H Mukohyama","year":"2000","unstructured":"Mukohyama H, Ransjo M, Taniguchi H, et al. The inhibitory effects of vasoactive intestinal peptide and pituitary adenylate cyclase activating polypeptide on osteoclast formation are associated with upregulation of osteoprotegerin and downregulation of RANKL and RANK. Biochem Biophys Res Commun. 2000;271:158e63.","journal-title":"Biochem Biophys Res Commun"},{"key":"2486_CR13","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1089\/scd.2019.0148","volume":"29","author":"L Shi","year":"2020","unstructured":"Shi L, Feng L, Zhu ML, et al. Vasoactive intestinal peptide stimulates bone marrow-mesenchymal stem cells osteogenesis differentiation by activating Wnt\/\u03b2-catenin signaling pathway and promotes rat skull defect repair. Stem Cells Dev. 2020;29:1\u201331.","journal-title":"Stem Cells Dev"},{"key":"2486_CR14","doi-asserted-by":"publisher","first-page":"590","DOI":"10.1302\/0301-620X.81B4.0810590","volume":"81","author":"N Sugano","year":"1999","unstructured":"Sugano N, Kubo T, Takaoka K, Ohzono K, Hotokebuchi T, Matsumoto T, et al. Diagnostic criteria for non-traumatic osteonecrosis of the femoral head. A multicentre study. J Bone Joint Surg (Br). 1999;81:590\u20135.","journal-title":"J Bone Joint Surg (Br)"},{"key":"2486_CR15","unstructured":"Chow S, Shao J, Wang H. Sample size calculations in clinical research. 2nd ed: Chapman & Hall\/CRC Biostatistics Series; 2008. p. 58."},{"key":"2486_CR16","doi-asserted-by":"publisher","first-page":"2636","DOI":"10.1007\/s11999-012-2416-2","volume":"470","author":"MU Jawad","year":"2012","unstructured":"Jawad MU, Haleem AA, Scully SP. In brief: Ficat classification: avascular necrosis of the femoral head. Clin Orthop Relat Res. 2012;470:2636\u20139.","journal-title":"Clin Orthop Relat Res"},{"key":"2486_CR17","first-page":"781","volume":"17","author":"DA Fishbain","year":"2016","unstructured":"Fishbain DA, Gao J, Lewis JE, et al. At completion of a multidisciplinary treatment program, are psychophysical variables associated with a VAS improvement of 30% or more, a minimal clinically important difference, or an absolute VAS score improvement of 1.5 cm or more? Pain Med. 2016;17:781\u20139.","journal-title":"Pain Med"},{"key":"2486_CR18","doi-asserted-by":"publisher","first-page":"737","DOI":"10.2106\/00004623-196951040-00012","volume":"51","author":"WH Harris","year":"1969","unstructured":"Harris WH. Traumatic arthritis of the hip after dislocation and acetabular fractures: treatment by mold arthroplasty. An end-result study using a new method of result evaluation. J Bone Joint Surg Am. 1969;51:737\u201355.","journal-title":"J Bone Joint Surg Am"},{"key":"2486_CR19","doi-asserted-by":"publisher","first-page":"4","DOI":"10.1186\/s41232-016-0002-9","volume":"36","author":"Y Kuroda","year":"2016","unstructured":"Kuroda Y, Matsuda S, Akiyama H. Joint-preserving regenerative therapy for patients with early-stage osteonecrosis of the femoral head. Inflamm Regen. 2016;36:4.","journal-title":"Inflamm Regen"},{"key":"2486_CR20","doi-asserted-by":"publisher","first-page":"1911","DOI":"10.1016\/j.arth.2014.05.022","volume":"29","author":"K Issa","year":"2014","unstructured":"Issa K, Jauregui JJ, McElroy M, et al. Unnecessary magnetic resonance imaging of hips: an economic burden to patients and the healthcare system. J Arthroplast. 2014;29:1911\u20134.","journal-title":"J Arthroplast"},{"key":"2486_CR21","doi-asserted-by":"crossref","unstructured":"Cost-effectiveness of MRI to assess for posttraumatic ligamentous cervical spine injury. Orthopedics. 2014;37:e148\u201352.","DOI":"10.3928\/01477447-20140124-16"},{"key":"2486_CR22","doi-asserted-by":"publisher","first-page":"579","DOI":"10.1007\/s00210-007-0232-0","volume":"377","author":"S Onoue","year":"2008","unstructured":"Onoue S, Misaka S, Yamada S. Structure-activity relationship of vasoactive intestinal peptide (VIP): potent agonists and potential clinical applications. Naunyn Schmiedeberg's Arch Pharmacol. 2008;377:579\u201390.","journal-title":"Naunyn Schmiedeberg's Arch Pharmacol"},{"key":"2486_CR23","doi-asserted-by":"publisher","first-page":"367","DOI":"10.3390\/ijms19020367","volume":"19","author":"S Gr\u00e4ssel","year":"2018","unstructured":"Gr\u00e4ssel S, Muschter D. Do neuroendocrine peptides and their receptors qualify as novel therapeutic targets in osteoarthritis? Int J Mol Sci. 2018;19:367.","journal-title":"Int J Mol Sci"}],"container-title":["Journal of Orthopaedic Surgery and Research"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13018-021-02486-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1186\/s13018-021-02486-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1186\/s13018-021-02486-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2021,5,20]],"date-time":"2021-05-20T07:21:22Z","timestamp":1621495282000},"score":1,"resource":{"primary":{"URL":"https:\/\/josr-online.biomedcentral.com\/articles\/10.1186\/s13018-021-02486-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2021,5,20]]},"references-count":23,"journal-issue":{"issue":"1","published-print":{"date-parts":[[2021,12]]}},"alternative-id":["2486"],"URL":"https:\/\/doi.org\/10.1186\/s13018-021-02486-3","relation":{},"ISSN":["1749-799X"],"issn-type":[{"value":"1749-799X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2021,5,20]]},"assertion":[{"value":"18 April 2021","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"13 May 2021","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"20 May 2021","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"This study was approved by Linyi People\u2019s Hospital Ethics Committee. All the patients signed written informed consent.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"The authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"325"}}