{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T18:34:18Z","timestamp":1790706858667,"version":"4.1.0"},"reference-count":43,"publisher":"MDPI AG","issue":"23","license":[{"start":{"date-parts":[[2024,11,27]],"date-time":"2024-11-27T00:00:00Z","timestamp":1732665600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"name":"NIH","award":["R01 HL13197"],"award-info":[{"award-number":["R01 HL13197"]}]},{"name":"NIH","award":["DGE 1650604"],"award-info":[{"award-number":["DGE 1650604"]}]},{"DOI":"10.13039\/100000001","name":"NSF","doi-asserted-by":"publisher","award":["R01 HL13197"],"award-info":[{"award-number":["R01 HL13197"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100000001","name":"NSF","doi-asserted-by":"publisher","award":["DGE 1650604"],"award-info":[{"award-number":["DGE 1650604"]}],"id":[{"id":"10.13039\/100000001","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Diagnostics"],"abstract":"<jats:p>Background: In boys with Duchenne muscular dystrophy (DMD), cardiomyopathy has become the primary cause of death. Although both positive late gadolinium enhancement (LGE) and reduced left ventricular ejection fraction (LVEF) are late findings in a DMD cohort, LV end-systolic circumferential strain at middle wall (Ecc) serves as a biomarker for detecting early impairment in cardiac function associated with DMD. However, Ecc derived from cine Displacement Encoding with Stimulated Echoes (DENSE) has not been quantified in boys with DMD. We aim to: (1) use cine DENSE to quantify regional Ecc in LGE negative (-) boys with DMD and healthy controls; and (2) compare Ecc with LVEF in terms of differentiating DMD boys with LGE (-) from healthy boys. Methods: 10 LGE (-) boys with DMD and 12 healthy boys were enrolled prospectively in an IRB-approved study for CMR at 3T. Navigator-gated cine DENSE was used to obtain short-axis mid-ventricular data and estimate global and regional Ecc. Group-wise differences were tested via a Wilcoxon rank-sum test. Within-group differences were tested via a Skillings-Mack test followed by pairwise Wilcoxon signed-rank tests. A binomial logistic regression model was adopted to differentiate between DMD boys with LGE (-) and healthy boys. Results: When compared to healthy boys, LGE (-) boys with DMD demonstrated significantly impaired septal Ecc [\u22120.13 (0.01) vs. \u22120.16 (0.03), p = 0.019]. In comparison to the Ecc in other segments, both groups of boys exhibited significantly reduced septal Ecc and significantly elevated lateral Ecc. Septal Ecc outperformed LVEF in distinguishing DMD boys with LGE (-) from healthy boys. Conclusions: Reduced septal Ecc may serve as an early indicator of cardiac involvement in LGE (-) DMD boys prior to reduced LVEF and a positive LGE finding.<\/jats:p>","DOI":"10.3390\/diagnostics14232673","type":"journal-article","created":{"date-parts":[[2024,11,27]],"date-time":"2024-11-27T07:18:42Z","timestamp":1732691922000},"page":"2673","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["MRI-Based Circumferential Strain in Boys with Early Duchenne Muscular Dystrophy Cardiomyopathy"],"prefix":"10.3390","volume":"14","author":[{"ORCID":"https:\/\/orcid.org\/0000-0002-6873-9501","authenticated-orcid":false,"given":"Zhan-Qiu","family":"Liu","sequence":"first","affiliation":[{"name":"Department of Radiology, Stanford University, Palo Alto, CA 94305, USA"},{"name":"Cardiovascular Institute, Stanford University, Palo Alto, CA 94305, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nyasha G.","family":"Maforo","sequence":"additional","affiliation":[{"name":"Physics and Biology in Medicine Interdepartmental Program, University of California, Los Angeles, CA 90095, USA"},{"name":"Department of Radiological Sciences, University of California, Los Angeles, CA 90095, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Patrick","family":"Magrath","sequence":"additional","affiliation":[{"name":"Department of Radiological Sciences, University of California, Los Angeles, CA 90095, USA"},{"name":"Department of Bioengineering, University of California, Los Angeles, CA 90095, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-8615-5246","authenticated-orcid":false,"given":"Ashley","family":"Prosper","sequence":"additional","affiliation":[{"name":"Department of Radiological Sciences, University of California, Los Angeles, CA 90095, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pierangelo","family":"Renella","sequence":"additional","affiliation":[{"name":"Department of Radiological Sciences, University of California, Los Angeles, CA 90095, USA"},{"name":"Department of Medicine, Division of Pediatric Cardiology, CHOC Children\u2019s Hospital, Orange, CA 92868, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Nancy","family":"Halnon","sequence":"additional","affiliation":[{"name":"Department of Pediatrics, University of California, Los Angeles, CA 90095, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2585-5916","authenticated-orcid":false,"given":"Holden H.","family":"Wu","sequence":"additional","affiliation":[{"name":"Physics and Biology in Medicine Interdepartmental Program, University of California, Los Angeles, CA 90095, USA"},{"name":"Department of Radiological Sciences, University of California, Los Angeles, CA 90095, USA"},{"name":"Department of Bioengineering, University of California, Los Angeles, CA 90095, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Daniel B.","family":"Ennis","sequence":"additional","affiliation":[{"name":"Department of Radiology, Stanford University, Palo Alto, CA 94305, USA"},{"name":"Cardiovascular Institute, Stanford University, Palo Alto, CA 94305, USA"},{"name":"Maternal & Child Health Research Institute, Stanford University, Palo Alto, CA 94305, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,11,27]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1590","DOI":"10.1161\/CIRCULATIONAHA.114.015151","article-title":"Contemporary cardiac issues in Duchenne muscular dystrophy","volume":"131","author":"McNally","year":"2015","journal-title":"Circulation"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"177","DOI":"10.1016\/S1474-4422(09)70272-8","article-title":"Diagnosis and management of Duchenne muscular dystrophy, part 2: Implementation of multidisciplinary care","volume":"9","author":"Bushby","year":"2010","journal-title":"Lancet Neurol."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"e006340","DOI":"10.1161\/JAHA.117.006340","article-title":"Predictors of Death in Adults With Duchenne Muscular Dystrophy\u2013Associated Cardiomyopathy","volume":"6","author":"Cheeran","year":"2017","journal-title":"J. Am. Heart Assoc."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1186\/1532-429X-15-107","article-title":"Prevalence and distribution of late gadolinium enhancement in a large population of patients with Duchenne muscular dystrophy: Effect of age and left ventricular systolic function","volume":"15","author":"Hor","year":"2013","journal-title":"J. Cardiovasc. Magn. Reson."},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"e001338","DOI":"10.1161\/JAHA.114.001338","article-title":"Myocardial fibrosis burden predicts left ventricular ejection fraction and is associated with age and steroid treatment duration in Duchenne muscular dystrophy","volume":"4","author":"Tandon","year":"2015","journal-title":"J. Am. Heart Assoc."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"1874","DOI":"10.1016\/j.jacc.2006.10.078","article-title":"Myocardial delayed enhancement by magnetic resonance imaging in patients with muscular dystrophy","volume":"49","author":"Silva","year":"2007","journal-title":"J. Am. Coll. Cardiol."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"77","DOI":"10.1016\/S1474-4422(09)70271-6","article-title":"Diagnosis and management of Duchenne muscular dystrophy, part 1: Diagnosis, and pharmacological and psychosocial management","volume":"9","author":"Bushby","year":"2010","journal-title":"Lancet Neurol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"e12843","DOI":"10.1111\/eci.12843","article-title":"Oedema-fibrosis in Duchenne Muscular Dystrophy: Role of cardiovascular magnetic resonance imaging","volume":"47","author":"Mavrogeni","year":"2017","journal-title":"Eur. J. Clin. Investig."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"3738","DOI":"10.1161\/CIRCULATIONAHA.105.561423","article-title":"Influence of Ejection Fraction on Cardiovascular Outcomes in a Broad Spectrum of Heart Failure Patients","volume":"112","author":"Solomon","year":"2005","journal-title":"Circulation"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"1938","DOI":"10.1016\/j.ejrad.2015.07.007","article-title":"Comparison of right and left ventricular function and size in Duchenne muscular dystrophy","volume":"84","author":"Mehmood","year":"2015","journal-title":"Eur. J. Radiol."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"81","DOI":"10.1186\/s12968-014-0081-1","article-title":"Left ventricular systolic function and the pattern of late-gadolinium-enhancement independently and additively predict adverse cardiac events in muscular dystrophy patients","volume":"16","author":"Florian","year":"2014","journal-title":"J. Cardiovasc. Magn. Reson."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1271","DOI":"10.2217\/bmm-2018-0125","article-title":"Cardiac MRI biomarkers for Duchenne muscular dystrophy","volume":"12","author":"Magrath","year":"2018","journal-title":"Biomark. Med."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"1204","DOI":"10.1016\/j.jacc.2008.12.032","article-title":"Circumferential strain analysis identifies strata of cardiomyopathy in Duchenne muscular dystrophy: A cardiac magnetic resonance tagging study","volume":"53","author":"Hor","year":"2009","journal-title":"J. Am. Coll. Cardiol."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"2462","DOI":"10.1161\/CIRCULATIONAHA.104.516716","article-title":"Occult cardiac contractile dysfunction in dystrophin-deficient children revealed by cardiac magnetic resonance strain imaging","volume":"112","author":"Ashford","year":"2005","journal-title":"Circulation"},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"1159","DOI":"10.1007\/s00246-012-0622-z","article-title":"Abnormal Circumferential Strain is Present in Young Duchenne Muscular Dystrophy Patients","volume":"34","author":"Ryan","year":"2013","journal-title":"Pediatr. Cardiol."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1007\/s00246-014-0972-9","article-title":"Regional Circumferential Strain is a Biomarker for Disease Severity in Duchenne Muscular Dystrophy Heart Disease: A Cross-Sectional Study","volume":"36","author":"Hor","year":"2015","journal-title":"Pediatr. Cardiol."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"1495","DOI":"10.1007\/s00246-015-1192-7","article-title":"Myocardial Fibrosis and Left Ventricular Dysfunction in Duchenne Muscular Dystrophy Carriers Using Cardiac Magnetic Resonance Imaging","volume":"36","author":"Lang","year":"2015","journal-title":"Pediatr. Cardiol."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"148","DOI":"10.1016\/j.mri.2016.08.009","article-title":"Reproducibility of cine displacement encoding with stimulated echoes (DENSE) in human subjects","volume":"35","author":"Lin","year":"2017","journal-title":"Magn. Reson. Imaging"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1186\/s12968-015-0119-z","article-title":"Validation of in vivo, 2D displacements from spiral cine DENSE at 3T","volume":"17","author":"Wehner","year":"2015","journal-title":"J. Cardiovasc. Magn. Reson."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"1089","DOI":"10.1002\/mrm.22503","article-title":"Imaging three-dimensional myocardial mechanics using navigator-gated volumetric spiral cine DENSE MRI","volume":"64","author":"Zhong","year":"2010","journal-title":"Magn. Reson. Med."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"1557","DOI":"10.1002\/mrm.22153","article-title":"High spatial and temporal resolution cardiac cine MRI from retrospective reconstruction of data acquired in real time using motion correction and resorting","volume":"62","author":"Kellman","year":"2009","journal-title":"Magn. Reson. Med."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"102","DOI":"10.1186\/1532-429X-15-102","article-title":"High spatial and temporal resolution retrospective cine cardiovascular magnetic resonance from shortened free breathing real-time acquisitions","volume":"15","author":"Xue","year":"2013","journal-title":"J. Cardiovasc. Magn. Reson."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"864","DOI":"10.1002\/mrm.26137","article-title":"Effect of free-breathing on left ventricular rotational mechanics in healthy subjects and patients with duchenne muscular dystrophy","volume":"77","author":"Reyhan","year":"2017","journal-title":"Magn. Reson. Med."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"194","DOI":"10.1002\/mrm.20333","article-title":"Motion-corrected free-breathing delayed enhancement imaging of myocardial infarction","volume":"53","author":"Kellman","year":"2005","journal-title":"Magn. Reson. Med."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"1598","DOI":"10.1161\/CIRCRESAHA.119.313572","article-title":"Heart Failure with Preserved Ejection Fraction in Perspective","volume":"124","author":"Pfeffer","year":"2019","journal-title":"Circ. Res."},{"key":"ref_26","unstructured":"Gilliam, A., Scott, A., vanMaanen, D., and Suever, J. (2016, June 01). DENSEanalysis. Available online: https:\/\/github.com\/denseanalysis\/denseanalysis."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"105","DOI":"10.1016\/j.media.2008.06.016","article-title":"Motion-guided segmentation for cine DENSE MRI","volume":"13","author":"Spottiswoode","year":"2009","journal-title":"Med. Image Anal."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1109\/TMI.2006.884215","article-title":"Tracking myocardial motion from cine DENSE images using spatiotemporal phase unwrapping and temporal fitting","volume":"26","author":"Spottiswoode","year":"2007","journal-title":"IEEE Trans. Med. Imaging"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"29","DOI":"10.1186\/s12968-015-0111-7","article-title":"Normal values for cardiovascular magnetic resonance in adults and children","volume":"17","author":"Maceira","year":"2015","journal-title":"J. Cardiovasc. Magn. Reson."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"1474","DOI":"10.1093\/cvr\/cvx160","article-title":"The overloaded right heart and ventricular interdependence","volume":"113","author":"Naeije","year":"2017","journal-title":"Cardiovasc. Res."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"195","DOI":"10.1016\/j.cardiores.2004.08.011","article-title":"Cardiac cellular heterogeneity and remodelling","volume":"64","author":"Kohl","year":"2004","journal-title":"Cardiovasc. Res."},{"key":"ref_32","first-page":"31","article-title":"Heterogeneity of the myocardium. Function of the left and right ventricle under normal and pathological conditions","volume":"40","author":"Kvasnicka","year":"1991","journal-title":"Physiol. Res."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"249","DOI":"10.1016\/j.pbiomolbio.2015.12.007","article-title":"Mechano-electric heterogeneity of the myocardium as a paradigm of its function","volume":"120","author":"Solovyova","year":"2016","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_34","unstructured":"Widmaier, E., Raff, H., and Strang, K. (2006). Cardiovascular patterns in health and disease. Vander\u2019s Human Physiology: The Mechanism of Body Function, Mc Graw Hill.. [10th ed.]."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"S126","DOI":"10.1016\/j.ejcts.2006.02.048","article-title":"The septal motor of biventricular function","volume":"29","author":"Saleh","year":"2006","journal-title":"Eur. J. Cardiothorac. Surg."},{"key":"ref_36","doi-asserted-by":"crossref","unstructured":"Asgeirsson, D., Hedstr\u00f6m, E., J\u00f6gi, J., Pahlm, U., Steding-Ehrenborg, K., Engblom, H., Arheden, H., and Carlsson, M. (2017). Longitudinal shortening remains the principal component of left ventricular pumping in patients with chronic myocardial infarction even when the absolute atrioventricular plane displacement is decreased. BMC Cardiovasc. Disord., 17.","DOI":"10.1186\/s12872-017-0641-z"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"H303","DOI":"10.1152\/ajpheart.00485.2014","article-title":"Early right ventricular fibrosis and reduction in biventricular cardiac reserve in the dystrophin-deficient mdx heart","volume":"308","author":"Meyers","year":"2015","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"ref_38","doi-asserted-by":"crossref","unstructured":"Larcher, T., Lafoux, A., Tesson, L., Remy, S., Thepenier, V., Fran\u00e7ois, V., Le Guiner, C., Goubin, H., Dutilleul, M., and Guigand, L. (2014). Characterization of Dystrophin Deficient Rats: A New Model for Duchenne Muscular Dystrophy. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0110371"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"1987","DOI":"10.1001\/jama.285.15.1987","article-title":"The CONSORT Statement: Revised Recommendations for Improving the Quality of Reports of Parallel-Group Randomized Trials","volume":"285","author":"Moher","year":"2001","journal-title":"JAMA"},{"key":"ref_40","unstructured":"Harrell, F.E. (2017). Regression modeling strategies. BIOS, 330."},{"key":"ref_41","unstructured":"Dobson, A.J., and Barnett, A.G. (2018). An Introduction to Generalized Linear Models, CRC Press."},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"McCullagh, P. (2018). Generalized Linear Models, Routledge.","DOI":"10.1201\/9780203753736"},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"716","DOI":"10.1109\/TAC.1974.1100705","article-title":"A new look at the statistical model identification","volume":"19","author":"Akaike","year":"1974","journal-title":"IEEE Trans. Autom. Control"}],"container-title":["Diagnostics"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2075-4418\/14\/23\/2673\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:40:40Z","timestamp":1760114440000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2075-4418\/14\/23\/2673"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,11,27]]},"references-count":43,"journal-issue":{"issue":"23","published-online":{"date-parts":[[2024,12]]}},"alternative-id":["diagnostics14232673"],"URL":"https:\/\/doi.org\/10.3390\/diagnostics14232673","relation":{},"ISSN":["2075-4418"],"issn-type":[{"value":"2075-4418","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,11,27]]}}}