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Fourier analysis of collagen bundle orientation in myocardial infarction scars

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Fourier analysis of collagen bundle orientation in myocardial infarction scars

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dc.contributor.author Marcos-Garcés, Víctor es_ES
dc.contributor.author Rios-Navarro, Cesar es_ES
dc.contributor.author Gómez-Torres, Fabián es_ES
dc.contributor.author Gavara-Doñate, Josep es_ES
dc.contributor.author De Dios, Elena es_ES
dc.contributor.author Diaz, Ana es_ES
dc.contributor.author Miñana, Gema es_ES
dc.contributor.author Chorro, Francisco Javier es_ES
dc.contributor.author Bodi, Vicente es_ES
dc.contributor.author Ruiz-Sauri, Amparo es_ES
dc.date.accessioned 2023-12-04T19:02:14Z
dc.date.available 2023-12-04T19:02:14Z
dc.date.issued 2022-11 es_ES
dc.identifier.issn 0948-6143 es_ES
dc.identifier.uri http://hdl.handle.net/10251/200491
dc.description.abstract [EN] Collagen bundle orientation (CBO) in myocardial infarct scars plays a major role in scar mechanics and complications after infarction. We aim to compare four histopathological methods for CBO measurement in myocardial scarring. Myocardial infarction was induced in 21 pigs by balloon coronary occlusion. Scar samples were obtained at 4 weeks, stained with Masson's trichrome, Picrosirius red, and Hematoxylin-Eosin (H&E), and photographed using light, polarized light microscopy, and confocal microscopy, respectively. Masson's trichrome images were also optimized to remove non-collagenous structures. Two observers measured CBO by means of a semi-automated, Fourier analysis protocol. Interrater reliability and comparability between techniques were studied by the intraclass correlation coefficient (ICC) and Bland-Altman (B&A) plots and limits of agreement. Fourier analysis showed an almost perfect interrater reliability for each technique (ICC >= 0.95, p < 0.001 in all cases). CBO showed more randomly oriented values in Masson's trichrome and worse comparability with other techniques (ICC vs. Picrosirius red: 0.79 [0.47-0.91], p = 0.001; vs. H&E-confocal: 0.70 [0.26-0.88], p = 0.005). However, optimized Masson's trichrome showed almost perfect agreement with Picrosirius red (ICC 0.84 [0.6-0.94], p < 0.001) and H&E-confocal (ICC 0.81 [0.54-0.92], p < 0.001), as well as these latter techniques between each other (ICC 0.84 [0.60-0.93], p < 0.001). In summary, a semi-automated, Fourier-based method can provide highly reproducible CBO measurements in four different histopathological techniques. Masson's trichrome tends to provide more randomly oriented CBO index values, probably due to non-specific visualization of non-collagenous structures. However, optimization of Masson's trichrome microphotographs to remove non-collagenous components provides an almost perfect comparability between this technique, Picrosirius red and H&E-confocal. es_ES
dc.description.sponsorship Open Access funding provided thanks to the CRUE-CSIC agreement with Springer Nature. This work was supported by grants from "Instituto de Salud Carlos III" and "Fondos Europeos de Desarrollo Regional FEDER" [Grant numbers PI20/00637, and CIBERCV16/11/00486, a postgraduate contract FI18/00320 to C.R.-N. and CM21/00175 to V. M.-G.], by Conselleria de Educacion-Generalitat Valenciana (PROMETEO/2021/008). J. G. acknowledges financial support from the "Agencia Estatal de Investigacion" (Grant FJC2020-043981-I/AEI/1013039/501100011033). es_ES
dc.language Inglés es_ES
dc.publisher Springer-Verlag es_ES
dc.relation.ispartof Histochemistry and Cell Biology es_ES
dc.rights Reconocimiento (by) es_ES
dc.subject Myocardial infarction es_ES
dc.subject Scar es_ES
dc.subject Collagen es_ES
dc.subject Orientation es_ES
dc.subject Fourier es_ES
dc.title Fourier analysis of collagen bundle orientation in myocardial infarction scars es_ES
dc.type Artículo es_ES
dc.identifier.doi 10.1007/s00418-022-02132-x es_ES
dc.relation.projectID info:eu-repo/grantAgreement/ISCIII/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020 (ISCIII)/PI20%2F00637/ES/RESOLUCION DE LA OBSTRUCCION MICROVASCULAR TRAS UN INFARTO DE MIOCARDIO: EVALUACION DE LAS CONSECUENCIAS ESTRUCTURALES Y CLINICAS Y BUSQUEDA DE NUEVAS OPCIONES TERAPEUTICAS./ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/FEDER//CIBERCV16%2F11%2F00486/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/GVA//PROMETEO%2F2021%2F008/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/ISCIII//FI18%2F00320/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/ISCIII//CM21%2F00175/ es_ES
dc.relation.projectID info:eu-repo/grantAgreement/AEI//FJC2020-043981-I/ es_ES
dc.rights.accessRights Abierto es_ES
dc.description.bibliographicCitation Marcos-Garcés, V.; Rios-Navarro, C.; Gómez-Torres, F.; Gavara-Doñate, J.; De Dios, E.; Diaz, A.; Miñana, G.... (2022). Fourier analysis of collagen bundle orientation in myocardial infarction scars. Histochemistry and Cell Biology. 158(5):471-483. https://doi.org/10.1007/s00418-022-02132-x es_ES
dc.description.accrualMethod S es_ES
dc.relation.publisherversion https://doi.org/10.1007/s00418-022-02132-x es_ES
dc.description.upvformatpinicio 471 es_ES
dc.description.upvformatpfin 483 es_ES
dc.type.version info:eu-repo/semantics/publishedVersion es_ES
dc.description.volume 158 es_ES
dc.description.issue 5 es_ES
dc.identifier.pmid 35948735 es_ES
dc.identifier.pmcid PMC9630212 es_ES
dc.relation.pasarela S\481713 es_ES
dc.contributor.funder Generalitat Valenciana es_ES
dc.contributor.funder Instituto de Salud Carlos III es_ES
dc.contributor.funder Agencia Estatal de Investigación es_ES
dc.contributor.funder European Regional Development Fund es_ES
dc.description.references Baak JPA (2002) The framework of pathology: good laboratory practice by quantitative and molecular methods. J Pathol 198:277–283. https://doi.org/10.1002/path.1233 es_ES
dc.description.references Bancroft JD, Layton C (2013) Chapter 11: Connective and mesenchymal tissues with their stains. Bancroft’s Theory and Practice of Histological Techniques, 7th edn. Churchill Livingstone. Elsevier, Amsterdam, pp 187–214 es_ES
dc.description.references Bland JM, Altman DG (1986) Statistical methods for assessing agreement between two methods of clinical measurement. Lancet Lond Engl 1:307–310 es_ES
dc.description.references Bugg D, Bretherton R, Kim P et al (2020) Infarct Collagen topography regulates fibroblast fate via p38-yes-associated protein transcriptional enhanced associate domain signals. Circ Res 127:1306–1322. https://doi.org/10.1161/CIRCRESAHA.119.316162 es_ES
dc.description.references Fomovsky GM, Rouillard AD, Holmes JW (2012) Regional mechanics determine collagen fiber structure in healing myocardial infarcts. J Mol Cell Cardiol 52:1083–1090. https://doi.org/10.1016/j.yjmcc.2012.02.012 es_ES
dc.description.references Frangogiannis NG (2014) The inflammatory response in myocardial injury, repair and remodelling. Nat Rev Cardiol 11:255–265. https://doi.org/10.1038/nrcardio.2014.28 es_ES
dc.description.references Frangogiannis NG (2017) The extracellular matrix in myocardial injury, repair, and remodeling. J Clin Invest 127:1600–1612. https://doi.org/10.1172/JCI87491 es_ES
dc.description.references Gabriel-Costa D (2018) The pathophysiology of myocardial infarction-induced heart failure. Pathophysiology 25:277–284. https://doi.org/10.1016/j.pathophys.2018.04.003 es_ES
dc.description.references Hervas A, Ruiz-Sauri A, de Dios E et al (2016) Inhomogeneity of collagen organization within the fibrotic scar after myocardial infarction: results in a swine model and in human samples. J Anat 228:47–58. https://doi.org/10.1111/joa.12395 es_ES
dc.description.references Heusch G (2020) Myocardial ischaemia–reperfusion injury and cardioprotection in perspective. Nat Rev Cardiol 17:773–789. https://doi.org/10.1038/s41569-020-0403-y es_ES
dc.description.references Heusch G, Gersh BJ (2016) The pathophysiology of acute myocardial infarction and strategies of protection beyond reperfusion: a continual challenge. Eur Heart J. https://doi.org/10.1093/eurheartj/ehw224 es_ES
dc.description.references Iles LM, Ellims AH, Llewellyn H et al (2015) Histological validation of cardiac magnetic resonance analysis of regional and diffuse interstitial myocardial fibrosis. Eur Heart J - Cardiovasc Imaging 16:14–22. https://doi.org/10.1093/ehjci/jeu182 es_ES
dc.description.references Junqueira LC, Bignolas G, Brentani RR (1979) Picrosirius staining plus polarization microscopy, a specific method for collagen detection in tissue sections. Histochem J 11:447–455. https://doi.org/10.1007/BF01002772 es_ES
dc.description.references Kanitakis J (2002) Anatomy, histology and immunohistochemistry of normal human skin. Eur J Dermatol EJD 12:390–399 (quiz 400–401) es_ES
dc.description.references Kischer CW, Shetlar MR (1979) Electron microscopic studies of connective tissue repair after myocardial injury. Tex Rep Biol Med 39:357–369 es_ES
dc.description.references Korenczuk CE, Barocas VH, Richardson WJ (2019) Effects of collagen heterogeneity on myocardial infarct mechanics in a multiscale fiber network model. J Biomech Eng 141:091015. https://doi.org/10.1115/1.4043865 es_ES
dc.description.references Laurinavicius A, Laurinaviciene A, Dasevicius D et al (2012) Digital image analysis in pathology: benefits and obligation. Anal Cell Pathol Amst 35:75–78. https://doi.org/10.3233/ACP-2011-0033 es_ES
dc.description.references Li W (2020) Biomechanics of infarcted left ventricle: a review of modelling. Biomed Eng Lett 10:387–417. https://doi.org/10.1007/s13534-020-00159-4 es_ES
dc.description.references Lin J, Shi Y, Men Y et al (2020) Mechanical roles in formation of oriented collagen fibers. Tissue Eng Part B Rev 26:116–128. https://doi.org/10.1089/ten.teb.2019.0243 es_ES
dc.description.references Lindsey ML, Brunt KR, Kirk JA et al (2021) Guidelines for in vivo mouse models of myocardial infarction. Am J Physiol-Heart Circ Physiol 321:H1056–H1073. https://doi.org/10.1152/ajpheart.00459.2021 es_ES
dc.description.references Ma Y, de Castro Brás LE, Toba H et al (2014) Myofibroblasts and the extracellular matrix network in post-myocardial infarction cardiac remodeling. Pflüg Arch - Eur J Physiol. https://doi.org/10.1007/s00424-014-1463-9 es_ES
dc.description.references Marcos-Garcés V, Harvat M, Molina Aguilar P et al (2017) Comparative measurement of collagen bundle orientation by Fourier analysis and semiquantitative evaluation: reliability and agreement in Masson’s trichrome, Picrosirius red and confocal microscopy techniques. J Microsc. https://doi.org/10.1111/jmi.12553 es_ES
dc.description.references Moreo A, Ambrosio G, De Chiara B et al (2009) Influence of myocardial fibrosis on left ventricular diastolic function: noninvasive assessment by cardiac magnetic resonance and echo. Circ Cardiovasc Imaging 2:437–443. https://doi.org/10.1161/CIRCIMAGING.108.838367 es_ES
dc.description.references Mostaço-Guidolin L, Rosin N, Hackett T-L (2017) Imaging collagen in scar tissue: developments in second harmonic generation microscopy for biomedical applications. Int J Mol Sci 18:1772. https://doi.org/10.3390/ijms18081772 es_ES
dc.description.references Nong Z, O’Neil C, Lei M et al (2011) Type I collagen cleavage is essential for effective fibrotic repair after myocardial infarction. Am J Pathol 179:2189–2198. https://doi.org/10.1016/j.ajpath.2011.07.017 es_ES
dc.description.references Osman OS, Selway JL, Harikumar PE et al (2013) A novel method to assess collagen architecture in skin. BMC Bioinformatics 14:260. https://doi.org/10.1186/1471-2105-14-260 es_ES
dc.description.references Perez-Terol I, Rios-Navarro C, de Dios E et al (2019) Magnetic resonance microscopy and correlative histopathology of the infarcted heart. Sci Rep 9:20017. https://doi.org/10.1038/s41598-019-56436-5 es_ES
dc.description.references Prabhu SD, Frangogiannis NG (2016) The biological basis for cardiac repair after myocardial infarction: from inflammation to fibrosis. Circ Res 119:91–112. https://doi.org/10.1161/CIRCRESAHA.116.303577 es_ES
dc.description.references Quinn KP, Sullivan KE, Liu Z et al (2016) Optical metrics of the extracellular matrix predict compositional and mechanical changes after myocardial infarction. Sci Rep. https://doi.org/10.1038/srep35823 es_ES
dc.description.references Richardson W, Clarke S, Quinn T, Holmes J (2015) Physiological implications of myocardial scar structure. Compr Physiol 5:1877–1909. https://doi.org/10.1002/cphy.c140067 es_ES
dc.description.references Richardson WJ, Holmes JW (2016) Emergence of collagen orientation heterogeneity in healing infarcts and an agent-based model. Biophys J 110:2266–2277. https://doi.org/10.1016/j.bpj.2016.04.014 es_ES
dc.description.references Rog-Zielinska EA, Norris RA, Kohl P, Markwald R (2016) The living scar-cardiac fibroblasts and the injured heart. Trends Mol Med 22:99–114. https://doi.org/10.1016/j.molmed.2015.12.006 es_ES
dc.description.references Ross Stewart KM, Walker SL, Baker AH et al (2021) Hooked on heart regeneration: the zebrafish guide to recovery. Cardiovasc Res. https://doi.org/10.1093/cvr/cvab214 es_ES
dc.description.references Rouillard AD, Holmes JW (2012) Mechanical regulation of fibroblast migration and collagen remodelling in healing myocardial infarcts: Mechanics determine infarct collagen alignment. J Physiol 590:4585–4602. https://doi.org/10.1113/jphysiol.2012.229484 es_ES
dc.description.references Rusu M, Hilse K, Schuh A et al (2019) Biomechanical assessment of remote and postinfarction scar remodeling following myocardial infarction. Sci Rep 9:16744. https://doi.org/10.1038/s41598-019-53351-7 es_ES
dc.description.references Ryan R, Moyse BR, Richardson RJ (2020) Zebrafish cardiac regeneration—looking beyond cardiomyocytes to a complex microenvironment. Histochem Cell Biol 154:533–548. https://doi.org/10.1007/s00418-020-01913-6 es_ES
dc.description.references Saeed M, Weber O, Lee R et al (2006) Discrimination of myocardial acute and chronic (Scar) infarctions on delayed contrast enhanced magnetic resonance imaging with intravascular magnetic resonance contrast media. J Am Coll Cardiol 48:1961–1968. https://doi.org/10.1016/j.jacc.2006.03.071 es_ES
dc.description.references Seo BR, Chen X, Ling L et al (2020) Collagen microarchitecture mechanically controls myofibroblast differentiation. Proc Natl Acad Sci 117:11387–11398. https://doi.org/10.1073/pnas.1919394117 es_ES
dc.description.references Shechtman O (2013) The Coefficient of Variation as an Index of Measurement Reliability. In: Doi SAR, Williams GM (eds) Methods of Clinical Epidemiology. Springer, Berlin Heidelberg, Berlin, Heidelberg, pp 39–49 es_ES
dc.description.references van Zuijlen PPM, de Vries HJC, Lamme EN et al (2002) Morphometry of dermal collagen orientation by Fourier analysis is superior to multi-observer assessment. J Pathol 198:284–291. https://doi.org/10.1002/path.1219 es_ES
dc.description.references Verhaegen PD, Schouten HJ, Tigchelaar-Gutter W et al (2012a) Adaptation of the dermal collagen structure of human skin and scar tissue in response to stretch: an experimental study: collagen adaptation in response to stretch. Wound Repair Regen 20:658–666. https://doi.org/10.1111/j.1524-475X.2012.00827.x es_ES
dc.description.references Verhaegen PDHM, Marle JV, Kuehne A et al (2012b) Collagen bundle morphometry in skin and scar tissue: a novel distance mapping method provides superior measurements compared to Fourier analysis. J Microsc 245:82–89. https://doi.org/10.1111/j.1365-2818.2011.03547.x es_ES
dc.description.references Voorhees AP, Han H-C (2014) A model to determine the effect of collagen fiber alignment on heart function post myocardial infarction. Theor Biol Med Model 11:6. https://doi.org/10.1186/1742-4682-11-6 es_ES
dc.description.references Wang L, Singh H, Mulyala RR et al (2020) The association between left ventricular diastolic dysfunction and myocardial scar and their collective impact on all-cause mortality. J Am Soc Echocardiogr 33:161–170. https://doi.org/10.1016/j.echo.2019.09.022 es_ES
dc.description.references Whittaker P, Boughner DR, Kloner RA (1989) Analysis of healing after myocardial infarction using polarized light microscopy. Am J Pathol 134:879–893 es_ES
dc.description.references Zimmerman SD, Karlon WJ, Holmes JW et al (2000) Structural and mechanical factors influencing infarct scar collagen organization. Am J Physiol Heart Circ Physiol 278:H194-200. https://doi.org/10.1152/ajpheart.2000.278.1.H194 es_ES


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