Skip to main content
Top
Published in: Journal of Cardiovascular Translational Research 4/2016

01-08-2016 | Original Article

A Multidisciplinary Assessment of Remote Myocardial Fibrosis After Reperfused Myocardial Infarction in Swine and Patients

Authors: Arantxa Hervas, Amparo Ruiz-Sauri, Jose Gavara, Jose V. Monmeneu, Elena de Dios, Cesar Rios-Navarro, Nerea Perez-Sole, Itziar Perez, Daniel Monleon, Jose M. Morales, Gema Minana, Julio Nunez, Clara Bonanad, Ana Diaz, Jose M. Vila, Francisco J. Chorro, Vicente Bodi

Published in: Journal of Cardiovascular Translational Research | Issue 4/2016

Login to get access

Abstract

In extensive nonreperfused myocardial infarction (MI), remote fibrosis has been documented. Early reperfusion by primary angioplasty represents the gold standard method to minimize the extension of the infarction. We aimed to ascertain whether fibrosis also affects remote regions in reperfused MI in swine and patients. Swine were subjected to a transient occlusion of the left anterior descending artery followed by 1-week or 1-month reperfusion. Collagen content in the remote area macroscopically, microscopically, by magnetic resonance microimaging, and at the molecular level was similar to controls. In patients with previous MI, samples from autopsies displayed a significant increase in collagen content only in the infarct region. In patients with previous MI submitted to cardiac magnetic resonance-T1 mapping, the extracellular volume fraction in remote segments was similar to that for controls. In all scenarios, the remote region did not show a significant increase of collagen content in comparison with controls.
Appendix
Available only for authorised users
Literature
1.
go back to reference van den Borne, S. W. M., Diez, J., Blankesteijn, W. M., Verjans, J., Hofstra, L., & Narula, J. (2010). Myocardial remodeling after infarction: the role of myofibroblasts. Nature Reviews Cardiology, 7, 30–37.CrossRefPubMed van den Borne, S. W. M., Diez, J., Blankesteijn, W. M., Verjans, J., Hofstra, L., & Narula, J. (2010). Myocardial remodeling after infarction: the role of myofibroblasts. Nature Reviews Cardiology, 7, 30–37.CrossRefPubMed
2.
go back to reference Daskalopoulos, E. P., Janssen, B. J. A., & Blankesteijn, W. M. (2012). Myofibroblasts in the infarct area: concepts and challenges. Microscopy and Microanalysis, 18, 35–49.CrossRefPubMed Daskalopoulos, E. P., Janssen, B. J. A., & Blankesteijn, W. M. (2012). Myofibroblasts in the infarct area: concepts and challenges. Microscopy and Microanalysis, 18, 35–49.CrossRefPubMed
3.
go back to reference Beltrami, C. A., Finato, N., Rocco, M., Feruglio, G. A., Puricelli, C., Cigola, E., Quaini, F., Sonnenblick, E. H., Olivetti, G., & Anversa, P. (1994). Structural basis of end-stage failure in ischemic cardiomyopathy in humans. Circulation, 89, 151–163.CrossRefPubMed Beltrami, C. A., Finato, N., Rocco, M., Feruglio, G. A., Puricelli, C., Cigola, E., Quaini, F., Sonnenblick, E. H., Olivetti, G., & Anversa, P. (1994). Structural basis of end-stage failure in ischemic cardiomyopathy in humans. Circulation, 89, 151–163.CrossRefPubMed
4.
go back to reference Cleutjens, J. P. M., Verluyten, M. J. A., Smiths, J. F. M., & Daemen, M. J. A. P. (1995). Collagen remodeling after myocardial infarction in the rat heart. American Journal of Pathology, 147, 325–338.PubMedPubMedCentral Cleutjens, J. P. M., Verluyten, M. J. A., Smiths, J. F. M., & Daemen, M. J. A. P. (1995). Collagen remodeling after myocardial infarction in the rat heart. American Journal of Pathology, 147, 325–338.PubMedPubMedCentral
5.
go back to reference Sun, Y., & Weber, K. T. (2000). Infarct scar: a dynamic tissue. Cardiovascular Research, 46, 250–256.CrossRefPubMed Sun, Y., & Weber, K. T. (2000). Infarct scar: a dynamic tissue. Cardiovascular Research, 46, 250–256.CrossRefPubMed
6.
go back to reference Sun, Y., Zhang, J. Q., Zhang, J., & Lamparter, S. (2000). Cardiac remodeling by fibrous tissue after infarction in rats. Journal of Laboratory and Clinical Medicine, 135, 316–323.CrossRefPubMed Sun, Y., Zhang, J. Q., Zhang, J., & Lamparter, S. (2000). Cardiac remodeling by fibrous tissue after infarction in rats. Journal of Laboratory and Clinical Medicine, 135, 316–323.CrossRefPubMed
7.
go back to reference Sun, Y. (2009). Myocardial repair/remodelling following infarction: roles of local factors. Cardiovascular Research, 81, 482–490.CrossRefPubMed Sun, Y. (2009). Myocardial repair/remodelling following infarction: roles of local factors. Cardiovascular Research, 81, 482–490.CrossRefPubMed
8.
go back to reference dos Santos, L., Gonçalves, G. A., Davel, A. P., Santos, A. A., Krieger, J. E., Rossoni, L. V., & Tucci, P. J. (2013). Cell therapy prevents structural, functional and molecular remodeling of remote non-infarcted myocardium. International Journal of Cardiology, 168, 3829–3836.CrossRefPubMed dos Santos, L., Gonçalves, G. A., Davel, A. P., Santos, A. A., Krieger, J. E., Rossoni, L. V., & Tucci, P. J. (2013). Cell therapy prevents structural, functional and molecular remodeling of remote non-infarcted myocardium. International Journal of Cardiology, 168, 3829–3836.CrossRefPubMed
9.
go back to reference Hervas, A., de Dios, E., Forteza, M. J., Miñana, G., Nuñez, J., Ruiz-Sauri, A., Bonanad, C., Perez-Sole, N., Chorro, F. J., & Bodi, V. (2015). Intracoronary infusion of thioflavin-S to study microvascular obstruction in a model of myocardial infarction. Revista Española de Cardiología, 68, 928–934.CrossRefPubMed Hervas, A., de Dios, E., Forteza, M. J., Miñana, G., Nuñez, J., Ruiz-Sauri, A., Bonanad, C., Perez-Sole, N., Chorro, F. J., & Bodi, V. (2015). Intracoronary infusion of thioflavin-S to study microvascular obstruction in a model of myocardial infarction. Revista Española de Cardiología, 68, 928–934.CrossRefPubMed
10.
go back to reference Hervas, A., Ruiz-Sauri, A., de Dios, E., Forteza, M. J., Minana, G., Nunez, J., Gomez, C., Bonanad, C., Perez-Sole, N., Gavara, J., Chorro, F. J., & Bodi, V. (2016). Inhomogeneity of collagen organization within the fibrotic scar after myocardial infarction: results in a swine model and in human samples. Journal of Anatomy, 228, 47–58.CrossRefPubMed Hervas, A., Ruiz-Sauri, A., de Dios, E., Forteza, M. J., Minana, G., Nunez, J., Gomez, C., Bonanad, C., Perez-Sole, N., Gavara, J., Chorro, F. J., & Bodi, V. (2016). Inhomogeneity of collagen organization within the fibrotic scar after myocardial infarction: results in a swine model and in human samples. Journal of Anatomy, 228, 47–58.CrossRefPubMed
11.
go back to reference Marijianowski, M. M. H., Teeling, P., & Becker, A. E. (1997). Remodeling after myocardial infarction in humans is not associated with interstitial fibrosis of noninfarcted myocardium. Journal of the American College of Cardiology, 30, 76–82.CrossRefPubMed Marijianowski, M. M. H., Teeling, P., & Becker, A. E. (1997). Remodeling after myocardial infarction in humans is not associated with interstitial fibrosis of noninfarcted myocardium. Journal of the American College of Cardiology, 30, 76–82.CrossRefPubMed
12.
go back to reference Tarkia, M., Stark, C., Haavisto, M., Kentala, R., Vähäsilta, T., Savunen, T., Strandberg, M., Hynninen, V. V., Saunavaara, V., Tolvanen, T., Teräs, M., Rokka, J., Pietilä, M., Saukko, P., Roivainen, A., Saraste, A., & Knuuti, J. (2015). Cardiac remodeling in a new pig model of chronic heart failure: assessment of left ventricular functional, metabolic, and structural changes using PET, CT, and echocardiography. Journal of Nuclear Cardiology, 22, 655–665.CrossRefPubMed Tarkia, M., Stark, C., Haavisto, M., Kentala, R., Vähäsilta, T., Savunen, T., Strandberg, M., Hynninen, V. V., Saunavaara, V., Tolvanen, T., Teräs, M., Rokka, J., Pietilä, M., Saukko, P., Roivainen, A., Saraste, A., & Knuuti, J. (2015). Cardiac remodeling in a new pig model of chronic heart failure: assessment of left ventricular functional, metabolic, and structural changes using PET, CT, and echocardiography. Journal of Nuclear Cardiology, 22, 655–665.CrossRefPubMed
13.
go back to reference van den Borne, S. W. M., Isobe, S., Verjans, J. W., Petrov, A., Lovhaug, D., Li, P., Zandbergen, H. R., Ni, Y., Frederik, P., Zhou, J., Arbo, B., Rogstad, A., Cuthbertson, A., Chettibi, S., Reutelingsperger, C., Blankesteijn, W. M., Smits, J. F., Daemen, M. J., Zannad, F., Vannan, M. A., Narula, N., Pitt, B., Hofstra, L., & Narula, J. (2008). Molecular imaging of interstitial alterations in remodeling myocardium after myocardial infarction. Journal of the American College of Cardiology, 52, 2017–2028.CrossRefPubMed van den Borne, S. W. M., Isobe, S., Verjans, J. W., Petrov, A., Lovhaug, D., Li, P., Zandbergen, H. R., Ni, Y., Frederik, P., Zhou, J., Arbo, B., Rogstad, A., Cuthbertson, A., Chettibi, S., Reutelingsperger, C., Blankesteijn, W. M., Smits, J. F., Daemen, M. J., Zannad, F., Vannan, M. A., Narula, N., Pitt, B., Hofstra, L., & Narula, J. (2008). Molecular imaging of interstitial alterations in remodeling myocardium after myocardial infarction. Journal of the American College of Cardiology, 52, 2017–2028.CrossRefPubMed
14.
go back to reference Prat-Vidal, C., Gálvez-Montón, C., Nonell, L., Puigdecanet, E., Astier, L., Solé, F., & Bayes-Genis, A. (2013). Identification of temporal and region-specific myocardial gene expression patterns in response to infarction in swine. PLoS ONE, 8, e54785.CrossRefPubMedPubMedCentral Prat-Vidal, C., Gálvez-Montón, C., Nonell, L., Puigdecanet, E., Astier, L., Solé, F., & Bayes-Genis, A. (2013). Identification of temporal and region-specific myocardial gene expression patterns in response to infarction in swine. PLoS ONE, 8, e54785.CrossRefPubMedPubMedCentral
15.
go back to reference Monreal, G., Nicholson, L. M., Han, B., Joshi, M. S., Phillips, A. B., Wold, L. E., Bauer, J. A., & Gerhardt, M. A. (2008). Cytoskeletal remodeling of desmin is a more accurate measure of cardiac dysfunction than fibrosis or myocyte hypertrophy. Life Sciences, 83, 786–794.CrossRefPubMed Monreal, G., Nicholson, L. M., Han, B., Joshi, M. S., Phillips, A. B., Wold, L. E., Bauer, J. A., & Gerhardt, M. A. (2008). Cytoskeletal remodeling of desmin is a more accurate measure of cardiac dysfunction than fibrosis or myocyte hypertrophy. Life Sciences, 83, 786–794.CrossRefPubMed
16.
17.
go back to reference Vilahur, G., Juan-Babot, O., Peña, E., Oñate, B., Casaní, L., & Badimon, L. (2011). Molecular and cellular mechanisms involved in cardiac remodeling after acute myocardial infarction. Journal of Molecular and Cellular Cardiology, 50, 522–533.CrossRefPubMed Vilahur, G., Juan-Babot, O., Peña, E., Oñate, B., Casaní, L., & Badimon, L. (2011). Molecular and cellular mechanisms involved in cardiac remodeling after acute myocardial infarction. Journal of Molecular and Cellular Cardiology, 50, 522–533.CrossRefPubMed
18.
go back to reference Hao, J., Ju, H., Zhao, S., Junaid, A., Scammell-La Fleur, T., & Dixon, I. M. C. (1999). Elevation of expression of Smads 2, 3, and 4, decorin and TGF-beta in the chronic phase of myocardial infarct scar healing. Journal of Molecular and Cellular Cardiology, 31, 667–678.CrossRefPubMed Hao, J., Ju, H., Zhao, S., Junaid, A., Scammell-La Fleur, T., & Dixon, I. M. C. (1999). Elevation of expression of Smads 2, 3, and 4, decorin and TGF-beta in the chronic phase of myocardial infarct scar healing. Journal of Molecular and Cellular Cardiology, 31, 667–678.CrossRefPubMed
19.
go back to reference Willems, I. E. M. G., Havenith, M. G., De Mey, J. G. R., & Daemen, M. J. A. P. (1994). The alpha-smooth muscle actin-positive cells in healing human myocardial scars. American Journal of Pathology, 145, 868–875.PubMedPubMedCentral Willems, I. E. M. G., Havenith, M. G., De Mey, J. G. R., & Daemen, M. J. A. P. (1994). The alpha-smooth muscle actin-positive cells in healing human myocardial scars. American Journal of Pathology, 145, 868–875.PubMedPubMedCentral
20.
go back to reference Gonzalez-Segura, A., Morales, J. M., Gonzalez-Darder, J. M., Cardona-Marsal, R., Lopez-Gines, C., Cerda-Nicolas, M., & Monleon, D. (2011). Magnetic resonance microscopy at 14 Tesla and correlative histopathology of human brain tumor tissue. PLoS One, 6, e27442.CrossRefPubMedPubMedCentral Gonzalez-Segura, A., Morales, J. M., Gonzalez-Darder, J. M., Cardona-Marsal, R., Lopez-Gines, C., Cerda-Nicolas, M., & Monleon, D. (2011). Magnetic resonance microscopy at 14 Tesla and correlative histopathology of human brain tumor tissue. PLoS One, 6, e27442.CrossRefPubMedPubMedCentral
21.
go back to reference White, S. K., Sado, D. M., Fontana, M., Banypersad, S. M., Maestrini, V., Flett, A. S., Piechnik, S. K., Robson, M. D., Hausenloy, D. J., Sheikh, A. M., Hawkins, P. N., & Moon, J. C. (2013). T1 mapping for myocardial extracellular volume measurement by CMR: bolus only versus primed infusion technique. JACC. Cardiovascular Imaging, 6, 955–962.CrossRefPubMed White, S. K., Sado, D. M., Fontana, M., Banypersad, S. M., Maestrini, V., Flett, A. S., Piechnik, S. K., Robson, M. D., Hausenloy, D. J., Sheikh, A. M., Hawkins, P. N., & Moon, J. C. (2013). T1 mapping for myocardial extracellular volume measurement by CMR: bolus only versus primed infusion technique. JACC. Cardiovascular Imaging, 6, 955–962.CrossRefPubMed
22.
go back to reference Ugander, M., Oki, A. J., Hsu, L. Y., Kellman, P., Greiser, A., Aletras, A. H., Sibley, C. T., Chen, M. Y., Bandettini, W. P., & Arai, A. E. (2012). Extracellular volume imaging by magnetic resonance imaging provides insights into overt and sub-clinical myocardial pathology. European Heart Journal, 33, 1268–1278.CrossRefPubMedPubMedCentral Ugander, M., Oki, A. J., Hsu, L. Y., Kellman, P., Greiser, A., Aletras, A. H., Sibley, C. T., Chen, M. Y., Bandettini, W. P., & Arai, A. E. (2012). Extracellular volume imaging by magnetic resonance imaging provides insights into overt and sub-clinical myocardial pathology. European Heart Journal, 33, 1268–1278.CrossRefPubMedPubMedCentral
24.
go back to reference Olivetti, G., Melissari, M., Capasso, J. M., & Anversa, P. (1991). Cardiomyopathy of the aging human heart. Myocyte loss and reactive cellular hypertrophy. Circulation Research, 68, 1560–1568.CrossRefPubMed Olivetti, G., Melissari, M., Capasso, J. M., & Anversa, P. (1991). Cardiomyopathy of the aging human heart. Myocyte loss and reactive cellular hypertrophy. Circulation Research, 68, 1560–1568.CrossRefPubMed
Metadata
Title
A Multidisciplinary Assessment of Remote Myocardial Fibrosis After Reperfused Myocardial Infarction in Swine and Patients
Authors
Arantxa Hervas
Amparo Ruiz-Sauri
Jose Gavara
Jose V. Monmeneu
Elena de Dios
Cesar Rios-Navarro
Nerea Perez-Sole
Itziar Perez
Daniel Monleon
Jose M. Morales
Gema Minana
Julio Nunez
Clara Bonanad
Ana Diaz
Jose M. Vila
Francisco J. Chorro
Vicente Bodi
Publication date
01-08-2016
Publisher
Springer US
Published in
Journal of Cardiovascular Translational Research / Issue 4/2016
Print ISSN: 1937-5387
Electronic ISSN: 1937-5395
DOI
https://doi.org/10.1007/s12265-016-9698-9

Other articles of this Issue 4/2016

Journal of Cardiovascular Translational Research 4/2016 Go to the issue