Abstract
Aim:
To investigate the relationship between the collateral circulation and contrast-enhanced MR signal change for myocardial infarction (MI) in pigs.
Methods:
Pigs underwent permanent ligation of two diagonal branches of the left anterior descending artery. First-pass perfusion (FPP) MRI (for detecting myocardial perfusion abnormalities) and delayed enhancement (DE) MRI (for estimating myocardial infarction) using Gd-DTPA were performed at 2 h, 7 d and 4 weeks after the coronary occlusion. Myocardial blood flow (MBF) was evaluated using nonradioactive red-colored microspheres. Histological examination was performed to characterize the infarcts.
Results:
Acute MI performed at 2 h afterwards was characterized by hypoenhancement in both FPP- and DE-MRI, with small and almost unchanged FPP-signal intensity (SI) and DE-SI due to negligible MBF. Subacute MI detected 7 d afterwards showed small but significantly increaseing FPP-SI, and was visible as a sluggish hyperenhancement in DE-MRI with considerably higher DE-SI compared to the normal myocardium; the MBF approached the half-normal value. Chronic MI detected at 4 weeks afterwards showed increasing FPP-SI comparable to the normal myocardium, and a rapid hyperenhancement in DE-MRI with even higher DE-SI; the MBF was close to the normal value. The MBF was correlated with FPP-SI (r=+0.94, P<0.01) and with the peak DE-SI (r=+0.92, P<0.01) at the three MI stages. Remodeled vessels were observed at intra-infarction and peri-infarction zones during the subacute and chronic periods.
Conclusion:
Progressive collateral recovery determines the characteristic profiles of contrast-enhanced MRI in acute, subacute and chronic myocardial infarction in pigs. The FPP- and DE-MRI signal profiles not only depend on the loss of tissue viability and enlarged interstitial space, but also on establishing a collateral circulation.
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References
Klein C, Schmal TR, Nekolla SG, Schnackenburg B, Fleck E, Nagel E . Mechanism of late gadolinium enhancement in patients with acute myocardial infarction. J Cardiovasc Magn Reson 2007; 9: 653–8.
Pereira RS, Prato FS, Wisenberg G, Sykes J . The determination of myocardial viability using Gd-DTPA in a canine model of acute myocardial ischemia and reperfusion. Magn Reson Med 1996; 36: 684–93.
Pereira RS, Prato FS, Lekx KS, Sykes J, Wisenberg G . Contrast-enhanced MRI for the assessment of myocardial viability after permanent coronary artery occlusion. Magn Reson Med 2000; 44: 309–16.
Rehwald WG, Fieno DS, Chen EL, Kim RJ, Judd RM . Myocardial magnetic resonance imaging contrast agent concentrations after reversible and irreversible ischemic injury. Circulation 2002; 105: 224–9.
Klein C, Nekolla SG, Balbach T, Schnackenburg B, Nagel E, Fleck E, et al. The influence of myocardial blood flow and volume of distribution on late Gd-DTPA kinetics in ischemic heart failure. J Magn Reson Imaging 2004; 20: 588–93.
Kirschner R, Toth L, Varga-Szemes A, Simor T, Suranyi P, Kiss P, et al. Differentiation of acute and four-week old myocardial infarct with Gd(ABE-DTTA)-enhanced CMR. J Cardiovasc Magn Reson 2010; 12: 22.
Abdel-Aty H, Zagrosek A, Schulz-Menger J, Taylor AJ, Messroghli D, Kumar A, et al. Delayed enhancement and T2-weighted cardiovascular magnetic resonance imaging differentiate acute from chronic myocardial infarction. Circulation 2004; 109: 2411–6.
Judd RM, Lugo-Olivieri CH, Arai M, Kondo T, Croisille P, Lima JA, et al. Physiological basis of myocardial contrast enhancement in fast magnetic resonance images of 2-day-old reperfused canine infarcts. Circulation 1995; 92: 1902–10.
Rochitte CE, Lima JA, Bluemke DA, Reeder SB, McVeigh ER, Furuta T, et al. Magnitude and time course of microvascular obstruction and tissue injury after acute myocardial infarction. Circulation 1998; 98: 1006–14.
Bremerich J, Wendland MF, Arheden H, Wyttenbach R, Gao DW, Huberty JP, et al. Microvascular injury in reperfused infarcted myocardium: noninvasive assessment with contrast-enhanced echoplanar magnetic resonance imaging. J Am Coll Cardiol 1998; 32: 787–93.
Kim RJ, Chen EL, Lima JA, Judd RM . Myocardial Gd-DTPA kinetics determine MRI contrast enhancement and reflect the extent and severity of myocardial injury after acute reperfused infarction. Circulation 1996; 94: 3318–26.
Yang Y, Graham JJ, Connelly K, Foltz WD, Dick AJ, Wright GA . MRI manifestations of persistent microvascular obstruction and acute left ventricular remodeling in an experimental reperfused myocardial infarction. Quant Imaging Med Surg 2012; 2: 12–20.
Mather AN, Fairbairn TA, Artis NJ, Greenwood JP, Plein S . Timing of cardiovascular MR imaging after acute myocardial infarction: effect on estimates of infarct characteristics and prediction of late ventricular remodeling. Radiology 2011; 261: 116–26.
Hearse DJ . Species variation in the coronary collateral circulation during regional myocardial ischaemia: a critical determinant of the rate of evolution and extent of myocardial infarction. Cardiovasc Res 2000; 45: 213–9.
Roth DM, Maruoka Y, Rogers J, White FC, Longhurst JC, Bloor CM . Development of coronary collateral circulation in left circumflex ameroid-occluded swine myocardium. Am J Physiol 1987; 253: H1279–88.
Simonetti OP, Kim RJ, Fieno DS, Hillenbrand HB, Wu E, Bundy JM, et al. An improved MR imaging technique for the visualization of myocardial infarction. Radiology 2001; 218: 215–23.
Lund GK, Stork A, Saeed M, Bansmann MP, Gerken JH, Müller V, et al. Acute myocardial infarction: evaluation with first-pass enhancement and delayed enhancement MR imaging compared with 201Tl SPECT imaging. Radiology 2004; 232: 49–57.
Gerber BL, Garot J, Bluemke DA, Wu KC, Lima JA . Accuracy of contrast-enhanced magnetic resonance imaging in predicting improvement of regional myocardial function in patients after acute myocardial infarction. Circulation 2002; 106: 1083–9.
Wilke N, Simm C, Zhang J, Ellermann J, Ya X, Merkle H, et al. Contrast-enhanced first pass myocardial perfusion imaging: correlation between myocardial blood flow in dogs at rest and during hyperemia. Magn Reson Med 1993; 29: 485–97.
Su MY, Yang KC, Wu CC, Wu YW, Yu HY, Tseng RY, et al. First-pass myocardial perfusion cardiovascular magnetic resonance at 3 Tesla. J Cardiovasc Magn Reson 2007; 9: 633–44.
Wilke N, Jerosch-Herold M, Wang Y, Huang Y, Christensen BV, Stillman AE, et al. Myocardial perfusion reserve: assessment with multisection, quantitative, first-pass MR imaging. Radiology 1997; 204: 373–84.
Lee SS, Goo HW, Park SB, Lim CH, Gong G, Seo JB, et al. MR imaging of reperfused myocardial infarction: comparison of necrosis-specific and intravascular contrast agents in a cat model. Radiology 2003; 226: 739–47.
Wang Y, Sun W, Cao G, Meng L, Song L, Du X . Delayed hyperenhancement patterns in occlusive and reperfused myocardial infarcts during different healing stages. J Magn Reson Imaging 2006; 24: 851–7.
Görge G, Schmidt T, Ito BR, Pantely GA, Schaper W . Microvascular and collateral adaptation in swine hearts following progressive coronary artery stenosis. Basic Res Cardiol 1989; 84: 524–35.
Bloor CM, Liebow AA . Coronary collateral circulation. Am J Cardiol 1965; 16: 238–52.
Wang J, Liu HY, Lv H, Xiang B, Gruwel M, Tomanek B, et al. Identification of chronic myocardial infarction with extracellular or intravascular contrast agents in magnetic resonance imaging. Acta Pharmacol Sin 2008; 29: 65–73.
Wang J, Xiang B, Lin HY, Liu H, Freed D, Arora RC, et al. Pathological mechanism for delayed hyperenhancement of chronic scarred myocardium in contrast agent enhanced magnetic resonance imaging. PLoS One 2014; 9: e96463.
White FC, Carroll SM, Magnet A, Bloor CM . Coronary collateral development in swine after coronary artery occlusion. Circ Res 1992; 71: 1490–500.
Acknowledgements
We would like to acknowledge the funding support provided by the National Natural Science Foundation of China (No 81200105), the China Postdoctoral Science Foundation (No 20100470050), the Canadian Institute of Health Research (CIHR), and the National Research Council of Canada (NRC).
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Wang, J., Xiang, B., Lin, Hy. et al. Collateral circulation formation determines the characteristic profiles of contrast-enhanced MRI in the infarcted myocardium of pigs. Acta Pharmacol Sin 36, 463–472 (2015). https://doi.org/10.1038/aps.2014.158
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DOI: https://doi.org/10.1038/aps.2014.158


