Cardiovascular Imaging in Mice

Colin K.L. Phoon1, Daniel H. Turnbull2

1 Division of Pediatric Cardiology, Department of Pediatrics, New York University School of Medicine, New York, New York, 2 Skirball Institute of Biomolecular Medicine, New York University School of Medicine, New York, New York
Publication Name:  Current Protocols in Mouse Biology
Unit Number:   
DOI:  10.1002/9780470942390.mo150122
Online Posting Date:  March, 2016
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Abstract

The mouse is the mammalian model of choice for investigating cardiovascular biology, given our ability to manipulate it by genetic, pharmacologic, mechanical, and environmental means. Imaging is an important approach to phenotyping both function and structure of cardiac and vascular components. This review details commonly used imaging approaches, with a focus on echocardiography and magnetic resonance imaging and brief overviews of other imaging modalities. We also briefly outline emerging imaging approaches but caution that reliability and validity data may be lacking. © 2016 by John Wiley & Sons, Inc.

Keywords: Doppler; echocardiography; magnetic resonance imaging; mouse models; ultrasound biomicroscopy

     
 
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Table of Contents

  • Introduction
  • Imaging Conscious Versus Anesthetized Mice: Considerations for Anesthesia
  • Cardiac Imaging: Ultrasound (Echocardiography)
  • Vascular Imaging: Ultrasound
  • Cardiovascular MRI
  • Additional Specialized Cardiovascular Imaging Approaches
  • Acknowledgments
  • Conflicts of Interest
  • Literature Cited
  • Figures
  • Tables
     
 
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Materials

Basic Protocol 1:

  Materials
  • Mouse of interest
  • Isoflurane
  • Medical oxygen (optional)
  • 70% ethanol
  • Depilatory cream (if fur clippers are used for shaving)
  • Ultrasound (acoustic coupling) gel
  • Scale (to weigh mouse)
  • Anesthesia setup
  • Anesthetic induction chamber
  • Isoflurane distributor
  • Mouse anesthesia nosecone delivery system
  • High‐resolution ultrasound imaging system coupled to the anesthesia setup and to a warming pad that doubles as an imaging platform
  • Electrocardiography (EKG) system including EKG leads and electrodes (usually incorporated into imaging platform)
  • Strips of tape, cut to size (for paws)
  • Hair dryer (for warm air convection) or warming lamp
  • Razor blade (not safety razor) or fur clippers
  • Gauze pads or Kimwipes
  • Thermistor
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Figures

Videos

Literature Cited

Literature Cited
  Adams, D., Baldock, R., Bhattacharya, S., Copp, A.J., Dickinson, M., Greene, N.D., Henkelman, M., Justice, M., Mohun, T., Murray, S.A., Pauws, E., Raess, M., Rossant, J., Weaver, T., and West, D. 2013. Bloomsbury report on mouse embryo phenotyping: Recommendations from the IMPC workshop on embryonic lethal screening. Dis. Model Mech. 6:571‐579. doi: 10.1242/dmm.011833.
  Akki, A., Gupta, A., and Weiss, R.G. 2013. Magnetic resonance imaging and spectroscopy of the murine cardiovascular system. Am. J. Physiol. Heart Circ. Physiol. 304:H633‐H648.
  Anderson, G.A., Wong, M.D., Yang, J., and Henkelman, R.M. 2013. 3D imaging, registration, and analysis of the early mouse embryonic vasculature. Dev. Dynam. 242:527‐538. doi: 10.1002/dvdy.23947.
  Aristizábal, O., Ketterling, J.A., and Turnbull, D.H. 2006. 40‐MHz annular array imaging of mouse embryos. Ultrasound Med. Biol. 32:1631‐1637. doi: 10.1016/j.ultrasmedbio.2006.05.020.
  Aristizábal, O., Mamou, J., Turnbull, D.H., and Ketterling, J.A. 2009. Doppler‐derived trigger signals for high‐frame‐rate mouse cardiovascular imaging. Conf. Proc. IEEE Eng. Med. Biol. Soc. 1:1987‐1990.
  Aristizábal, O., Mamou, J., Ketterling, J.A., and Turnbull, D.H. 2013. High‐throughput, high‐frequency 3‐D ultrasound for in utero analysis of embryonic mouse brain development. Ultrasound Med. Biol. 39:2321‐2332. doi: 10.1016/j.ultrasmedbio.2013.06.015.
  Artemov, D., Bhujwalla, Z.M., and Bulte, J.W. 2004. Magnetic resonance imaging of cell surface receptors using targeted contrast agents. Curr. Pharm. Biotechnol. 5:485‐494. doi: 10.2174/1389201043376553.
  Bamforth, S.D., Bragança, J., Farthing, C.R., Schneider, J.E., Broadbent, C., Michell, A.C., Clarke, K., Neubauer, S., Norris, D., Brown, N.A., Anderson, R.H., and Bhattacharya, S. 2004. Cited2 controls left‐right patterning and heart development through a Nodal‐Pitx2c pathway. Nat. Genet. 36:1189‐1196. doi: 10.1038/ng1446.
  Bartelle, B.B., Berrios‐Otero, C.A., Rodriguez, J.J., Friedland, A.E., Aristizábal, O., and Turnbull, D.H. 2012. Novel genetic approach for in vivo vascular imaging in mice. Circ. Res. 110:938‐947. doi: 10.1161/CIRCRESAHA.111.254375.
  Bauer, M., Cheng, S., Unno, K., Lin F‐C, and Liao, R. 2013. Regional cardiac dysfunction and dyssynchrony in a murine model of afterload stress. PLoS One 8:e59915. doi: 10.1371/journal.pone.0059915.
  Bauer, M., Cheng, S., Jain, M., Ngoy, S., Theodoropoulos, C., Trujillo, A., Lin F‐C, and Liao, R. 2011. Echocardiographic speckle‐tracking based strain imaging for rapid cardiovascular phenotyping in mice. Circ. Res. 108:908‐916. doi: 10.1161/CIRCRESAHA.110.239574.
  Bernstein, D. 2003. Exercise assessment of transgenic models of human cardiovascular disease. Physiol. Genomics 13:217‐226. doi: 10.1152/physiolgenomics.00188.2002.
  Berrios‐Otero, C.A., Nieman, B.J., Parasoglou, P., and Turnbull, D.H. 2012. In utero phenotyping of mouse embryonic vasculature with MRI. Magn. Reson. Med. 67:251‐257. doi: 10.1002/mrm.22991.
  Berrios‐Otero, C.A., Wadghiri, Y.Z., Nieman, B.J., Joyner, A.L., and Turnbull, D.H. 2009. Three‐dimensional micro‐MRI analysis of cerebral artery development in mouse embryos. Magn. Reson. Med. 62:1431‐1439. doi: 10.1002/mrm.22113.
  Berry, C.J., Thedens, D.R., Light‐McGroary, K., Miller, J.D., Kutschke, W., Zimmerman, K.A., and Weiss, R.M. 2009. Effects of deep sedation or general anesthesia on cardiac function in mice undergoing cardiovascular magnetic resonance. J. Cardiovasc. Magn. Reson. 11:16. doi: 10.1186/1532‐429X‐11‐16.
  Bhan, A., Sirker, A., Zhang, J., Protti, A., Catibog, N., Driver, W., Botnar, R., Monaghan, M.J., and Shah, A.M. 2014. High‐frequency speckle tracking echocardiography in the assessment of left ventricular function and remodeling after murine myocardial infarction. Am. J. Physiol. Heart Circ. Physiol. 306:H1371‐H1383. doi: 10.1152/ajpheart.00553.2013.
  Boyd, A.C., Schiller, N.B., and Thomas, L. 2015. Principles of transthoracic echocardiographic evaluation. Nat. Rev. Cardiol. 12:426‐440. doi: 10.1038/nrcardio.2015.57.
  Buonincontri, G., Methner, C., Krieg, T., Carpenter, T.A., and Sawiak, S.J. 2014. Functional assessment of the mouse heart by MRI with a 1‐min acquisition. NMR Biomed. 27:733‐737. doi: 10.1002/nbm.3116.
  Chatterjee, S., Bedja, D., Mishra, S., Amuzie, C., Avolio, A., Kass, D.A., Berkowitz, D., and Renehan, M. 2014. Inhibition of glycosphingolipid synthesis ameliorates atherosclerosis and arterial stiffness in apolipoprotein E ‐/‐ mice and rabbits fed a high‐fat and ‐cholesterol diet. Circulation 129:2403‐2413. doi: 10.1161/CIRCULATIONAHA.113.007559.
  Choudhury, R.P., Fuster, V., and Fayad, Z.A. 2004. Molecular, cellular and functional imaging of atherothrombosis. Nat. Rev. Drug Discov. 3:913‐925. doi: 10.1038/nrd1548.
  Colas J‐F. and Sharpe, J. 2009. Live optical projection tomography. Organogenesis 5:211‐216. doi: 10.4161/org.5.4.10426.
  Collis, L.P., Meyers, M.B., Zhang, J., Phoon, C.K.L., Sobie, E.A., Coetzee, W.A., and Fishman, G.I. 2007. Expression of a sorcin missense mutation in the heart modulates excitation‐contraction coupling. FASEB J. 21:475‐487. doi: 10.1096/fj.06‐6292com.
  Cua, M., Lin, E., Lee, L., Sheng, X., Wong, K.S., Tibbits, G.F., Beg, M.F., and Sarunic, M.V. 2014. Morphological phenotyping of mouse hearts using optical coherence tomography. J. Biomed. Opt. 19:116007. doi: 10.1117/1.JBO.19.11.116007.
  Danielson, L.S., Park, D.S., Rotllan, N., Chamorro‐Jorganes, A., Guijarro, M.V., Fernandez‐Hernando, C., Fishman, G.I., Phoon, C.K.L., and Hernando, E. 2013. Cardiovascular dysregulation of miR‐17‐92 causes a lethal hypertrophic cardiomyopathy and arrhythmogenesis. FASEB J. 27:1460‐1467. doi: 10.1096/fj.12‐221994.
  Dhenain, M., Ruffins, S.W., and Jacobs, R.E. 2001. Three‐dimensional digital mouse atlas using high‐resolution MRI. Dev. Biol. 232:458‐470. doi: 10.1006/dbio.2001.0189.
  Dorr, A., Sled, J.G., and Kabani, N. 2007. Three‐dimensional cerebral vasculature of the CBA mouse brain: A magnetic resonance imaging and micro computed tomography study. Neuroimage 35:1409‐1423. doi: 10.1016/j.neuroimage.2006.12.040.
  Drexler, W., Liu, M., Kumar, A., Kamali, T., Unterhuber, A., and Leitgeb, R.A. 2014. Optical coherence tomography today: Speed, contrast, and multimodality. J. Biomed. Opt. 19:071412. doi: 10.1117/1.JBO.19.7.071412.
  Epstein, F.H. 2007. MR in mouse models of cardiac disease. NMR Biomed. 20:238‐255. doi: 10.1002/nbm.1152.
  Favreau, J.T., Liu, C., Yu, P., Tao, M., Mauro, C., Gaudette, G.R., and Ozaki, C.K. 2014. Acute reductions in mechanical wall strain precede the formation of intimal hyperplasia in a murine model of arterial occlusive disease. J. Vasc. Surg. 60:1340‐1347. doi: 10.1016/j.jvs.2013.07.113.
  Fayssoil, A., and Tournoux, F. 2013. Analyzing left ventricular function in mice with Doppler echocardiography. Heart Fail. Rev. 18:511‐516. doi: 10.1007/s10741‐012‐9345‐8.
  Filoux, E., Mamou, J., Aristizábal, O., and Ketterling, J.A. 2011. Characterization of the spatial resolution of different high‐frequency imaging systems using a novel anechoic‐sphere phantom. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 58:994‐1005.
  Filoux, E., Mamou, J., Moran, C.M., Pye, S.D., and Ketterling, J.A. 2012. Correspondence ‐ Characterization of the effective performance of a high‐frequency annular‐array‐based imaging system using anechoic‐pipe phantoms. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 59:2825‐2830. doi: 10.1109/TED.2012.2209650.
  Forsey, J., Friedberg, M.K., and Mertens, L. 2013. Speckle tracking echocardiography in pediatric and congenital heart disease. Echocardiography 30:447‐459. doi: 10.1111/echo.12131.
  Foss, C.A., Bedja, D., Mease, R.C., Wang, H., Kass, D.A., Chatterjee, S., and Pomper, M.G. 2015. Molecular imaging of inflammation in the ApoE‐/‐ mouse model of atherosclerosis with IodoDPA. Biochem. Biophys. Res. Commun. 461:70‐75. doi: 10.1016/j.bbrc.2015.03.171.
  Foster, F.S., Hossack, J., and Adamson, S.L. 2011. Micro‐ultrasound for preclinical imaging. Interface Focus 1:576‐601. doi: 10.1098/rsfs.2011.0037.
  Fujikura, K., Luo, J., Gamarnik, V., Pernot, M., Fukumoto, R., Tilson M.D. 3rd, and Konofagou, E.E. 2007. A novel noninvasive technique for pulse‐wave imaging and characterization of clinically‐significant vascular mechanical properties in vivo. Ultrason. Imaging 29:137‐154. doi: 10.1177/016173460702900301.
  Fujimoto, J.G. 2003. Optical coherence tomography for ultrahigh resolution in vivo imaging. Nat. Biotech. 21:1361‐1367. doi: 10.1038/nbt892.
  Gao, S., Ho, D., Vatner, D.E., and Vatner, S.F. 2011. Echocardiography in mice. Curr. Protocols. Mouse. Biol. 1:71‐83.
  Garcia, M.D., Lopez AL 3rd, Larin, K.V., and Larina, I.V. 2015. Imaging of cardiovascular development in mammalian embryos using optical coherence tomography. Methods Mol. Biol. 1214:151‐161. doi: 10.1007/978‐1‐4939‐1462‐3_8.
  Gardin, J.M., Siri, F.M., Kitsis, R.N., Edwards, J.G., and Leinwand, L.A. 1995. Echocardiographic assessment of left ventricular mass and systolic function in mice. Circ. Res. 76:907‐914. doi: 10.1161/01.RES.76.5.907.
  Ghanavati, S., Lerch, J.P., and Sled, J.G. 2014. Automatic anatomical labeling of the complete cerebral vasculature in mouse models. Neuroimage 95:117‐128. doi: 10.1016/j.neuroimage.2014.03.044.
  Ghanavati, S., Yu, L.X., Lerch, J.P., and Sled, J.G. 2014. A perfusion procedure for imaging of the mouse cerebral vasculature by X‐ray micro‐CT. J. Neurosci. Methods 221:70‐77. doi: 10.1016/j.jneumeth.2013.09.002.
  Gorcsan J 3rd and Tanaka, H. 2011. Echocardiographic assessment of myocardial strain. J. Am. Coll. Cardiol. 58:1401‐1413. doi: 10.1016/j.jacc.2011.06.038.
  Gray, G.A., White, C.I., Thomson, A., Kozak, A., Moran, C., and Jansen, M.A. 2013. Imaging the healing murine myocardial infarct in vivo: Ultrasound, magnetic resonance imaging and fluorescence molecular tomography. Exp. Physiol. 98:606‐613. doi: 10.1113/expphysiol.2012.064741.
  Greco, A., Ragucci, M., Coda, A.R., Rosa, A., Gargiulo, S., Liuzzi, R., Gramanzini, M., Albanese, S., Pappatà S, Mancini, M., Brunetti, A., and Salvatore, M. 2013. High frequency ultrasound for in vivo pregnancy diagnosis and staging of placental and fetal development in mice. PLoS One 8:e77205. doi: 10.1371/journal.pone.0077205.
  Gui, Y.H., Linask, K.K., Khowsathit, P., and Huhta, J.C. 1996. Doppler echocardiography of normal and abnormal embryonic mouse heart. Pediatr. Res. 40:633‐642. doi: 10.1203/00006450‐199610000‐00020.
  Hartley, C.J., Reddy, A.K., Madala, S., Entman ml, Michael, L.H., and Taffet, G.E. 2011. Doppler velocity measurements from large and small arteries of mice. Am. J. Physiol. Heart Circ. Physiol. 301:H269‐278. doi: 10.1152/ajpheart.00320.2011.
  Hoffman, J.I.E. 1995. Incidence of congenital heart disease: II. Prenatal incidence. Pediatr. Cardiol. 16:155‐165.
  Hoffman, J.I.E. and Kaplan, S. 2002. The incidence of congenital heart disease. J. Am. Coll. Cardiol. 39:1890‐1900. doi: 10.1016/S0735‐1097(02)01886‐7.
  Huang, G.Y., Wessels, A., Smith, B.R., Linask, K.K., Ewart, J.L., and Lo, C.W. 1998. Alteration in connexin 43 gap junction gene dosage impairs conotruncal heart development. Dev. Biol. 198:32‐44. doi: 10.1006/dbio.1998.8891.
  Ji, R.P. and Phoon, C.K.L. 2005. Non‐invasive localization of NFATc1‐/‐ mouse embryos by ultrasound biomicroscopy‐Doppler allows genotype‐phenotype correlation. J. Am. Soc. Echocardiogr. 18:1415‐1421. doi: 10.1016/j.echo.2005.04.006.
  Ji, R.P., Phoon, C.K.L., Aristizábal, O., McGrath, K.E., Palis, J., and Turnbull, D.H. 2003. Onset of cardiac function during early mouse embryogenesis coincides with entry of primitive erythroblasts into the embryo proper. Circ. Res. 92:133‐135. doi: 10.1161/01.RES.0000056532.18710.C0.
  Ketterling, J.A. and Aristizábal, O. 2009. Prospective ECG‐gated mouse cardiac imaging with a 34‐MHz annular array transducer. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 56:1394‐1404.
  Kober, F., Iltis, I., Cozzone, P.J., and Bernard, M. 2004. Cine‐MRI assessment of cardiac function in mice anesthetized with ketamine/xylazine and isoflurane. MAGMA 17:157‐161. doi: 10.1007/s10334‐004‐0086‐0.
  Krishnan, A., Samtani, R., Dhanantwari, P., Lee, E., Yamada, S., Shiota, K., Donofrio, M.T., Leatherbury, L., and Lo, C.W. 2014. A detailed comparison of mouse and human cardiac development. Pediatr. Res. 76:500‐507. doi: 10.1038/pr.2014.128.
  Kuo, M.M., Barodka, V., Abraham, T.P., Steppan, J., Shoukas, A.A., Butlin, M., Avolio, A., Berkowitz, D.E., and Santhanam, L. 2014. Measuring ascending aortic stiffness in vivo in mice using ultrasound. J. Vis. Exp.94:e52200. doi: 10.3791/52200.
  Larina, I.V., Larin, K.V., Justice, M.V., and Dickinson, M.E. 2011. Optical coherence tomography for live imaging of mammalian development. Curr. Opin. Genet. Dev. 21:579‐584. doi: 10.1016/j.gde.2011.09.004.
  Larina, I.V., Garcia, M.D., Vadakkan, T.J., Larin, K.V., and Dickinson, M.E. 2012. Imaging mouse embryonic cardiovascular development. Cold. Spring. Harb. Protoc. 2012:1035‐1043. doi: 10.1101/pdb.top071498.
  Larina, I.V., Sudheendran, N., Ghosn, M., Jiang, J., Cable, A., Larin, K.V., and Dickinson, M.E. 2008. Live imaging of blood flow in mammalian embryos using Doppler swept‐source optical coherence tomography. J. Biomed. Opt. 13:060506. doi: 10.1117/1.3046716.
  Lindner, J.R. 2010. Molecular imaging of myocardial and vascular disorders with ultrasound. JACC Cardiovasc. Imaging 3:204‐211. doi: 10.1016/j.jcmg.2009.09.021.
  Liu, J. and Rigel, D.F. 2009. Echocardiographic examination in rats and mice. Methods Mol. Biol. 573:139‐155. doi: 10.1007/978‐1‐60761‐247‐6_8.
  Liu, X., Tobita, K., Francis, R.J., and Lo, C.W. 2013. Imaging techniques for visualizing and phenotyping congenital heart defects in murine models. Birth Defects Res. C. Embryo. Today 99:93‐105. doi: 10.1002/bdrc.21037.
  Liu, X., Francis, R., Kim, A.J., Ramirez, R., Chen, G., Subramanian, R., Anderton, S., Kim, Y., Wong, L., Morgan, J., Pratt, H.C., Reinholdt, L., Devine, W., Leatherbury, L., Tobita, K., and Lo, C.W. 2014. Interrogating congenital heart defects with noninvasive fetal echocardiography in a mouse forward genetic screen. Circ. Cardiovasc. Imaging 7:31‐42. doi: 10.1161/CIRCIMAGING.113.000451.
  Lopez A.L. 3rd, Garcia, M.D., Dickinson, M.E., and Larina, I.V. 2015. Live confocal microscopy of the developing mouse embryonic yolk sac vasculature. Methods Mol. Biol. 1214:163‐172. doi: 10.1007/978‐1‐4939‐1462‐3_9.
  Luo, J. and Konofagou, E.E. 2008. High‐frame rate, full‐view myocardial elastography with automated contour tracking in murine left ventricles in vivo. IEEE Trans. Ultrason. Ferroelectr. Freq. Control 55:240‐248. doi: 10.1109/TUFFC.2008.633.
  Manning, W.J., Wei, J.Y., Katz, S.E., Litwin, S.E., and Douglas, P.S. 1994. In vivo assessment of LV mass in mice using high‐frequency cardiac ultrasound: Necropsy validation. Am. J. Physiol. 266:H1672‐675.
  Mercier, N., Kiviniemi, T.O., Saraste, A., Miiluniemi, M., Silvola, J., Jalkanen, S., and Yegutkin, G.G. 2012. Impaired ATP‐induced coronary blood flow and diminished aortic NTPDase activity precede lesion formation in apolipoprotein E‐deficient mice. Am. J. Pathol. 180:419‐428. doi: 10.1016/j.ajpath.2011.10.002.
  Millon, A., Canet‐Soulas, E., Boussel, L., Fayad, Z., and Douek, P. 2014. Animal models of atherosclerosis and magnetic resonance imaging for monitoring plaque progression. Vascular 22:221‐237. doi: 10.1177/1708538113478758.
  Moran, C.M., Thomson, A.J.W., Rog‐Zielinska, E., and Gray, G.A. 2013. High‐resolution echocardiography in the assessment of cardiac physiology and disease in preclinical models. Exp. Physiol. 98:629‐644. doi: 10.1113/expphysiol.2012.068577.
  Mozaffarian, D., Benjamin, E.J., Go, A.S., Arnett, D.K., Blaha, M.J., Cushman, M., de Ferranti, S., Després, J.P., Fullerton, H.J., Howard, V.J., Huffman, M.D., Judd, S.E., Kissela, B.M., Lackland, D.T., Lichtman, J.H., Lisabeth, L.D., Liu, S., Mackey, R.H., Matchar, D.B., McGuire, D.K., Mohler ER 3rd, Moy, C.S., Muntner, P., Mussolino, M.E., Nasir, K., Neumar, R.W., Nichol, G., Palaniappan, L., Pandey, D.K., Reeves, M.J., Rodriguez, C.J., Sorlie, P.D., Stein, J., Towfighi, A., Turan, T.N., Virani, S.S., Willey, J.Z., Woo, D., Yeh, R.W., and Turner, M.B. 2015. American Heart Association Statistics Committee and Stroke Statistics Subcommittee. Heart disease and stroke statistics – 2015 update: A report from the American Heart Association. Circulation 131:e29‐322. doi: 10.1161/CIR.0000000000000152.
  Nandlall, S.D., Goldklang, M.P., Kalashian, A., Dangra, N.A., D'Armiento, J.M., and Konofagou, E.E. 2014. Monitoring and staging abdominal aortic aneurysm disease with pulse wave imaging. Ultrasound Med. Biol. 40:2404‐2414. doi: 10.1016/j.ultrasmedbio.2014.04.013.
  Nieman, B.J. and Turnbull, D.H. 2010. Ultrasound and magnetic resonance microimaging of mouse development. Methods Enzymol. 476:379‐400. doi: 10.1016/S0076‐6879(10)76021‐3.
  Nieman, B.J., Szulc, K.U., and Turnbull, D.H. 2009. Three‐dimensional in vivo MRI with self‐gating and image coregistration in the mouse. Magn. Reson. Med. 61:1148‐1157. doi: 10.1002/mrm.21945.
  Nomura‐Kitabayashi, A., Phoon, C.K.L., Kishigami, S., Rosenthal, J., Yamauchi, Y., Abe, K., Yamamura, K., Samtani, R., Lo, C.W., and Mishina, Y. 2009. Outflow tract cushions perform a critical valve‐like function in the early embryonic heart requiring BMPRIA‐mediated signaling in cardiac neural crest. Am. J. Physiol. Heart. Circ. Physiol. 297:H1617‐H1628. doi: 10.1152/ajpheart.00304.2009.
  Norris, F.C., Wong, M.D., Greene, N.D.E., Scambler, P.J., Weaver, T., Weninger, W.J., Mohun, T.J., Henkelman, R.M., and Lythgoe, M.F. 2013. A coming of age: Advanced imaging technologies for characterising the developing mouse. Trends Genet. 29:700‐711. doi: 10.1016/j.tig.2013.08.004.
  Pachon, R.E., Scharf, B.A., Vatner, D.E., and Vatner, S.F. 2015. Best anesthetics for assessing left ventricular systolic function by echocardiography in mice. Am. J. Physiol. Heart. Circ. Physiol. 308:H1525‐H1529. doi: 10.1152/ajpheart.00890.2014.
  Parasoglou, P., Berrios‐Otero, C.A., Nieman, B.J., and Turnbull, D.H. 2013. High‐resolution MRI of early‐stage mouse embryos. NMR Biomed. 26:224‐231. doi: 10.1002/nbm.2843.
  Peng, Y., Popvić, Z.B., Sopko, N., Drinko, J., Zhang, Z., Thomas, J.D., and Penn, M.S. 2009. Speckle tracking echocardiography in the assessment of mouse models of cardiac dysfunction. Am. J. Physiol. Heart Circ. Physiol. 297:H811‐H820. doi: 10.1152/ajpheart.00385.2009.
  Petiet, A.E., Kaufman, M.H., Goddeeris, M.M., Brandenburg, J., Elmore, S.A., and Johnson, G.A. 2008. High‐resolution magnetic resonance histology of the embryonic and neonatal mouse: A 4D atlas and morphologic database. Proc. Natl. Acad. Sci. USA. 105:12331‐12336. doi: 10.1073/pnas.0805747105.
  Phoon, C.K.L. 2001. Circulatory physiology in the developing embryo. Curr. Opin. Pediatr. 13:456‐464. doi: 10.1097/00008480‐200110000‐00013.
  Phoon, C.K.L. 2006. Imaging tools for the developmental biologist: Ultrasound biomicroscopy of mouse embryonic development. Pediatr. Res. 60:14‐21. doi: 10.1203/01.pdr.0000219441.28206.79.
  Phoon, C.K.L. and Turnbull, D.H. 2003. Ultrasound biomicroscopy‐Doppler in mouse cardiovascular development. Physiol. Genomics 14:3‐15. doi: 10.1152/physiolgenomics.00008.2003.
  Phoon, C.K.L., Aristizábal, O., and Turnbull, D.H. 2000. 40 MHz Doppler characterization of umbilical and dorsal aortic blood flow in the early mouse embryo. Ultrasound Med. Biol. 26:1275‐1283. doi: 10.1016/S0301‐5629(00)00278‐7.
  Phoon, C.K.L., Aristizábal, O., and Turnbull, D.H. 2002. Spatial velocity profile in mouse embryonic aorta and Doppler‐derived volumetric flow: A preliminary model. Am. J. Physiol. Heart Circ. Physiol. 283:908‐916. doi: 10.1152/ajpheart.00869.2001.
  Phoon, C.K., Ji, R.P., and Chowdhury, P.D. 2007. Transposition of the great arteries and double outlet right ventricle have related early developmental origins: Fundamental insights from in vivo imaging. Circulation 116(Suppl):511.
  Phoon, C.K.L., Ji, R.P., Aristizábal, O., Worrad, D.M., Zhou, B., Baldwin, H.S., and Turnbull, D.H. 2004. Embryonic heart failure in NFATc1‐/‐ mice: Novel mechanistic insights from in utero ultrasound biomicroscopy. Circ. Res. 95:92‐99. doi: 10.1161/01.RES.0000133681.99617.28.
  Phoon, C.K.L., Acehan, D., Schlame, M., Stokes, D.L., Edelman‐Novemsky, I., Yu, D., Xu, Y., Viswanathan, N., and Ren, M. 2012. Tafazzin knockdown in mice leads to a developmental cardiomyopathy with early diastolic dysfunction preceding myocardial noncompaction. JAHA: J. Am. Heart. Assoc. 1:jah3‐e000455. doi:JAHA.111.000455
  Poole, K.M., Tucker‐Schwartz, J.M., Sit, W.W., Walsh, A.J., Duvall, C.L., and Skala, M.C. 2013. Quantitative optical imaging of vascular response in vivo in a model of peripheral arterial disease. Am. J. Physiol. Heart Circ. Physiol. 305:H1168‐H1180. doi: 10.1152/ajpheart.00362.2013.
  Prieto, C., Andia, M.E., von Bary, C., Onthank, D.C., Schaeffter, T., and Botnar, R.M. 2012. Accelerating three‐dimensional molecular cardiovascular MR imaging using compressed sensing. J. Magn. Reson. Imaging. 36:1362‐1371. doi: 10.1002/jmri.23763.
  Ram, R., Mickelsen, D.M., Theodoropoulos, C., and Blaxall, B.C. 2011. New approaches in small animal echocardiography: Imaging the sounds of silence. Am. J. Physiol. Heart Circ. Physiol. 301:H1765‐1780. doi: 10.1152/ajpheart.00559.2011.
  Roth, D.M., Swaney, J.S., Dalton, N.D., Gilpin, E.A., and Ross J Jr. 2002. Impact of anesthesia on cardiac function during echocardiography in mice. Am. J. Physiol. Heart Circ. Physiol. 282:H2134‐H2140. doi: 10.1152/ajpheart.00845.2001.
  Ruijter, J.M., Soufan, A.T., Hagoort, J., and Moorman, A.F.M. 2004. Molecular imaging of the embryonic heart: Fables and facts on 3D imaging of gene expression patterns. Birth. Defects. Res. Part, C. 72:224‐240. doi: 10.1002/bdrc.20018.
  Scherrer‐Crosbie, M. and Kurtz, B. 2010. Ventricular remodeling and function: Insights using murine echocardiography. J. Mol. Cell. Cardiol. 48:512‐517. doi: 10.1016/j.yjmcc.2009.07.004.
  Schneider, J.E., Böse, J., Bamforth, S.D., Gruber, A.D., Broadbent, C., Clarke, K., Neubauer, S., Lengeling, A., and Bhattacharya, S. 2004. Identification of cardiac malformations in mice lacking Ptdsr using a novel high‐throughput magnetic resonance imaging technique. BMC Dev. Biol. 4:16. doi: 10.1186/1471‐213X‐4‐16.
  Sharpe, J., Ahlgren, U., Perry, P., Hill, B., Ross, A., Hecksher‐Serensen, J., Baldock, R., and Davidson, D. 2002. Optical projection tomography as a tool for 3D microscopy and gene expression studies. Science 296:541‐545. doi: 10.1126/science.1068206.
  Smith, B.R. 2000. Magnetic resonance imaging analysis of embryos. Methods Mol. Biol. 135:211‐216.
  Smith, B.R. 2001. Magnetic resonance microscopy in cardiac development. Microsc. Res. Tech. 52:323‐330. doi: 10.1002/1097‐0029(20010201)52:3<3c323::AID‐JEMT1016>3e3.0.CO;2‐F.
  Smith, B.R., Johnson, G.A., Groman, E.V., and Linney, E. 1994. Magnetic resonance microscopy of mouse embryos. Proc. Natl. Acad. Sci. USA 91:3530‐3533. doi: 10.1073/pnas.91.9.3530.
  Srinivasan, S., Baldwin, H.S., Aristizabal, O., Kwee, L., Labow, M., Artman, M., and Turnbull, D.H. 1998. Noninvasive, in utero imaging of mouse embryonic heart development with 40‐MHz echocardiography. Circulation 98:912‐918. doi: 10.1161/01.CIR.98.9.912.
  Thibault, H.B., Kurtz, B., Raher, M.J., Shaik, R.S., Waxman, A., Derumeaux, G., Halpern, E.F., Bloch, K.D., and Scherrer‐Crosbie, M. 2010. Noninvasive assessment of murine pulmonary arterial pressure: Validation and application to models of pulmonary hypertension. Circ. Cardiovasc. Imaging 3:157‐163. doi: 10.1161/CIRCIMAGING.109.887109.
  Turnbull, D.H. and Mori, S. 2007. MRI in mouse developmental biology. NMR Biomed. 20:265‐274. doi: 10.1002/nbm.1146.
  Vandsburger, M.H. and Epstein, F.H. 2011. Emerging MRI methods in translational cardiovascular research. J. Cardiovasc. Transl. Res. 4:477‐492. doi: 10.1007/s12265‐011‐9275‐1.
  Vinegoni, C., Fumene Feruglio, P., Razansky, D., Gorbatov, R., Ntziachristos, V., Sbarbati, A., Nahrendorf, M., and Weissleder, R. 2012. Mapping molecular agents distributions in whole mice hearts using born‐normalized optical projection tomography. PLoS One 7:e34427. doi: 10.1371/journal.pone.0034427.
  Wadghiri, Y.Z., Schneider, A.E., Gray, E.N., Aristizabal, O., Berrios, C., Turnbull, D.H., and Gutstein, D.E. 2007. Contrast‐enhanced MRI of right ventricular abnormalities in Cx43 mutant mouse embryos. NMR Biomed. 20:366‐374. doi: 10.1002/nbm.1113.
  Walls, J.R., Coultas, L., Rossant, J., and Henkelman, R.M. 2008. Three‐dimensional analysis of vascular development in the mouse embryo. PLoS One 3:e2853. doi: 10.1371/journal.pone.0002853.
  Wang, X., Hagemeyer, C.E., Hohmann, J.D., Leitner, E., Armstrong, P.C., Jia, F., Olschewski, M., Needles, A., Peter, K., and Ahrens, I. 2012. Novel single‐chain antibody‐targeted microbubbles for molecular ultrasound imaging of thrombosis: Validation of a unique noninvasive method for rapid and sensitive detection of thrombi and monitoring of success or failure of thrombolysis in mice. Circulation 125:3117‐3126. doi: 10.1161/CIRCULATIONAHA.111.030312.
  Yang, J., Yu, L.X., Rennie, M.Y., Sled, J.G., and Henkelman, R.M. 2010. Comparative structural and hemodynamic analysis of vascular trees. Am. J. Physiol. Heart Circ. Physiol. 298:H1249‐59. doi: 10.1152/ajpheart.00363.2009.
  Zamyadi, M., Baghdadi, L., Lerch, J.P., Bhattacharya, S., Schneider, J.E., Henkelman, R.M., and Sled, J.G. 2010. Mouse embryonic phenotyping by morphometric analysis of MR images. Physiol. Genomics 42A:89‐95. doi: 10.1152/physiolgenomics.00091.2010.
  Zhang, X., Schneider, J.E., Portnoy, S., Bhattacharya, S., and Henkelman, R.M. 2010. Comparative SNR for high‐throughput mouse embryo MR microscopy. Magn. Reson. Med. 63:1703‐1707. doi: 10.1002/mrm.22352.
  Zhang, X., Ha, S., Wei, W., Duan, S., Shi, Y., and Yang, Y. 2015. Noninvasive imaging of aortic atherosclerosis by ultrasound biomicroscopy in a mouse model. J. Ultrasound Med. 34:111‐116. doi: 10.7863/ultra.34.1.111.
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