Abstract
The aim of this study was to perform fetal cardiac magnetic resonance imaging (MRI) with triggering of the fetal heart beat in utero in a sheep model. All experimental protocols were reviewed and the usage of ewes and fetuses was approved by the local animal protection authorities. Images of the hearts of six pregnant ewes were obtained by using a 1.5-T MR system (Philips Medical Systems, Best, Netherlands). The fetuses were chronically instrumented with a carotid catheter to measure the fetal heart frequency for the cardiac triggering. Pulse wave triggered, breath-hold cine-MRI with steady-state free precession (SSFP) was achieved in short axis, two-, four- and three-chamber views. The left ventricular volume and thus the function were measured from the short axis. The fetal heart frequencies ranged between 130 and 160 bpm. The mitral, tricuspid, aortic, and pulmonary valves could be clearly observed. The foramen ovale could be visualized. Myocardial contraction was shown in cine sequences. The average blood volume at the end systole was 3.4 ± 0.2 ml (± SD). The average volume at end diastole was 5.2 ± 0.2 ml; thus the stroke volumes of the left ventricle in the systole were between 1.7 and 1.9 ml with ejection fractions of 38.6% and 39%, respectively. The pulse wave triggered cardiac MRI of the fetal heart allowed evaluation of anatomical structures and functional information. This feasibility study demonstrates the applicability of MRI for future evaluation of fetuses with complex congenital heart defects, once a noninvasive method has been developed to perform fetal cardiac triggering.
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Blondin D, Schaper J, Klee D, Reihs T, Hammer R, Modder U, Messing-Junger M (2008) Evaluation of malformations of the fetal central nervous system using fetal MRI. Rofo 180:715–721
Busing KA, Kilian AK, Schaible T, Endler C, Schaffelder R, Neff KW (2008) MR relative fetal lung volume in congenital diaphragmatic hernia: survival and need for extracorporeal membrane oxygenation. Radiology 248:240–246
Perkins L, Hughes E, Srinivasan L, Allsop J, Glover A, Kumar S, Fisk N, Rutherford M (2008) Exploring cortical subplate evolution using magnetic resonance imaging of the fetal brain. Dev Neurosci. 30:211–220
Liu F, Garland M, Duan Y, Stark RI, Xu D, Dong Z, Bansal R, Peterson BS, Kangarlu A (2008) Study of the development of fetal baboon brain using magnetic resonance imaging at 3 Tesla. Neuroimage 40:148–159
Righini A, Avagliano L, Doneda C, Pinelli L, Parazzini C, Rustico M, Triulzi F, Bulfamante G (2008) Prenatal magnetic resonance imaging of optic nerve head coloboma. Prenat Diagn 28(3):242–246
Kappeler C, Dhenain M, Phan Dinh Tuy F, Saillour Y, Marty S, Fallet-Bianco C, Souville I, Souil E, Pinard JM, Meyer G, Encha-Razavi F, Volk A, Beldjord C, Chelly J, Francis F (2007) Magnetic resonance imaging and histological studies of corpus callosal and hippocampal abnormalities linked to doublecortin deficiency. J Comp Neurol 500:239–254
Ramenghi LA, Fumagalli M, Righini A, Bassi L, Groppo M, Parazzini C, Bianchini E, Triulzi F, Mosca F (2007) Magnetic resonance imaging assessment of brain maturation in preterm neonates with punctate white matter lesions. Neuroradiology 49:161–167
Wedegartner U, Tchirikov M, Schafer S, Priest AN, Walther M, Adam G, Schroder HJ (2005) Fetal sheep brains: findings at functional blood oxygen level-dependent 3-T MR imaging—relationship to maternal oxygen saturation during hypoxia. Radiology 237:919–926
Wedegartner U, Tchirikov M, Schafer S, Priest AN, Kooijman H, Adam G, Schroder HJ (2006) Functional MR imaging: comparison of BOLD signal intensity changes in fetal organs with fetal and maternal oxyhemoglobin saturation during hypoxia in sheep. Radiology 238:872–880
Wedegartner U, Tchirikov M, Koch M, Adam G, Schroder H (2002) Functional magnetic resonance imaging (fMRI) for fetal oxygenation during maternal hypoxia: initial results. Rofo 174:700–703
Gharib AM, Herzka DA, Ustun AO, Desai MY, Locklin J, Pettigrew RI, Stuber M (2007) Coronary MR angiography at 3 T during diastole and systole. J Magn Reson Imaging 26:921–926
Gharib AM, Ho VB, Rosing DR, Herzka DA, Stuber M, Arai AE, Pettigrew RI (2008) Coronary artery anomalies and variants: technical feasibility of assessment with coronary MR angiography at 3 T. Radiology 247:220–227
Finn JP, Nael K, Deshpande V, Ratib O, Laub G (2006) Cardiac MR imaging: state of the technology. Radiology 241:338–354
Cury RC, Shash K, Nagurney JT, Rosito G, Shapiro MD, Nomura CH, Abbara S, Bamberg F, Ferencik M, Schmidt EJ, Brown DF, Hoffmann U, Brady TJ (2008) Cardiac magnetic resonance with T2-weighted imaging improves detection of patients with acute coronary syndrome in the emergency department. Circulation 118(8):837–844
Ebeling Barbier C, Bjerner T, Hansen T, Andersson J, Lind L, Hulthe J, Johansson L, Ahlstrom H (2007) Clinically unrecognized myocardial infarction detected at MR imaging may not be associated with atherosclerosis. Radiology 245:103–110
Manganaro L, Savelli S, Di Maurizio M, Perrone A, Francioso A, La Barbera L, Totaro P, Fierro F, Tomei A, Coratella F, Giancotti A, Ballesio L,Ventriglia F (2008) Assessment of congenital heart disease (CHD): is there a role for fetal magnetic resonance imaging (MRI)? Eur J Radiol. doi:10.1016/j.ejrad.2008.06.016
Coakley FV, Glenn OA, Qayyum A, Barkovich AJ, Goldstein R, Filly RA (2004) Fetal MRI: a developing technique for the developing patient. AJR Am J Roentgenol 182:243–252
Coakley FV, Hricak H, Filly RA, Barkovich AJ, Harrison MR (1999) Complex fetal disorders: effect of MR imaging on management—preliminary clinical experience. Radiology 213:691–696
Huisman TA, Wisser J, Martin E, Kubik-Huch R, Marincek B (2002) Fetal magnetic resonance imaging of the central nervous system: a pictorial essay. Eur Radiol 12:1952–1961
Guo WY, Wong TT (2003) Screening of fetal CNS anomalies by MR imaging. Childs Nerv Syst 19:410–414
Guo Y, Luo BN (2006) The state of the art of fetal magnetic resonance imaging. Chin Med J (Engl) 119:1294–1299
Stoll C, Benoit F, Peter MO, Gasser B (1999) Familial association of camptodactyly, mental retardation, whistling face and Pierre Robin sequence. Clin Dysmorphol 8:247–251
Allen LM, Silverman RK (2000) Prenatal ultrasound evaluation of fetal diastematomyelia: two cases of type I split cord malformation. Ultrasound Obstet Gynecol 15:78–82
Deng J, Brookes JA, Gardener JE, Rodeck CH, Lees WR (1996) Three-dimensional magnetic resonance imaging of the postmortem fetal heart. Fetal Diagn Ther 11:417–421
Deng J, Rodeck CH (2004) New fetal cardiac imaging techniques. Prenat Diagn 24:1092–1103
Meyer-Wittkopf M, Cook A, McLennan A, Summers P, Sharland GK, Maxwell DJ (1996) Evaluation of three-dimensional ultrasonography and magnetic resonance imaging in assessment of congenital heart anomalies in fetal cardiac specimens. Ultrasound Obstet Gynecol 8:303–308
Wang XF, Deng YB, Nanda NC, Deng J, Miller AP, Xie MX (2003) Live three-dimensional echocardiography: imaging principles and clinical application. Echocardiography 20:593–604
Chang CH, Yu CH, Chang FM, Ko HC, Chen HY (2003) Volumetric assessment of normal fetal lungs using three-dimensional ultrasound. Ultrasound Med Biol 29:935–942
Chang CH, Yu CH, Chang FM, Ko HC, Chen HY (2003) Three-dimensional ultrasound in the assessment of normal fetal thigh volume. Ultrasound Med Biol 29:361–366
Meyer-Wittkopf M (2002) Interventional fetal cardiac therapy—possible perspectives and current shortcomings. Ultrasound Obstet Gynecol 20:527–531
Deng J, Rodeck CH (2006) Current applications of fetal cardiac imaging technology. Curr Opin Obstet Gynecol 18:177–184
Manganaro L, Savelli S, Di Maurizio M, Perrone A, Tesei J, Francioso A, Angeletti M, Coratella F, Irimia D, Fierro F, Ventriglia F, Ballesio L (2008) Potential role of fetal cardiac evaluation with magnetic resonance imaging: preliminary experience. Prenat Diagn 28:148–156
Fogel MA, Wilson RD, Flake A, Johnson M, Cohen D, McNeal G, Tian ZY, Rychik J (2005) Preliminary investigations into a new method of functional assessment of the fetal heart using a novel application of ‘real-time’ cardiac magnetic resonance imaging. Fetal Diagn Ther 20:475–480
Smith FW, MacLennan F, Abramovich DR, MacGilivray I, Hutchison JM (1984) NMR imaging in human pregnancy: a preliminary study. Magn Reson Imaging 2:57–64
Smith FW, Adam AH, Phillips WD (1983) NMR imaging in pregnancy. Lancet 1:61–62
Hiba B, Richard N, Thibault H, Janier M (2007) Cardiac and respiratory self-gated cine MRI in the mouse: comparison between radial and rectilinear techniques at 7 T. Magn Reson Med 58:745–753
Crowe ME, Larson AC, Zhang Q, Carr J, White RD, Li D, Simonetti OP (2004) Automated rectilinear self-gated cardiac cine imaging. Magn Reson Med 52:782–788
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Yamamura, J., Schnackenburg, B., Kooijmann, H. et al. High resolution MR imaging of the fetal heart with cardiac triggering: a feasibility study in the sheep fetus. Eur Radiol 19, 2383–2390 (2009). https://doi.org/10.1007/s00330-009-1420-8
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DOI: https://doi.org/10.1007/s00330-009-1420-8