Skip to main content
Top
Published in: European Radiology 10/2009

01-10-2009 | Experimental

High resolution MR imaging of the fetal heart with cardiac triggering: a feasibility study in the sheep fetus

Authors: Jin Yamamura, Bernhard Schnackenburg, Hendrik Kooijmann, Michael Frisch, Kurt Hecher, Gerhard Adam, Ulrike Wedegärtner

Published in: European Radiology | Issue 10/2009

Login to get access

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.
Literature
1.
go back to reference 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 180:715–721PubMed 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 180:715–721PubMed
2.
go back to reference 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 248:240–246PubMedCrossRef 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 248:240–246PubMedCrossRef
3.
go back to reference 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. 30:211–220PubMedCrossRef 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. 30:211–220PubMedCrossRef
4.
go back to reference 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 40:148–159PubMedCrossRef 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 40:148–159PubMedCrossRef
5.
go back to reference 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):242–246PubMedCrossRef 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):242–246PubMedCrossRef
6.
go back to reference 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 500:239–254PubMedCrossRef 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 500:239–254PubMedCrossRef
7.
go back to reference 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 49:161–167PubMedCrossRef 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 49:161–167PubMedCrossRef
8.
go back to reference 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 237:919–926PubMedCrossRef 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 237:919–926PubMedCrossRef
9.
go back to reference 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 238:872–880PubMedCrossRef 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 238:872–880PubMedCrossRef
10.
go back to reference 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 174:700–703PubMed 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 174:700–703PubMed
11.
go back to reference 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 26:921–926PubMedCrossRef 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 26:921–926PubMedCrossRef
12.
go back to reference 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 247:220–227PubMed 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 247:220–227PubMed
13.
go back to reference Finn JP, Nael K, Deshpande V, Ratib O, Laub G (2006) Cardiac MR imaging: state of the technology. Radiology 241:338–354PubMedCrossRef Finn JP, Nael K, Deshpande V, Ratib O, Laub G (2006) Cardiac MR imaging: state of the technology. Radiology 241:338–354PubMedCrossRef
14.
go back to reference 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):837–844PubMedCrossRef 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):837–844PubMedCrossRef
15.
go back to reference 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 245:103–110PubMedCrossRef 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 245:103–110PubMedCrossRef
16.
go back to reference 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 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
17.
go back to reference 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 182:243–252PubMed 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 182:243–252PubMed
18.
go back to reference Coakley FV, Hricak H, Filly RA, Barkovich AJ, Harrison MR (1999) Complex fetal disorders: effect of MR imaging on management—preliminary clinical experience. Radiology 213:691–696PubMed Coakley FV, Hricak H, Filly RA, Barkovich AJ, Harrison MR (1999) Complex fetal disorders: effect of MR imaging on management—preliminary clinical experience. Radiology 213:691–696PubMed
19.
go back to reference 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 12:1952–1961PubMed 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 12:1952–1961PubMed
20.
go back to reference Guo WY, Wong TT (2003) Screening of fetal CNS anomalies by MR imaging. Childs Nerv Syst 19:410–414PubMedCrossRef Guo WY, Wong TT (2003) Screening of fetal CNS anomalies by MR imaging. Childs Nerv Syst 19:410–414PubMedCrossRef
21.
go back to reference Guo Y, Luo BN (2006) The state of the art of fetal magnetic resonance imaging. Chin Med J (Engl) 119:1294–1299 Guo Y, Luo BN (2006) The state of the art of fetal magnetic resonance imaging. Chin Med J (Engl) 119:1294–1299
22.
go back to reference Stoll C, Benoit F, Peter MO, Gasser B (1999) Familial association of camptodactyly, mental retardation, whistling face and Pierre Robin sequence. Clin Dysmorphol 8:247–251PubMedCrossRef Stoll C, Benoit F, Peter MO, Gasser B (1999) Familial association of camptodactyly, mental retardation, whistling face and Pierre Robin sequence. Clin Dysmorphol 8:247–251PubMedCrossRef
23.
go back to reference Allen LM, Silverman RK (2000) Prenatal ultrasound evaluation of fetal diastematomyelia: two cases of type I split cord malformation. Ultrasound Obstet Gynecol 15:78–82PubMedCrossRef Allen LM, Silverman RK (2000) Prenatal ultrasound evaluation of fetal diastematomyelia: two cases of type I split cord malformation. Ultrasound Obstet Gynecol 15:78–82PubMedCrossRef
24.
go back to reference Deng J, Brookes JA, Gardener JE, Rodeck CH, Lees WR (1996) Three-dimensional magnetic resonance imaging of the postmortem fetal heart. Fetal Diagn Ther 11:417–421PubMedCrossRef Deng J, Brookes JA, Gardener JE, Rodeck CH, Lees WR (1996) Three-dimensional magnetic resonance imaging of the postmortem fetal heart. Fetal Diagn Ther 11:417–421PubMedCrossRef
25.
26.
go back to reference 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 8:303–308PubMedCrossRef 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 8:303–308PubMedCrossRef
27.
go back to reference Wang XF, Deng YB, Nanda NC, Deng J, Miller AP, Xie MX (2003) Live three-dimensional echocardiography: imaging principles and clinical application. Echocardiography 20:593–604PubMedCrossRef Wang XF, Deng YB, Nanda NC, Deng J, Miller AP, Xie MX (2003) Live three-dimensional echocardiography: imaging principles and clinical application. Echocardiography 20:593–604PubMedCrossRef
28.
go back to reference Chang CH, Yu CH, Chang FM, Ko HC, Chen HY (2003) Volumetric assessment of normal fetal lungs using three-dimensional ultrasound. Ultrasound Med Biol 29:935–942PubMedCrossRef Chang CH, Yu CH, Chang FM, Ko HC, Chen HY (2003) Volumetric assessment of normal fetal lungs using three-dimensional ultrasound. Ultrasound Med Biol 29:935–942PubMedCrossRef
29.
go back to reference 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 29:361–366PubMedCrossRef 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 29:361–366PubMedCrossRef
30.
go back to reference Meyer-Wittkopf M (2002) Interventional fetal cardiac therapy—possible perspectives and current shortcomings. Ultrasound Obstet Gynecol 20:527–531PubMedCrossRef Meyer-Wittkopf M (2002) Interventional fetal cardiac therapy—possible perspectives and current shortcomings. Ultrasound Obstet Gynecol 20:527–531PubMedCrossRef
31.
go back to reference Deng J, Rodeck CH (2006) Current applications of fetal cardiac imaging technology. Curr Opin Obstet Gynecol 18:177–184PubMedCrossRef Deng J, Rodeck CH (2006) Current applications of fetal cardiac imaging technology. Curr Opin Obstet Gynecol 18:177–184PubMedCrossRef
32.
go back to reference 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 28:148–156PubMedCrossRef 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 28:148–156PubMedCrossRef
33.
go back to reference 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 20:475–480PubMedCrossRef 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 20:475–480PubMedCrossRef
34.
go back to reference Smith FW, MacLennan F, Abramovich DR, MacGilivray I, Hutchison JM (1984) NMR imaging in human pregnancy: a preliminary study. Magn Reson Imaging 2:57–64PubMedCrossRef Smith FW, MacLennan F, Abramovich DR, MacGilivray I, Hutchison JM (1984) NMR imaging in human pregnancy: a preliminary study. Magn Reson Imaging 2:57–64PubMedCrossRef
36.
go back to reference 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 58:745–753PubMedCrossRef 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 58:745–753PubMedCrossRef
37.
go back to reference 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 52:782–788PubMedCrossRef 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 52:782–788PubMedCrossRef
Metadata
Title
High resolution MR imaging of the fetal heart with cardiac triggering: a feasibility study in the sheep fetus
Authors
Jin Yamamura
Bernhard Schnackenburg
Hendrik Kooijmann
Michael Frisch
Kurt Hecher
Gerhard Adam
Ulrike Wedegärtner
Publication date
01-10-2009
Publisher
Springer-Verlag
Published in
European Radiology / Issue 10/2009
Print ISSN: 0938-7994
Electronic ISSN: 1432-1084
DOI
https://doi.org/10.1007/s00330-009-1420-8

Other articles of this Issue 10/2009

European Radiology 10/2009 Go to the issue