Hostname: page-component-cd9895bd7-hc48f Total loading time: 0 Render date: 2024-12-28T14:19:16.354Z Has data issue: false hasContentIssue false
  • English
  • Français

Cardiac magnetic resonance imaging: insights into developmental programming and its consequences for aging

Part of: Advance Imaging in DOHaD

Published online by Cambridge University Press:  22 December 2020

G.D. Clarke Open the ORCID record for G.D. Clarke [Opens in a new window] ,
J. Li ,
A.H. Kuo ,
A.J. Moody  and
P.W. Nathanielsz
G.D. Clarke*
Affiliation:
Department of Radiology, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA Research Imaging Institute, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA
J. Li
Affiliation:
Department of Radiology, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA Research Imaging Institute, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA
A.H. Kuo
Affiliation:
Department of Radiology, Massachusetts General Hospital, Boston, MA, USA
A.J. Moody
Affiliation:
Department of Radiology, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA Research Imaging Institute, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA
P.W. Nathanielsz
Affiliation:
Department of Animal Science, University of Wyoming, Laramie, WY, USA
*
Address for correspondence: GD Clarke, Department of Radiology, University of Texas Health Science Center at San Antonio and Research Imaging Institute, University of Texas Health Science Center at San Antonio and Research Imaging Institute, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA. Email: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Cardiovascular diseases (CVD) are important consequences of adverse perinatal conditions such as fetal hypoxia and maternal malnutrition. Cardiac magnetic resonance imaging (CMR) can produce a wealth of physiological information related to the development of the heart. This review outlines the current state of CMR technologies and describes the physiological biomarkers that can be measured. These phenotypes include impaired ventricular and atrial function, maladaptive ventricular remodeling, and the proliferation of myocardial steatosis and fibrosis. The discussion outlines the applications of CMR to understanding the developmental pathways leading to impaired cardiac function. The use of CMR, both in animal models of developmental programming and in human studies, is described. Specific examples are given in a baboon model of intrauterine growth restriction (IUGR). CMR offers great potential as a tool for understanding the sequence of dysfunctional adaptations of developmental origin that can affect the human cardiovascular system.

Keywords

Heart diseasecardiac MRIventricular remodelingdevelopmental programming
Type
Review
Information
Journal of Developmental Origins of Health and Disease , Volume 12 , Issue 2 , April 2021 , pp. 203 - 219
Check for updates
Copyright
© The Author(s), 2020. Published by Cambridge University Press in association with International Society for Developmental Origins of Health and Disease

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Barker, DJ. Fetal nutrition and cardiovascular disease in later life. Brit Med Bul. 1997; 53, 96–108.CrossRefGoogle ScholarPubMed
Dong, M, Zheng, Q, Ford, SP, Nathanielsz, PW, Ren, J. Maternal obesity, lipotoxicity and cardiovascular diseases in offspring. J Mol Cell Cardiol. 2013; 55, 111–116.CrossRefGoogle ScholarPubMed
Roseboom, TJ, van der Meulen, JH, Osmond, C, et al. Coronary heart disease after prenatal exposure to the Dutch famine, 1944–45. Heart. 2000; 84, 595–598.CrossRefGoogle ScholarPubMed
Barker, DJ, Bagby, SP. Developmental antecedents of cardiovascular disease: a historical perspective. J Am Soc Nephrol. 2005; 16, 2537–2544.CrossRefGoogle ScholarPubMed
Gluckman, PD, Hanson, MA, Buklijas, T, Low, FM, Beedle, AS. Epigenetic mechanisms that underpin metabolic and cardiovascular diseases. Nat Rev Endocrinol. 2009; 5, 401–408.CrossRefGoogle ScholarPubMed
Agarwal, P, Morriseau, TS, Kereliuk, SM, Doucette, CA, Wicklow, BA, Dolinsky, VW. Maternal obesity, diabetes during pregnancy and epigenetic mechanisms that influence the developmental origins of cardiometabolic disease in the offspring. Crit Rev Clin Lab Sci. 2018; 55, 71–101.CrossRefGoogle ScholarPubMed
Nathanielsz, PW. Life in the Womb: The Origin of Health and Disease, 1999. Promethean Press, Ithaca, NY.Google Scholar
Watson, CJ, Collier, P, Tea, I, et al. Hypoxia-induced epigenetic modifications are associated with cardiac tissue fibrosis and the development of a myofibroblast-like phenotype. Hum Mol Gen. 2014; 23, 2176–2188.CrossRefGoogle ScholarPubMed
Lee, L, Lupo, P. Maternal smoking during pregnancy and the risk of congenital heart defects in offspring: a systematic review and metaanalysis. Pediatr Cardiol. 2013; 34, 398–407.CrossRefGoogle ScholarPubMed
Reid, N, Akison, LK, Hoy, W, Moritz, KM. Adverse health outcomes associated with fetal alcohol exposure: a systematic review focused on cardio–renal outcomes. J Stud Alcohol Drugs. 2019; 80, 515–523.CrossRefGoogle ScholarPubMed
Govindsamy, A, Naidoo, S, Cerf, ME. Cardiac development and transcription factors: insulin signalling, insulin resistance, and intrauterine nutritional programming of cardiovascular disease. J Nutr Metab. 2018; Article ID 8547976, 12.Google ScholarPubMed
Blackmore, HL, Ozanne, SE. Programming of cardiovascular disease across the life-course. J Molec Cell Cardiol. 2015; 83, 122–130.CrossRefGoogle ScholarPubMed
van der Harst, P, de Windt, LJ, Chambers, JC. Translational perspective on epigenetics in cardiovascular disease. JACC. 2017; 70, 590–606.10.1016/j.jacc.2017.05.067CrossRefGoogle ScholarPubMed
Muralimanoharan, S, Li, C, Nakayasu, ES, et al. Sexual dimorphism in the fetal cardiac response to maternal nutrient restriction. J Mol Cell Cardiol. 2017; 108, 181–193.CrossRefGoogle ScholarPubMed
Maloyan, A, Muralimanoharan, S, Huffman, S, Cox, LA, Nathanielsz, PW, Myatt, L, Nijland, MJ. Identification and comparative analyses of myocardial miRNAs involved in the fetal response to maternal obesity. Physiol Genomics. 2013; 45: 889–900.CrossRefGoogle ScholarPubMed
Alfonso, F, Macaya, C, Goicolea, J, In, A, Hernandez, R, Zamorano, J, Perez-Vizcayne, MJ, Zarco, P. Intravascular ultrasound imaging of angiographically normal coronary segments in patients with coronary artery disease. Am Heart J. 1994; 127, 536–544.CrossRefGoogle ScholarPubMed
Crispi, F, Miranda, J, Gratacos, E. Long-term cardiovascular consequences of fetal growth restriction: biology, clinical implications, and opportunities for prevention of adult disease. Am J Obstet Gynecol. 2018; 218, S869–S879.CrossRefGoogle ScholarPubMed
Rodríguez-López, M, Cruz-Lemini, M, Valenzuela-Alcaraz, B, et al. Descriptive analysis of different phenotypes of cardiac remodeling in fetal growth restriction. Ultrasound Obst Gyn. 2017; 50, 207–214.CrossRefGoogle ScholarPubMed
Comas, M, Crispi, F, Cruz-Martinez, R, Figueras, F, Gratacos, E. Tissue Doppler echocardiographic markers of cardiac dysfunction in small-for-gestational age fetuses. Am J Obstet Gynecol. 2011; 205, 57–e1.CrossRefGoogle ScholarPubMed
Cruz-Lemini, M, Crispi, F, Valenzuela-Alcaraz, B, et al. Fetal cardiovascular remodeling persists at 6 months in infants with intrauterine growth restriction. Ultrasound Obst Gyn. 2016; 48, 349–356.CrossRefGoogle ScholarPubMed
Sehgal, A, Doctor, T, Menahem, S. Cardiac function and arterial biophysical properties in small for gestational age infants: postnatal manifestations of fetal programming. J Pediatr. 2013; 163, 1296–1300.10.1016/j.jpeds.2013.06.030CrossRefGoogle ScholarPubMed
Rueda-Clausen, CF, Morton, JS, Dolinsky, VW, Dyck, JR, Davidge, ST. Synergistic effects of prenatal hypoxia and postnatal high-fat diet in the development of cardiovascular pathology in young rats. Am J Physiol Regul Integr Comp Physiol. 2012; 303, R418–R426.10.1152/ajpregu.00148.2012CrossRefGoogle ScholarPubMed
Aljunaidy, MM, Morton, JS, Kirschenman, R, et al. Maternal treatment with a placental-targeted antioxidant (MitoQ) impacts offspring cardiovascular function in a rat model of prenatal hypoxia. Pharm Res. 2018; 134, 332–342.CrossRefGoogle Scholar
Zohdi, V, Pearson, JT, Kett, MM, et al. When early life growth restriction in rats is followed by attenuated postnatal growth: effects on cardiac function in adulthood. Eur J Nutr. 2015; 54, 743–750.CrossRefGoogle ScholarPubMed
Keller, AM, Peshock, RM, Malloy, CR, et al. In vivo measurement of myocardial mass using nuclear magnetic resonance imaging. J Am Coll Cardiol. 1986; 8, 113–117.CrossRefGoogle ScholarPubMed
Buser, PT, Auffermann, W, Holt, WW, Wagner, S, Kircher, B, Wolfe, C, Higgins, CB. Noninvasive evaluation of global left ventricular function with use of cine nuclear magnetic resonance. JACC. 1989; 13, 1294–300.CrossRefGoogle ScholarPubMed
Soldo, SJ, Norris, SL, Gober, JR, et al. MRI-derived ventricular volume curves for the assessment of left ventricular function. Magn Reson Imag. 1994; 12, 711–717.CrossRefGoogle ScholarPubMed
Spielmann, RP, Schneider, O, Thiele, F, Heller, M, Bücheler, E. Appearance of poststenotic jets in MRI: dependence on flow velocity and on imaging parameters. Magn Reson Imag. 1991; 9, 67–72.10.1016/0730-725X(91)90098-7CrossRefGoogle ScholarPubMed
Peng, P, Lekadir, K, Gooya, A, Shao, Ling, Petersen, Steffen E, Frangi, Alejandro F. A review of heart chamber segmentation for structural and functional analysis using cardiac magnetic resonance imaging. Magn Reson Mater Phy. 2016; 29, 155–195.CrossRefGoogle ScholarPubMed
Heiberg, E, Sjögren, J, Ugander, M, Carlsson, M, Engblom, H, Arheden, H. Design and validation of segment: freely available software for cardiovascular image analysis. BMC Med Imag. 2010; 10, 1–13.10.1186/1471-2342-10-1CrossRefGoogle ScholarPubMed
Leng, S, Ge, H, He, J, et al. Long-term prognostic value of cardiac MRI left atrial strain in ST-segment elevation myocardial infarction. Radiology. 2020; 296, 299–309.CrossRefGoogle ScholarPubMed
Trattner, S, Chelliah, A, Prinsen, P, et al. Estimating effective dose of radiation from pediatric cardiac CT angiography using a 64-MDCT scanner: new conversion factors relating dose-length product to effective dose. AJR Am J Roentgenol. 2017; 208, 585–594.10.2214/AJR.15.15908CrossRefGoogle ScholarPubMed
Kleiber, M. Body size and metabolic rate. Physiol Rev. 1947; 27, 511–541.CrossRefGoogle ScholarPubMed
Gutgesell, HP, Rembold, CM. Growth of the human heart relative to body surface area. Am J Cardiol. 1990; 65, 662–668.CrossRefGoogle ScholarPubMed
D’Oronzio, U, Senn, O, Biaggi, P, et al. Right heart assessment by echocardiography: gender and body size matters. J Am Soc Echocardiog. 2012; 25, 1251–1258.CrossRefGoogle ScholarPubMed
Beygui, F, Furber, A, Delépine, S, et al. Routine breath-hold gradient echo MRI-derived right ventricular mass, volumes and function: accuracy, reproducibility and coherence study. Int J Cardiovasc Imag. 2004; 20, 509–516.CrossRefGoogle ScholarPubMed
Wiesmann, F, Frydrychowicz, A, Rautenberg, J, et al. Analysis of right ventricular function in healthy mice and a murine model of heart failure by in vivo MRI. Am J Physiol Heart Circ Physiol. 2002; 283, H1065–H1071.CrossRefGoogle Scholar
Kuo, AH, Li, C, Huber, HF, et al. Maternal nutrient restriction during pregnancy and lactation leads to impaired right ventricular function in young adult baboons. J Physiol. 2017; 595, 4245–4260.CrossRefGoogle ScholarPubMed
Kuehne, T, Yilmaz, S, Steendijk, P, et al. Magnetic resonance imaging analysis of right ventricular pressure-volume loops: in vivo validation and clinical application in patients with pulmonary hypertension. Circulation. 2004; 110, 2010–2016.CrossRefGoogle ScholarPubMed
Saba, TS, Foster, J, Cockburn, M, Cowan, M, Peacock, AJ. Ventricular mass index using magnetic resonance imaging accurately estimates pulmonary artery pressure. Euro Respir J. 2002; 20, 1519–1524.CrossRefGoogle ScholarPubMed
Szczepanska-Sadowska, E, Czarzasta, K, Cudnoch-Jedrzejewska, A. (2018) Dysregulation of the renin-angiotensin system and the vasopressinergic system interactions in cardiovascular disorders. Curr Hypertension Rep. 20, 19.10.1007/s11906-018-0823-9CrossRefGoogle ScholarPubMed
Houben, AJ, van der Zander, K, de Leeuw, PW. Vascular and renal actions of brain natriuretic peptide in man: physiology and pharmacology. Fund Clin Pharm. 2005; 19, 411–419.CrossRefGoogle ScholarPubMed
Perrone-Filardi, P, Coca, A, Galderisi, M, et al. Noninvasive cardiovascular imaging for evaluating subclinical target organ damage in hypertensive patients: a consensus article from the European Association of Cardiovascular Imaging, the European Society of Cardiology Council on Hypertension and the European Society of Hypertension. J Hypertension. 2017; 35, 1727–1741.CrossRefGoogle Scholar
Hoit, BD. Left atrial size and function: role in prognosis. JACC. 2014; 63, 493–505.CrossRefGoogle ScholarPubMed
Axel, L, Dougherty, L. Heart wall motion: improved method of spatial modulation of magnetization for MR imaging. Radiology. 1989; 172, 349–350.Google Scholar
Kraitchman, DL, Young, AA, Chang, CN, Axel, L. Semi-automatic tracking of myocardial motion in MR tagged images. IEEE Trans Med Imag. 1995; 14, 422–433.10.1109/42.414606CrossRefGoogle ScholarPubMed
Schuster, A, Hor, KN, Kowallick, JT, Beerbaum, P, Kutty, S. Cardiovascular magnetic resonance myocardial feature tracking: concepts and clinical applications. Circ Cardiovasc Imag. 2016; 9, e004077. doi: 10.1161/CIRCIMAGING.115.004077.CrossRefGoogle ScholarPubMed
Barreiro-Pérez, M, Curione, D, Symons, R, Claus, P, Voigt, JU, Bogaert, J. Left ventricular global myocardial strain assessment comparing the reproducibility of four commercially available CMR-feature tracking algorithms. Euro Radiol. 2018; 28, 5137–5147.10.1007/s00330-018-5538-4CrossRefGoogle ScholarPubMed
El Ghannudi, S, Germain, P, Jeung, MY, et al. Discrepancy between regional left ventricular regional circumferential strain assessed by MR-tagging and by speckle tracking echocardiography. J Biomed Graph Comput. 2013; 3, 75–84.Google Scholar
Moon, JC, Messroghli, DR, Kellman, P, et al. Myocardial T1 mapping and extracellular volume quantification: a society for cardiovascular magnetic resonance (SCMR) and CMR working group of the European society of cardiology consensus statement. J Cardiovasc Magn Reson. 2013; 15, 92.CrossRefGoogle Scholar
Salemi, VM, Rochitte, CE, Shiozaki, AA, et al. Late gadolinium enhancement magnetic resonance imaging in the diagnosis and prognosis of endomyocardial fibrosis patients. Circ Cardiovasc Imag. 2011; 4(3):304–311.CrossRefGoogle ScholarPubMed
Khalique, Z, Ferreira, PF, Scott, AD, Nielles-Vallespin, S, Firmin, DN, Pennell, DJ. Diffusion tensor cardiovascular magnetic resonance imaging: a clinical perspective. JACC Cardiovasc Imag. 2019. doi: 10.1016/j.jcmg.2019.07.016.Google ScholarPubMed
Guglielmi, V, Sbraccia, P. Epicardial adipose tissue: at the heart of the obesity complications. Acta Diabet. 2017; 54(9), 805–812.CrossRefGoogle ScholarPubMed
Kuo, AH, Li, C, Mattern, V, Huber, HF, et al. Sex-dimorphic acceleration of pericardial, subcutaneous, and plasma lipid increase in offspring of poorly nourished baboons. Intl J Obes. 2018; 42, 1092–1096.CrossRefGoogle ScholarPubMed
Gastl, M, Peereboom, SM, Gotschy, A, et al. Myocardial triglycerides in cardiac amyloidosis assessed by proton cardiovascular magnetic resonance spectroscopy. J Cardiovasc Magn Reson. 2019; 21(1), 10.CrossRefGoogle ScholarPubMed
Fillmer, A, Hock, A, Cameron, D, Henning, A. Non-water-suppressed 1 H MR spectroscopy with orientational prior knowledge shows potential for separating intra-and extramyocellular lipid signals in human myocardium. Sci Rep. 2017; 7, 1–4.CrossRefGoogle ScholarPubMed
Pelc, NJ, Herfkens, RJ, Shimakawa, A, Enzmann, DR. Phase contrast cine magnetic resonance imaging. Magn Reson Quart. 1991; 7, 229–254.Google ScholarPubMed
Hundley, WG, Lange, RA, Clarke, GD, et al. Assessment of coronary arterial flow and flow reserve in humans with magnetic resonance imaging. Circulation. 1996; 93, 1502–1508.CrossRefGoogle ScholarPubMed
Sensky, PR, Jivan, A, Hudson, NM, et al. Coronary artery disease: combined stress MR imaging protocol—one-stop evaluation of myocardial perfusion and function. Radiology. 2000; 215, 608–614.CrossRefGoogle ScholarPubMed
Markl, M, Frydrychowicz, A, Kozerke, S, Hope, M, Wieben, O. 4D flow MRI. J Magn Reson Imag. 2012: 36, 1015–1036.CrossRefGoogle ScholarPubMed
Puntmann, VO, Valbuena, S, Hinojar, R, et al. Society for cardiovascular magnetic resonance (SCMR) expert consensus for CMR imaging endpoints in clinical research: part I-analytical validation and clinical qualification. J Cardiovasc Magn Reson. 2018; 20, 1–23.CrossRefGoogle ScholarPubMed
Kawel-Boehm, N, Maceira, A, Valsangiacomo-Buechel, ER, et al. Normal values for cardiovascular magnetic resonance in adults and children. J Cardiovasc Magn Reson. 2015; 17, 29. doi: 10.1186/s12968-015-0111-7.CrossRefGoogle ScholarPubMed
Petersen, SE, Aung, N, Sanghvi, MM, et al. Reference ranges for cardiac structure and function using cardiovascular magnetic resonance (CMR) in Caucasians from the UK Biobank population cohort. J Cardiovasc Magn Reson. 2017; 19:18. doi: 10.1186/s12968-017-0327-9.CrossRefGoogle ScholarPubMed
Le Ven, F, Bibeau, K, De Larochellière, É, et al. Cardiac morphology and function reference values derived from a large subset of healthy young Caucasian adults by magnetic resonance imaging. Eur Heart J Cardiovasc Imaging. 2016; 17, 981–990.CrossRefGoogle ScholarPubMed
Maceira, AM, Cosin-Sales, J, Prasad, SK, Pennell, DJ. Characterization of left and right atrial function in healthy volunteers by cardiovascular magnetic resonance. J Cardiovasc Magn Reson. 2016; 18, 64. doi: 10.1186/s12968-016-0284-8.CrossRefGoogle ScholarPubMed
Sarikouch, S, Peters, B, Gutberlet, M, et al. Sex-specific pediatric percentiles for ventricular size and mass as reference values for cardiac MRI: assessment by steady-state free-precession and phase-contrast MRI flow. Circ Cardiovasc Imaging. 2010; 3, 65–76.CrossRefGoogle ScholarPubMed
Sarikouch, S, Koerperich, H, Boethig, D, et al. Reference values for atrial size and function in children and young adults by cardiac MR: a study of the German competence network congenital heart defects. J Magn Reason Imag. 2011; 33, 1028–1039.CrossRefGoogle Scholar
Natori, S, Lai, S, Finn, JP, Gomes, AS, et al. Cardiovascular function in multi-ethnic study of atherosclerosis: normal values by age, sex, and ethnicity. AJR Am J Roentgenol. 2006; 186, S357–S365.CrossRefGoogle ScholarPubMed
Zemrak, F, Ambale-Venkatesh, B, Captur, G, et al. Left atrial structure in relationship to age, sex, ethnicity, and cardiovascular risk factors: MESA (Multi-ethnic study of atherosclerosis). Circ Cardiovasc Imaging. 2017; 10, e005379. doi: 10.1161/CIRCIMAGING.116.005379.CrossRefGoogle Scholar
Le, TT, San Tan, R, De Deyn, M, et al. Cardiovascular magnetic resonance reference ranges for the heart and aorta in Chinese at 3T. J Cardiovasc Magn Reson. 2016; 18, 21. doi: 10.1186/s12968–016–0236.CrossRefGoogle ScholarPubMed
Kim, PK, Hong, YJ, Im, DJ, et al. Myocardial T1 and T2 mapping: techniques and clinical applications. Korean J Radiol. 2017; 18, 113–131.CrossRefGoogle ScholarPubMed
Lee, JJ, Liu, S, Nacif, MS, et al. Myocardial T1 and extracellular volume fraction mapping at 3 tesla. J Cardiovasc Magn Reson. 2011; 13, 75. doi: 10.1186/1532–429X-13–75.CrossRefGoogle ScholarPubMed
Roy, C, Slimani, A, de Meester, C, et al. Age and sex corrected normal reference values of T1, T2 T2* and ECV in healthy subjects at 3T CMR. J Cardiovasc Magn Reson. 2017; 19, 72. doi: 10.1186/s12968-017-0371-5.CrossRefGoogle ScholarPubMed
Barczuk-Falęcka, M, Małek, ŁA, Werys, K, Roik, D, Adamus, K, Brzewski, M. (2020) Normal values of native T1 and T2 relaxation times on 3T cardiac MR in a healthy pediatric population aged 9–18 years. J Magn Reson Imag. 51, 912–918.CrossRefGoogle Scholar
Burkhardt, BE, Menghini, C, Rücker, B, Kellenberger, CJ, Valsangiacomo Buechel, ER. Normal myocardial native T1 values in children using single-point saturation recovery and modified look–locker inversion recovery (MOLLI). J Magn Reason Imag. 2020; 51, 897–903.CrossRefGoogle Scholar
Dabir, D, Child, N, Kalra, A, et al. Reference values for healthy human myocardium using a T1 mapping methodology: results from the International T1 Multicenter cardiovascular magnetic resonance study. J Cardiovasc Magn Reson. 2014; 16, 69. doi: 10.1186/s12968–014–0069-x.CrossRefGoogle ScholarPubMed
Magri, D, Sciomer, S, Fedele, F, et al. Early impairment of myocardial function in young patients with β-thalassemia major. Eur J Haematol. 2008; 80, 515–522.CrossRefGoogle ScholarPubMed
Boss, A, Oppitz, M, Wehrl, HF, et al. Measurement of T1, T2, and magnetization transfer properties during embryonic development at 7 Tesla using the chicken model. J Magn Reson Imag. 2008; 28, 1510–1514.CrossRefGoogle ScholarPubMed
Broadhouse, KM, Finnemore, AE, Price, AN, et al. Cardiovascular magnetic resonance of cardiac function and myocardial mass in preterm infants: a preliminary study of the impact of patent ductus arteriosus. J Cardiovasc Magn Reson. 2014; 16, 54.CrossRefGoogle ScholarPubMed
Toemen, L, Jelic, G, Kooijman, MN, et al. Third trimester fetal cardiac blood flow and cardiac outcomes in school-age children assessed by magnetic resonance imaging. J Am Heart Assoc. 2019; 8, e012821. doi: 10.1161/JAHA.119.01282.CrossRefGoogle ScholarPubMed
Groves, AM, Chiesa, G, Durighel, G, et al. Functional cardiac MRI in preterm and term newborns. Arch Dis Child Fetal Neonatal Ed. 2011; 96, F86–F91.CrossRefGoogle ScholarPubMed
Poon, CY, Edwards, JM, Evans, CJ, et al. Assessment of pulmonary artery pulse wave velocity in children: an MRI pilot study. Magn Reson Imag. 2013; 31, 1690–1694.CrossRefGoogle ScholarPubMed
André, F, Robbers-Visser, D, Helling-Bakki, A, et al. Quantification of myocardial deformation in children by cardiovascular magnetic resonance feature tracking: determination of reference values for left ventricular strain and strain rate. J Cardiovasc Magn Reson. 2017; 19, 8. doi: 10.1186/s12968-016-0310-x.CrossRefGoogle Scholar
Roy, CW, Marini, D, Seed, M, Macgowan, CK. Fetal Cardiac MRI: a review of technical advancements. Top Magn Reason Imag. 2019; 28, 235–244.CrossRefGoogle ScholarPubMed
Cho, SK, Darby, JR, Saini, BS, et al. Feasibility of ventricular volumetry by cardiovascular MRI to assess cardiac function in the fetal sheep. J Physiol. 2020; 598, 2557–2573.CrossRefGoogle ScholarPubMed
Roberts, TA, van Amerom, JF, Uus, A, et al. Fetal whole heart blood flow imaging using 4D cine MRI. Nat Commun. 2020; 11, 1–3.Google ScholarPubMed
Schrauben, EM, Saini, BS, Darby, JR, et al. Fetal hemodynamics and cardiac streaming assessed by 4D flow cardiovascular magnetic resonance in fetal sheep. J Cardiovasc Magn Reson. 2019; 21, 8.CrossRefGoogle ScholarPubMed
Saini, BS, Darby, JR, Portnoy, S, et al. Normal human and sheep fetal vessel oxygen saturations by T2 magnetic resonance imaging. J Physiol. 2020; 598, 3259–3281.Google Scholar
Zhu, MY, Milligan, N, Keating, S, et al. The hemodynamics of late-onset intrauterine growth restriction by MRI. Am J Obstet Gynecol. 2016; 214, 367.e1–367.e17. doi: 10.1016/j.ajog.2015.10.004.CrossRefGoogle ScholarPubMed
Toemen, L, Gaillard, R, Roest, AA, et al. Fetal and infant growth patterns and left and right ventricular measures in childhood assessed by cardiac MRI. Eur J Prev Cardiol. 2019. doi: 10.1177/2047487319866022.Google ScholarPubMed
Kingdom, T, Zhu, MY, Porayette, P, et al. The absolute and relative sizes of the brains and bodies of fetuses with different forms of congenital heart disease and intrauterine growth restriction. J Cardiovasc Magn Reson. 2016; 18. doi: 10.1186/1532–429X-18-S1-P151.CrossRefGoogle Scholar
Cohn, HE, Sacks, EJ, Heymann, MA, Rudolph, AM. Cardiovascular responses to hypoxemia and acidemia in fetal lambs. Obstet Gynecol. 1974; 120, 817–824.Google ScholarPubMed
Cox, DJ, Bai, W, Price, AN, Edwards, AD, Rueckert, D, Groves, AM. Ventricular remodeling in preterm infants: computational cardiac magnetic resonance atlasing shows significant early remodeling of the left ventricle. Pediatr Res. 2019; 85, 807–815.CrossRefGoogle ScholarPubMed
Rabadan-Diehl, C, Nathanielsz, P. From Mice to men: research models of developmental programming. J Dev Origins Health Dis. 2013; 4, 3–9.CrossRefGoogle ScholarPubMed
Schlabritz-Loutsevitch, NE, Howell, K, Rice, K, et al. Development of a system for individual feeding of baboons maintained in an outdoor group social environment. J Med Primatol. 2004; 33, 117–126.CrossRefGoogle Scholar
Kuo, AH, Li, C, Li, J, Huber, HF, Nathanielsz, PW, Clarke, GD. Cardiac remodeling in a baboon model of intrauterine growth restriction mimics accelerated ageing. J Physiol. 2017; 595, 1093–1110.CrossRefGoogle Scholar
Rozance, PJ, Seedorf, GJ, Brown, A, et al. Intrauterine growth restriction decreases pulmonary alveolar and vessel growth and causes pulmonary artery endothelial cell dysfunction in vitro in fetal sheep. Am J Physio Lung Cell Mol Physiol. 2011; 301: L860–L871.CrossRefGoogle ScholarPubMed
Kuo, AH, Li, J, Li, C, Huber, HF, Nathanielsz, PW, Clarke, GD. Poor perinatal growth impairs baboon aortic windkessel function. J Dev Orig Health Dis. 2018; 9, 137–142.CrossRefGoogle ScholarPubMed
Kuo, AH, Li, C, Huber, HF, Clarke, GD, Nathanielsz, PW. Intrauterine growth restriction results in persistent vascular mismatch in adulthood. J Physiol. 2018; 596, 5777–5790.CrossRefGoogle ScholarPubMed
Corstius, HB, Zimanyi, MA, Maka, N, et al. Effect of intrauterine growth restriction on the number of cardiomyocytes in rat hearts. Pediatr Res. 2005; 57, 796–800.CrossRefGoogle ScholarPubMed
Botting, KJ, McMillen, IC, Forbes, H, Nyengaard, JR, Morrison, JL. Chronic hypoxemia in late gestation decreases cardiomyocyte number but does not change expression of hypoxia-responsive genes. J Am Heart Assoc. 2014; 3(4), e000531.CrossRefGoogle Scholar
Morrison, JL, Botting, KJ, Dyer, JL, Williams, SJ, Thornburg, KL, McMillen, IC. Restriction of placental function alters heart development in the sheep fetus. Am J Physiol Regul Integr Comp Physiol. 2007; 293, R306–R313.CrossRefGoogle ScholarPubMed
Bubb, KJ, Cock, ML, Black, MJ, et al. Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep. J Physiol (Lond). 2007; 578, 871–881.CrossRefGoogle ScholarPubMed
Harvey, TJ, Murphy, RM, Morrison, JL, Posterino, GS. Maternal nutrient restriction alters Ca2 handling properties and contractile function of isolated left ventricle bundles in male but not female juvenile rats. PLoS One. 2015; 10, e0138388.CrossRefGoogle Scholar
Iruretagoyena, JI, Gonzalez-Tendero, A, Garcia-Canadilla, P, et al. Cardiac dysfunction is associated with altered sarcomere ultrastructure in intrauterine growth restriction. Obstet Gynecol. 2014; 210, 550.e1–550.e7.Google ScholarPubMed
Bezerra, DG, Andrade, LML, da Cruz, FOP, Mandarim-de-Lacerda, CA. Atorvastatin attenuates cardiomyocyte loss in adult rats from protein-restricted dams. J Card Fail. 2008; 14, 151–160.CrossRefGoogle ScholarPubMed
Nakamori, S, Dohi, K, Ishida, M, et al. Native T1 mapping and extracellular volume mapping for the assessment of diffuse myocardial fibrosis in dilated cardiomyopathy. JACC Cardiovasc Imag. 2018; 11, 48–59.CrossRefGoogle ScholarPubMed
Enriquez-Sarano, M, Rossi, A, Seward, JB, Bailey, KR, Tajik, AJ. Determinants of pulmonary hypertension in left ventricular dysfunction. J Am Coll Cardiol. 1997; 29, 153–159.CrossRefGoogle ScholarPubMed
Thompson, JA, Gros, R, Richardson, BS, Piorkowska, K, Regnault, TR. Central stiffening in adulthood linked to aberrant aortic remodeling under suboptimal intrauterine conditions. Am J Physiol Regul Integr Comp Physiol. 2011; 301, 1731–1737.CrossRefGoogle ScholarPubMed
Khorram, O, Momeni, M, Desai, M, Ross, MG. Nutrient restriction in utero induces remodeling of the vascular extracellular matrix in rat offspring. Reprod Sci. 2007; 14(1), 73–80.CrossRefGoogle ScholarPubMed
Dodson, RB, Rozance, PJ, Petrash, CC, Hunter, KS, Ferguson, VL. Thoracic and abdominal aortas stiffen through unique extracellular matrix changes in intrauterine growth restricted fetal sheep. Am J Physiol Heart Circ Physiol. 2014; 306, H429–H437.CrossRefGoogle ScholarPubMed
Strait, JB, Lakatta, EG. Aging-associated cardiovascular changes and their relationship to heart failure. Heart Fail Clin. 2012; 8, 143–164.CrossRefGoogle ScholarPubMed
Sampath, S, Parimal, AS, Feng, D, et al. Quantitative MRI biomarkers to characterize regional left ventricular perfusion and function in nonhuman primates during dobutamine-induced stress: a reproducibility and reliability study. J Magn Reson Imag. 2017; 45, 556–569.CrossRefGoogle ScholarPubMed
Pashakhanloo, F, Herzka, DA, Ashikaga, H, et al. Myofiber architecture of the human atria as revealed by submillimeter diffusion tensor imaging. Circ Arrhythm Electrophysiol. 2016; 9, e004133.CrossRefGoogle ScholarPubMed
Mekkaoui, C, Reese, TG, Jackowski, MP, Bhat, H, Sosnovik, DE. Diffusion MRI in the heart. NMR Biomed. 2017; 30, e3426.CrossRefGoogle ScholarPubMed
Darby, JR, McMillen, IC, Morrison, JL. Maternal undernutrition in late gestation increases IGF2 signaling molecules and collagen deposition in the right ventricle of the fetal sheep heart. J Physiol. 2018; 596, 2345–2358.CrossRefGoogle ScholarPubMed
Ohno, Y, Hatabu, H, Murase, K, et al. Primary pulmonary hypertension: 3D dynamic perfusion MRI for quantitative analysis of regional pulmonary perfusion. Am J Roentgenol. 2007; 188, 48–56.CrossRefGoogle ScholarPubMed
Clarke, GD, Eckels, R, Chaney, C, et al. Measurement of absolute epicardial coronary artery flow and flow reserve using breath-hold cine phase-contrast magnetic resonance imaging. Circulation. 1995; 91, 2627–2634.CrossRefGoogle ScholarPubMed
Guensch, DP, Friedrich, MG. Novel approaches to myocardial perfusion: 3D first-pass CMR perfusion imaging and oxygenation-sensitive CMR. Curr Cardiovasc Imaging Rep. 2014; 7, 9261.CrossRefGoogle Scholar
Cox, LA, Nijland, MJ, Gilbert, JS, et al. Effect of 30 per cent maternal nutrient restriction from 0.16 to 0.5 gestation on fetal baboon kidney gene expression. J Physiol. 2006; 572, 67–85.CrossRefGoogle ScholarPubMed
Zhang, JL, Lee, VS. Renal perfusion imaging by MRI. J MAGN Reson Imag. 2020; 52, 369–379.CrossRefGoogle ScholarPubMed
Khatir, DS, Pedersen, M, Jespersen, B, Buus, NH. Evaluation of renal blood flow and oxygenation in CKD using magnetic resonance imaging. Am J Kid Dis. 2015; 66, 402–411.CrossRefGoogle ScholarPubMed
Collinot, H, Marchiol, C, Lagoutte, I, et al. Preeclampsia induced by STOX1 overexpression in mice induces intrauterine growth restriction, abnormal ultrasonography and BOLD MRI signatures. J Hypertension. 2018; 36, 1399–1406.CrossRefGoogle ScholarPubMed
Catalano, PM, Presley, L, Minium, J, Hauguel-de Mouzon, S. Fetuses of obese mothers develop insulin resistance in utero. Diabetes Care. 2009; 32, 1076–1080.CrossRefGoogle ScholarPubMed
Choi, J, Li, C, McDonald, TJ, Comuzzie, A, Mattern, V, Nathanielsz, PW. Emergence of insulin resistance in juvenile baboon offspring of mothers exposed to moderate maternal nutrient reduction. Am J Physiol Reg Integr Comp Physiol. 2011; 301, R757–R762.CrossRefGoogle ScholarPubMed
Reingold, JS, McGavock, JM, Kaka, S, Tillery, T, Victor, RG, Szczepaniak, LS. Determination of triglyceride in the human myocardium by magnetic resonance spectroscopy: reproducibility and sensitivity of the method. Am J Physiol Endo Metab. 2005; 289, E935–E939.CrossRefGoogle ScholarPubMed
Holloway, CJ, Cochlin, LE, Emmanuel, Y, et al. A high-fat diet impairs cardiac high-energy phosphate metabolism and cognitive function in healthy human subjects. Am J Clin Nutr. 2011; 93, 748–755.CrossRefGoogle ScholarPubMed
Somerville, LH, Bookheimer, SY, Buckner, RL, et al. The lifespan human connectome project in development: a large-scale study of brain connectivity development in 5–21 year olds. Neuroimage. 2018; 183, 456–468.CrossRefGoogle ScholarPubMed
Arthurs, OJ, Rega, A, Guimiot, F, et al. Diffusion-weighted magnetic resonance imaging of the fetal brain in intrauterine growth restriction. Ultrasound Obst Gyn. 2017; 50, 79–87.CrossRefGoogle ScholarPubMed
Polat, A, Barlow, S, Ber, R, Achiron, R, Katorza, E. Volumetric MRI study of the intrauterine growth restriction fetal brain. Euro Radiol. 2017; 27, 2110–2118.CrossRefGoogle ScholarPubMed
Andersson, C, Johnson, AD, Benjamin, EJ, Levy, D, Vasan, RS. 70-year legacy of the Framingham Heart Study. Nat Rev Cardiol. 2019; 16, 687.CrossRefGoogle ScholarPubMed
Hooghiemstra, AM, Bertens, AS, Leeuwis, AE, et al. The missing link in the pathophysiology of vascular cognitive impairment: design of the Heart-Brain Study. Cerebrovasc Dis Extra. 2017; 7, 140–152.CrossRefGoogle ScholarPubMed