Human fetal hearts with tetralogy of Fallot have altered fluid dynamics and forces

Wiputra, Hadi; Chen, Ching Kit; Talbi, Elias; Lim, Guat Ling; Soomar, Sanah Merchant; Biswas, Arijit; Mattar, Citra Nurfarah Zaini; Bark, David; Leo, Hwa Liang; Yap, Choon Hwai

doi:10.1152/ajpheart.00235.2018

Cited by 24 publications

(28 citation statements)

References 36 publications

(44 reference statements)

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“…Accurate estimations of cardiac motion from clinical scans is an important task, and can be used to aid the evaluation of cardiac function 1 , detection of dysfunction in cases such as cardiomyopathy 2 , chemotherapy toxicity 3 and infraction 4 . It has also been used to assist with bio-mechanic studies to understand cardiac physiology based on its experience stress and strain 5 , 6 .…”

Section: Introductionmentioning

confidence: 99%

Cardiac motion estimation from medical images: a regularisation framework applied on pairwise image registration displacement fields

Wiputra

Chan

Foo

et al. 2020

Sci Rep

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Accurate cardiac motion estimation from medical images such as ultrasound is important for clinical evaluation. We present a novel regularisation layer for cardiac motion estimation that will be applied after image registration and demonstrate its effectiveness. The regularisation utilises a spatio-temporal model of motion, b-splines of Fourier, to fit to displacement fields from pairwise image registration. In the process, it enforces spatial and temporal smoothness and consistency, cyclic nature of cardiac motion, and better adherence to the stroke volume of the heart. Flexibility is further given for inclusion of any set of registration displacement fields. The approach gave high accuracy. When applied to human adult Ultrasound data from a Cardiac Motion Analysis Challenge (CMAC), the proposed method is found to have 10% lower tracking error over CMAC participants. Satisfactory cardiac motion estimation is also demonstrated on other data sets, including human fetal echocardiography, chick embryonic heart ultrasound images, and zebrafish embryonic microscope images, with the average Dice coefficient between estimation motion and manual segmentation at 0.82–0.87. The approach of performing regularisation as an add-on layer after the completion of image registration is thus a viable option for cardiac motion estimation that can still have good accuracy. Since motion estimation algorithms are complex, dividing up regularisation and registration can simplify the process and provide flexibility. Further, owing to a large variety of existing registration algorithms, such an approach that is usable on any algorithm may be useful.

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Section: Introductionmentioning

confidence: 99%

Cardiac motion estimation from medical images: a regularisation framework applied on pairwise image registration displacement fields

Wiputra

Chan

Foo

et al. 2020

Sci Rep

Self Cite

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“…The heart trabeculae is characterized as a ‘spongy’ or porous tissue that develops inside the heart ventricles, and in our samples was evident from semithin transverse heart sections ( Figure 4 ), but could also be approximately quantified as the extracellular portion of the images ( Figure 8 ). It has been shown that the heart trabecular architecture is sensitive to blood flow conditions during development ( Sedmera et al, 1999 ), and thus a disrupted trabecular architecture may be a characteristic of many CHD hearts due to their anomalous flow characteristics during fetal stages ( Wiputra et al, 2018 ). However, the trabecular and myocardial architecture can also exhibit variations from heart to heart ( Gilbert et al, 2007 ), therefore further analysis with a larger sample size is required before we can make conclusions related to TOF.…”

Section: Discussionmentioning

confidence: 99%

“…These hearts were collected at stages corresponding to about 5–6 months of human fetal development, when the heart is already formed but maturing in preparation for birth/hatching. We imaged: (1) a control heart with no structural defects and (2) a heart with tetralogy of Fallot (TOF), a combination of structural heart malformations found in humans ( Bailliard and Anderson, 2009 ; Wiputra et al, 2018 ). Our results show the morphology and ultrastructure of these two hearts, and emphasize the need for a multiscale approach to deepen our understanding of CHD and enable the development of effective strategies to combat heart failure in CHD.…”

Section: Introductionmentioning

confidence: 99%

Multiscale cardiac imaging spanning the whole heart and its internal cellular architecture in a small animal model

Rykiel

López

Riesterer

et al. 2020

eLife

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Cardiac pumping depends on the morphological structure of the heart, but also on its sub-cellular (ultrastructural) architecture, which enables cardiac contraction. In cases of congenital heart defects, localized ultrastructural disruptions that increase the risk of heart failure are only starting to be discovered. This is in part due to a lack of technologies that can image the three dimensional (3D) heart structure, to assess malformations; and its ultrastructure, to assess organelle disruptions. We present here a multiscale, correlative imaging procedure that achieves high-resolution images of the whole heart, using 3D micro-computed tomography (micro-CT); and its ultrastructure, using 3D scanning electron microscopy (SEM). In a small animal model (chicken embryo), we achieved uniform fixation and staining of the whole heart, without losing ultrastructural preservation on the same sample, enabling correlative multiscale imaging. Our approach enables multiscale studies in models of congenital heart disease and beyond.

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“…The heart trabeculae is characterized as a “spongy” or porous tissue that develops inside the heart ventricles, and in our samples was evident from semithin transverse heart sections ( Figure 4 ), but could also be approximately quantified as the extracellular portion of the images ( Figure 7 ). It has been shown that the heart trabecular architecture is sensitive to blood flow conditions during development 54 , and thus a disrupted trabecular architecture may be a characteristic of TOF hearts due to their anomalous flow characteristics during fetal stages 18 . However, the trabecular and myocardial architecture can also exhibit variations from heart to heart 11 , therefore further analysis with a larger sample size is required before we can make conclusions related to TOF.…”

Section: Discussionmentioning

confidence: 99%

“…These hearts were collected at stages corresponding to about 5-6 months of human fetal development, when the heart is already formed but maturing in preparation for birth/hatching. We imaged: 1) a control heart with no structural defects; and 2) a heart with tetralogy of Fallot (TOF), a combination of structural heart malformations found in humans 17,18 . Our results suggest differences in the ultrastructure of these two hearts, emphasizing the need for a multiscale approach to deepen our understanding of CHD and enable the development of effective strategies to combat heart failure in CHD.…”

Section: Introductionmentioning

confidence: 99%

Multiscale cardiac imaging to capture the whole heart and its internal cellular architecture, with applications to congenital heart disease

Rykiel

López

McQuiston

et al. 2020

Preprint

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9Efficient cardiac pumping depends on the morphological structure of the heart, but also on its 10 sub-cellular (ultrastructural) architecture, which enables cardiac contraction. In cases of 11 congenital heart defects, localized sub-cellular disruptions in architecture that increase the risk 12 of heart failure are only starting to be discovered. This is in part due to a lack of technologies 13 that can image the three dimensional (3D) heart structure, assessing malformations; and its 14 ultrastructure, assessing disruptions. We present here a multiscale, correlative imaging 15 procedure that achieves high-resolution images of the whole heart, using 3D micro-computed 16 tomography (micro-CT); and its ultrastructure, using 3D scanning electron microscopy (SEM). 17This combination of technologies has not been possible before in imaging the same cardiac 18 sample due to the heart large size, even when studying small fetal and neonatal animal models 19 (~5x5x5mm 3 ). Here, we achieved uniform fixation and staining of the whole heart, without losing 20 ultrastructural preservation (at the nm resolution range). Our approach enables multiscale 21 studies of cardiac architecture in models of congenital heart disease and beyond. 22 23 51 whole heart morphology and its sub-cellular organization (ultrastructural architecture). Our 52 multiscale procedure uses micro computed tomography (micro-CT) imaging to capture heart 53 morphology at micrometer resolution, and scanning electron microscopy (SEM) to capture 54 cardiac tissue ultrastructure at nanometer resolution. Current SEM technologies allow for three-55 dimensional (3D) imaging of sub-cellular architecture, enabling reconstruction and quantification 56 of ultrastructural features within a tissue volume 14-16 . Among 3D SEM methods, we have 57 selected serial block-face SEM (SBF-SEM) for ultrastructural imaging, as it allows 3D imaging of 58 relatively large volumes (sample size 40x60x40 µm 3 ). The methodology we present herein 59 improves upon previous protocols by achieving uniform staining of a relatively large heart 60 sample (3-4 mm wide, 5-6 mm long), circumventing micro-CT x-ray penetration issues, and 61 allowing sample screening and selection prior to full sample preparation. Our multiscale imaging, 62 further, enables mapping of structural and ultrastructural heart features. 63 129 thickening and enlargement of the RV wall. RV hypertrophy in TOF, however, develops over 130 time as the stenosis of the pulmonary artery increases pressure in the RV after birth 17 and was 131 not present in the heart examined in this study (see Figure 3 for a comparison of the selected 132 normal and TOF hearts). The TOF heart analyzed here featured supravalvular pulmonary 133 stenosis, a ventricular septal defect, and an overriding aorta. The right ventricle was enlarged 134and thin-walled compared to the control heart (Figure 3). Further, the TOF heart was missing 135 the right branch of the pulmonary artery. In humans, this rare condition, called unilateral 136

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Human fetal hearts with tetralogy of Fallot have altered fluid dynamics and forces

Cited by 24 publications

References 36 publications

Cardiac motion estimation from medical images: a regularisation framework applied on pairwise image registration displacement fields

Cardiac motion estimation from medical images: a regularisation framework applied on pairwise image registration displacement fields

Multiscale cardiac imaging spanning the whole heart and its internal cellular architecture in a small animal model

Multiscale cardiac imaging to capture the whole heart and its internal cellular architecture, with applications to congenital heart disease

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