Comparative physiology of the ductus arteriosus among vertebrates

Dzialowski, Edward M.

doi:10.1053/j.semperi.2018.05.002

Cited by 18 publications

(15 citation statements)

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“…A) arises via the foramen ovale, a small opening between the left and right atria that permits a bypass of the non‐functional lungs (R–L shunt) until closure of the foramen ovale at birth (see Section II.2 a ). Extracardiac vascular shunting in mammals occurs via the ductus arteriosus (ductus Botalli) that connects the main pulmonary artery to the proximal descending aorta (Dzialowski, ; Reese, ). The ductus arteriosus, like the intracardiac foramen ovale, provides a R–L shunt for bypass of the fetal lungs.…”

Section: Cardiovascular Shunts In Ectothermic Vertebrates: Theories mentioning

confidence: 99%

“…Numerous extravascular shunts, both L-R and R-L, occur as congenital defects in humans (Martinez-Jimenez et al, 2010). For example, the ductus arteriosus is a blood vessel connecting the base of the pulmonary artery to the proximal descending aorta in birds and mammals that provides a foetal R-L shunt, presumably conserving cardiac energy by reducing blood perfusion of the non-functional developing lungs (Bergwerff, DeRuiter, & Gittenberger-de Groot, 1999;Dzialowski, 2018). A patent ductus arteriosus occurs when the ductus arteriosus fails to close (Giroud & Jacobs, 2007;Anilkumar, 2013).…”

Section: (B) Extracardiac Shuntsmentioning

confidence: 99%

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Cardiovascular shunting in vertebrates: a practical integration of competing hypotheses

2019

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This review explores the long‐standing question: ‘Why do cardiovascular shunts occur?’ An historical perspective is provided on previous research into cardiac shunts in vertebrates that continues to shape current views. Cardiac shunts and when they occur is then described for vertebrates. Nearly 20 different functional reasons have been proposed as specific causes of shunts, ranging from energy conservation to improved gas exchange, and including a plethora of functions related to thermoregulation, digestion and haemodynamics. It has even been suggested that shunts are merely an evolutionary or developmental relic. Having considered the various hypotheses involving cardiovascular shunting in vertebrates, this review then takes a non‐traditional approach. Rather than attempting to identify the single ‘correct’ reason for the occurrence of shunts, we advance a more holistic, integrative approach that embraces multiple, non‐exclusive suites of proposed causes for shunts, and indicates how these varied functions might at least co‐exist, if not actually support each other as shunts serve multiple, concurrent physiological functions. It is argued that deposing the ‘monolithic’ view of shunting leads to a more nuanced view of vertebrate cardiovascular systems. This review concludes by suggesting new paradigms for testing the function(s) of shunts, including experimentally placing organ systems into conflict in terms of their perfusion needs, reducing sources of variation in physiological experiments, measuring possible compensatory responses to shunt ablation, moving experiments from the laboratory to the field, and using cladistics‐related approaches in the choice of experimental animals.

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Section: Cardiovascular Shunts In Ectothermic Vertebrates: Theories mentioning

confidence: 99%

Section: (B) Extracardiac Shuntsmentioning

confidence: 99%

Cardiovascular shunting in vertebrates: a practical integration of competing hypotheses

2019

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“…For example, it was noted from our analysis that the RV of the TOF heart exhibited a larger volume and thinner ventricular walls than that of the control (CON) heart examined here (see Figure 3 ). During fetal life, the lungs are not functional, and blood to the lungs is shunted to the systemic circulation through the ductus arteriosus 48 (a pair of ducti in chick 49 ). The RV hypertrophy characteristic of TOF, develops over time after the baby is born 50 .…”

Section: Discussionmentioning

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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“…In mammals this is accomplished by the ductus arteriosus, which connects the pulmonary arteries to the aorta. In avians, in contrast, there are instead two ductus arteriosi, the left ductus arteriosus and the right ductus arteriosus [210]. Both circulations, in addition, have a right to left atrial shunt, the foramen ovale.…”

Section: The Fully Formed Heartmentioning

confidence: 99%

“…Both circulations, in addition, have a right to left atrial shunt, the foramen ovale. When lung oxygenation is established right after birth or hatching, increased oxygen leads to the closure of these right-left shunts [210].…”

Section: The Fully Formed Heartmentioning

confidence: 99%

Follow Me! A Tale of Avian Heart Development with Comparisons to Mammal Heart Development

Lansford

Rugonyi

2020

JCDD

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Avian embryos have been used for centuries to study development due to the ease of access. Because the embryos are sheltered inside the eggshell, a small window in the shell is ideal for visualizing the embryos and performing different interventions. The window can then be covered, and the embryo returned to the incubator for the desired amount of time, and observed during further development. Up to about 4 days of chicken development (out of 21 days of incubation), when the egg is opened the embryo is on top of the yolk, and its heart is on top of its body. This allows easy imaging of heart formation and heart development using non-invasive techniques, including regular optical microscopy. After day 4, the embryo starts sinking into the yolk, but still imaging technologies, such as ultrasound, can tomographically image the embryo and its heart in vivo. Importantly, because like the human heart the avian heart develops into a four-chambered heart with valves, heart malformations and pathologies that human babies suffer can be replicated in avian embryos, allowing a unique developmental window into human congenital heart disease. Here, we review avian heart formation and provide comparisons to the mammalian heart. J. Cardiovasc. Dev. Dis. 2020, 7, 8 3 of 26 Avian ModelsStudies on avian embryos date back to Aristotle, and even further back, to the Egyptians. Historically, the avian model has played an important role in establishing the foundations in circulation research. Chicken eggs were easy to obtain and could be incubated in ovens [17] to observe different periods of embryo development [18]. William Harvey, for example, used chicken eggs to watch the development of the heart and blood, and was the first to notice the directional flow of blood from the heart into the brain and body during systemic circulation [19]. The existence of capillaries that connected the veins and arteries was confirmed with the aid of a simple microscope by Marcello Malpighi, who also discovered that the heart began to beat before blood started to form [20,21].Avian models have unique characteristics that make them invaluable for embryonic developmental studies and, in particular, heart development research. First of all, like mammals, chickens and quails are amniotes, animals whose embryos develop within an amnion and chorion, and developmental processes are highly conserved among amniotes [22]. Specifically, the development of the avian heart is similar to that of the human heart [23]. The mature avian heart consists of four chambers with valves as well as inflow and outflow connections (veins and arteries, respectively), and despite some differences, it resembles the human heart [24][25][26][27]. Importantly, cardiac defects found in humans can be recapitulated in avian embryos [26][27][28][29]. Second, like humans, avian embryos remain relatively flat from early to late gastrulation stages [30], enabling time-lapse observation of both dorsal and ventral tissues by means of whole-mount ex ovo culture techniques [31,32]. Pioneering w...

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Comparative physiology of the ductus arteriosus among vertebrates

Cited by 18 publications

References 59 publications

Cardiovascular shunting in vertebrates: a practical integration of competing hypotheses

Cardiovascular shunting in vertebrates: a practical integration of competing hypotheses

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

Follow Me! A Tale of Avian Heart Development with Comparisons to Mammal Heart Development

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