Body, eye, and chorioallantoic vessel growth are not dependent on cardiac output level in day 3–4 chicken embryos

Abstract

Normal aerobic metabolic rates persist in the early chicken embryo after elimination of cardiac output, but the dependence of tissue growth and differentiation on blood flow is unknown in these early stages. We partially ligated (25-50% occlusion) the ventricular outflow tract of Hamburger-Hamilton stage (HH) 16-18 embryos, producing a wide range of cardiac output. For the next approximately 48 h (to HH 24), we measured heart rate (HR), stroke volume (SV), and cardiac output (CO), as well as these growth indicators: eye diameter, chorioallantoic vessel density, and body mass. Acutely, HR declined with partial ligation (from 108 to 98 beats/min). Paradoxically, SV and CO decreased sharply in most embryos but increased in others, collectively producing the desired large variation (up to 25-fold) in CO and permitting assessment of tissue growth over a very large range of blood perfusion. Eye diameter doubled (from 0.6 to 1.2 mm) with development from HH 16 to HH 24, but within a developmental cohort there was no significant correlation between eye diameter and CO over a 25-fold range of CO. Similarly, chorioallantoic membrane vessel index was independent of CO over the CO range at all stages. Finally, body mass increase during development was not significantly affected by partial conal truncal ligation. Collectively, these data suggest that normal eye and vessel growth and body mass accumulation occur independent of their rate of blood perfusion, supporting the hypothesis of prosynchronotropy-that the heart begins to beat and generate blood flow in advance of the actual need for convective blood flow to tissues.

Reduced Heart Rate and Cardiac Output Differentially Affect Angiogenesis, Growth, and Development in Early Chicken Embryos (Gallus domesticus)

“…11). Thus, experimentally reduced CO slowed absolute growth (measured by reduced body mass) but not development per se, as measured by eye diameter and cervical flexure, aligning with earlier experimental findings of Burggren et al (2004).…”

“…A complicating factor is that blood pressure and flow are not an absolute requirement for organogenesis and growth in the early vertebrate embryo, because development in early embryos will continue for some time when convective blood flow and mass transport are experimentally eliminated (Mellish et al 1994;Pelster and Burggren 1996;Burggren et al 2000Burggren et al , 2004. This independence of development and growth from convective blood flow occurs because diffusion provides adequate mass transport during early embryo development.…”

Egg yolk environment differentially influences physiological and morphological development of broiler and layer chicken embryos

“…Interestingly, the phenotypic differences between the two chicken breeds arise as early as the first few days of embryonic development (Clum et al, 1995;Burggren et al, 2004;Boerjan, 2004), potentially setting the stage for the breed-specific differences observed in latestage embryonic (Sato et al, 2006;Everaert et al, 2008), juvenile (Martinez-Lemus et al, 1999;Latimer and Brisbin, 1987;Odom et al, 2004) and adult (Martinez-Lemus et al, 1998;Koenen et al, 2002;Schreurs et al, 1995;McRae et al, 2006) phenotypes. Broiler embryos have faster overall development rates than layer embryos, which is first evident at 48h of development (Boerjan, 2004;Everaert et al, 2008).…”

Role of Hypoxia in the Evolution and Development of the Cardiovascular System

“…1, much as in its simple, avascular primitive ancestors. However, as the embryo rapidly grows, its O 2 demand outstrips diffusional oxygen delivery, and the internal circulation (which has already begun to form and propel blood) takes on an increasingly important function in convective gas transport (13,15). In mammals, concurrent with the elaboration of the embryonic circulation, the placenta forms as a necessary interface for gas and nutrient exchange with the maternal circulation.…”

“…Of note, in very early stages of development, the dependence on diffusion for a supply of O 2 appears not to be a limitation to continuing growth and development. Chicken embryo development (and development of other vertebrates) can proceed normally in the complete absence of blood convection until eventually the embryonic metabolic rate outstrips diffusional mechanisms for oxygen and nutrient supply (13,18). At the later stages of development (HH 25-32), reduction of ambient O 2 concentrations to 5-7.5% (from 21%) results in demise of the embryo because of circulatory arrest within hours (96,97).…”