Respiratory and cardiovascular responses to acute hypoxia and hyperoxia in
internally pipped chicken embryos
☆
Stephanie Sbong, Edward M. Dzialowski
⁎
Department of Biological Sciences, University of North Texas, P.O. Box 305220, Denton, TX 76203, USA
Received 31 January 2007; received in revised form 9 March 2007; accepted 10 March 2007
Available online 16 March 2007
Abstract
During the first day of hatching, the developing chicken embryo internally pips the air cell and relies on both the lungs and chorioallantoic
membrane (CAM) for gas exchange. Our objective in this study was to examine respiratory and cardiovascular responses to acute changes in
oxygen at the air cell or the rest of the egg during internal pipping. We measured lung (V
·
O
2
lung
) and CAM (V
·
O
2
CAM
) oxygen consumption
independently before and after 60 min exposure to combinations of hypoxia, hyperoxia, and normoxia to the air cell and the remaining egg.
Significant changes in V
·
O
2
total
were only observed with combined egg and air cell hypoxia (decreased V
·
O
2
total
) or egg hyperoxia and air cell
hypoxia (increased V
·
O
2
total
). In response to the different O
2
treatments, a change in V
·
O
2
lung
was compensated by an inverse change in V
·
O
2
CAM
of
similar magnitude. To test for the underlying mechanism, we focused on ventilation and cardiovascular responses during hypoxic and hyperoxic
air cell exposure. Ventilation frequency and minute ventilation (V
E
) were unaffected by changes in air cell O
2
, but tidal volume (V
T
) increased
during hypoxia. Both V
T
and V
E
decreased significantly in response to decreased P
CO
2
. The right-to-left shunt of blood away from the lungs
increased significantly during hypoxic air cell exposure and decreased significantly during hyperoxic exposure. These results demonstrate the
internally pipped embryo's ability to control the site of gas exchange by means of altering blood flow between the lungs and CAM.
© 2007 Elsevier Inc. All rights reserved.
Keywords: Chicken; Egg; Oxygen consumption; Hypoxia; Hyperoxia; Chorioallantoic membrane; Lungs; Ductus arteriosus
1. Introduction
The chicken embryo utilizes two modes of gas exchange
prior to hatching. During the prenatal period, the transfer of
oxygen and carbon dioxide occurs at the chorioallantoic
membrane (CAM). On day 19 of incubation, the embryo
internally pips by piercing the air cell inner membrane with its
beak and begins lung ventilation on air cell gas. This air cell gas
is both hypoxic and hypercapnic (Visschedijk, 1968b; Wan-
gensteen and Rahn, 1970/71). During internal pipping, oxygen
uptake at the lungs (V
·
O
2
lung
) accounts for between 27 and 39%
of the total oxygen uptake of the egg (V
·
O
2
total
; Visschedijk,
1968a; Menna and Mortola, 2002). Up to 12 hours after internal
pipping, the embryo breaks the eggshell with its beak during
external pipping and the contribution of the lungs to V
·
O
2
total
increases to 77% (Menna and Mortola, 2002). Upon hatching,
all oxygen uptake occurs by lung ventilation (Rahn et al., 1985;
Visschedijk, 1968a).
Associated with the switch in the site of gas exchange during
hatching is a shift in the pattern of blood flow. Prior to internal
pipping, the embryo has interatrial foramina and two patent
ductus arteriosi that allow for a right-to-left shunt of blood flow
away from the non-ventilating lungs and towards the CAM and
systemic tissues (White, 1974; Tazawa and Takenaka 1985;
Rahn et al., 1985). With the initiation of internal pipping, right
atrial and ventricle output flowing to the lungs increases and
output flowing to the systemic tissues and CAM decreases. At
this point, approximately 40% of the right atrial outflow passes
through the pulmonary arteries to the lungs while 60% bypasses
the lungs through the ductus arteriosi and interatrial foramina
(Rahn et al., 1985). As hatching progresses, blood flow through
the ductus arteriosi decreases such that during external pipping
Available online at www.sciencedirect.com
Comparative Biochemistry and Physiology, Part A 148 (2007) 761 – 768
www.elsevier.com/locate/cbpa
☆
First presented in the symposium on Developmental Transitions in
Respiratory Physiology at the first International Congress of Respiratory
Biology in Bad Honnef, Germany, August 2006.
⁎
Corresponding author. Tel.: +1 940 565 3631; fax: +1 940 565 3821.
E-mail address: edzial@unt.edu (E.M. Dzialowski).
1095-6433/$ - see front matter © 2007 Elsevier Inc. All rights reserved.
doi:10.1016/j.cbpa.2007.03.013