Embryonic control of heart rate: Examining developmental patterns and temperature and oxygenation influences using embryonic avian models

Respiratory Physiology and Neurobiology

Volumn 178, Issue 1, 2011, Pages 84-96

  Andrewartha, Sarah J ^a   Tazawa, Hiroshi ^a   Burggren, Warren W ^a  

^a UNIVERSITY OF NORTH TEXAS   (United States)

Author keywords

Avian: chicken, duck, emu; Embryo and hatchlings; Endothermic response; Environmental challenge: hypoxia, hyperoxia and temperature; Heart rate: mean and instantaneous, variability and irregularities; Thermoregulation

Indexed keywords

BLOOD FLOW; CIRCADIAN RHYTHM; COLD EXPOSURE; DECELERATION; DIFFUSION; DUCK; EMBRYO; EMBRYO DEVELOPMENT; EMU; FOWL; HATCHING; HEART RATE; HEART RATE VARIABILITY; HEART STROKE VOLUME; HEAT TOLERANCE; HYPEROXIA; HYPOXIA; INCUBATION TEMPERATURE; NONHUMAN; ONTOGENY; OXYGEN CONSUMPTION; OXYGEN TRANSPORT; OXYGENATION; PARASYMPATHETIC FUNCTION; PRIORITY JOURNAL; REVIEW; STEADY STATE; SURVIVAL; SYMPATHETIC FUNCTION; TEMPERATURE; THERMOREGULATION; WARMING;

ANIMALS; BIRDS; BODY TEMPERATURE REGULATION; CARDIOVASCULAR SYSTEM; HEART RATE; MODELS, BIOLOGICAL; OXYGEN CONSUMPTION;

EID: 79960698992     PISSN: 15699048     EISSN: 18781519     Source Type: Journal    
DOI: 10.1016/j.resp.2011.04.014     Document Type: Review

References (100)

1. Adolph E.F. Responses to hypothermia in several species of infant mammals. Am. J. Physiol. 1951, 166:75-91.
2. Akiyama R., Matsuhisa A., Pearson J.T., Tazawa H. Long-term measurement of heart rate in chicken eggs. Comp. Biochem. Physiol. A 1999, 124:483-490.
3. Akiyama R., Mitsubayashi H., Tazawa H., Burggren W.W. Heart rate responses to altered ambient oxygen in early (days 3-9) chick embryos in the intact egg. J. Comp. Physiol. B 1999, 169:85-92.
4. Akiyama R., Kambara A., Komoro T., Kataoka T., Yoneta H., Moriya K., Tazawa H. Continuous long-term observation of early development of chicken embryos in ovo. New Insights into Fundamental Physiology and Peri-natal Adaptation of Domestic Fowl 2006, 117-124. Nottingham University Press, UK. S. Yahav, B. Tzschentke (Eds.).
5. Altimiras J., Crossley D.A. Control of blood pressure mediated by baroreflex changes of heart rate in the chicken embryo (Gallus gallus). Am. J. Physiol. 2000, 278:R980-R986.
6. Altimiras J., Crossley D.A., Villamor E. Prenatal development of cardiovascular regulation in avian species. Cardio-Respiratory Control in Vertebrates 2009, 397-427. Springer-Verlag, Berlin. M.L. Glass, S.C. Wood (Eds.).
7. Askelrod S., Gordon D., Ubel F.A., Shanon D.C., Barger A.C., Cohen R.J. Power spectrum analysis of heart rate fluctuation: a quantitative probe of beat-to-beat cardiovascular control. Science 1981, 213:220-222.
8. Azzam M.A., Mortola J.P. Organ growth in chicken embryos during hypoxia: implications on organ "sparing" and "catch-up growth" Respir. Physiol. Neurobiol. 2007, 159:155-162.
9. Baarendse P.J.J., Debonne M., Decuypere E., Kemp B., Van Den Brand H. Ontogeny of avian thermoregulation from a neural point of view. World Poult. Sci. J. 2007, 63:267-276.
10. Bartels H., Baumann F. Metabolic rate of early embryos (4-22 somites) at varying oxygen pressure. Respir. Physiol. 1972, 16:1-15.
11. Burggren W., Crossley D.A. Comparative cardiovascular development: improving the conceptual framework. Comp. Biochem. Physiol. A 2002, 132:661-674.
12. Burggren W.W. What is the purpose of the embryonic heart beat? Or how facts can ultimately prevail over physiological dogma. Physiol. Biochem. Zool. 2004, 77:333-345.
13. Burggren W.W., Warburton S.J. Patterns of form and function in developing hearts: contributions from non-mammalian vertebrates. Cardioscience 1994, 5:183-191.
14. Burggren W.W., Warburton S.J., Slivkoff M.D. Interruption of cardiac output does not affect short-term growth and metabolic rate in day 3 and 4 chick embryos. J. Exp. Biol. 2000, 203:3831-3838.
15. Burggren W.W., Khorrami S., Pinder A., Sun T. Body, eye, and chorioallantoic vessel growth are not dependent on cardiac output level in day 3-4 chicken embryos. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 287:R1399-R1406.
16. Carey C. The ecology of avian incubation. Bioscience 1980, 30:819-824.
17. Chan T., Burggren W. Hypoxic incubation creates differential morphological effects during specific developmental critical windows in the embryo of the chicken (Gallus gallus). Respir. Physiol. Neurobiol. 2005, 145:251-263.
18. Chiba Y., Fukuoka S., Niiya A., Akiyama R., Tazawa H. Development of cholinergic chronotropic control in chick (Gallus gallus domesticus) embryos. Comp. Biochem. Physiol. A 2004, 137:65-73.
19. Chiba Y., Yoneta H., Fukuoka S., Akiyama R., Tazawa H. Ontogeny of respiratory sinus arrhythmia in the domestic fowl. Avian Poult. Biol. Rev. 2004, 15:179-187.
20. Crossley D., Burggren W.W., Altimiras J. Cardiovascular regulation during hypoxia in embryos of the domestic chicken Gallus gallus. Am. J. Physiol. 2002, 284:R219-R226.
21. Dzialowski E.M., von Plettenberg D., Elmonoufy N.A., Burggren W.W. Chronic hypoxia alters the physiological and morphological trajectories of developing chicken embryos. Comp. Biochem. Physiol. A 2002, 131:713-724.
22. Dzialowski E.M., Burggren W.W., Komoro T., Tazawa H. Development of endothermic metabolic response in embryos and hatchlings of the emu (Dromaius novaehollandiae). Respir. Physiol. Neurobiol. 2007, 155:286-292.
23. Dunster K.R. Physiologic variability in the perinatal period. Origins, measurement, and applications. Clin. Perinatol. 1999, 26:801-809.
24. Everaert N., De Smit L., Debonne M., Witters A., Kamers B., Decuypere E., Bruggeman V. Changes in acid-base balance and related physiological responses as a result of external hypercapnia during the second half of incubation in the chicken embryo. Poult. Sci. 2008, 87:362-367.
25. Everaert N., Willemsen H., Kamers B., Decuypere E., Bruggeman V. Regulatory capacities of a broiler and layer strain exposed to high CO2 levels during the second half of incubation. Comp. Biochem. Physiol. A 2011, 158:215-220.
26. Ferner K., Mortola J.P. Ventilatory response to hypoxia in chicken hatchlings: a developmental window of sensitivity to embryonic hypoxia. Respir. Physiol. Neurobiol. 2009, 165:49-53.
27. Fukuoka S., Khandoker A.H., Dzialowski E.M., Burggren W.W., Tazawa H. Development of endothermic heart response in emu (Dromaius novaehollandiae) embryos. New Insights into Fundamental Physiology and Peri-natal Adaptation of Domestic Fowl 2006, 29-42. Nottingham University Press, UK. S. Yahav, B. Tzschentke (Eds.).
28. Gui Y., Linask K., Khowsathit P., Huhta J. Doppler echocardiography of normal and abnormal embryonic mouse heart. Pediatr. Res. 1996, 40:633-642.
29. Ho D., Reed W.L., Burggren W.W. Egg yolk environment differentially influences physiological and morphological development of broiler and layer chicken embryos. J. Exp. Biol. 2011, 214:619-628.
30. Hochachka P.W., Somero G.H. Biochemical Adaptation: Mechanism and Process in Physiological Evolution 2002, Oxford University Press, Oxford.
31. Höchel J., Akiyama R., Masuko T., Pearson J.T., Nichelmann M., Tazawa H. Development of heart rate irregularities in chick embryos. Am. J. Physiol. Heart Circ. Physiol. 1998, 275:H527-H533.
32. Höchel J., Mohr E., Nichelmann M., Pirow R., Tazawa H. Development of heart rate rhythmicity in Muscovy duck embryos. Comp. Biochem. Physiol. A 1999, 124:501-509.
33. Hoiby M., Aulie A., Reite O.B. Oxygen uptake in fowl eggs incubated in air and pure oxygen. Comp. Biochem. Physiol. A 1983, 74:315-318.
34. Howe R.S., Burggren W.W., Warburton S.J. Fixed patterns of bradycardia during late embryonic development in domestic fowl with C locus pleiotropic mutations. Am. J. Physiol. 1994, 268:H56-H60.
35. Hulbert A.J. Thyroid hormones and their effects: a new perspective. Biol. Rev. 2000, 5:519-631.
36. Kato K., Moriya K., Dzialowski E., Burggren W.W., Tazawa H. Cardiac rhythms in prenatal and perinatal emu embryos. Comp. Biochem. Physiol. A 2002, 131:775-785.
37. Khandoker A.H., Dzialowski E.M., Burggren W.W., Tazawa H. Cardiac rhythms of late pre-pipped and pipped chick embryos exposed to altered oxygen environments. Comp. Biochem. Physiol. A 2003, 136:289-299.
38. Khandoker A.H., Fukazawa K., Dzialowski E.M., Burggren W.W., Tazawa H. Maturation of the homeothermic response of heart rate to altered ambient temperature in developing chick hatchlings (Gallus gallus domesticus). Am. J. Physiol. Regul. Integr. Comp. Physiol. 2004, 286:R129-R137.
39. Kitney R.I. An analysis of the thermoregulatory influences on heart-rate variability. The Study of Heart Rate Variability 1980, 81-113. Clarendon, Oxford. R.I. Kitney, O. Rompleman (Eds.).
40. Kuroda O., Matsunaga C., Whittow G.C., Tazawa H. Comparative metabolic responses to prolonged cooling in precocial duck (Anas domestica) and altricial pigeon (Columba domestica) embryos. Comp. Biochem. Physiol. A 1990, 95:407-410.
41. Khorrami S., Tazawa H., Burggren W. 'Blood-doping' effects on hematocrit regulation and oxygen consumption in late-state chicken embryos (Gallus gallus). J. Exp. Biol. 2008, 211:883-889.
42. McNabb F.M.A. Avian thyroid development and adaptive plasticity. Gen. Comp. Endocrinol. 2006, 147:93-101.
43. Martin T.E., Auer S.K., Bassar R.D., Niklison A.M., Lloyd P. Geographic variation in avian incubation periods and parental influences on embryonic temperature. Evolution 2007, 61:2558-2569.
44. Menna T.M., Mortola J.P. Ventilatory chemosensitivity in the chick embryo. Respir. Physiol. Neurobiol. 2003, 137:69-79.
45. Miller S.L., Green L.R., Peebles D.M., Hanson M.A., Blanco C.E. Effects of chronic hypoxia and protein malnutrition on growth in the developing chick. Am. J. Obstet. Gynecol. 2002, 186:261-267.
46. Milsom W.K., Burleson M.L. Peripheral arterial chemoreceptors and the evolution of the carotid body. Respir. Physiol. Neurobiol. 2007, 175:4-11.
47. Moriya K., Höchel J., Pearson J.T., Tazawa H. Cardiac rhythms in developing chicks. Comp. Biochem. Physiol. A 1999, 124:461-468.
48. Moriya K., Pearson J.T., Burggren W.W., Ar A., Tazawa H. Continuous measurements of instantaneous heart rate and its fluctuations before and after hatching in chickens. J. Exp. Biol. 2000, 203:895-903.
49. Moriya K., Kato K., Matsumura M., Dzialowski E., Burggren W.W., Tazawa H. Cardiac rhythms in developing emu hatchlings. Comp. Biochem. Physiol. A 2002, 131:787-795.
50. Moriya K., Akiyama R., Dzialowski E.M., Burggren B.B., Tazawa H. Development of heart rate circadian rhythm in chickens. Avian Poult. Biol. Rev. 2004, 15:211-218.
51. Mortola J.P. Influence of temperature on metabolism and breathing during mammalian ontogenesis. Respir. Physiol. Neurobiol. 2005, 149:155-164.
52. Mortola J.P. Gas exchange in avian embryos and hatchlings. Comp. Biochem. Physiol. A 2009, 153:359-377.
53. Mortola J.P., Rezzonico R., Lanthier C. Ventilation and oxygen consumption during acute hypoxia in newborn mammals: a comparative analysis. Respir. Physiol. 1989, 78:31-43.
54. Mortola J.P., Wills K., Trippenbach T., Al Awam K. Interactive effects of temperature and hypoxia on heart rate and oxygen consumption of the 3-day old chicken embryo. Comp. Biochem. Physiol. A 2010, 155:301-308.
55. Ono H., Hou P.-C.L., Tazawa H. Responses of developing chicken embryos to acute changes in ambient temperature: noninvasive study of heart rate. Israel J. Zool. 1994, 40:467-479.
56. Pearson J.T., Tsudzuki M., Nakane Y., Akiyama R., Tazawa H. Development of heart rate in the precocial king quail Coturnix chinensis. J. Exp. Biol. 1998, 201:931-941.
57. Pearson J.T., Tazawa H. Ontogeny of heart rate in embryonic and nestling crows (Corvus corone and Corvus macrorhynchos). J. Comp. Physiol. B 1999, 169:256-262.
58. Pearson J.T., Moriya K., Yoneta M., Tazawa H. Development and regulation of heart rate in embryos and hatchlings of gulls (Larus schistisagus and Larus crassirostris) in relation to growth. J. Comp. Physiol. B 2000, 170:429-438.
59. Pilarski J.Q., Hempleman S.C. Development of avian intrapulmonary chemoreceptor. Respir. Physiol. Neurobiol. 2007, 157:393-402.
60. Phoon C.K.L. Circulatory physiology in the developing embryo. Curr. Opin. Pediatr. 2001, 13:456-464.
61. Raddatz E., Kučera P. Mapping the oxygen consumption in the gastrulating chick embryo. Respir. Physiol. 1983, 51:153-166.
62. Rahn H., Ackerman R.A., Paganelli C.V. Humidity in the avian nest and egg water loss during incubation. Physiol. Zool. 1977, 50:269-283.
63. Reyna, K.S., 2010. Thermal stress during pre-incubation induces subsequent developmental plasticity in Northwestern bobwhites. Ph.D. Dissertation, University of North Texas.
64. Ruck, S.A., 2010. Induced bradycardia effects on angiogenesis, growth, and development in early development in chicken embryos, Gallus domesticus. Master Thesis, University of North Texas.
65. Schifferli P., Caldeyro-Barcia R. Effects of atropine and beta-adrenergic drugs on the heart rate of the human fetus. Fetal Pharmacology 1973, 259-279. Raven Press, New York. L. Boreus (Ed.).
66. Shah R., Greyner H., Dzialowski E.M. Autonomic control of heart rate and its variability during normoxia and hypoxia in emu (Dromaius novaehollandiae) hatchlings. Poult. Sci. 2010, 89:135-144.
67. Silva J.E. The thermogenic effect of thyroid hormone and it's clinical implications. Ann. Int. Med. 2003, 139:205-213.
68. Silva J.E. Thermogenic mechanisms and their hormonal regulation. Physiol. Rev. 2006, 86:438-464.
69. Suzuki H., Sugawara J., Kimura Y., Murakami T., Okamura K. Contribution of the fetal baroreceptor reflex to the low frequency component of fetal heart rate fluctuations. Gynecol. Obstet. Invest. 2003, 55:156-161.
70. Szdzuy K., Mortola J.P. Ventilatory chemosensitivity and thermogenesis of the chicken hatchling after embryonic hypercapnia. Respir. Physiol. Neurobiol. 2008, 162:55-62.
71. Tamura A., Akiyama R., Chiba Y., Moriya K., Dzialowski E.M., Burggren W.W., Tazawa H. Heart rate responses to cooling in emu hatchlings. Comp. Biochem. Physiol. A 2003, 134:829-838.
72. Tazawa H. Effect of O2 and CO2 in N2, He, and SF6 on chick embryo blood pressure and heart rate. J. Appl. Physiol.: Respir. Environ. Exerc. Physiol. 1981, 51:1017-1022.
73. Tazawa H., Nakagawa S. Response of egg temperature, heart rate and blood pressure in the chick embryo to hypothermal stress. J. Comp. Physiol. B 1985, 155:195-200.
74. Tazawa H., Lomholt J.P., Johansen K. Direct measurement of allantoic blood flow in the chicken, Gallus domesticus. Responses to alteration in ambient temperature and PO2. Comp. Biochem. Physiol. A 1985, 81:641-642.
75. Tazawa H., Rahn H. Tolerance of chick embryos to low temperatures in reference to the heart rate. Comp. Biochem. Physiol. A 1986, 85:531-534.
76. Tazawa H., Rahn H. Temperature and metabolism of chick embryos and hatchlings after prolonged cooling. J. Exp. Zool. Suppl. 1987, 1:105-109.
77. Tazawa H., Wakayama H., Turner J.S., Paganelli C.V. Metabolic compensation for gradual cooling in developing chick embryos. Comp. Biochem. Physiol. A 1988, 89:125-129.
78. Tazawa H., Suzuki Y., Musashi H. Simultaneous acquisition of ECG, BCG, and blood pressure from chick embryos in the egg. J. Appl. Physiol. 1989, 67:478-483.
79. Tazawa H., Hashimoto Y., Nakazawa S., Whittows G.C. Metabolic responses of chicken embryos and hatchlings to altered O2 environments. Respir. Physiol. 1992, 88:37-50.
80. Tazawa H., Yamaguchi M., Yamada M., Doi K. Embryonic heart rate of the domestic fowl (Gallus domesticus) in a quasiequilibrium state of altered ambient temperatures. Comp. Biochem. Physiol. A 1992, 101:103-108.
81. Tazawa H., Hou P.-C.L. Avian cardiovascular development. Development of Cardiovascular Systems: Molecules to Organisms 1997, 193-210. Cambridge University Press, Cambridge. W.W. Burggren, B. Keller (Eds.).
82. Tazawa H., Ar A., Pearson J.T., Moriya K., Geffen E. Heart rate in developing ostrich embryos. Br. Poult. Sci. 1998, 39:161-166.
83. Tazawa H., Mitsubayashi H., Hirata M., Höchel J., Pearson J.T. Cardiac rhythms in chick embryos during hatching. Comp. Biochem. Physiol. A 1999, 124:511-521.
84. Tazawa H., Pearson J.T., Komoro T., Ar A. Allometric relationship between embryonic heart rate and fresh egg mass in birds. J. Exp. Biol. 2001, 204:165-174.
85. Tazawa H., Moriya K., Tamura A., Komoro T., Akiyama R. Ontogenic study of thermoregulation in birds. J. Therm. Biol. 2001, 26:281-286.
86. Tazawa H., Moriya K., Tamura A., Akiyama R. Low-frequency oscillation of instantaneous heart rate in newly hatched chicks. Comp. Biochem. Physiol. A 2002, 131:797-803.
87. Tazawa H., Akiyama R., Moriya K. Development of cardiac rhythms in birds. Comp. Biochem. Physiol. A 2002, 132:675-689.
88. Tazawa H. Embryonic cardiovascular variables during incubation. World Poult. Sci. J. 2004, 60:479-489.
89. Tazawa H., Chiba Y., Khandoker A.H., Dzialowski E.M., Burggren W.W. Early development of thermoregulatory competence in chickens: responses of heart rate and oxygen uptake to altered ambient temperatures. Avian Poult. Biol. Rev. 2004, 15:166-176.
90. Tazawa H. Cardiac rhythms in avian embryos and hatchlings. Avian Poult. Biol. Rev. 2005, 16:123-150.
91. Territo P., Burggren W.W. Cardio-respiratory ontogeny during chronic carbon monoxide induced hypoxemia in the clawed frog Xenopus laevis. J. Exp. Biol. 1998, 201:1461-1472.
92. Van Golde J., Mulder T., Blanco C.E. Changes in mean chorioallatoic artery blood flow and heart rate produced by hypoxia in the developing chick embryo. Pediatr. Res. 1997, 42:293-298.
93. Villamor E., Kessels C.G.A., Ruijtenbeek K., van Suylen R.J., Belik J., De Mey J.G.R., Blanco C.E. Chronic in ovo hypoxia decreases pulmonary arterial contractile reactivity and induces biventricular cardiac enlargement in the chicken embryo. Am. J. Physiol.: Regul. Integr. Comp. Physiol. 2004, 287:R642-R651.
94. Webb D.R. Thermal tolerance of avian embryos: a review. Condor 1987, 89:874-898.
95. Whittow G.C., Tazawa H. The early development of thermoregulation in birds. Physiol. Zool. 1991, 64:1371-1390.
96. Wispé J., Hu N., Clark E.B. Effect of environmental hypothermia on dorsal aortic blood flow in the chick embryo, stages 18-24. Pediatr. Res. 1983, 17:945-948.
97. Yoneta H., Akiyama R., Nakata W., Moriya K., Tazawa H. Video analysis of body movements and their relation to the heart rate fluctuations in chicken hatchlings. New Insights into Fundamental Physiology and Peri-natal Adaptation of Domestic Fowl 2006, 57-68. Nottingham University Press, UK. S. Yahav, B. Tzschentke (Eds.).
98. Yoneta H., Fukazawa K., Dzialowski E.M., Burggren W.W., Tazawa H. Does sequence of exposure to altered ambient temperatures affect the endothermic heart rate response of newly hatched chicks?. New Insights into Fundamental Physiology and Peri-natal Adaptation of Domestic Fowl 2006, 15-28. Nottingham University Press, UK. S. Yahav, B. Tzschentke (Eds.).
99. Yoneta H., Fukuoka S., Akiyama R., Tazawa H. Early development of cholinergic heart rate control in embryos of broiler and White Leghorn chickens. New Insights into Fundamental Physiology and Peri-natal Adaptation of Domestic Fowl 2006, 1-14. Nottingham University Press, UK. S. Yahav, B. Tzschentke (Eds.).
100. Yoneta H., Dzialowski E.M., Burggren W.W., Tazawa H. Endothermic heart rate response in broiler and White Leghorn chicks (Gallus gallus domesticus) during the first two days of post-hatch life. Comp. Biochem. Physiol. A 2007, 147:529-535.