Hostname: page-component-cd9895bd7-dzt6s Total loading time: 0 Render date: 2024-12-25T19:37:01.417Z Has data issue: false hasContentIssue false
  • English
  • Français

Cardiac and vascular disease prior to hatching in chick embryos incubated at high altitude

Published online by Cambridge University Press:  01 October 2009

C. E. Salinas ,
C. E. Blanco ,
M. Villena ,
E. J. Camm ,
J. D. Tuckett ,
R. A. Weerakkody ,
A. D. Kane ,
A. M. Shelley ,
F. B. P. Wooding  and
M. Quy
...Show all authors
C. E. Salinas
Affiliation:
Instituto Boliviano de Biología de Altura, Facultad de Medicina, Universidad Mayor de San Andrés, La Paz, Bolivia
C. E. Blanco
Affiliation:
Department of Pediatrics, Maastricht University, Maastricht, The Netherlands
M. Villena
Affiliation:
Instituto Boliviano de Biología de Altura, Facultad de Medicina, Universidad Mayor de San Andrés, La Paz, Bolivia
E. J. Camm
Affiliation:
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK
J. D. Tuckett
Affiliation:
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK
R. A. Weerakkody
Affiliation:
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK
A. D. Kane
Affiliation:
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK
A. M. Shelley
Affiliation:
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK
F. B. P. Wooding
Affiliation:
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK
M. Quy
Affiliation:
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK
D. A. Giussani*
Affiliation:
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK
*
Address for Correspondence: Dr D. A. Giussani, Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, CB2 3EG, UK. (Email dag26@cam.ac.uk)
Get access Rights & Permissions [Opens in a new window]

Abstract

The partial contributions of reductions in fetal nutrition and oxygenation to slow fetal growth and a developmental origin of cardiovascular disease remain unclear. By combining high altitude with the chick embryo model, we have previously isolated the direct effects of high-altitude hypoxia on growth. This study isolated the direct effects of high-altitude hypoxia on cardiovascular development. Fertilized eggs from sea-level or high-altitude hens were incubated at sea level or high altitude. Fertilized eggs from sea-level hens were also incubated at high altitude with oxygen supplementation. High altitude promoted embryonic growth restriction, cardiomegaly and aortic wall thickening, effects which could be prevented by incubating eggs from high-altitude hens at sea level or by incubating eggs from sea-level hens at high altitude with oxygen supplementation. Embryos from high-altitude hens showed reduced effects of altitude incubation on growth restriction but not on cardiovascular remodeling. The data show that: (1) high-altitude hypoxia promotes embryonic cardiac and vascular disease already evident prior to hatching and that this is associated with growth restriction; (2) the effects can be prevented by increased oxygenation; and (3) the effects are different in embryos from sea-level or high-altitude hens.

Keywords

cardiovascular diseasechick embryohigh altitudehypoxia.
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 1 , Issue 1 , February 2010 , pp. 60 - 66
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2009

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

1.Huxley, RR, Shiell, AW, Law, CM. The role of size at birth and postnatal catch-up growth in determining systolic blood pressure: a systematic review of the literature. J Hypertens. 2000; 18, 815–831.CrossRefGoogle ScholarPubMed
2.Lenfant, C. Low birth weight and blood pressure. Metab Clin Exp. 2008; 57, S32–S35.CrossRefGoogle ScholarPubMed
3.Godfrey, KM, Barker, DJ. Fetal programming and adult health. Public Health Nutr. 2001; 4, 611–624.CrossRefGoogle ScholarPubMed
4.Gluckman, PD, Hanson, MA, Cooper, C, Thornburg, KL. Effect of in utero and early-life conditions on adult health and disease. N Engl J Med. 2008; 359, 61–73.CrossRefGoogle ScholarPubMed
5.McMillen, IC, Robinson, JS. Developmental origins of the metabolic syndrome: prediction, plasticity, and programming. Physiol Rev. 2005; 85, 571–633.CrossRefGoogle ScholarPubMed
6.Armitage, JA, Taylor, PD, Poston, L. Experimental models of developmental programming: consequences of exposure to an energy rich diet during development. J Physiol. 2005; 565 (Pt 1), 3–8.CrossRefGoogle Scholar
7.Langley-Evans, SC, Bellinger, L, McMullen, S. Animal models of programming: early life influences on appetite and feeding behaviour. Matern Child Nutr. 2005; 1, 142–148.CrossRefGoogle ScholarPubMed
8.Zhang, L. Prenatal hypoxia and cardiac programming. J Soc Gynecol Investig. 2005; 12, 2–13.CrossRefGoogle ScholarPubMed
9.Fowden, AL, Giussani, DA, Forhead, AJ. Intrauterine programming of physiological systems: causes and consequences. Physiology (Bethesda). 2006; 21, 29–37.Google ScholarPubMed
10.Morrison, JL. Sheep models of intrauterine growth restriction: fetal adaptations and consequences. Clin Exp Pharmacol Physiol. 2008; 35, 730–743.CrossRefGoogle ScholarPubMed
11.Moore, LG. Maternal O2 transport and fetal growth in Colorado, Peru and Tibet high-altitude residents. Am J Hum Biol. 1990; 2, 627–637.CrossRefGoogle ScholarPubMed
12.Lichty, JA, Ting, RY, Bruns, P, Dyer, E. Studies of babies born at high altitude. 1. Relation of altitude to birth weight. Am J Dis Child. 1957; 93, 666–669.CrossRefGoogle Scholar
13.McClung, J. Effects of High Altitude on Human Birth, 1969. Harvard University Press, Cambridge.CrossRefGoogle Scholar
14.Haas, JD, Frongillo, EF, Stepcik, C, Beard, J, Hurtado, L. Altitude, ethnic and sex differences in birthweight and length in Bolivia. Hum Biol. 1980; 52, 459–477.Google Scholar
15.Moore, LG, Niermeyer, S, Zamudio, S. Human adaptation to high altitude: regional and life-cycle perspectives. Am J Phys Anthropol Suppl. 1998; 27, 25–64.3.0.CO;2-L>CrossRefGoogle Scholar
16.Giussani, DA, Phillips, PS, Anstee, S, Barker, DJ. Effects of altitude vs. economic status on birth weight and body shape at birth. Ped Res. 2001; 49, 490–494.CrossRefGoogle Scholar
17.Zamudio, S, Postigo, L, Illsley, NP, et al. Maternal oxygen delivery is not related to altitude- and ancestry-associated differences in human fetal growth. J Physiol. 2007; 582 (Pt 2), 883–895.CrossRefGoogle Scholar
18.Giussani, DA, Salinas, CE, Villena, M, Blanco, CE. The role of oxygen in prenatal growth: studies in the chick embryo. J Physiol. 2007; 585 (Pt 3), 911–917.CrossRefGoogle ScholarPubMed
19.West, JB. Respiratory Physiology. The Essentials, 7th edn, 2004. Lippincott Williams & Wilkins, Baltimore.Google Scholar
20.Burton, GJ, Palmer, ME. Eradicating fetomaternal fluid shift during perfusion fixation of the human placenta. Placenta. 1998; 9, 327–332.CrossRefGoogle Scholar
21.Armitage, P, Berry, G. Further analyses of straight-line data. In Statistical Methods in Medical Research (eds. Armitage P, Berry G, Matthews JNS), 1994; 292–305. Blackwell, Oxford.Google Scholar
22.Clark, KE, Durnwald, M, Austin, JE. A model for studying chronic reduction in uterine blood flow in pregnant sheep. Am J Physiol. 1982; 242, H297–H301.Google Scholar
23.Jensen, A, Roman, C, Rudolph, AM. Effects of reducing uterine blood flow on fetal blood flow distribution and oxygen delivery. J Dev Physiol. 1991; 15, 309–323.Google ScholarPubMed
24.Richardson, BS, Bocking, AD. Metabolic and circulatory adaptations to chronic hypoxia in the fetus. Comp Biochem Physiol A Mol Integr Physiol. 1998; 119, 717–723.CrossRefGoogle ScholarPubMed
25.Gardner, DS, Fletcher, AJ, Fowden, AL, Giussani, DA. A novel method for controlled and reversible long term compression of the umbilical cord in fetal sheep. J Physiol. 2001; 535(Pt 1), 217–229.CrossRefGoogle ScholarPubMed
26.Murotsuki, J, Challis, JR, Han, VK, Fraher, LJ, Gagnon, R. Chronic fetal placental embolization and hypoxemia cause hypertension and myocardial hypertrophy in fetal sheep. Am J Physiol. 1997; 272(1 Pt 2), R201–R207.Google ScholarPubMed
27.Walker, AM, de Preu, ND, Horne, RS, Berger, PJ. Autonomic control of heart rate differs with electrocortical activity and chronic hypoxaemia in fetal lambs. J Dev Physiol. 1990; 14, 43–48.Google ScholarPubMed
28.Robinson, JS, Kingston, EJ, Jones, CT, Thorburn, GD. Studies on experimental growth retardation in sheep. The effect of removal of endometrial caruncles on fetal size and metabolism. J Dev Physiol. 1979; 1, 379–398.Google ScholarPubMed
29.Kitanaka, T, Alonso, JG, Gilbert, RD, Siu, BL, Clemons, GK, Longo, LD. Fetal responses to long-term hypoxemia in sheep. Am J Physiol. 1989; 256, R1348–R1354.Google ScholarPubMed
30.Kamitomo, M, Longo, LD, Gilbert, RD. Right and left ventricular function in fetal sheep exposed to long-term high-altitude hypoxemia. Am J Physiol. 1992; 262(2 Pt 2), H399–H405.Google ScholarPubMed
31.Thompson, LP, Dong, Y. Chronic hypoxia decreases endothelial nitric oxide synthase protein expression in fetal guinea pig hearts. J Soc Gynecol Investig. 2005; 12, 388–395.CrossRefGoogle ScholarPubMed
32.Williams, SJ, Hemmings, DG, Mitchell, JM, McMillen, IC, Davidge, ST. Effects of maternal hypoxia or nutrient restriction during pregnancy on endothelial function in adult male rat offspring. J Physiol. 2005; 565, 125–135.CrossRefGoogle ScholarPubMed
33.Xu, Y, Williams, SJ, O’Brien, D, Davidge, ST. Hypoxia or nutrient restriction during pregnancy in rats leads to progressive cardiac remodeling and impairs postischemic recovery in adult male offspring. FASEB J. 2006; 20, 1251–1253.CrossRefGoogle ScholarPubMed
34.Rueda-Clausen, CF, Morton, JS, Davidge, ST. Effects of hypoxia-induced intrauterine growth restriction on cardiopulmonary structure and function during adulthood. Cardiovasc Res. 2009; 81, 713–722.CrossRefGoogle ScholarPubMed
35.De Grauw, TJ, Myers, R, Scott, WJ. Fetal growth in rats from different levels of hypoxia. Biol Neonate. 1986; 49, 85–89.CrossRefGoogle ScholarPubMed
36.Ruijtenbeek, K, le Noble, FAC, Janssen, GMJ, et al. Chronic hypoxia stimulates periarterial sympathetic nerve development in chicken embryo. Circulation. 2000; 102, 2892–2897.CrossRefGoogle ScholarPubMed
37.Rouwet, EV, Tintu, AN, Schellings, MW, et al. Hypoxia induces aortic hypertrophic growth, left ventricular dysfunction, and sympathetic hyperinnervation of peripheral arteries in the chick embryo. Circulation. 2002; 105, 2791–2796.CrossRefGoogle ScholarPubMed
38.Villamor, E, Kessels, CG, Ruijtenbeek, K, et al. 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.CrossRefGoogle ScholarPubMed
39.Tintu, A, Rouwet, E, Verlohren, S, et al. Hypoxia induces dilated cardiomyopathy in the chick embryo: mechanism, intervention, and long-term consequences. PLoS ONE. 2009; 4, e5155.CrossRefGoogle ScholarPubMed
40.Anderson, PA, Kleinman, CS, Lister, G, Talner, NS. Cardiovascular function during normal fetal and neonatal development and with hypoxic stress. In Fetal and Neonatal Physiology (eds. Polin AR, Fox WW), 1998; pp. 876–889. W.B. Saunders, Philadelphia.Google Scholar
41.Kempf, H, Linares, C, Corvol, P, Gasc, JM. Pharmacological inactivation of the endothelin type A receptor in the early chick embryo: a model of mispatterning of the branchial arch derivatives. Development. 1998; 125, 4931–4941.CrossRefGoogle Scholar
42.Byrne, AM, Bouchier-Hayes, DJ, Harmey, JH. Angiogenic and cell survival functions of vascular endothelial growth factor (VEGF). J Cell Mol Med. 2005; 9, 777–794.CrossRefGoogle ScholarPubMed
43.Skilton, MR, Evans, N, Griffiths, KA, Harmer, JA, Celermajer, DS. Aortic wall thickness in newborns with intrauterine growth restriction. Lancet. 2005; 365, 1484–1486.CrossRefGoogle ScholarPubMed
44.Koklu, E, Kurtoglu, S, Akcakus, M, et al. Increased aortic intima-media thickness is related to lipid profile in newborns with intrauterine growth restriction. Horm Res. 2006; 65, 269–275.Google ScholarPubMed
45.Akira, M, Yoshiyuki, S. Placental circulation, fetal growth, and stiffness of the abdominal aorta in newborn infants. J Pediatr. 2006; 148, 49–53.CrossRefGoogle ScholarPubMed