Hostname: page-component-8448b6f56d-t5pn6 Total loading time: 0 Render date: 2024-04-20T03:43:40.366Z Has data issue: false hasContentIssue false
  • English
  • Français

High altitude hypoxia and blood pressure dysregulation in adult chickens

Published online by Cambridge University Press:  19 September 2012

E. A. Herrera ,
C. E. Salinas ,
C. E. Blanco ,
M. Villena  and
D. A. Giussani
E. A. Herrera
Affiliation:
Laboratorio de Función y Reactividad Vascular, Programa de Fisiopatología, Instituto de Ciencias Biomédicas, Facultad de Medicina, Universidad de Chile, Santiago, Chile
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:
National Children's Research Centre, Our Lady's Children's Hospital, Crumlin, Dublin, Ireland
M. Villena
Affiliation:
Instituto Boliviano de Biología de Altura, Facultad de Medicina, Universidad Mayor de San Andrés, La Paz, Bolivia
D. A. Giussani*
Affiliation:
Department of Physiology, Development and Neuroscience, University of Cambridge, Cambridge, UK
*
*Address for correspondence: Prof. 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

Although it is accepted that impaired placental perfusion in complicated pregnancy can slow fetal growth and programme an increased risk of cardiovascular dysfunction at adulthood, the relative contribution of reductions in fetal nutrition and in fetal oxygenation as the triggering stimulus remains unclear. By combining high altitude (HA) with the chick embryo model, we have previously isolated the direct effects of HA hypoxia on embryonic growth and cardiovascular development before hatching. This study isolated the effects of developmental hypoxia on cardiovascular function measured in vivo in conscious adult male and female chickens. Chick embryos were incubated, hatched and raised at sea level (SL, nine males and nine females) or incubated, hatched and raised at HA (seven males and seven females). At 6 months of age, vascular catheters were inserted under general anaesthesia. Five days later, basal blood gas status, basal cardiovascular function and cardiac baroreflex responses were investigated. HA chickens had significantly lower basal arterial PO2 and haemoglobin saturation, and significantly higher haematocrit than SL chickens, independent of the sex of the animal. HA chickens had significantly lower arterial blood pressure than SL chickens, independent of the sex of the animal. Although the gain of the arterial baroreflex was decreased in HA relative to SL male chickens, it was increased in HA relative to SL female chickens. We show that development at HA lowers basal arterial blood pressure and alters baroreflex sensitivity in a sex-dependent manner at adulthood.

Keywords

baroreflexcardiovascular diseasechronic hypoxiafetal programming
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 4 , Issue 1 , February 2013 , pp. 69 - 76
Copyright
Copyright © Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2012 

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.Barker, DJ. In utero programming of chronic disease. Clin Sci (Lond). 1998; 95, 115–128.CrossRefGoogle ScholarPubMed
2.Fowden, AL, Giussani, DA, Forhead, AJ. Intrauterine programming of physiological systems: causes and consequences. Physiology (Bethesda). 2006; 21, 29–37.Google Scholar
3.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.Google Scholar
4.Martin-Gronert, MS, Ozanne, SE. Mechanisms underlying the developmental origins of disease. Rev Endocr Metab Disord. 2012; 13, 85–92.CrossRefGoogle ScholarPubMed
5.Thompson, LP. Effects of chronic hypoxia on fetal coronary responses. High Alt Med Biol. 2003; 4, 215–224.Google Scholar
6.Hauton, D, Ousley, V. Prenatal hypoxia induces increased cardiac contractility on a background of decreased capillary density. BMC Cardiovasc Disord. 2009; 9, 1.CrossRefGoogle ScholarPubMed
7.Patterson, AJ, Zhang, L. Hypoxia and fetal heart development. Curr Mol Med. 2010; 10, 653–666.Google Scholar
8.Rueda-Clausen, CF, Morton, JS, Davidge, ST. The early origins of cardiovascular health and disease: who, when, and how. Semin Reprod Med. 2011; 29, 197–210.Google Scholar
9.Giussani, DA, Camm, EJ, Niu, Y, et al. Developmental programming of cardiovascular dysfunction by prenatal hypoxia and oxidative stress. PLoS One. 2012; 7, e31017.Google Scholar
10.Li, G, Xiao, Y, Estrella, JL, et al. Effect of fetal hypoxia on heart susceptibility to ischemia and reperfusion injury in the adult rat. J Soc Gynecol Investig. 2003; 10, 265–274.Google Scholar
11.Morton, JS, Rueda-Clausen, CF, Davidge, ST. Mechanisms of endothelium-dependent vasodilation in male and female, young and aged offspring born growth restricted. Am J Physiol Regul Integr Comp Physiol. 2010; 298, R930–R938.CrossRefGoogle Scholar
12.de Grauw, TJ, Myers, RE, Scott, WJ. Fetal growth retardation in rats from different levels of hypoxia. Biol Neonate. 1986; 49, 85–89.Google Scholar
13.Camm, EJ, Hansell, JA, Kane, AD, et al. Partial contributions of developmental hypoxia and undernutrition to prenatal alterations in somatic growth and cardiovascular structure and function. Am J Obstet Gynecol. 2010; 203(5), 495.e24–34.Google Scholar
14.Moore, LG, Charles, SM, Julian, CG. Humans at high altitude: hypoxia and fetal growth. Respir Physiol Neurobiol. 2011; 178, 181–190.Google Scholar
15.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.Google Scholar
16.McClung, J. Effects of High Altitude on Human Birth, 1969. Harvard University Press: Cambridge.Google Scholar
17.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
18.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.Google Scholar
19.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.Google Scholar
20.Niermeyer, S. Cardiopulmonary transition in the high altitude infant. High Alt Med Biol. 2003; 4, 225–239.Google Scholar
21.Peñaloza, D, Arias-Stella, J, Sime, F, Recavarren, S, Marticorena, E. The heart and pulmonary circulation in children at high altitudes: physiological, anatomical, and clinical observations. Pediatrics. 1964; 34, 568–582.Google Scholar
22.Peñaloza, D, Sime, F, Ruiz, L. Pulmonary hemodynamics in children living at high altitudes. High Alt Med Biol. 2008; 9, 199–207.CrossRefGoogle ScholarPubMed
23.Huicho, L, Niermeyer, S. Cardiopulmonary pathology among children resident at high altitude in Tintaya, Peru: a cross-sectional study. High Alt Med Biol. 2006; 7, 168–179.Google Scholar
24.Ruijtenbeek, K, De Mey, JG, Blanco, CE. The chicken embryo in developmental physiology of the cardiovascular system: a traditional model with new possibilities. Am J Physiol Regul Integr Comp Physiol. 2002; 283, R549–R550.Google Scholar
25.Miller, SL, Green, LR, Peebles, DM, Hanson, MA, Blanco, CE. Effects of chronic hypoxia and protein malnutrition on growth in the developing chick. Am J Obstet Gynecol. 2002; 186, 261–267.Google Scholar
26.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
27.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.Google Scholar
28.Salinas, CE, Blanco, CE, Villena, M, et al. Developmental origin of cardiac and vascular disease in chick embryos incubated at high attitude. J DOHaD. 2010; 1, 60–66.Google Scholar
29.Gilbert, JS, Nijland, MJ. Sex differences in the developmental origins of hypertension and cardiorenal disease. Am J Physiol Regul Integr Comp Physiol. 2008; 295, R1941–R1952.Google Scholar
30.McDowall, LM, Dampney, RA. Calculation of threshold and saturation points of sigmoidal baroreflex function curves. Am J Physiol Heart Circ Physiol. 2006; 291, H2003–H2007.CrossRefGoogle ScholarPubMed
31.Gobel, FL, Norstrom, LA, Nelson, RR, Jorgensen, CR, Wang, Y. The rate-pressure product as an index of myocardial oxygen consumption during exercise in patients with angina pectoris. Circulation. 1978; 57, 549–556.Google Scholar
32.Langley, SC, Jackson, AA. Increased systolic blood pressure in adult rats induced by fetal exposure to maternal low protein diets. Clin Sci (Lond). 1994; 86, 217–222.Google Scholar
33.Woodall, SM, Johnston, BM, Breier, BH, Gluckman, PD. Chronic maternal undernutrition in the rat leads to delayed postnatal growth and elevated blood pressure of offspring. Pediatr Res. 1996; 40, 438–443.Google Scholar
34.Gardner, DS, Jackson, AA, Langley-Evans, SC. Maintenance of maternal diet-induced hypertension in the rat is dependent on glucocorticoids. Hypertension. 1997; 30, 1525–1530.CrossRefGoogle ScholarPubMed
35.Manning, J, Vehaskari, VM. Low birth weight-associated adult hypertension in the rat. Pediatr Nephrol. 2001; 16, 417–422.Google Scholar
36.Gilbert, JS, Lang, AL, Grant, AR, Nijland, MJ. Maternal nutrient restriction in sheep: hypertension and decreased nephron number in offspring at 9 months of age. J Physiol. 2005; 565(Pt 1), 137–147.Google Scholar
37.Cambonie, G, Comte, B, Yzydorczyk, C, et al. Antenatal antioxidant prevents adult hypertension, vascular dysfunction, and microvascular rarefaction associated with in utero exposure to a low-protein diet. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R1236–R1245.Google Scholar
38.Watkins, AJ, Wilkins, A, Cunningham, C, et al. Low protein diet fed exclusively during mouse oocyte maturation leads to behavioural and cardiovascular abnormalities in offspring. J Physiol. 2008; 586, 2231–2244.Google Scholar
39.Langley-Evans, SC, Clamp, AG, Grimble, RF, Jackson, AA. Influence of dietary fats upon systolic blood pressure in the rat. Int J Food Sci Nutr. 1996; 47, 417–425.Google Scholar
40.Langley-Evans, SC. Intrauterine programming of hypertension in the rat: nutrient interactions. Comp Biochem Physiol A Physiol. 1996; 114, 327–333.Google Scholar
41.Khan, IY, Taylor, PD, Dekou, V, et al. Gender-linked hypertension in offspring of lard-fed pregnant rats. Hypertension. 2003; 41, 168–175.CrossRefGoogle ScholarPubMed
42.Armitage, JA, Lakasing, L, Taylor, PD, et al. Developmental programming of aortic and renal structure in offspring of rats fed fat-rich diets in pregnancy. J Physiol. 2005; 565(Pt 1), 171–184.Google Scholar
43.Elahi, MM, Cagampang, FR, Anthony, FW, et al. Statin treatment in hypercholesterolemic pregnant mice reduces cardiovascular risk factors in their offspring. Hypertension. 2008; 51, 939–944.Google Scholar
44.Dodic, M, Abouantoun, T, O'Connor, A, Wintour, EM, Moritz, KM. Programming effects of short prenatal exposure to dexamethasone in sheep. Hypertension. 2002; 40, 729–734.Google Scholar
45.Ortiz, LA, Quan, A, Zarzar, F, Weinberg, A, Baum, M. Prenatal dexamethasone programs hypertension and renal injury in the rat. Hypertension. 2003; 41, 328–334.Google Scholar
46.Shaltout, HA, Rose, JC, Figueroa, JP, et al. Acute AT(1)-receptor blockade reverses the hemodynamic and baroreflex impairment in adult sheep exposed to antenatal betamethasone. Am J Physiol Heart Circ Physiol. 2010; 299, H541–H547.CrossRefGoogle ScholarPubMed
47.Roghair, RD, Wemmie, JA, Volk, KA, et al. Maternal antioxidant blocks programmed cardiovascular and behavioural stress responses in adult mice. Clin Sci (Lond). 2011; 121, 427–436.Google Scholar
48.Soleymanlou, N, Jurisica, I, Nevo, O, et al. Molecular evidence of placental hypoxia in preeclampsia. J Clin Endocrinol Metab. 2005; 90, 4299–4308.Google Scholar
49.Baschat, AA. Fetal responses to placental insufficiency: an update. BJOG. 2004; 111, 1031–1041.CrossRefGoogle ScholarPubMed
50.Ruijtenbeek, K, Kessels, CG, Janssen, BJ, et al. Chronic moderate hypoxia during in ovo development alters arterial reactivity in chickens. Pflugers Arch. 2003; 447, 158–167.Google Scholar
51.Lindgren, I, Crossley, D II, Villamor, E, Altimiras, J. Hypotension in the chronically hypoxic chicken embryo is related to the β-adrenergic response of chorioallantoic and femoral arteries and not to bradycardia. Am J Physiol Regul Integr Comp Physiol. 2011; 301, R1161–R1168.Google Scholar
52.Crossley, DA II, Altimiras, J. Cardiovascular development in embryos of the American alligator Alligator mississippiensis: effects of chronic and acute hypoxia. J Exp Biol. 2005; 208(Pt 1), 31–39.Google Scholar
53.Coney, AM, Marshall, JM. Effects of maternal hypoxia on muscle vasodilatation evoked by acute systemic hypoxia in adult rat offspring: changed roles of adenosine and A1 receptors. J Physiol. 2010; 588(Pt 24), 5115–5125.Google Scholar
54.Herrera, EA, Pulgar, VM, Riquelme, RA, et al. High-altitude chronic hypoxia during gestation and after birth modifies cardiovascular responses in newborn sheep. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R2234–R2240.Google Scholar
55.Martini, J, Carpentier, B, Negrete, AC, Frangos, JA, Intaglietta, M. Paradoxical hypotension following increased hematocrit and blood viscosity. Am J Physiol Heart Circ Physiol. 2005; 289, H2136–H2143.Google Scholar
56.Martini, J, Carpentier, B, Chávez Negrete, A, et al. Beneficial effects due to increasing blood and plasma viscosity. Clin Hemorheol Microcirc. 2006; 35, 51–57.Google ScholarPubMed
57.Pladys, P, Lahaie, I, Cambonie, G, et al. Role of brain and peripheral angiotensin II in hypertension and altered arterial baroreflex programmed during fetal life in rat. Pediatr Res. 2004; 55, 1042–1049.Google Scholar
58.Gardner, DS, Pearce, S, Dandrea, J, et al. Peri-implantation undernutrition programs blunted angiotensin II evoked baroreflex responses in young adult sheep. Hypertension. 2004; 43, 1290–1296.Google Scholar
59.Gopalakrishnan, GS, Gardner, DS, Rhind, SM, et al. Programming of adult cardiovascular function after early maternal undernutrition in sheep. Am J Physiol Regul Integr Comp Physiol. 2004; 287, R12–R20.CrossRefGoogle ScholarPubMed
60.Fletcher, AJ, McGarrigle, HH, Edwards, CM, Fowden, AL, Giussani, DA. Effects of low dose dexamethasone treatment on basal cardiovascular and endocrine function in fetal sheep during late gestation. J Physiol. 2002; 545(Pt 2), 649–660.Google Scholar
61.Segar, JL, Roghair, RD, Segar, EM, et al. Early gestation dexamethasone alters baroreflex and vascular responses in newborn lambs before hypertension. Am J Physiol Regul Integr Comp Physiol. 2006; 291, R481–R488.CrossRefGoogle ScholarPubMed
62.Roghair, RD, Segar, JL, Volk, KA, et al. Vascular nitric oxide and superoxide anion contribute to sex-specific programmed cardiovascular physiology in mice. Am J Physiol Regul Integr Comp Physiol. 2009; 296, R651–R662.Google Scholar
63.Pulgar, VM, Hong, JK, Jessup, JA, et al. Mild chronic hypoxemia modifies expression of brain stem angiotensin peptide receptors and reflex responses in fetal sheep. Am J Physiol Regul Integr Comp Physiol. 2009; 297, R446–R452.Google Scholar
64.Peyronnet, J, Dalmaz, Y, Ehrström, M, et al. Long-lasting adverse effects of prenatal hypoxia on developing autonomic nervous system and cardiovascular parameters in rats. Pflugers Arch. 2002; 443, 858–865.Google Scholar
65.Gilbert, JS, Nijland, MJ. Sex differences in the developmental origins of hypertension and cardiorenal disease. Am J Physiol Regul Integr Comp Physiol. 2008; 295, R1941–R1952.CrossRefGoogle ScholarPubMed
66.do Carmo Pinho Franco, M, Nigro, D, Fortes, ZB, et al. Intrauterine undernutrition – renal and vascular origin of hypertension. Cardiovasc Res. 2003; 60, 228–234.Google Scholar
67.Igosheva, N, Taylor, PD, Poston, L, Glover, V. Prenatal stress in the rat results in increased blood pressure responsiveness to stress and enhanced arterial reactivity to neuropeptide Y in adulthood. J Physiol. 2007; 582(Pt 2), 665–674.Google Scholar
68.Hemmings, DG, Williams, SJ, Davidge, ST. Increased myogenic tone in 7-month-old adult male but not female offspring from rat dams exposed to hypoxia during pregnancy. Am J Physiol Heart Circ Physiol. 2005; 289, H674–H682.Google Scholar
69.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.Google Scholar
70.Morton, JS, Rueda-Clausen, CF, Davidge, ST. Flow-mediated vasodilation is impaired in adult rat offspring exposed to prenatal hypoxia. J Appl Physiol. 2011; 110, 1073–1082.Google Scholar
71.Xue, Q, Zhang, L. Prenatal hypoxia causes a sex-dependent increase in heart susceptibility to ischemia and reperfusion injury in adult male offspring: role of protein kinase C epsilon. J Pharmacol Exp Ther. 2009; 330, 624–632.Google Scholar
72.Gluckman, PD, Hanson, MA. Mismatch: the lifestyle diseases timebomb. Oxford University Press. 2006; 6, 137–211.Google Scholar