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Poor perinatal growth impairs baboon aortic windkessel function

Published online by Cambridge University Press:  11 October 2017

A. H. Kuo Open the ORCID record for A. H. Kuo [Opens in a new window] ,
J. Li ,
C. Li ,
H. F. Huber ,
P. W. Nathanielsz  and
G. D. Clarke
A. H. Kuo*
Affiliation:
Department of Radiology and Research Imaging Institute, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA
J. Li
Affiliation:
Xiangya School of Medicine, Central South University, Changsha, Hunan, China Southwest National Primate Research Center, San Antonio, TX, USA
C. Li
Affiliation:
Department of Animal Science, University of Wyoming, Laramie, Wyoming Southwest National Primate Research Center, San Antonio, TX, USA
H. F. Huber
Affiliation:
Department of Animal Science, University of Wyoming, Laramie, Wyoming
P. W. Nathanielsz
Affiliation:
Department of Animal Science, University of Wyoming, Laramie, Wyoming Southwest National Primate Research Center, San Antonio, TX, USA
G. D. Clarke
Affiliation:
Department of Radiology and Research Imaging Institute, University of Texas Health Science Center at San Antonio, San Antonio, TX, USA Southwest National Primate Research Center, San Antonio, TX, USA
*
*Address for correspondence: A. H. Kuo, MD, Department of Radiology, University of Texas Health Science Center at San Antonio, 7703 Floyd Curl Drive, MC 7800, San Antonio, TX 78229-3900, USA. (Email [email protected])
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Abstract

The ability of the aorta to buffer blood flow and provide diastolic perfusion (Windkessel function) is a determinant of cardiovascular health. We have reported cardiac dysfunction indicating downstream vascular abnormalities in young adult baboons who were intrauterine growth restricted (IUGR) at birth as a result of moderate maternal nutrient reduction. Using 3 T MRI, we examined IUGR offspring (eight male, eight female; 5.7 years; human equivalent 25 years) and age-matched controls (eight male, eight female; 5.6 years) to quantify distal descending aortic cross-section (AC) and distensibility (AD). ANOVA showed decreased IUGR AC/body surface area (0.9±0.05 cm2/m2v. 1.2±0.06 cm2/m2, M±s.e.m., P<0.005) and AD (1.7±0.2 v. 4.0±0.5×10−3/mmHg, P<0.005) without sex difference or group-sex interaction, suggesting intrinsic vascular pathology and impaired development persisting in adulthood. Future studies should evaluate potential consequences of these changes on coronary perfusion, afterload and blood pressure.

Keywords

aortababoonsdevelopmental programingintrauterine growth restrictionmaternal nutrient restriction
Type
Brief Report
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 2 , April 2018 , pp. 137 - 142
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

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References

1. Rich-Edwards, JW, Kleinman, K, Michels, KB, et al. Longitudinal study of birth weight and adult body mass index in predicting risk of coronary heart disease and stroke in women. BMJ. 2005; 330, 1115.Google Scholar
2. Curhan, GC, Willett, WC, Rimm, EB, et al. Birth weight and adult hypertension, diabetes mellitus, and obesity in US men. Circulation. 1996; 94, 3246–3250.Google Scholar
3. Kuo, AH, Li, C, Li, J, et al. Cardiac remodelling in a baboon model of intrauterine growth restriction mimics accelerated ageing. J Physiol. 2016; 595, 1093–1110.Google Scholar
4. Belz, GG. Elastic properties and windkessel function of the human aorta. Cardiovasc Drugs Ther. 1995; 9, 73–83.Google Scholar
5. Klassen, SA, Chirico, D, Dempster, KS, Shoemaker, JK, O’Leary, DD. Role of aortic arch vascular mechanics in cardiovagal baroreflex sensitivity. Am J Physiol Regul Integr Comp Physiol. 2016; 311, R24–R32.Google Scholar
6. Li, C, McDonald, TJ, Wu, G, Nijland, MJ, Nathanielsz, PW. Intrauterine growth restriction alters term fetal baboon hypothalamic appetitive peptide balance. J Endocrinol. 2013; 217, 275–282.CrossRefGoogle ScholarPubMed
7. VandeBerg, JL, Williams-Blangero, S, Tardif, SD. The baboon in biomedical research. 2009. Springer Science & Business Media: New York, NY.Google Scholar
8. Sun, C, Burgner, DP, Ponsonby, A, et al. Effects of early-life environment and epigenetics on cardiovascular disease risk in children: Highlighting the role of twin studies. Pediatr Res. 2013; 73, 523–530.CrossRefGoogle ScholarPubMed
9. Tauzin, L, Rossi, P, Giusano, B, et al. Characteristics of arterial stiffness in very low birth weight premature infants. Pediatr Res. 2006; 60, 592–596.Google Scholar
10. Mori, A, Uchida, N, Inomo, A, Izumi, S. Stiffness of systemic arteries in appropriate- and small-for-gestational-age newborn infants. Pediatrics. 2006; 118, 1035–1041.CrossRefGoogle ScholarPubMed
11. Cheung, YF, Wong, KY, Lam, BC, Tsoi, NS. Relation of arterial stiffness with gestational age and birth weight. Arch Dis Child. 2004; 89, 217–221.Google Scholar
12. Ley, D, Stale, H, Marsal, K. Aortic vessel wall characteristics and blood pressure in children with intrauterine growth retardation and abnormal foetal aortic blood flow. Acta Paediatrica. 1997; 86, 299–305.Google Scholar
13. Brodszki, J, Lanne, T, Marsal, K, Ley, D. Impaired vascular growth in late adolescence after intrauterine growth restriction. Circulation. 2005; 111, 2623–2628.CrossRefGoogle ScholarPubMed
14. Schack-Nielsen, L, Mølgaard, C, Larsen, D, Martyn, C, Michaelsen, KF. Arterial stiffness in 10-year-old children: current and early determinants. Br J Nutr. 2005; 94, 1004–1011.CrossRefGoogle ScholarPubMed
15. Dodson, RB, Rozance, PJ, Hunter, KS, Ferguson, VL. Increased stiffness of the abdominal aorta with intrauterine growth restriction in the near-term fetal sheep. ASME 2012 Summer Bioengineering Conference. 2012; 1251–1252.Google Scholar
16. Thompson, JA, Richardson, BS, Gagnon, R, Regnault, TR. Chronic intrauterine hypoxia interferes with aortic development in the late gestation ovine fetus. J Physiol (Lond ). 2011; 589, 3319–3332.Google Scholar
17. Thompson, JA, Gros, R, Richardson, BS, Piorkowska, K, Regnault, TR. Central stiffening in adulthood linked to aberrant aortic remodeling under suboptimal intrauterine conditions. Am J Physiol Regul Integr Comp Physiol. 2011; 301, R1731–R1737.Google Scholar
18. Looker, T, Berry, CL. The growth and development of the rat aorta. II. Changes in nucleic acid and scleroprotein content. J Anat. 1972; 113(Pt 1), 17–34.Google Scholar
19. 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.Google Scholar
20. Dodson, RB, Rozance, PJ, Petrash, CC, Hunter, KS, Ferguson, VL. Thoracic and abdominal aortas stiffen through unique extracellular matrix changes in intrauterine growth restricted fetal sheep. Am J Physiol Heart Circ Physiol. 2014; 306, H429–H437.Google Scholar
21. Ozaki, T, Nishina, H, Hanson, M, Poston, L. Dietary restriction in pregnant rats causes gender‐related hypertension and vascular dysfunction in offspring. J Physiol (Lond). 2001; 530, 141–152.CrossRefGoogle ScholarPubMed
22. 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
23. Franklin, SS, Gustin, W 4th, Wong, ND, et al. Hemodynamic patterns of age-related changes in blood pressure. The Framingham Heart Study. Circulation. 1997; 96, 308–315.Google Scholar
24. Nethononda, RM, Lewandowski, AJ, Stewart, R, et al. Gender specific patterns of age-related decline in aortic stiffness: a cardiovascular magnetic resonance study including normal ranges. J Cardiovasc Magn Reson. 2015; 17, 20.Google Scholar
25. Molnar, J, Howe, DC, Nijland, MJ, Nathanielsz, PW. Prenatal dexamethasone leads to both endothelial dysfunction and vasodilatory compensation in sheep. J Physiol (Lond). 2003; 547, 61–66.Google Scholar
26. 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
27. 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 (Lond). 2005; 565, 137–147.CrossRefGoogle ScholarPubMed
28. Ponzio, BF, Carvalho, MHC, Fortes, ZB, do Carmo Franco, M. Implications of maternal nutrient restriction in transgenerational programming of hypertension and endothelial dysfunction across F1–F3 offspring. Life Sci. 2012; 90, 571–577.CrossRefGoogle ScholarPubMed
29. Kawamura, M, Itoh, H, Yura, S, et al. Undernutrition in utero augments systolic blood pressure and cardiac remodeling in adult mouse offspring: possible involvement of local cardiac angiotensin system in developmental origins of cardiovascular disease. Endocrinology. 2007; 148, 1218–1225.Google Scholar
30. Cavalcante, JL, Lima, JA, Redheuil, A, Al-Mallah, MH. Aortic stiffness: current understanding and future directions. J Am Coll Cardiol. 2011; 57, 1511–1522.Google Scholar