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Maternal nutritional restriction during gestation impacts differently on offspring muscular and elastic arteries and is associated with increased carotid resistance and ventricular afterload in maturity

Published online by Cambridge University Press:  29 May 2019

Yanina Zócalo ,
Rodolfo Ungerfeld ,
Raquel Pérez-Clariget  and
Daniel Bia
Yanina Zócalo*
Affiliation:
Departamento de Fisiología, Facultad de Medicina, Núcleo Interdisciplinario CUiiDARTE, Universidad de la República, Montevideo, Uruguay
Rodolfo Ungerfeld
Affiliation:
Departamento de Fisiología, Facultad de Veterinaria, Universidad de la República, Montevideo, Uruguay
Raquel Pérez-Clariget
Affiliation:
Departamento de Producción Animal y Pasturas, Facultad de Agronomía, Universidad de la República, Montevideo, Uruguay
Daniel Bia
Affiliation:
Departamento de Fisiología, Facultad de Medicina, Núcleo Interdisciplinario CUiiDARTE, Universidad de la República, Montevideo, Uruguay
*
Address for correspondence: Yanina Zócalo, Departmento de Fisiología, Facultad de Medicina, Núcleo Interdisciplinario CUiiDARTE, Universidad de la República, Montevideo, Uruguay. Email: yana@fmed.edu.uy
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Abstract

Background:

Intrauterine undernutrition could impact offspring left ventricle (LV) afterload and arterial function. The changes observed in adulthood could differ depending on the arterial type, pathway and properties studied. Aim: To analyze whether undernutrition during early and mid-gestation is associated with changes in cardiovascular properties in adulthood.

Methods:

Pregnant ewes were assigned to one of the two treatment groups: (1) standard nutritional offer (high pasture-allowance, HPA; n = 16) or (2) nutritional restriction (50–75% of control intake) from before conception until day 122 of gestation (≈85% term) (low pasture allowance, LPA; n = 17). When offspring reached adult life, cardiovascular parameters were assessed in conscious animals (applanation tonometry, vascular echography).

Measurements:

Peripheral and aortic pressure, carotid and femoral arteries diameters, intima-media thickness and stiffness, blood flow, local and regional resistances and LV afterload were measured. Blood samples were collected. Parameters were compared before and after adjustment for nutritional characteristics at birth and at the time of the cardiovascular evaluation.

Results:

Doppler-derived cerebral vascular resistances, mean pressure/flow ratio (carotid resistance) and afterload indexes were higher in descendants from LPA than in descendants from HPA ewes (p < 0.05). Descendants from LPA had lower femoral diameters (p < 0.05). Cardiovascular changes associated with nutritional restriction during pregnancy did not depend on the offsprings’ nutritional conditions at birth and/or in adult life.

Conclusion:

Pregnant ewes that experienced undernutrition gave birth to female offspring that exhibited increased carotid pathway resistances (cerebral microcirculatory resistances) and LV afterload when they reached the age of 2.5 years. There were differences in the impact of nutritional deficiency on elastic and muscular arteries.

Keywords

Aortic pressurecardiovascular structure and functionintrauterine nutritional restrictionleft ventricle afterloadsheep
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 11 , Issue 1 , February 2020 , pp. 7 - 17
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2019 

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References

Vorster, HH, Kruger, A. Poverty, malnutrition, underdevelopment and cardiovascular disease: a South African perspective. Cardiovasc J Afr. 2007; 18(5), 321–324.Google ScholarPubMed
Bergmann, R, Bergmann, K, Dudenhausen, J. Undernutrition and growth restriction in pregnancy. In: Barker, DJP, Bergmann, RL, Ogra, PL (eds): The Window of Opportunity: Pre-Pregnancy to 24 Months of Age. NestléNutr Workshop Ser Pediatr Program, vol. 61, pp. 103–121. 2008. Nestec Ltd., Vevey/S. Karger AG: Basel.CrossRefGoogle Scholar
Dodson, RB, Rozance, PJ, Fleenor, BS, et al. Increased arterial stiffness and extracellular matrix reorganization in intrauterine growth-restricted fetal sheep. Pediatr Res. 2013; 73(2), 147–154.CrossRefGoogle ScholarPubMed
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(3), H429–H437.CrossRefGoogle ScholarPubMed
Torrens, C, Brawley, L, Barker, AC, et al. Maternal protein restriction in the rat impairs resistance artery but not conduit artery function in pregnant offspring. J Physiol. 2003; 547(Pt 1), 77–84.CrossRefGoogle Scholar
Bubb, KJ, Cock, ML, Black, MJ, et al. Intrauterine growth restriction delays cardiomyocyte maturation and alters coronary artery function in the fetal sheep. J Physiol. 2007; 578(Pt 3), 871–881.CrossRefGoogle ScholarPubMed
Symonds, ME, Stephenson, T, Gardner, DS, Budge, H. Long-term effects of nutritional programming of the embryo and fetus: mechanisms and critical windows. Reprod Fertil Dev. 2007; 19(1), 53–63.CrossRefGoogle ScholarPubMed
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(6), 1290–1296.CrossRefGoogle ScholarPubMed
Schlabritz-Loutsevitch, N, Ballesteros, B, Dudley, C, Jenkins, S, Hubbard, G, Burton, GJ, Nathanielsz, P. Moderate maternal nutrient restriction, but not glucocorticoid administration, leads to placental morphological changes in the baboon (Papio sp.). Placenta. 2007; 28, 783–793.CrossRefGoogle Scholar
McDonald, TJ, Wu, G, Nijland, MJ, Jenkins, SL, Nathanielsz, PW, Jansson, T. Effect of 30% nutrient restriction in the first half of gestation on maternal and fetal baboon serum amino acid concentrations. Br J Nutr. 2013; 109(8), 1382–1388.CrossRefGoogle ScholarPubMed
Nutrition for Health and Development. A global agenda for combating malnutrition. World Health Organization. Nutrition for Health and Development (NHD). Sustainable Development and Healthy Environments (SDE). Progress Report. 2000. http://apps.who.int/iris/handle/10665/66509.Google Scholar
Cleal, JK, Poore, KR, Boullin, JP, et al. Mismatched pre- and postnatal nutrition leads to cardiovascular dysfunction and altered renal function in adulthood. Proc Natl Acad Sci USA. 2007; 104, 9529–9533.CrossRefGoogle ScholarPubMed
Franco, M, Arruda, R, Dantas, A, et al. Intrauterine undernutrition: expression and activity of the endothelial nitric oxide synthase in male and female adult offspring. Cardiovasc Res. 2002; 56, 145–153.CrossRefGoogle Scholar
Nishina, H, Green, LR, McGarrigle, HH, et al. Effect of nutritional restriction in early pregnancy on isolated femoral artery function in mid-gestation fetal sheep. J Physiol. 2003; 553(Pt 2), 637–647.CrossRefGoogle ScholarPubMed
Vianna, CA, Horta, BL, Gigante, DP, de Barros, FC. Pulse wave velocity at early adulthood: breastfeeding and nutrition during pregnancy and childhood. PLoS One. 2016; 11(4), e0152501.CrossRefGoogle ScholarPubMed
Vlachopoulos, C, O’Rourke, M, Nichols, W. McDonald’s Blood Flow in Arteries: Theoretical, Experimental and Clinical Principles, 6th edn, 2011. CRC Press: London.CrossRefGoogle Scholar
Armitage, JA, Khan, IY, Taylor, PD, Nathanielsz, PW, Poston, L. Developmental programming of the metabolic syndrome by maternal nutritional imbalance: how strong is the evidence from experimental models in mammals? J Physiol. 2004; 561(Pt 2), 355–377.CrossRefGoogle ScholarPubMed
Sathishkumar, K, Elkins, R, Yallampalli, U, Yallampalli, C. Protein restriction during pregnancy induces hypertension and impairs endothelium-dependent vascular function in adult female offspring. J Vasc Res. 2009; 46(3), 229–239.CrossRefGoogle ScholarPubMed
Russel, AJF, Doney, JM, Gunn, RG. Subjective assessment of body fat in live sheep. J Agric Sci. 1969; 72, 451–454.CrossRefGoogle Scholar
Freitas-de-Melo, A, Ungerfeld, R, Hötzel, MJ, et al. Mother–young behaviours at lambing in grazing ewes: effects of lamb sex and food restriction in pregnancy. Appl Anim Behav Sci. 2015; 168, 31–36.CrossRefGoogle Scholar
Freitas-de-Melo, A, Ungerfeld, R, Hötzel, MJ, Orihuela, A, Pérez-Clariget, R. Low pasture allowance until late gestation in ewes: behavioural and physiological changes in ewes and lambs from lambing to weaning. Animal. 2017; 11(2), 285–294.CrossRefGoogle ScholarPubMed
Haydock, KP, Shaw, NH. The comparative yield method for estimating dry matter yield of pasture. Aust J Exp Agric Anim Husb. 1975; 15, 663–670.Google Scholar
Hawkins, P, Steyn, C, McGarrigle, HH, et al. Cardiovascular and hypothalamic-pituitary-adrenal axis development in late gestation fetal sheep and young lambs following modest maternal nutrient restriction in early gestation. Reprod Fertil Dev. 2000; 12, 443–456.CrossRefGoogle Scholar
Trim, CM, Hofmeister, EH, Peroni, JF, Thoresen, M. Evaluation of an oscillometric blood pressure monitor for use in anesthetized sheep. Vet Anaesth Analg. 2013; 40(6), e31–e39.CrossRefGoogle ScholarPubMed
Zócalo, Y, Curcio, S, García-Espinosa, V, et al. Comparative analysis of arterial parameters variations associated with inter-individual variations in peripheral and aortic blood pressure: cross-sectional study in healthy subjects aged 2-84 years. High Blood Press Cardiovasc Prev. 2017; 24(4), 437–451.CrossRefGoogle ScholarPubMed
Zócalo, Y, Marotta, M, García-Espinosa, V, et al. Children and adolescents macrovascular reactivity level and dynamics, but not the microvascular response, is associated with body mass index and arterial stiffness levels. High Blood Press Cardiovasc Prev. 2017; 24(4), 371–386.CrossRefGoogle Scholar
Santana, DB, Barra, J, Grignola, J, Ginés, F, Armentano, R. Pulmonary artery smooth muscle activation attenuates arterial dysfunction during acute pulmonary hypertension. J Appl Physiol. (1985). 2005; 98(2), 605–613.CrossRefGoogle ScholarPubMed
Bude, RO, Rubin, JM. Relationship between the resistive index and vascular compliance and resistance. Radiology. 1999; 211(2), 411–417.CrossRefGoogle ScholarPubMed
Li, JK-J. Time domain resolution of forward and reflected waves in the aorta. IEEE Trans Biomed Eng. 1986; 33, 783–785.CrossRefGoogle ScholarPubMed
Eng, J. Sample size estimation: how many individuals should be studied? Radiology. 2003; 227(2), 309–313.CrossRefGoogle ScholarPubMed
Brawley, L, Poston, L, Hanson, MA. Mechanisms underlying the programming of small artery dysfunction: review of the model using ow protein diet in pregnancy in the rat. Arch Physiol Biochem. 2003; 111, 23–35.CrossRefGoogle Scholar
Ozaki, T, Nishina, H, Hanson, MA,Poston, L. Dietary restriction in pregnant rats causes gender-related hypertension and vascular dysfunction in offspring. J Physiol. 2001; 530, 141–152.CrossRefGoogle ScholarPubMed
Ozaki, T, Hawkins, P, Nishina, H, et al. Effects of undernutrition in early pregnancy on systemic small artery function in late-gestation fetal sheep. Am J Obstet Gynecol. 2000; 183(5), 1301–1307.CrossRefGoogle ScholarPubMed
Faury, G. Function-structure relationship of elastic arteries in evolution: from microfibrils to elastin and elastic fibres. Pathol Biol. 2001; 49, 310–325.CrossRefGoogle ScholarPubMed
Peluso, G, García-Espinosa, V, Curcio, S, et al. High central aortic rather than brachial blood pressure is associated with carotid wall remodeling and increased arterial stiffness in childhood. High Blood Press Cardiovasc Prev. 2017; 24(1), 49–60.CrossRefGoogle Scholar
Barker, D. Chapter 8: Fetal origins of adult disease. In: Grace, F., Vivienne, N. (editors), Growing Up in the UK – Ensuring a Healthy Future for Our Children, pp. 149–168, 2013. BMA Board of Science. https://www.bma.org.uk/-/media/files/pdfs/working%20for%20change/improving%20health/child%20health/growingupinuk_may2013.pdf?la=en Google Scholar
Hanson, MA, Hawkins, P, Ozaki, T, et al. Effects of experimental dietary manipulation during early pregnancy on cardiovascular and endocrine function in fetal sheep. In: O’Brien, PMS, Wheeler, T,Barker, DJP (eds): Fetal Programming: Influences on Development and Disease in Later Life, pp. 365–373, 1999. RCOG Press: London.Google Scholar
Bloomfield, FH, Oliver, MH, Harding, JE. The late effects of fetal growth patterns. Arch Dis Child Fetal Neonatal Ed. 2006; 91(4), F299—F304.CrossRefGoogle ScholarPubMed
Hoet, JJ, Hanson, MA. Intrauterine nutrition: its importance during critical periods for cardiovascular and endocrine development. J Physiol. 1999; 514(Pt 3), 617–627.CrossRefGoogle ScholarPubMed
Barry, J, Anthony, R. The pregnant sheep as a model for human pregnancy. Theriogenology. 2008; 69(1), 55–67.CrossRefGoogle ScholarPubMed
Bia, D, Zócalo, Y, Armentano, R, et al. Increased reversal and oscillatory shear stress cause smooth muscle contraction-dependent changes in sheep aortic dynamics: role in aortic balloon pump circulatory support. Acta Physiol (Oxf). 2008; 192(4), 487–503.CrossRefGoogle ScholarPubMed
Bia, D, Zócalo, Y, Wray, S, Cabrera-Fischer, EI. Comparative in vivo analysis of the role of the adventitia and the endothelium on arterial mechanical function: relevance for aortic counterpulsation. Int J Artif Organs. 2017; 40(6), 286–293.CrossRefGoogle ScholarPubMed
Dasinger, JH, Alexander, BT. Gender differences in developmental programming of cardiovascular diseases. Clin Sci (Lond). 2016; 130(5), 337–348.CrossRefGoogle ScholarPubMed
Fall, CH. Fetal malnutrition and long-term outcomes. Nestle Nutr Inst Workshop Ser. 2013; 74, 11–25.CrossRefGoogle ScholarPubMed
Limones, M, Sevillano, J, Sánchez-Alonso, MG, Herrera, E, Ramos-Álvarez, MDP. Metabolic alterations associated with maternal undernutrition during the first half of gestation lead to a diabetogenic state in the rat. Eur J Nutr. 2018. doi: 10.1007/s00394-018-1805-z.Google Scholar
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