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Sodium overload during postnatal phases impairs diastolic function and exacerbates reperfusion arrhythmias in adult rats

Published online by Cambridge University Press:  09 May 2024

Marina Conceição dos Santos Moreira
Affiliation:
Department of Academic Areas, Federal Institute of Education, Science, and Technology of Goiás, Formosa, Brazil
Allancer Divino de Carvalho Nunes
Affiliation:
Institute on the Biology of Aging and Metabolism, University of Minnesota, Minneapolis, MN, USA
Paulo Ricardo Lopes
Affiliation:
Department of Physiological Science, Biological Sciences Institute, Federal University of Goiás, Goiânia, Brazil
Cintia do Carmo Silva
Affiliation:
Department of Physiological Science, Biological Sciences Institute, Federal University of Goiás, Goiânia, Brazil
Stefanne Madalena Marques
Affiliation:
Department of Physiological Science, Biological Sciences Institute, Federal University of Goiás, Goiânia, Brazil
Lara Marques Naves
Affiliation:
Department of Physiological Science, Biological Sciences Institute, Federal University of Goiás, Goiânia, Brazil
Matheus Lobo Perez Dias
Affiliation:
Department of Physiological Science, Biological Sciences Institute, Federal University of Goiás, Goiânia, Brazil
Fernanda Cristina Alcântara Santos
Affiliation:
Department of Histology, Embryology, and Cell Biology, Federal University of Goiás, Goiânia, Brazil
Rodrigo Mello Gomes
Affiliation:
Department of Physiological Science, Biological Sciences Institute, Federal University of Goiás, Goiânia, Brazil
Carlos Henrique Xavier
Affiliation:
Department of Physiological Science, Biological Sciences Institute, Federal University of Goiás, Goiânia, Brazil
Carlos Henrique de Castro
Affiliation:
Department of Physiological Science, Biological Sciences Institute, Federal University of Goiás, Goiânia, Brazil
Gustavo Rodrigues Pedrino*
Affiliation:
Department of Physiological Science, Biological Sciences Institute, Federal University of Goiás, Goiânia, Brazil
*
Corresponding author: G. R. Pedrino; Email: pedrino@ufg.br

Abstract

Sodium overload during childhood impairs baroreflex sensitivity and increases arterial blood pressure and heart rate in adulthood; these effects persist even after high-salt diet (HSD) withdrawal. However, the literature lacks details on the effects of HSD during postnatal phases on cardiac ischemia/reperfusion responses in adulthood. The current study aimed to elucidate the impact of HSD during infancy adolescence on isolated heart function and cardiac ischemia/reperfusion responses in adulthood. Male 21-day-old Wistar rats were treated for 60 days with hypertonic saline solution (NaCl; 0.3M; experimental group) or tap water (control group). Subsequently, both groups were maintained on a normal sodium diet for 30 days. Subsequently, the rats were euthanized, and their hearts were isolated and perfused according to the Langendorff technique. After 30 min of the basal period, the hearts were subjected to 20 min of anoxia, followed by 20 min of reperfusion. The basal contractile function was unaffected by HSD. However, HSD elevated the left ventricular end-diastolic pressure during reperfusion (23.1 ± 5.2 mmHg vs. 11.6 ± 1.4 mmHg; p < 0.05) and increased ectopic incidence period during reperfusion (208.8 ± 32.9s vs. 75.0 ± 7.8s; p < 0.05). In conclusion, sodium overload compromises cardiac function after reperfusion events, diminishes ventricular relaxation, and increases the severity of arrhythmias, suggesting a possible arrhythmogenic effect of HSD in the postnatal phases.

Type
Original Article
Copyright
© The Author(s), 2024. Published by Cambridge University Press in association with The International Society for Developmental Origins of Health and Disease (DOHaD)

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References

Roth, GA, Huffman, MD, Moran, AE, et al. Global and regional patterns in cardiovascular mortality from 1990 to 2013. Circulation. 2015; 132(17), 16671678.CrossRefGoogle ScholarPubMed
WHO. Global Action Plan for The Prevention and Control of Noncommunicable Diseases 2013-2020, 2013. World Health Organization. ISBN: 978-92-4-150623-6. https://www.who.int/southeastasia/publications-detail/9789241506236 Google Scholar
Kalogeris, T, Baines, CP, Krenz, M, Korthuis, RJ. Cell biology of ischemia/Reperfusion injury. Int Rev Cell Mol Biol. 2012; 298, 229317.CrossRefGoogle ScholarPubMed
Rout, A, Tantry, US, Novakovic, M, Sukhi, A, Gurbel, PA. Targeted pharmacotherapy for ischemia reperfusion injury in acute myocardial infarction. Expert Opin Pharmacother. 2020; 21(15), 18511865.CrossRefGoogle ScholarPubMed
del Monte, F, Lebeche, D, Guerrero, JL, et al. Abrogation of ventricular arrhythmias in a model of ischemia and reperfusion by targeting myocardial calcium cycling. Proc Nat Acad Sci. 2004; 101, 56225627.CrossRefGoogle Scholar
Jong, S, van Veen, TAB, van Rijen, HVM, de Bakker, JMT. Fibrosis and cardiac arrhythmias. J Cardiovasc Pharmacol. 2011; 57(6), 630638.CrossRefGoogle ScholarPubMed
Ten Tusscher, KHWJ, Panfilov, AV. Influence of diffuse fibrosis on wave propagation in human ventricular tissue. EP Eur. 2007; 9(suppl_6), vi38vi45.Google ScholarPubMed
Coronel, R, Casini, S, Koopmann, TT, et al. Right ventricular fibrosis and conduction delay in a patient with clinical signs of brugada syndrome. Circulation. 2005; 112(18), 27692777.CrossRefGoogle Scholar
Whaley-Connell, AT, Habibi, J, Aroor, A, et al. Salt loading exacerbates diastolic dysfunction and cardiac remodeling in young female Ren2 rats. Metabolis. 2013; 62(12), 17611771.CrossRefGoogle ScholarPubMed
Gao, F, Han, Z-Q, Zhou, X, et al. High salt intake accelerated cardiac remodeling in spontaneously hypertensive rats: time window of left ventricular functional transition and its relation to salt-loading doses. Clin Exp Hypertens. 2011; 33(7), 492499.CrossRefGoogle ScholarPubMed
Mozaffari, MS, Patel, C, Ballas, C, Schaffer, SW. Effects of excess salt and fat intake on myocardial function and infarct size in rat. Life Sci. 2006; 78(16), 18081813.CrossRefGoogle ScholarPubMed
Costa, APR, de Paula, RCS, Carvalho, GF, et al. High sodium intake adversely affects oxidative-inflammatory response, cardiac remodelling and mortality after myocardial infarction. Atherosclerosis. 2012; 222(1), 284291.CrossRefGoogle ScholarPubMed
Cohen, HW, Hailpern, SM, Fang, J, Alderman, MH. Sodium intake and mortality in the NHANES II follow-up study. Am J Med. 2006; 119(3), 275.e7275.e14.CrossRefGoogle ScholarPubMed
Aiello, EA, Jabr, RI, Cole, WC. Arrhythmia and delayed recovery of cardiac action potential during reperfusion after ischemia. Role of oxygen radical-induced no-reflow phenomenon. Circ Res. 1995; 77(1), 153162.CrossRefGoogle ScholarPubMed
Kukreja, RC, Hess, ML. The oxygen free radical system: from equations through membrane-protein interactions to cardiovascular injury and protection. Cardiovasc Res. 1992; 26(7), 641655.CrossRefGoogle ScholarPubMed
Moore, AM, Fisher, JO, Morris, KS, Croce, CM, Paluch, RA, Kong, KL. Frequency of sweet and salty snack food consumption is associated with higher intakes of overconsumed nutrients and weight-for-length z-scores during infancy and toddlerhood. J Acad Nutr Diet. 2022; 122(8), 15341542.CrossRefGoogle ScholarPubMed
Roess, AA, Jacquier, EF, Catellier, DJ, et al. Food consumption patterns of infants and toddlers: findings from the feeding infants and toddlers study (FITS) 2016. J Nutr. 2018; 148, 1525S1535S.CrossRefGoogle ScholarPubMed
Lava, SAG, Bianchetti, MG, Simonetti, GD. Salt intake in children and its consequences on blood pressure. Pediatr Nephrol. 2015; 30(9), 13891396.CrossRefGoogle ScholarPubMed
He, FJ, MacGregor, GA. Importance of salt in determining blood pressure in children: meta-analysis of controlled trials. Hypertension. 2006; 48(5), 861869.CrossRefGoogle ScholarPubMed
Langley-Evans, SC, McMullen, S. Developmental origins of adult disease. Med Princ Pract. 2010; 19(2), 8798.CrossRefGoogle ScholarPubMed
Moreira, MCS, da Silva, EF, Silveira, LL, et al. High sodium intake during postnatal phases induces an increase in arterial blood pressure in adult rats. Brit J Nutr. 2014; 112(12), 19231932.CrossRefGoogle ScholarPubMed
Reeves, PG, Nielsen, FH, Fahey, GC. AIN-93 purified diets for laboratory rodents: final report of the American institute of nutrition ad hoc writing committee on the reformulation of the AIN-76A rodent diet. J Nutr. 1993; 123(11), 19391951.CrossRefGoogle Scholar
Neely, JR, Liebermeister, H, Battersby, EJ, Morgan, HE. Effect of pressure development on oxygen consumption by isolated rat heart. American Journal of Physiology-Legacy Content. 1967; 212(4), 804814.CrossRefGoogle ScholarPubMed
Lesnefsky, EJ, Moghaddas, S, Tandler, B, Kerner, J, Hoppel, CL. Mitochondrial dysfunction in cardiac disease: ischemia-reperfusion, aging, and heart failure. J Mol Cell Cardiol. 2001; 33(6), 10651089.CrossRefGoogle ScholarPubMed
Ferreira, AJ, Santos, RAS, Almeida, AP. Angiotensin-(1-7): cardioprotective effect in myocardial ischemia/Reperfusion. Hypertension. 2001; 38(3), 665668.CrossRefGoogle ScholarPubMed
Frey, N, Olson, EN. Cardiac hypertrophy: the good, the bad, and the ugly. Annu Rev Physiol. 2003; 65(1), 4579.CrossRefGoogle ScholarPubMed
Weibel, ER. Principles and methods for the morphometric study of the lung and other organs. Lab Invest. 1963; 12, 131155.Google ScholarPubMed
Abdalla, AM, Tingari, MD, Abdalla, MA. Histomorphometric parameters of normal full term placenta of Sudanese women. Heliyon. 2016; 2(7), e00135.CrossRefGoogle ScholarPubMed
Costa, JR, Campos, MS, Lima, RF, et al. Endocrine-disrupting effects of methylparaben on the adult gerbil prostate. Environ Toxicol. 2017; 32(6), 18011812.CrossRefGoogle ScholarPubMed
do Carmo e Silva, C, de Almeida, JFQ, Macedo, LM, et al. Mas receptor contributes to pregnancy-induced cardiac remodelling. Clin Sci. 2016; 130(24), 23052316.CrossRefGoogle ScholarPubMed
Taboga, SR, Vidal, Bde C. Collagen fibers in human prostatic lesions: histochemistry and anisotropies. J Submicrosc Cytol Pathol. 2003; 35(1), 1116.Google ScholarPubMed
Funtikova, AN, Navarro, E, Bawaked, RA, Fíto, M, Schröder, H. Impact of diet on cardiometabolic health in children and adolescents. Nutr J. 2015; 14(1), 118. DOI: 10.1186/s12937-015-0107-z.CrossRefGoogle ScholarPubMed
Honicky, M, Cardoso, SM, Kunradi Vieira, FG, et al. Ultra-processed food intake is associated with children and adolescents with congenital heart disease clustered by high cardiovascular risk factors. Br J Nutr. 2022; 129(7), 11631171.CrossRefGoogle Scholar
Störk, T, Möckel, M, Danne, O, et al. Left ventricular hypertrophy and diastolic dysfunction: their relation to coronary heart disease. Cardiovasc Drugs Ther. 1995; 9(S3), 533537.CrossRefGoogle ScholarPubMed
LeGrice, IJ, Pope, AJ, Sands, GB, et al. Progression of myocardial remodeling and mechanical dysfunction in the spontaneously hypertensive rat. Am J Physiol-HEART C. 2012; 303(11), H1353H1365.CrossRefGoogle ScholarPubMed
Matsui, H, Ando, K, Kawarazaki, H, et al. Salt excess causes left ventricular diastolic dysfunction in rats with metabolic disorder. Hypertension. 2008; 52(2), 287294.CrossRefGoogle ScholarPubMed
Tzemos, N, Lim, PO, Wong, S, Struthers, AD, MacDonald, TM. Adverse cardiovascular effects of acute salt loading in young normotensive individuals. Hypertension. 2008; 51(6), 15251530.CrossRefGoogle ScholarPubMed
Iwamoto, T, Kita, S. Na+/Ca2+ exchanger, and Na+, K+-ATPase. Hypertension. 2006; 69, 21482154.Google ScholarPubMed
Güler, MC, Tanyeli, A, Ekinci Akdemir, FN, et al. An overview of ischemia-reperfusion injury: review on oxidative stress and inflammatory response. Eurasian J Med. 2022; 54(Suppl1), S62S65.CrossRefGoogle ScholarPubMed
Perrelli, MG, Pagliaro, P, Penna, C. Ischemia/reperfusion injury and cardioprotective mechanisms: role of mitochondria and reactive oxygen species. World J Cardiol. 2011; 3(6), 186200.CrossRefGoogle ScholarPubMed
Wagner, S, Rokita, AG, Anderson, ME, Maier, LS. Redox regulation of sodium and calcium handling. Antioxid Redox Signal. 2013; 18(9), 10631077.CrossRefGoogle ScholarPubMed
Kong, P, Christia, P, Frangogiannis, NG. The pathogenesis of cardiac fibrosis. Cell Mol Life Sci. 2014; 71(4), 549574.CrossRefGoogle ScholarPubMed
Li, J-Y, Zhang, S-L, Ren, M, Wen, Y-L, Yan, L, Cheng, H. High-sodium intake aggravates myocardial injuries induced by aldosterone via oxidative stress in Sprague-Dawley rats. Acta Pharmacol Sin. 2012; 33(3), 393400.CrossRefGoogle ScholarPubMed
Vulin, M, Muller, A, Drenjančević, I, Šušnjara, P, Mihaljević, Z, Stupin, A. High dietary salt intake attenuates nitric oxide mediated endothelium-dependent vasodilation and increases oxidative stress in pregnancy. J Hypertens. 2024; 42(4), 672684.CrossRefGoogle ScholarPubMed
Yu, HCM, Burrell, LM, Black, MJ, et al. Salt induces myocardial and renal fibrosis in normotensive and hypertensive rats. Circulation. 1998; 98(23), 26212628.CrossRefGoogle ScholarPubMed
Brilla, CG, Janicki, JS, Weber, KT. Impaired diastolic function and coronary reserve in genetic hypertension. Role of interstitial fibrosis and medial thickening of intramyocardial coronary arteries. Circ Res. 1991; 69(1), 107115.CrossRefGoogle ScholarPubMed
Laurent, GJ. Dynamic state of collagen: pathways of collagen degradation in vivo and their possible role in regulation of collagen mass. Am J Physiol-CELL Ph. 1987; 252(1), C1C9.CrossRefGoogle ScholarPubMed
Collier, P, Watson, CJ, van Es, MH, et al. Getting to the heart of cardiac remodeling; how collagen subtypes may contribute to phenotype. J Mol Cell Cardiol. 2012; 52(1), 148153.CrossRefGoogle Scholar
Weber, KT, Brilla, CG, Janicki, JS. Myocardial fibrosis: functional significance and regulatory factors. Cardiovasc Res. 1993; 27(3), 341348.CrossRefGoogle ScholarPubMed
Baldo, MP, Teixeira, AKG, Rodrigues, SL, Mill, JG. Acute arrhythmogenesis after myocardial infarction in normotensive rats: influence of high salt intake. Food Chem Toxicol. 2012; 50(3-4), 473477.CrossRefGoogle ScholarPubMed
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