Hostname: page-component-586b7cd67f-dlnhk Total loading time: 0 Render date: 2024-11-27T22:08:45.944Z Has data issue: false hasContentIssue false
  • English
  • Français

Postnatal undernutrition in mice causes cardiac arrhythmogenesis which is exacerbated when pharmacologically stressed

Part of: French DOHaD

Published online by Cambridge University Press:  12 April 2018

J. R. Visker Open the ORCID record for J. R. Visker [Opens in a new window]  and
D. P. Ferguson
J. R. Visker*
Affiliation:
Department of Kinesiology, Michigan State University, East Lansing, MI, USA
D. P. Ferguson
Affiliation:
Department of Kinesiology, Michigan State University, East Lansing, MI, USA
*
Address for correspondence: J. R. Visker, Department of Kinesiology, Michigan State University, 308 West Circle Drive Room 27S, East Lansing, MI, 48824, USA. E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Growth restriction caused by postnatal undernutrition increases risk for cardiovascular disease in adulthood with the potential to induce arrhythmogenesis. Thus, the purpose was to determine if undernutrition during development produced arrhythmias at rest and when stressed with dobutamine in adulthood. Mouse dams were fed (CON: 20% protein), or low-protein (LP: 8%) diet before mating. A cross-fostering model was used where pups nursed by dams fed LP diet in early [EUN; postnatal day (PN) 1–10], late (LUN; PN11–21) and whole (PUN; 1–21) phases of postnatal life. Weaned pups were switched to CON diets for the remainder of the study (PN80). At PN80, body composition (magnetic resonance imaging), and quantitative electrocardiogram (ECG) measurements were obtained under 1% isoflurane anesthesia. After baseline ECG, an IP injection (1.5 µg/g body weight) of dobutamine was administered and ECG repeated. Undernutrition significantly (P<0.05) reduced body weight in LUN (22.68±0.88 g) and PUN (19.96±0.32 g) but not in CON (25.05±0.96 g) and EUN (25.28±0.9207 g). Fat mass decreased in all groups compared with controls (CON: 8.00±1.2 g, EUN: 6.32±0.65 g, LUN: 5.11±1.1 g, PUN: 3.90±0.25 g). Lean mass was only significantly reduced in PUN (CON: 17.99±0.26 g, EUN: 17.78±0.39 g, LUN: 17.34±0.33 g, PUN: 15.85±0.28 g). Absolute heart weights were significantly less from CON, with PUN having the smallest. ECG showed LUN had occurrences of atrial fibrillation; EUN had increases of 1st degree atrioventricular block upon stimulation, and PUN had increased risk for ventricular depolarization arrhythmias. CON did not display arrhythmias. Undernutrition in early life resulted in ventricular arrhythmias under stressed conditions, but undernutrition occurring in later postnatal life there is an increased incidence of atrial arrhythmias.

Keywords

cardiovascular arrhythmiasDevelopmental Origins of Health and Diseasedevelopmental programming
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 9 , Issue 4: Themed Issue: French DOHaD , August 2018 , pp. 417 - 424
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2018 

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. Mozaffarian, D, Benjamin, EJ, Go, AS, et al. Heart disease and stroke statistics-2016 update: a report from the American Heart Association. Circulation. 2016; 133, e38–360.Google Scholar
2. Barker, DJ. The fetal origins of coronary heart disease. Acta Paediatr Suppl. 1997; 422, 78–82.Google Scholar
3. Barker, DJ. In utero programming of cardiovascular disease. Theriogenology. 2000; 53, 555–574.Google Scholar
4. Barker, DJ. The origins of the developmental origins theory. J Intern Med. 2007; 261, 412–417.Google Scholar
5. Thornburg, KL. The programming of cardiovascular disease. J Dev Orig Health Dis. 2015; 6, 366–376.Google Scholar
6. Feltes, BC, de Faria Poloni, J, Bonatto, D. The developmental aging and origins of health and disease hypotheses explained by different protein networks. Biogerontology. 2011; 12, 293–308.Google Scholar
7. Barker, DJ, Winter, PD, Osmond, C, Margetts, B, Simmonds, SJ. Weight in infancy and death from ischaemic heart disease. Lancet. 1989; 2, 984–985.Google Scholar
8. Ritchey, MD, Loustalot, F, Bowman, BA, Hong, Y. Trends in mortality rates by subtypes of heart disease in the United States, 2000–2010. JAMA. 2014; 312, 2037–2039.Google Scholar
9. Fall, CH, Barker, DJ, Osmond, C, et al. Relation of infant feeding to adult serum cholesterol concentration and death from ischaemic heart disease. BMJ. 1992; 304, 801–805.Google Scholar
10. Wells, JC. Environmental quality, developmental plasticity and the thrifty phenotype: a review of evolutionary models. Evol Bioinform Online. 2007; 3, 109–120.Google Scholar
11. Louey, S, Jonker, SS, Giraud, GD, Thornburg, KL. Placental insufficiency decreases cell cycle activity and terminal maturation in fetal sheep cardiomyocytes. J Physiol. 2007; 580, 639–648.Google Scholar
12. Morton, M, Tsang, H, Hohimer, R, et al. Left ventricular size, output, and structure during guinea pig pregnancy. Am J Physiol. 1984; 246, R40–48.Google Scholar
13. Black, RE, Victoria, CG, Walker, SP, et al. Maternal and child undernutrition and overweight in low-income and middle-income countries. Lancet. 2013; 382, 427–451.Google Scholar
14. 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, 871–881.Google Scholar
15. Ferguson, DP, Dangott, LJ, Schmitt, EE, Vellers, HL, Lightfoot, JT. Differential skeletal muscle proteome of high- and low-active mice. J Appl Physiol (1985). 2014; 116, 1057–1067.Google Scholar
16. Taffet, GE, Tate, CA. CaATPase content is lower in cardiac sarcoplasmic reticulum isolated from old rats. Am J Physiol. 1993; 264, H1609–H1614.Google Scholar
17. Taffet, GE, Pham, TT, Bick, DL, et al. The calcium uptake of the rat heart sarcoplasmic reticulum is altered by dietary lipid. J Membr Biol. 1993; 131, 35–42.Google Scholar
18. Baum, M, Ortiz, L, Quan, A. Fetal origins of cardiovascular disease. Curr Opin Pediatr. 2003; 15, 166–170.Google Scholar
19. Skilton, MR, Phang, M. From the α to the ω-3: breaking the link between impaired fetal growth and adult cardiovascular disease. Nutrition. 2016; 32, 725–731.Google Scholar
20. Hannan, RD, Jenkins, A, Jenkins, AK, Brandenburger, Y. Cardiac hypertrophy: a matter of translation. Clin Exp Pharmacol Physiol. 2003; 30, 517–527.Google Scholar
21. Fenske, S, Probstle, R, Auer, F, et al. Comprehensive multilevel in vivo and in vitro analysis of heart rate fluctuations in mice by ECG telemetry and electrophysiology. Nat Protoc. 2016; 11, 61–86.Google Scholar
22. SC, W. A practical approach to using mice in atherosclerosis research. Clin Biochem Rev. 2004; 25, 81–93.Google Scholar
23. Mongue-Din, H, Salmon, A, Fiszman, MY, Fromes, Y. Non-invasive restrained ECG recording in conscious small rodents: a new tool for cardiac electrical activity investigation. Pflugers Arch. 2007; 454, 165–171.Google Scholar
24. Drenckhahn, JD, Schwarz, QP, Gray, S, et al. Compensatory growth of healthy cardiac cells in the presence of diseased cells restores tissue homeostasis during heart development. Dev Cell. 2008; 15, 521–533.Google Scholar
25. Drenckhahn, JD, Strasen, J, Heinecke, K, et al. Impaired myocardial development resulting in neonatal cardiac hypoplasia alters postnatal growth and stress response in the heart. Cardiovasc Res. 2015; 106, 43–54.Google Scholar
26. Boiten, HJ, van Domburg, RT, Geleijnse, ML, et al. Cardiac stress imaging for the prediction of very long-term outcomes: dobutamine stress echocardiography or dobutamine (99m)Tc-sestamibi SPECT? J Nucl Cardiol. 2016; https://doi.org/10.1007/s12350-016-0521-4.Google Scholar
27. Cortigiani, L, Sorbo, S, Miccoli, M, et al. Prognostic value of cardiac power output to left ventricular mass in patients with left ventricular dysfunction and dobutamine stress echo negative by wall motion criteria. Eur Heart J Cardiovasc Imaging. 2016; 18, 153–158.Google Scholar
28. Henri, C, Piérard, LA, Lancellotti, P, et al. Exercise testing and stress imaging in valvular heart disease. Can J Cardiol. 2014; 30, 1012–1026.Google Scholar
29. Kim, MN, Kim, SA, Kim, YH, et al. Head to head comparison of stress echocardiography with exercise electrocardiography for the detection of coronary artery stenosis in women. J Cardiovasc Ultrasound. 2016; 24, 135–143.Google Scholar
30. Standbridge, K, Reyes, E. The role of pharmacological stress testing in women. J Nucl Cardiol. 2016; 23, 997–1007.Google Scholar
31. Fiorotto, ML, Davis, TA, Sosa, HA, et al. Ribosome abundance regulates the recovery of skeletal muscle protein mass upon recuperation from postnatal undernutrition in mice. J Physiol. 2014; 592, 5269–5286.Google Scholar
32. Reeves, PG, Nielsen, FH, Fahey, GC Jr. 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, 1939–1951.Google Scholar
33. Sampson, DA, Hunsaker, HA, Jansen, GR. Dietary protein quality, protein quantity and food intake: effects on lactation and on protein synthesis and tissue composition in mammary tissue and liver in rats. J Nutr. 1986; 116, 365–375.Google Scholar
34. Grimble, RF, Mansaray, YK. Effects in rats of dietary protein inadequacy on lactose production, milk volume and components of the lactose synthetase complex (EC 2.4.1.22). Ann Nutr Metab. 1987; 31, 179–184.Google Scholar
35. Crnic, LS, Chase, HP. Models of infantile undernutrition in rats: effects on milk. J Nutr. 1978; 108, 1755–1760.Google Scholar
36. Grigor, MR, Allan, JE, Carrington, JM, et al. Effect of dietary protein and food restriction on milk production and composition, maternal tissues and enzymes in lactating rats. J Nutr. 1987; 117, 1247–1258.Google Scholar
37. Pine, AP, Jessop, NS, Oldham, JD. Maternal protein reserves and their influence on lactational performance in rats. J Nutr. 1994; 71, 13–27.Google Scholar
38. Mueller, AJ, Cox, WM Jr. The effect of changes in diet on the volume and composition of rat milk. J Nutr. 1946; 31, 249–259.Google Scholar
39. Lim, K, Zimanyi, MA, Black, MJ. Effect of maternal protein restriction in rats on cardiac fibrosis and capillarization in adulthood. Pediatr Res. 2006; 60, 83–87.Google Scholar
40. Ferguson, DP, Dangott, LJ, Vellers, HL, Schmitt, EE, Lightfoot, JT. Differential protein expression in the nucleus accumbens of high and low active mice. Behav Brain Res. 2015; 291, 283–288.Google Scholar
41. Berul, CI, Aronovitz, MJ, Wang, PJ, Mendelsohn, ME. In vivo cardiac electrophysiology studies in the mouse. Circulation. 1996; 94, 2641–2648.Google Scholar
42. Zwanenburg, A, Jellema, RK, Jennekens, W, et al. Heart rate-mediated blood pressure control in preterm fetal sheep under normal and hypoxic-ischemic conditions. Pediatr Res. 2013; 73, 420–426.Google Scholar
43. Álvarez-García, J, Vives-Borras, M, Gomis, P, et al. Electrophysiological effects of selective atrial coronary artery occlusion in humans. Circulation. 2016; 133, 2235–2242.Google Scholar
44. Han, Y, Jing, J, Tian, F, et al. ST elevation acute myocardial infarction accelerates non-culprit coronary lesion atherosclerosis. Int J Cardiovac Imaging. 2014; 30, 253–261.Google Scholar
45. Gouma, E, Simos, Y, Verginadis, I, et al. A simple procedure for estimation of total body surface area and determination of a new value of Meeh’s constant in rats. Lab Anim. 2012; 46, 40–45.Google Scholar
46. Byers, SL, Wiles, MV, Dunn, SL, Taft, RA. Mouse estrous cycle identification tool and images. PLoS One. 2012; 7, e35538.Google Scholar
47. Matthews, PA, Sameulsson, AM, Seed, P, et al. Fostering in mice induces cardiovascular and metabolic dysfunction in adulthood. J Physiol. 2011; 589, 3869–3881.Google Scholar
48. Botting, KJ, Wang, KC, Padhee, M, et al. Early origins of heart disease: low birth weight and determinants of cardiomyocyte endowment. Clin Exp Pharmacol Physiol. 2012; 39, 814–823.Google Scholar
49. Dusick, AM, Poindexter, BB, Ehrenkranz, RA, Lemons, JA. Growth failure in the preterm infant: can we catch up? Semin Perinatol. 2003; 27, 302–310.Google Scholar
50. Woo, M, Isganaitis, E, Fitzpatrick, C, et al. Early life nutrition modulates muscle stem cell number: implications for muscle mass and repair. Stem Cells Dev. 2011; 20, 1763–1769.Google Scholar
51. Wang, J, Li, D, Dangott, LJ, Wu, G. Proteomics and its role in nutrition research. J Nutr. 2006; 136, 1759–1762.Google Scholar
52. Wei, L, Taffet, GE, Khoury, DS, et al. Disruption of Rho signaling results in progressive atrioventricular conduction defects while ventricular function remains preserved. FASEB. 2004; 18, 857–859.Google Scholar
53. Yagi, S, Akaike, M, Aihara, K, et al. Endothelial nitric oxide synthase-independent protective action of statin against angiotensin II-induced atrial remodeling via reduced oxidant injury. Hypertension. 2010; 55, 918–923.Google Scholar
54. Jansen, HJ, Moghtadaei, M, Mackasey, M, et al. Atrial structure, function and arrhythmogenesis in aged and frail mice. Sci Rep. 2017; 7, 44336.Google Scholar
55. Allessie, MA, Konings, K, Kirchhof, CJ, Wijffels, M. Electrophysiologic mechanisms of perpetuation of atrial fibrillation. Am J Cardiol. 1996; 77, 10A–23A.Google Scholar
56. Devkota, A, Bakhit, A, Dufresne, A, et al. Arrhythmias and electrocardiographic changes in systolic heart failure. N Am J Med Sci. 2017; 8, 171–174.Google Scholar
57. Friedrichs, GS. Experimental models of atrial fibrillation/flutter. J Pharmacol Toxicol Methods. 2000; 43, 117–123.Google Scholar
58. Ozcan, C, Battaglia, E, Young, R, Suzuki, G. LKB1 knockout mouse develops spontaneous atrial fibrillation and provides mechanistic insights into human disease process. J Am Heart Assoc. 2015; 4, e001733.Google Scholar
59. Zhang, Q, Timofeyev, V, Lu, L, et al. Functional roles of a Ca2+-activated K+ channel in atrioventricular nodes. Circ Res. 2008; 102, 465–471.Google Scholar
60. van der Hooft, CS, Heeringa, J, van Herpen, G, et al. Drug-induced atrial fibrillation. J Am Coll Cardiol. 2004; 44, 2117–2124.Google Scholar
61. Velasco, A, Stirrup, Reyes E, Hage, FG. Guidelines in review: Comparison between AHA/ACC and ESC guidelines for the management of patients with ventricular arrhythmias and the prevention of sudden cardiac death. J Nucl Cardiol. 2017; 24, 1893–1901.Google Scholar
62. Iyer, V, Roman-Campos, D, Sampson, KJ, et al. Purkinje cells as sources of arrhythmias in long QT syndrome type 3. Sci Rep. 2017; 5, 13287.Google Scholar
63. Hamaguchi, S, Kawakami, Y, Honda, Y, et al. Developmental changes in excitation-contraction mechanisms of the mouse ventricular myocardium as revealed by functional and confocal imaging analyses. J Pharmacol Sci. 2013; 123, 167–175.Google Scholar