Skip to main content
SpringerLink
Log in

Influence of starvation on heart contractility and corticosterone level in rats

  • Organ physiology
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

The physiological changes, including cardiac modification, that occur during starvation are not yet completely understood. The purpose of this study is to examine the effects of a 2-week starvation period on heart contractility, muscle mass, and irisin and corticosterone levels in rats. Rats in the starved group showed a significant reduction in the body, heart, kidney, and muscle weight (n = 23, p < 0.05). Blood glucose, total protein, and albumin showed a 44, 17.5, and 10.3 % reduction, respectively (p < 0.05). Lipid reserves, such as total lipid, triglyceride, and free fatty acid, were also comparably reduced (p < 0.05). However, the bilirubin, creatinine, blood urea nitrogen, and creatine kinase levels were higher than in the control group (p < 0.05). The blood irisin level was unchanged, but the stress-related corticosterone level was significantly higher in the starved group. The differences observed in M-mode echocardiography were further compared with the body-weight-matched control group. Starvation reduced the left ventricle mass; however, this difference was not significant compared with the body-weight-matched group (p > 0.05). In the starvation group, the impairment of cardiac output was dependent on the reduction in stroke volume and heart rate. Starvation induced a severe reduction in ejection fraction and fractional shortening when compared with the body-weight-matched control group (p < 0.05). In summary, prolonged starvation, which leads to a deficiency of available nutrition, increases the stress-related corticosterone level, impairs the cardiac output, and is associated with changes in cardiac morphogeometry.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

References

  1. Abraham J, Abraham TP (2009) The role of echocardiography in hemodynamic assessment in heart failure. Heart Fail Clin 5(2):191–208

    Article  PubMed  Google Scholar 

  2. Andrews MH, Wood SA, Windle RJ, Lightman SL, Ingram CD (2012) Acute glucocorticoid administration rapidly suppresses basal and stress-induced hypothalamo-pituitary-adrenal axis activity. Endocrinology 153(1):200–211

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  3. Aronis KN, Moreno M, Polyzos SA, Moreno-Navarrete JM, Ricart W, Delgado E, de la Hera J, Sahin-Efe A, Chamberland JP, Berman R, Spiro Iii A, Vokonas P, Fernandez-Real JM, Mantzoros CS (2013) Circulating irisin levels and coronary heart disease: association with future acute coronary syndrome and major adverse cardiovascular events. Int J Obes (Lond) 39(1):156–161

  4. Barbosa-Saldivar JL, Van Itallie TB (1979) Semistarvation: an overview of an old problem. Bull N Y Acad Med 55(8):774–797

    PubMed Central  CAS  PubMed  Google Scholar 

  5. Bergendahl M, Huhtaniemi I (1994) The time since castration influences the effects of short-term starvation on gonadotrophin secretion in male rats. J Endocrinol 143(2):209–219

    Article  CAS  PubMed  Google Scholar 

  6. Braun TP, Szumowski M, Levasseur PR, Grossberg AJ, Zhu X, Agarwal A, Marks DL (2014) Muscle atrophy in response to cytotoxic chemotherapy is dependent on intact glucocorticoid signaling in skeletal muscle. PLoS One 9(9):e106489

    Article  PubMed Central  PubMed  Google Scholar 

  7. Cahill GF Jr (2006) Fuel metabolism in starvation. Annu Rev Nutr 26:1–22

    Article  CAS  PubMed  Google Scholar 

  8. Casiero D, Frishman WH (2006) Cardiovascular complications of eating disorders. Cardiol Rev 14(5):227–231

    Article  PubMed  Google Scholar 

  9. Challet E, le Maho Y, Robin JP, Malan A, Cherel Y (1995) Involvement of corticosterone in the fasting-induced rise in protein utilization and locomotor activity. Pharmacol Biochem Behav 50(3):405–412

    Article  CAS  PubMed  Google Scholar 

  10. Cherel Y, Robin JP, Heitz A, Calgari C, Le Maho Y (1992) Relationships between lipid availability and protein utilization during prolonged fasting. J Comp Physiol B 162(4):305–313

    Article  CAS  PubMed  Google Scholar 

  11. Choi HY, Kim S, Park JW, Lee NS, Hwang SY, Huh JY, Hong HC, Yoo HJ, Baik SH, Youn BS, Mantzoros CS, Choi KM (2014) Implication of circulating irisin levels with brown adipose tissue and sarcopenia in humans. J Clin Endocrinol Metab 99(8):2778–2785

    Article  CAS  PubMed  Google Scholar 

  12. Cryer PE (2007) Hypoglycemia, functional brain failure, and brain death. J Clin Invest 117(4):868–870

  13. Dallman MF, Akana SF, Bhatnagar S, Bell ME, Choi S, Chu A, Horsley C, Levin N, Meijer O, Soriano LR, Strack AM, Viau V (1999) Starvation: early signals, sensors, and sequelae. Endocrinology 140(9):4015–4023

    CAS  PubMed  Google Scholar 

  14. De P, Roy SG, Kar D, Bandyopadhyay A (2011) Excess of glucocorticoid induces myocardial remodeling and alteration of calcium signaling in cardiomyocytes. J Endocrinol 209(1):105–114

    Article  CAS  PubMed  Google Scholar 

  15. Fuglset TS, Endestad T, Landro NI, Ro O (2015) Brain structure alterations associated with weight changes in young females with anorexia nervosa: a case series. Neurocase 21(2):169–177

  16. Gold AJ, Yaffe SR (1978) Effects of prolonged starvation on cardiac energy metabolism in the rat. J Nutr 108(3):410–416

    CAS  PubMed  Google Scholar 

  17. Goodman MN, McElaney MA, Ruderman NB (1981) Adaptation to prolonged starvation in the rat: curtailment of skeletal muscle proteolysis. Am J Physiol 241(4):E321–E327

    CAS  PubMed  Google Scholar 

  18. Goodman MN, Ruderman NB (1980) Starvation in the rat. I. Effect of age and obesity on organ weights, RNA, DNA, and protein. Am J Physiol 239(4):E269–E276

    CAS  PubMed  Google Scholar 

  19. Habold C, Foltzer-Jourdainne C, Le Maho Y, Lignot JH (2006) Intestinal apoptotic changes linked to metabolic status in fasted and refed rats. Pflugers Arch 451(6):749–759

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  20. Huh JY, Panagiotou G, Mougios V, Brinkoetter M, Vamvini MT, Schneider BE, Mantzoros CS (2012) FNDC5 and irisin in humans: I. Predictors of circulating concentrations in serum and plasma and II. mRNA expression and circulating concentrations in response to weight loss and exercise. Metabolism 61(12):1725–1738

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  21. Kaneda T, Makino S, Nishiyama M, Asaba K, Hashimoto K (2001) Differential neuropeptide responses to starvation with ageing. J Neuroendocrinol 13(12):1066–1075

    Article  CAS  PubMed  Google Scholar 

  22. Kjeldsen K, Everts ME, Clausen T (1986) Effects of semi-starvation and potassium deficiency on the concentration of [3H]ouabain-binding sites and sodium and potassium contents in rat skeletal muscle. Br J Nutr 56(3):519–532

    Article  CAS  PubMed  Google Scholar 

  23. Lee SR, Kim HK, Youm JB, Dizon LA, Song IS, Jeong SH, Seo DY, Ko KS, Rhee BD, Kim N, Han J (2012) Non-genomic effect of glucocorticoids on cardiovascular system. Pflugers Arch 464(6):549–559

    Article  CAS  PubMed  Google Scholar 

  24. Liepinsh E, Makrecka M, Kuka J, Makarova E, Vilskersts R, Cirule H, Sevostjanovs E, Grinberga S, Pugovics O, Dambrova M (2014) The heart is better protected against myocardial infarction in the fed state compared to the fasted state. Metabolism 63(1):127–136

    Article  CAS  PubMed  Google Scholar 

  25. Makino S, Nishiyama M, Asaba K, Gold PW, Hashimoto K (1998) Altered expression of type 2 CRH receptor mRNA in the VMH by glucocorticoids and starvation. Am J Physiol 275(4 Pt 2):R1138–R1145

    CAS  PubMed  Google Scholar 

  26. Mazurak N, Gunther A, Grau FS, Muth ER, Pustovoyt M, Bischoff SC, Zipfel S, Enck P (2013) Effects of a 48-h fast on heart rate variability and cortisol levels in healthy female subjects. Eur J Clin Nutr 67(4):401–406

    Article  CAS  PubMed  Google Scholar 

  27. McCue MD (2010) Starvation physiology: reviewing the different strategies animals use to survive a common challenge. Comp Biochem Physiol A Mol Integr Physiol 156(1):1–18

    Article  PubMed  Google Scholar 

  28. Nazarloo HP, Nishiyama M, Tanaka Y, Asaba K, Hashimoto K (2002) Down-regulation of corticotropin-releasing hormone receptor type 2beta mRNA expression in the rat cardiovascular system following food deprivation. Regul Pept 105(2):121–129

    Article  CAS  PubMed  Google Scholar 

  29. Olivares JL, Vazquez M, Fleta J, Moreno LA, Perez-Gonzalez JM, Bueno M (2005) Cardiac findings in adolescents with anorexia nervosa at diagnosis and after weight restoration. Eur J Pediatr 164(6):383–386

    Article  PubMed  Google Scholar 

  30. Opie LH (1992) Cardiac metabolism–emergence, decline, and resurgence. Part I. Cardiovasc Res 26(8):721–733

    Article  CAS  PubMed  Google Scholar 

  31. Park KH, Zaichenko L, Peter P, Davis CR, Crowell JA, Mantzoros CS (2014) Diet quality is associated with circulating C-reactive protein but not irisin levels in humans. Metabolism 63(2):233–241

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  32. Patel R, Bookout AL, Magomedova L, Owen BM, Consiglio GP, Shimizu M, Zhang Y, Mangelsdorf DJ, Kliewer SA, Cummins CL (2015) Glucocorticoids regulate the metabolic hormone FGF21 in a feed-forward loop. Mol Endocrinol 29(2):213–223

  33. Pointer E, Reisman R, Windham R, Murray L (2013) Starvation and the clinicopathologic abnormalities associated with starved dogs: a review of 152 cases. J Am Anim Hosp Assoc 49(2):101–107

    Article  PubMed  Google Scholar 

  34. Robin JP, Decrock F, Herzberg G, Mioskowski E, Le Maho Y, Bach A, Groscolas R (2008) Restoration of body energy reserves during refeeding in rats is dependent on both the intensity of energy restriction and the metabolic status at the onset of refeeding. J Nutr 138(5):861–866 [corrected]

    CAS  PubMed  Google Scholar 

  35. Samarel AM, Parmacek MS, Magid NM, Decker RS, Lesch M (1987) Protein synthesis and degradation during starvation-induced cardiac atrophy in rabbits. Circ Res 60(6):933–941

    Article  CAS  PubMed  Google Scholar 

  36. Schakman O, Kalista S, Barbe C, Loumaye A, Thissen JP (2013) Glucocorticoid-induced skeletal muscle atrophy. Int J Biochem Cell Biol 45(10):2163–2172

    Article  CAS  PubMed  Google Scholar 

  37. Scheer P, Sverakova V, Doubek J, Janeckova K, Uhrikova I, Svoboda P (2012) Basic values of M-mode echocardiographic parameters of the left ventricle in outbreed Wistar rats. Vet Med 57(1):42–52

    Google Scholar 

  38. Schocken DD, Holloway JD, Powers PS (1989) Weight loss and the heart. Effects of anorexia nervosa and starvation. Arch Intern Med 149(4):877–881

    Article  CAS  PubMed  Google Scholar 

  39. Seashore JH (1984) Nutritional support of children in the intensive care unit. Yale J Biol Med 57(2):111–134

    PubMed Central  CAS  PubMed  Google Scholar 

  40. Seo DY, Lee SR, Kim N, Ko KS, Rhee BD, Han J (2014) Humanized animal exercise model for clinical implication. Pflugers Arch 466(9):1673–1687

    Article  CAS  PubMed  Google Scholar 

  41. Skverchinskaia EA, Tavrovskaia TV, Novozhilov AV (2013) Na, K-ATPase activity of erythrocytes of rats during prolonged starvation. Zh Evol Biokhim Fiziol 49(2):144–152

    CAS  PubMed  Google Scholar 

  42. Turner N, Cooney GJ, Kraegen EW, Bruce CR (2014) Fatty acid metabolism, energy expenditure and insulin resistance in muscle. J Endocrinol 220(2):T61–T79

    Article  CAS  PubMed  Google Scholar 

  43. Urbina EM, Gidding SS, Bao W, Pickoff AS, Berdusis K, Berenson GS (1995) Effect of body size, ponderosity, and blood pressure on left ventricular growth in children and young adults in the bogalusa heart study. Circulation 91(9):2400–2406

    Article  CAS  PubMed  Google Scholar 

  44. Vazquez-Medina JP, Sonanez-Organis JG, Rodriguez R, Viscarra JA, Nishiyama A, Crocker DE, Ortiz RM (2013) Prolonged fasting activates Nrf2 in post-weaned elephant seals. J Exp Biol 216(Pt 15):2870–2878

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  45. von Haehling S, Anker SD (2014) Prevalence, incidence and clinical impact of cachexia: facts and numbers-update 2014. J Cachexia Sarcopenia Muscle 5(4):261–263

    Article  Google Scholar 

  46. Webb JG, Kiess MC, Chan-Yan CC (1986) Malnutrition and the heart. CMAJ 135(7):753–758

    PubMed Central  CAS  PubMed  Google Scholar 

  47. Wing SS, Goldberg AL (1993) Glucocorticoids activate the ATP-ubiquitin-dependent proteolytic system in skeletal muscle during fasting. Am J Physiol 264(4 Pt 1):E668–E676

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National Research Foundation of Korea (NRF) and the Korean government (MSIP) [2010–0020224 and 2012R1A2A1A03007595]. In addition, we give thanks to Samkwang Medical Laboratories (Seoul, Korea) for assistance in analyzing blood chemical profiling.

Author information

Authors and Affiliations

  1. National Research Laboratory for Mitochondrial Signaling, Department of Physiology, College of Medicine, Cardiovascular and Metabolic Disease Center, Inje University, Bokji-Ro 57, Busanjin-gu, Busan, 614-735, Republic of Korea

    Sung Ryul Lee, Tae Hee Ko, Hyoung Kyu Kim, Jubert Marquez, Kyung Soo Ko, Byoung Doo Rhee & Jin Han

Authors
  1. Sung Ryul Lee
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Tae Hee Ko
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hyoung Kyu Kim
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jubert Marquez
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kyung Soo Ko
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Byoung Doo Rhee
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jin Han
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Jin Han.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Lee, S.R., Ko, T.H., Kim, H.K. et al. Influence of starvation on heart contractility and corticosterone level in rats. Pflugers Arch - Eur J Physiol 467, 2351–2360 (2015). https://doi.org/10.1007/s00424-015-1701-9

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-015-1701-9

Keywords

Search

Navigation