Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Original Article
  • Published:

Body composition, energy expenditure and physical activity

Body composition and body fat distribution are related to cardiac autonomic control in non-alcoholic fatty liver disease patients

European Journal of Clinical Nutrition volume 68, pages 241–246 (2014)Cite this article

Subjects

Abstract

Background/Objectives:

Heart rate recovery (HRR), a cardiac autonomic control marker, was shown to be related to body composition (BC), yet this was not tested in non-alcoholic fatty liver disease (NAFLD) patients. The aim of this study was to determine if, and to what extent, markers of BC and body fat (BF) distribution are related to cardiac autonomic control in NAFLD patients.

Subjects/Methods:

BC was assessed with dual-energy X-ray absorptiometry in 28 NAFLD patients (19 men, 51±13 years, and 9 women, 47±13 years). BF depots ratios were calculated to assess BF distribution. Subjects’ HRR was recorded 1 (HRR1) and 2 min (HRR2) immediately after a maximum graded exercise test.

Results:

BC and BF distribution were related to HRR; particularly weight, trunk BF and trunk BF-to-appendicular BF ratio showed a negative relation with HRR1 (r=−0.613, r=−0.597 and r=−0.547, respectively, P<0.01) and HRR2 (r=−0.484, r=−0.446, P<0.05, and r=−0.590, P<0.01, respectively). Age seems to be related to both HRR1 and HRR2 except when controlled for BF distribution. The preferred model in multiple regression should include trunk BF-to-appendicular BF ratio and BF to predict HRR1 (r2=0.549; P<0.05), and trunk BF-to-appendicular BF ratio alone to predict HRR2 (r2=0.430; P<0.001).

Conclusions:

BC and BF distribution were related to HRR in NAFLD patients. Trunk BF-to-appendicular BF ratio was the best independent predictor of HRR and therefore may be best related to cardiovascular increased risk, and possibly act as a mediator in age-related cardiac autonomic control variation.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Similar content being viewed by others

References

  1. Bellentani S, Saccoccio G, Masutti F, Croce LS, Brandi G, Sasso F et al. Prevalence of and risk factors for hepatic steatosis in Northern Italy. Ann Intern Med 2000; 132: 112–117.

    Article  CAS  PubMed  Google Scholar 

  2. Nomura H, Kashiwagi S, Hayashi J, Kajiyama W, Tani S, Goto M . Prevalence of fatty liver in a general population of Okinawa, Japan. Jpn J Med 1988; 27: 142–149.

    Article  CAS  PubMed  Google Scholar 

  3. Browning JD, Szczepaniak LS, Dobbins R, Nuremberg P, Horton JD, Cohen JC et al. Prevalence of hepatic steatosis in an urban population in the United States: impact of ethnicity. Hepatology 2004; 40: 1387–1395.

    Article  PubMed  Google Scholar 

  4. Clark JM . The epidemiology of nonalcoholic fatty liver disease in adults. J Clin Gastroenterol 2006; 40 (Suppl 1), S5–S10.

    PubMed  Google Scholar 

  5. Cortez-Pinto H, Moura MC, Day CP . Non-alcoholic steatohepatitis: from cell biology to clinical practice. J Hepatol 2006; 44: 197–208.

    Article  CAS  PubMed  Google Scholar 

  6. Angulo P . Nonalcoholic fatty liver disease. N Engl J Med 2002; 346: 1221–1231.

    Article  CAS  PubMed  Google Scholar 

  7. Targher G, Bertolini L, Padovani R, Rodella S, Zoppini G, Pichiri I et al. Prevalence of non-alcoholic fatty liver disease and its association with cardiovascular disease in patients with type 1 diabetes. J Hepatol 2010; 53: 713–718.

    Article  CAS  PubMed  Google Scholar 

  8. Rector RS, Thyfault JP, Uptergrove GM, Morris EM, Naples SP, Borengasser SJ et al. Mitochondrial dysfunction precedes insulin resistance and hepatic steatosis and contributes to the natural history of non-alcoholic fatty liver disease in an obese rodent model. J Hepatol 2010; 52: 727–736.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cote M, Mauriege P, Bergeron J, Almeras N, Tremblay A, Lemieux I et al. Adiponectinemia in visceral obesity: impact on glucose tolerance and plasma lipoprotein and lipid levels in men. J Clin Endocrinol Metab 2005; 90: 1434–1439.

    Article  CAS  PubMed  Google Scholar 

  10. Gnacinska M, Malgorzewicz S, Stojek M, Lysiak-Szydlowska W, Sworczak K . Role of adipokines in complications related to obesity: a review. Adv Med Sci 2009; 54: 150–157.

    Article  CAS  PubMed  Google Scholar 

  11. Imai K, Sato H, Hori M, Kusuoka H, Ozaki H, Yokoyama H et al. Vagally mediated heart rate recovery after exercise is accelerated in athletes but blunted in patients with chronic heart failure. J Am Coll Cardiol 1994; 24: 1529–1535.

    Article  CAS  PubMed  Google Scholar 

  12. Davrath LR, Akselrod S, Pinhas I, Toledo E, Beck A, Elian D et al. Evaluation of autonomic function underlying slow postexercise heart rate recovery. Med Sci Sports Exerc 2006; 38: 2095–2101.

    Article  PubMed  Google Scholar 

  13. Cole CR, Blackstone EH, Pashkow FJ, Snader CE, Lauer MS . Heart-rate recovery immediately after exercise as a predictor of mortality. N Engl J Med 1999; 341: 1351–1357.

    Article  CAS  PubMed  Google Scholar 

  14. Vivekananthan DP, Blackstone EH, Pothier CE, Lauer MS . Heart rate recovery after exercise is a predictor of mortality, independent of the angiographic severity of coronary disease. J Am Coll Cardiol 2003; 42: 831–838.

    Article  PubMed  Google Scholar 

  15. Diaz LA, Brunken RC, Blackstone EH, Snader CE, Lauer MS . Independent contribution of myocardial perfusion defects to exercise capacity and heart rate recovery for prediction of all-cause mortality in patients with known or suspected coronary heart disease. J Am Coll Cardiol 2001; 37: 1558–1564.

    Article  CAS  PubMed  Google Scholar 

  16. Arena R, Guazzi M, Myers J, Peberdy MA . Prognostic value of heart rate recovery in patients with heart failure. Am Heart J. 2006; 151: 851 e7–851.e13.

    Article  Google Scholar 

  17. Cheng YJ, Lauer MS, Earnest CP, Church TS, Kampert JB, Gibbons LW et al. Heart rate recovery following maximal exercise testing as a predictor of cardiovascular disease and all-cause mortality in men with diabetes. Diab Care 2003; 26: 2052–2057.

    Article  Google Scholar 

  18. Lipinski MJ, Vetrovec GW, Froelicher VF . Importance of the first two minutes of heart rate recovery after exercise treadmill testing in predicting mortality and the presence of coronary artery disease in men. Am J Cardiol 2004; 93: 445–449.

    Article  PubMed  Google Scholar 

  19. Chacko KM, Bauer TA, Dale RA, Dixon JA, Schrier RW, Estacio RO . Heart rate recovery predicts mortality and cardiovascular events in patients with type 2 diabetes. Med Sci Sports Exerc 2008; 40: 288–295.

    Article  PubMed  Google Scholar 

  20. Carnethon MR, Sternfeld B, Liu K, Jacobs DR Jr., Schreiner PJ, Williams OD et al. Correlates of heart rate recovery over 20 years in a healthy population sample. Med Sci Sports Exerc 2012; 44: 273–279.

    Article  PubMed  Google Scholar 

  21. Bray GA . Obesity, a disorder of nutrient partitioning: the MONA LISA hypothesis. J Nutr 1991; 121: 1146–1162.

    Article  CAS  PubMed  Google Scholar 

  22. Kim MK, Tanaka K, Kim MJ, Matsuo T, Tomita T, Ohkubo H et al. Epicardial fat tissue: relationship with cardiorespiratory fitness in men. Med Sci Sports Exerc 2010; 42: 463–469.

    Article  PubMed  Google Scholar 

  23. Esco MR, Williford HN, Olson MS . Skinfold thickness is related to cardiovascular autonomic control as assessed by heart rate variability and heart rate recovery. J Strength Cond Res 2011; 25: 2304–2310.

    Article  PubMed  Google Scholar 

  24. Kreier F, Kap YS, Mettenleiter TC, van Heijningen C, van der Vliet J, Kalsbeek A et al. Tracing from fat tissue, liver, and pancreas: a neuroanatomical framework for the role of the brain in type 2 diabetes. Endocrinology 2006; 147: 1140–1147.

    Article  CAS  PubMed  Google Scholar 

  25. Kizilbash MA, Carnethon MR, Chan C, Jacobs DR, Sidney S, Liu K . The temporal relationship between heart rate recovery immediately after exercise and the metabolic syndrome: the CARDIA study. Eur Heart J. 2006; 27: 1592–1596.

    Article  PubMed  Google Scholar 

  26. Christou DD, Jones PP, Pimentel AE, Seals DR . Increased abdominal-to-peripheral fat distribution contributes to altered autonomic-circulatory control with human aging. Am J Physiol Heart Circ Physiol 2004; 287: H1530–H1537.

    Article  CAS  PubMed  Google Scholar 

  27. Nilsson G, Hedberg P, Jonason T, Lonnberg I, Ohrvik J . Heart rate recovery is more strongly associated with the metabolic syndrome, waist circumference, and insulin sensitivity in women than in men among the elderly in the general population. Am Heart J. 2007; 154: 460. e1–e7.

    Article  Google Scholar 

  28. Kamel EG, McNeill G, Van Wijk MC . Usefulness of anthropometry and DXA in predicting intra-abdominal fat in obese men and women. Obes Res 2000; 8: 36–42.

    Article  CAS  PubMed  Google Scholar 

  29. Park YW, Heymsfield SB, Gallagher D . Are dual-energy X-ray absorptiometry regional estimates associated with visceral adipose tissue mass? Int J Obes Relat Metab Disord 2002; 26: 978–983.

    Article  PubMed  Google Scholar 

  30. Pimenta NM, Santa-Clara H, Sardinha LB, Fernhall B . Body fat responses to a 1-year combined exercise training program in male coronary artery disease patients. Obesity 2013; 21: 723–730.

    Article  PubMed  Google Scholar 

  31. Lohman TG, Roche AF, Martorell R . Anthropometric Standardization Reference Manual. Human Kinetics: Champaign, IL, USA, 1988.

    Google Scholar 

  32. Savgan-Gurol E, Bredella M, Russell M, Mendes N, Klibanski A, Misra M . Waist to hip ratio and trunk to extremity fat (DXA) are better surrogates for IMCL and for visceral fat respectively than for subcutaneous fat in adolescent girls. Nutr Metab (Lond) 2010; 7: 86.

    Article  Google Scholar 

  33. Ketel IJ, Volman MN, Seidell JC, Stehouwer CD, Twisk JW, Lambalk CB . Superiority of skinfold measurements and waist over waist-to-hip ratio for determination of body fat distribution in a population-based cohort of Caucasian Dutch adults. Eur J Endocrinol 2007; 156: 655–661.

    Article  CAS  PubMed  Google Scholar 

  34. Bruce RA . Exercise testing of patients with coronary heart disease. Principles and normal standards for evaluation. Ann Clin Res 1971; 3: 323–332.

    CAS  PubMed  Google Scholar 

  35. Howley ET, Bassett DR Jr., Welch HG . Criteria for maximal oxygen uptake: review and commentary. Med Sci Sports Exerc 1995; 27: 1292–1301.

    Article  CAS  PubMed  Google Scholar 

  36. Shetler K, Marcus R, Froelicher VF, Vora S, Kalisetti D, Prakash M et al. Heart rate recovery: validation and methodologic issues. J Am Coll Cardiol 2001; 38: 1980–1987.

    Article  CAS  PubMed  Google Scholar 

  37. Carnethon MR, Jacobs DR Jr, Sidney S, Sternfeld B, Gidding SS, Shoushtari C et al. A longitudinal study of physical activity and heart rate recovery: CARDIA, 1987-1993. Med Sci Sports Exerc 2005; 37: 606–612.

    Article  PubMed  Google Scholar 

  38. Cohen J, Cohen P . Applied Multiple Regression/Correlation Analysis for the Behavioral Sciences 2nd edn Lawrence Erkbaum Associates, Inc: Hillsdale, NJ, 1983, p 545.

    Google Scholar 

  39. Panzer C, Lauer MS, Brieke A, Blackstone E, Hoogwerf B . Association of fasting plasma glucose with heart rate recovery in healthy adults: a population-based study. Diabetes 2002; 51: 803–807.

    Article  CAS  PubMed  Google Scholar 

  40. Hargens TA, Guill SG, Zedalis D, Gregg JM, Nickols-Richardson SM, Herbert WG . Attenuated heart rate recovery following exercise testing in overweight young men with untreated obstructive sleep apnea. Sleep 2008; 31: 104–110.

    Article  PubMed  PubMed Central  Google Scholar 

  41. Chen MS, Blackstone EH, Pothier CE, Lauer MS . Heart rate recovery and impact of myocardial revascularization on long-term mortality. Circulation 2004; 110: 2851–2857.

    Article  PubMed  Google Scholar 

  42. Hadley DM, Dewey FE, Freeman JV, Myers JN, Froelicher VF . Prediction of cardiovascular death using a novel heart rate recovery parameter. Med Sci Sports Exerc 2008; 40: 1072–1079.

    Article  PubMed  Google Scholar 

  43. Myers J, Tan SY, Abella J, Aleti V, Froelicher VF . Comparison of the chronotropic response to exercise and heart rate recovery in predicting cardiovascular mortality. Eur J Cardiovasc Prev Rehabil 2007; 14: 215–221.

    Article  PubMed  Google Scholar 

  44. Nishime EO, Cole CR, Blackstone EH, Pashkow FJ, Lauer MS . Heart rate recovery and treadmill exercise score as predictors of mortality in patients referred for exercise ECG. JAMA 2000; 284: 1392–1398.

    Article  CAS  PubMed  Google Scholar 

  45. Horowitz JF . Adipose tissue lipid metabolism during exercise. In: Hargreaves M, Spriet L (eds). Exercise Metabolism. Human Kinetics: Champaign, IL, USA, 2006, pp 89–104.

    Google Scholar 

  46. Bartness TJ, Song CK . Thematic review series: adipocyte biology. Sympathetic and sensory innervation of white adipose tissue. J Lipid Res 2007; 48: 1655–1672.

    Article  CAS  PubMed  Google Scholar 

  47. Lafontan M, Berlan M . Fat cell adrenergic receptors and the control of white and brown fat cell function. J Lipid Res 1993; 34: 1057–1091.

    CAS  PubMed  Google Scholar 

  48. Bertin E, Marcus C, Ruiz JC, Eschard JP, Leutenegger M . Measurement of visceral adipose tissue by DXA combined with anthropometry in obese humans. Int J Obes Relat Metab Disord 2000; 24: 263–270.

    Article  CAS  PubMed  Google Scholar 

  49. Snijder MB, Visser M, Dekker JM, Seidell JC, Fuerst T, Tylavsky F et al. The prediction of visceral fat by dual-energy X-ray absorptiometry in the elderly: a comparison with computed tomography and anthropometry. Int J Obes Relat Metab Disord 2002; 26: 984–993.

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The present study was funded by the Centre for the Study of Human Performance, Portuguese Foundation for Science and Technology, Lisbon, Portugal.

Author information

Authors and Affiliations

  1. Exercise and Health Laboratory, Interdisciplinary Centre for the Study of Human Performance, Faculty of Human Kinetics, Technical University of Lisbon, Cruz-Quebrada, Portugal

    N M Pimenta, H Santa-Clara, M da Lapa Rosado, X Melo & L B Sardinha

  2. Physical Activity and Health MS, Sport Sciences School of Rio Maior, Polytechnic Institute of Santarém, Rio Maior, Portugal

    N M Pimenta

  3. Departamento de Gastrenterologia, Unidade de Nutrição e Metabolismo, IMM, FML, Hospital Universitário de Santa Maria, Lisbon, Portugal

    H Cortez-Pinto

  4. Endocrinology Department, Curry Cabral Hospital, Lisbon, Portugal

    J Silva-Nunes

  5. Cardiology Department, Santa Cruz Hospital, Carnaxide, Portugal

    P J Sousa

  6. Cardiology Department, Garcia de Orta Hospital, Almada, Portugal

    R Calé

  7. Dean of the College of Applied Health Sciences, University of Illinois, Chicago, IL, USA

    B Fernhall

Authors
  1. N M Pimenta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. H Santa-Clara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. H Cortez-Pinto
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. J Silva-Nunes
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. M da Lapa Rosado
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. P J Sousa
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. R Calé
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. X Melo
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. L B Sardinha
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. B Fernhall
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to N M Pimenta.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Pimenta, N., Santa-Clara, H., Cortez-Pinto, H. et al. Body composition and body fat distribution are related to cardiac autonomic control in non-alcoholic fatty liver disease patients. Eur J Clin Nutr 68, 241–246 (2014). https://doi.org/10.1038/ejcn.2013.249

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ejcn.2013.249

Keywords

This article is cited by

Search

Advanced search

Quick links