Skip to main content

Advertisement

SpringerLink
Log in

Age-related changes in basal substrate oxidation and visceral adiposity and their association with metabolic syndrome

  • Original Contribution
  • Published:
European Journal of Nutrition Aims and scope Submit manuscript

Abstract

Purpose

Ageing is directly associated with visceral fat (VAT) deposition and decline of metabolically active cellular mass, which may determine age-related shifts in substrate oxidation and increased cardiometabolic risk. We tested whether VAT and fasting respiratory quotient (RQ, an index of macronutrient oxidation) changed with age and if they were associated with increased risk of metabolic syndrome (MetSyn).

Methods

A total of 2819 adult participants (age range: 18–81 years; men/women: 894/1925) were included; we collected history, anthropometric measures, biochemistry, smoking habits, and physical activity. The body mass index range was 18.5–60.2 kg/m2. Gas exchanges (VO2 and VCO2) were measured by indirect calorimetry in fasting conditions, and RQ was calculated. Body composition was measured by bioelectrical impedance. Abdominal subcutaneous fat and VAT were measured by ultrasonography. MetSyn was diagnosed using harmonised international criteria. Multivariate linear and logistic regression models were utilised.

Results

VAT increased with age in both men (r = 0.31, p < 0.001) and women (r = 0.37, p < 0.001). Basal RQ was not significantly associated with age (p = 0.49) and VAT (p = 0.20); in addition, basal RQ was not a significant predictor of MetSyn (OR 3.31, 0.57–19.08, p = 0.27). VAT was the primary predictor of MetSyn risk in a fully adjusted logistic model (OR 4.25, 3.01–5.99, p < 0.001).

Conclusions

Visceral adiposity remains one of the most important risk factors for cardiometabolic risk and is a significant predictor of MetSyn. Post-absorptive substrate oxidation does not appear to play a significant role in age-related changes in body composition and cardiometabolic risk, except for a correlation with triglyceride concentration.

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

Similar content being viewed by others

References

  1. Roberts SB, Rosenberg I (2006) Nutrition and aging: changes in the regulation of energy metabolism with aging. Physiol Rev 86:651–667

    Article  CAS  Google Scholar 

  2. Siervo M et al (2015) Age-related changes in resting energy expenditure in normal weight, overweight and obese men and women. Maturitas 80(4):406–413

    Article  Google Scholar 

  3. St-Onge MP, Gallagher D (2010) Body composition changes with aging: the cause or the result of alterations in metabolic rate and macronutrient oxidation? Nutrition 26:152–155

    Article  CAS  Google Scholar 

  4. Tchernof A, Després J-P (2013) Pathophysiology of human visceral obesity: an update. Physiol Rev 93:359–404

    Article  CAS  Google Scholar 

  5. Schutz Y (1995) Abnormalities of fuel utilization as predisposing to the development of obesity in humans. Obes Res 3(Suppl 2):173s–178s

    Article  Google Scholar 

  6. Astrup A (2011) The relevance of increased fat oxidation for body-weight management: metabolic inflexibility in the predisposition to weight gain. Obe Rev 12:859–865

    Article  CAS  Google Scholar 

  7. Sial S et al (1996) Fat and carbohydrate metabolism during exercise in elderly and young subjects. Am J Physiol 271:E983–E989

    CAS  Google Scholar 

  8. Solomon TP et al (2008) Exercise and diet enhance fat oxidation and reduce insulin resistance in older obese adults. J Appl Physiol 104:1313–1319

    Article  Google Scholar 

  9. Kuk JL et al (2009) Age-related changes in total and regional fat distribution. Ageing Res Rev 8:339–348

    Article  Google Scholar 

  10. Konopka AR, Sreekumaran Nair K (2013) Mitochondrial and skeletal muscle health with advancing age. Mol Cell Endocrinol 379:19–29

    Article  CAS  Google Scholar 

  11. Huffman DM, Barzilai N (2009) Role of visceral adipose tissue in aging. Biochim Biophys Acta 1790:1117–1123

    Article  CAS  Google Scholar 

  12. Manini TM (2010) Energy expenditure and aging. Ageing Res Rev 9:1–11

    Article  CAS  Google Scholar 

  13. Slawik M, Vidal-Puig AJ (2006) Lipotoxicity, overnutrition and energy metabolism in aging. Age Res Rev 5:144–164

    Article  CAS  Google Scholar 

  14. Bergouignan A et al (2014) Twenty-four hour total and dietary fat oxidation in lean, obese and reduced-obese adults with and without a bout of exercise. PLoS One 9:e94181

    Article  Google Scholar 

  15. Croci I et al (2013) Whole-body substrate metabolism is associated with disease severity in patients with non-alcoholic fatty liver disease. Gut 62:1625–1633

    Article  CAS  Google Scholar 

  16. Ferro Y et al (2013) Fat utilization and arterial hypertension in overweight/obese subjects. J Transl Med 11:159

    Article  Google Scholar 

  17. Galgani JE et al (2014) Relationship between whole-body macronutrient oxidative partitioning and pancreatic insulin secretion/beta-cell function in non-diabetic humans. Metab Clin Exp 63:1426–1431

    Article  CAS  Google Scholar 

  18. Montalcini T et al (2013) Metabolic fuel utilization and subclinical atherosclerosis in overweight/obese subjects. Endocrine 44:380–385

    Article  CAS  Google Scholar 

  19. Montalcini T et al (2014) Subclinical cardiovascular damage and fat utilization in overweight/obese individuals receiving the same dietary and pharmacological interventions. Nutrients 6:5560–5571

    Article  CAS  Google Scholar 

  20. Montalcini T et al (2014) Nutrients utilization in obese individuals with and without hypertriglyceridemia. Nutrients 6:790–798

    Article  Google Scholar 

  21. Solomon TP et al (2008) Effects of aging on basal fat oxidation in obese humans. Metab Clin Exp 57:1141–1147

    Article  CAS  Google Scholar 

  22. Levadoux E et al (2001) Reduced whole-body fat oxidation in women and in the elderly. Int J Obes Relat Metab Disord 25:39–44

    Article  CAS  Google Scholar 

  23. Nagy TR et al (1996) Determinants of basal fat oxidation in healthy Caucasians. J Appl Physiol 80:1743–1748

    Article  CAS  Google Scholar 

  24. Toth MJ et al (1999) Hormonal and physiological correlates of energy expenditure and substrate oxidation in middle-aged, premenopausal women. J Clin Endocrinol Metab 84:2771–2775

    CAS  Google Scholar 

  25. Craig CL et al (2003) International Physical Activity Questionnaire: 12-country reliability and validity. Med Sci Sports Exerc 35:1381–1395

    Article  Google Scholar 

  26. Armellini F et al (1990) The contribution of sonography to the measurement of intra-abdominal fat. J Clin Ultrasound 18:563–567

    Article  CAS  Google Scholar 

  27. Isbell TR et al (1991) Measurement reliability and reactivity using repeated measurements of resting energy expenditure with a face mask, mouthpiece, and ventilated canopy. JPEN J Parenter Enteral Nutr 15:165–168

    Article  CAS  Google Scholar 

  28. Weir JBdV (1949) New methods for calculating metabolic rate with special reference to protein metabolism. J Physiol 109:1–9

    Article  Google Scholar 

  29. Lusk G (1924) Animal calorimetry. Analysis of the oxidation of mixtures of carbohydrate and fat. J Biol Chem 59:41–42

    CAS  Google Scholar 

  30. Schutz Y et al (1992) Role of fat oxidation in the long-term stabilization of body weight in obese women. Am J Clin Nutr 55:670–674

    CAS  Google Scholar 

  31. Chobanian AV et al (2003) Seventh report of the Joint National Committee on prevention, detection, evaluation, and treatment of high blood pressure. Hypertension 42:1206–1252

    Article  CAS  Google Scholar 

  32. Alberti KGMM et al (2009) Harmonizing the Metabolic Syndrome: a Joint Interim Statement of the International Diabetes Federation Task Force on Epidemiology and Prevention; National Heart, Lung, and Blood Institute; American Heart Association; World Heart Federation; International Atherosclerosis Society; and International Association for the Study of Obesity. Circulation 120:1640–1645

    Article  CAS  Google Scholar 

  33. Siervo M et al (2010) First-borns carry a higher metabolic risk in early adulthood: evidence from a prospective cohort study. PLoS One 5:e13907

    Article  Google Scholar 

  34. Klein S et al (2007) Waist circumference and cardiometabolic risk: a consensus statement from Shaping America’s Health: association for Weight Management and Obesity Prevention; NAASO, The Obesity Society; the American Society for Nutrition; and the American Diabetes Association. Am J Clin Nutr 85:1197–1202

    CAS  Google Scholar 

  35. Astrup A et al (1994) Obesity as an adaptation to a high-fat diet: evidence from a cross-sectional study. Am J Clin Nutr 59:350–355

    CAS  Google Scholar 

  36. Calles-Escandon J et al (1995) Basal fat oxidation decreases with aging in women. J Appl Physiol 78:266–271

    CAS  Google Scholar 

  37. Seidell JC et al (1992) Fasting respiratory exchange ratio and resting metabolic rate as predictors of weight gain: the Baltimore Longitudinal Study on Aging. Int J Obes Relat Metab Disord 16:667–674

    CAS  Google Scholar 

  38. Toth MJ et al (1998) Gender differences in fat oxidation and sympathetic nervous system activity at rest and during submaximal exercise in older individuals. Clin Sci 95:59–66

    Article  CAS  Google Scholar 

  39. Valtuena S et al (1997) The respiratory quotient as a prognostic factor in weight-loss rebound. Int J Obes Relat Metab Disord 21:811–817

    Article  CAS  Google Scholar 

  40. Weyer C et al (1999) Determinants of energy expenditure and fuel utilization in man: effects of body composition, age, sex, ethnicity and glucose tolerance in 916 subjects. Int J Obes Relat Metab Disord 23:715–722

    Article  CAS  Google Scholar 

  41. Zurlo F et al (1990) Low ratio of fat to carbohydrate oxidation as predictor of weight gain: study of 24-h RQ. Am J Physiol 259:E650–E657

    CAS  Google Scholar 

  42. Soares MJ et al (2000) Plasma leptin concentrations, basal metabolic rates and respiratory quotients in young and older adults. Int J Obes Relat Metab Disord 24:1592–1599

    Article  CAS  Google Scholar 

  43. López-Otín C et al (2013) The hallmarks of aging. Cell 153:1194–1217

    Article  Google Scholar 

  44. Navaratnarajah A, Jackson SHD (2013) The physiology of ageing. Medicine 41:5–8

    Article  Google Scholar 

  45. Raben A et al (1994) Evidence for an abnormal postprandial response to a high-fat meal in women predisposed to obesity. Am J Physiol 267:E549–E559

    CAS  Google Scholar 

  46. North BJ, Sinclair DA (2012) The intersection between aging and cardiovascular disease. Circ Res 110:1097–1108

    Article  CAS  Google Scholar 

  47. Pontiroli AE et al (2002) Ultrasound measurement of visceral and subcutaneous fat in morbidly obese patients before and after laparoscopic adjustable gastric banding: comparison with computerized tomography and with anthropometric measurements. Obes Surg 12:648–651

    Article  CAS  Google Scholar 

Download references

Statement of authorship

The manuscript was conceived by MS who analysed the data and wrote the first draft of the manuscript. Data were collected by AL, SB, AB and AT. All authors contributed to critical interpretation subsequent of results. All authors contributed to the final revision of the manuscript. The corresponding author (MS) is the guarantor for the manuscript and had full access to all of the data in the study and takes responsibility for the integrity of the data and the accuracy of the data analysis reported in the manuscript.

Funding

Core Budget.

Author information

Authors and Affiliations

  1. Human Nutrition Research Centre, Institute of Cellular Medicine, Newcastle University, Campus for Ageing and Vitality, Newcastle on Tyne, NE4 5PL, UK

    Mario Siervo, Jose Lara, Carlos Celis-Morales & Clio Oggioni

  2. MRC Human Nutrition Research, Fulbourn Road, Cambridge, CB1 9NL, UK

    Mario Siervo & Michele Vacca

  3. International Center for the Assessment of Nutritional Status (ICANS), Department of Food, Environmental and Nutritional Sciences (DeFENS), University of Milan, Sandro Botticelli, 21, 20133, Milan, Italy

    Alberto Battezzati, Alessandro Leone, Angela Spadafranca & Simona Bertoli

  4. Human Nutrition and Eating Disorders Research Centre, Department of Public Health, Experimental and Forensic Medicine, University of Pavia, Via Bassi, 21, 27100, Pavia, Italy

    Anna Tagliabue

Authors
  1. Mario Siervo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jose Lara
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Carlos Celis-Morales
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Michele Vacca
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Clio Oggioni
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alberto Battezzati
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Alessandro Leone
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Anna Tagliabue
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Angela Spadafranca
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Simona Bertoli
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mario Siervo.

Ethics declarations

Conflict of interest

All authors have no conflicts of interest to declare.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 137 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Siervo, M., Lara, J., Celis-Morales, C. et al. Age-related changes in basal substrate oxidation and visceral adiposity and their association with metabolic syndrome. Eur J Nutr 55, 1755–1767 (2016). https://doi.org/10.1007/s00394-015-0993-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00394-015-0993-z

Keywords

Search

Navigation