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Relation of leptin and insulin to adiposity-associated elevations in sympathetic activity with age in humans

Abstract

OBJECTIVE: To determine whether plasma leptin and insulin concentrations are related to adiposity-associated elevations in muscle sympathetic nerve activity (MSNA) with age in healthy adult humans.

DESIGN: Cross-sectional investigation of young and older adult men.

SUBJECTS: Thirty healthy adult men, 16 young (25±1 y, mean±s.e.) and 14 older (61±1 y).

MEASUREMENTS/RESULTS: The older men had higher (P<0.05) levels of body mass, BMI, total fat mass and truncal fat mass (dual energy X-ray absorptiometry) than the young men. MSNA burst frequency (microneurography) was 75% higher in the older men (P<0.001). Plasma leptin concentrations were 150% higher (P<0.01), whereas plasma insulin concentrations were 70% higher (P<0.05) in the older subjects. MSNA was related to both total (r=0.51, P<0.01) and truncal (r=0.56, P<0.01) fat mass. Plasma leptin concentrations were related to total and truncal fat mass (both r=0.83, P<0.001), and to MSNA (r=0.49, P<0.01). Plasma insulin concentrations were related to MSNA (r=0.38, P<0.05). We used partial correlation analyses to assess whether leptin and/or insulin are potential contributors to the relation between body fat and MSNA.

Adjusting for the effects of plasma leptin, but not insulin, concentrations eliminated the significant relations between MSNA and total and truncal fat mass.

CONCLUSION: Our results: (1) demonstrate a positive relation between MSNA and plasma leptin concentrations in young and older healthy men; and (2) support the concept that circulating leptin concentrations may act as a humoral signal contributing to adiposity-associated elevations in MSNA with age in adult humans.

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References

  1. Ng AV, Callister R, Johnson DG, Seals DR . Age and gender influence muscle sympathetic nerve activity at rest in healthy humans Hypertension 1993 21: 498–503.

    Article  CAS  Google Scholar 

  2. Sundlof G, Wallin BG . Human muscle nerve sympathetic activity at rest: relationship to blood pressure and age J Physiol (Lond) 1978 274: 621–637.

    Article  CAS  Google Scholar 

  3. Yamada Y, Miyajima E, Tochikubo O, Matsukawa T, Ishii M . Age-related changes in muscle sympathetic nerve activity in essential hypertension Hypertension 1989 13: 870–877.

    Article  CAS  Google Scholar 

  4. Ebert T, Morgan B, Barney J, Denahan T, Smith J . Effects of aging on baroreflex regulation of sympathetic activity in humans Am J Physiol 1992 263: H798–H803.

    CAS  PubMed  Google Scholar 

  5. Jones P, Davy K, Alexander S, Seals D . Age-related increase in muscle sympathetic nerve activity is associated with abdominal adiposity Am J Physiol 1997 272: E976–E980.

    Article  CAS  Google Scholar 

  6. Jones PP, Davy KP, Seals DR . Relations of total and abdominal adiposity to muscle sympathetic nerve activity in healthy older males Int J Obes Relat Metab Disord 1997 21: 1053–1057.

    Article  CAS  Google Scholar 

  7. Dunbar JC, Hu Y, Lu H . Intracerebroventricular leptin increases lumbar and renal sympathetic nerve activity and blood pressure in normal rats Diabetes 1997 46: 2040–2043.

    Article  CAS  Google Scholar 

  8. Haynes WG, Morgan DA, Walsh SA, Mark AL, Sivitz WI . Receptor-mediated regional sympathetic nerve activation by leptin J Clin Invest 1997 100: 270–278.

    Article  CAS  Google Scholar 

  9. Snitker S, Pratley RE, Nicolson M, Tataranni PA, Ravussin E . Relationship between muscle sympathetic nerve activity and plasma leptin concentration Obes Res 1997 5: 338–340.

    Article  CAS  Google Scholar 

  10. Solin MS, Ball J, Robertson I, Silva AD, Pasco JA, Kotowicz MA, Nicholson GC, Collier GR . Relationship of serum leptin to total and truncal body fat Clin Sci 1997 93: 581–584.

    Article  CAS  Google Scholar 

  11. Moller N, O'Brien P, Nair KS . Disruption of the relationship between fat content and leptin levels with aging in humans J Clin Endocrinol Metab 1998 83: 931–934.

    CAS  PubMed  Google Scholar 

  12. Ostlund RE, Yang JW, Klein S, Gingerich R . Relation between plasma leptin concentration and body fat, gender, diet, age and metabolic covariates J Clin Endocrinol Metab 1996 81: 3909–3913.

    CAS  PubMed  Google Scholar 

  13. Perry HM, Morley JE, Horowitz M, Kaiser FE, Miller DK, Wittert G . Body composition and age in African-American and Caucasian women: relationship to plasma leptin levels Metabolism 1997 46: 1399–1405.

    Article  CAS  Google Scholar 

  14. Caprio S, Tamborlane WV, Silver D, Robinson C, Leibel R, McCarthy S, Grozman A, Belous A, Maggs D, Sherwin RS . Hyperleptinemia: an early sign of juvenile obesity. Relations to body fat depots and insulin concentrations Am J Physiol 1996 271: E626–E630.

    CAS  PubMed  Google Scholar 

  15. Hickey MS, Israel RG, Gardiner SN, Considine RV, McCammon MR, Tyndall GL, Houmard JA, Marks RHL, Caro JF . Gender differences in serum leptin levels in humans Biochem Mol Med 1996 59: 1–6.

    Article  CAS  Google Scholar 

  16. Scherrer U, Randin D, Tappy L, Vollenweider P, Jequier E, Nicod P . Body fat and sympathetic nerve activity in healthy subjects Circulation 1994 89: 2634–2640.

    Article  CAS  Google Scholar 

  17. Gudbjornsdottir S, Lonnroth P, Sverrisdottir YB, Wallin BG, Elam M . Sympathetic nerve activity and insulin in obese normotensive and hypertensive men Hypertension 1996 27: 276–280.

    Article  CAS  Google Scholar 

  18. Spraul M, Ravussin E, Fontvielle AM, Rising R, Larson DE, Anderson EA . Reduced sympathetic nervous activity. A potential mechanism predisposing to body weight gain J Clin Invest 1993 92: 1730–1735.

    Article  CAS  Google Scholar 

  19. Bjorntorp P . Abdominal obesity and the development of non-insulin dependent diabetes mellitus Diabetes Metab Rev 1988 4: 615–622.

    Article  CAS  Google Scholar 

  20. Cigolini M, Seidell J, Targher G, Deslypere J, Ellsinger B, Charzewska J, Cruz A, Bjorntorp P . Fasting serum insulin in relation to components of the metabolic syndrome in European healthy men: the European Fat Distribution Study Metabolism 1995 44: 35–40.

    Article  CAS  Google Scholar 

  21. Landin K, Krotkiewski M, Smith U . Importance of obesity for the metabolic abnormalities associated with an abdominal fat distribution Metab Clin Exp 1989 38: 572–576.

    Article  CAS  Google Scholar 

  22. Lindberg O, Tilvis RS, Strandberg TE . Does fasting plasma insulin increase by age in the general elderly population? Aging Clin Exp Res 1997 9: 277–280.

    Article  CAS  Google Scholar 

  23. Perloff D, Grim C, Flack J, Frohlich ED, Hill M, McDonald M, Morgenstern BZ . Human blood pressure determination by sphygmomanometry Circulation 1993 88: 2460–2470.

    Article  CAS  Google Scholar 

  24. Jones PP, Spraul M, Matt KS, Seals DR, Skinner JS, Ravussin E . Gender does not influence sympathetic neural reactivity to stress in healthy humans Am J Physiol 1996 270: H350–H357.

    CAS  PubMed  Google Scholar 

  25. Wallin BG, Fagius J . Peripheral sympathetic neural activity in conscious humans Annu Rev Physiol 1988 50: 565–576.

    Article  CAS  Google Scholar 

  26. Van Pelt RE, Davy KP, Stevenson ET, Wilson TM, Jones PP, DeSouza CA, Seals DR . Smaller differences in total and regional adiposity with age in women who regularly perform endurance exercise Am J Physiol 1998 275: E626–E634.

    CAS  PubMed  Google Scholar 

  27. Svendsen OL, Hassager C, Bergmann I, Christiansen C . Measurement of abdominal and intra-abdominal fat in postmenopausal women by dual energy X-ray absorptiometry and anthropometry: comparison with computerized tomography Int J Obes Relat Metab Disord 1993 17: 45–51.

    CAS  PubMed  Google Scholar 

  28. Treuth MS, Hunter GR, Kekes-Szabo T . Estimating intraabdominal adipose tissue in women by dual-energy X-ray absorptiometry Am J Clin Nutr 1995 62: 527–532.

    Article  CAS  Google Scholar 

  29. Anderson EA, Hoffman RP, Balon TW, Sinkey CA, Mark AL . Hyperinsulinemia produces both sympathetic neural activation and vasodilation in normal humans J Clin Invest 1991 87: 2246–2252.

    Article  CAS  Google Scholar 

  30. Berne C, Fagius J, Pollare T, Hjemdahl P . The sympathetic response to euglycaemic hyperinsulinaemia: evidence from microelectrode nerve recordings in healthy subjects Diabetologia 1992 35: 873–879.

    Article  CAS  Google Scholar 

  31. Scherrer U, Vollenweider P, Randin D, Jequier E, Nicod P, Tappy L . Suppression of insulin induced sympathetic activation and vasodilation by dexamethasone in humans Circulation 1993 88: 388–394.

    Article  CAS  Google Scholar 

  32. Vollenweider P, Tappy L, Randin D, Schneiter P, Jequier E, Nicod P, Scherrer U . Differential effects of hyperinsulinemia and carbohydrate metabolism on sympathetic nerve activity and muscle blood flow in humans J Clin Invest 1993 92: 147–154.

    Article  CAS  Google Scholar 

  33. Hall JE, Brands MW, Zappe DH, Alonso-Galicia M . Cardiovascular actions of insulin: are they important in long-term blood pressure regulation? Clin Exp Pharmac Physiol 1995 22: 689–700.

    Article  CAS  Google Scholar 

  34. Spraul M, Anderson EA, Bogardus C, Ravussin E . Muscle sympathetic nerve activity in response to glucose ingestion: impact of plasma insulin and body fat Diabetes 1994 43: 191–196.

    Article  CAS  Google Scholar 

  35. Fagius J, Niklasson F, Berne C . Sympathetic outflow in human muscle nerves increases during hypoglycemia Diabetes 1986 35: 1124–1129.

    Article  CAS  Google Scholar 

Download references

Acknowledgements

The authors would like to thank Mary Jo Reiling and Sonya Craig for their technical assistance, and the Colorado Clinical Nutrition Research Unit (DK48520) for the plasma leptin analyses. This study was supported by NIH awards AG39966, AG06537, Institutional Training grant DK07658 (MBM), AG05705 and K01 AG00828 (PPJ).

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Correspondence to P Parker Jones.

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Monroe, M., Van Pelt, R., Schiller, B. et al. Relation of leptin and insulin to adiposity-associated elevations in sympathetic activity with age in humans. Int J Obes 24, 1183–1187 (2000). https://doi.org/10.1038/sj.ijo.0801364

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