Abstract
Centenarians are an outstanding model of successful aging, with genetics and healthy lifestyle certainly being key factors responsible for their longevity. Exercise capacity has been identified to play an important role in healthy aging, but a comprehensive assessment of the limitations to maximal exercise in this population is lacking. Following, health histories, lung function, and anthropometric measures, eight female centenarians (98–102 years old) and eight young females (18–22 years old) performed a series of graded maximal exercise tests on a cycle ergometer that facilitated absolute and relative work rate comparisons. Centenarians revealed a dramatically attenuated lung function, as measured by spirometry (forced expiratory volume in 1 s (FEV1/forced vital capacity (FVC), 55 ± 10%) compared to the young (FEV1/FVC, 77 ± 5%). During exercise, although the centenarians relied heavily on respiratory rate which yielded ∼50% higher dead space/tidal volume, minute ventilation was similar to that of the young at all but maximal exercise, and alveolar PO2 was maintained in both groups. In contrast, peak WR and VO2 were significantly reduced in the centenarians (33 ± 4 vs 179 ± 24 W; 7.5 ± 1.2 vs 39.6 ± 3.5 ml min−1 kg−1). Arterial PO2 of the centenarians fell steadily from the normal range of both groups to yield a large A-a gradient (57 ± 6 mmHg). Metabolic cost of a given absolute work rate was consistently lower, ∼46% less than the young at maximal effort. Centenarians have significant limitations to gas exchange across the lungs during exercise, but this limited oxygen transport is tempered by improved skeletal muscle mechanical efficiency that may play a vital role in maintaining physical function and therefore longevity in this population.
Similar content being viewed by others
References
Bell C, Paterson DH, Kowalchuk JM, Cunningham DA (1999) Oxygen uptake kinetics of older humans are slowed with age but are unaffected by hyperoxia. Exp Physiol 84(4):747–759
Cress ME, Gondo Y, Davey A, Anderson S, Kim SH, Poon LW (2010) Assessing physical performance in centenarians: norms and an extended scale from the Georgia centenarian study. Curr Gerontol Geriatr Res. doi:10.1155/2010/310610
Davis JA, Whipp BJ, Lamarra N, Huntsman DJ, Frank MH, Wasserman K (1982) Effect of ramp slope on determination of aerobic parameters from the ramp exercise test. Med Sci Sports Exerc 14(5):339–343
DeLorey DS, Babb TG (1999) Progressive mechanical ventilatory constraints with aging. Am J Respir Crit Care Med 160(1):169–177
DeLorey DS, Kowalchuk JM, Paterson DH (2004) Effect of age on O(2) uptake kinetics and the adaptation of muscle deoxygenation at the onset of moderate-intensity cycling exercise. J Appl Physiol 97(1):165–172. doi:10.1152/japplphysiol.01179.2003
DeLorey DS, Paterson DH, Kowalchuk JM (2007) Effects of ageing on muscle O2 utilization and muscle oxygenation during the transition to moderate-intensity exercise. Appl Physiol Nutr Metab 32(6):1251–1262. doi:10.1139/h07-121
Dempsey JA, McKenzie DC, Haverkamp HC, Eldridge MW (2008) Update in the understanding of respiratory limitations to exercise performance in fit, active adults. Chest 134(3):613–622. doi:10.1378/chest.07-2730
Fleg JL, Morrell CH, Bos AG, Brant LJ, Talbot LA, Wright JG, Lakatta EG (2005) Accelerated longitudinal decline of aerobic capacity in healthy older adults. Circulation 112(5):674–682. doi:10.1161/CIRCULATIONAHA.105.545459
Folstein MF, Folstein SE, McHugh PR (1975) Mini-mental state. A practical method for grading the cognitive state of patients for the clinician. J Psychiatr Res 12(3):189–198
Gaesser GA, Brooks GA (1975) Muscular efficiency during steady-rate exercise: effects of speed and work rate. J Appl Physiol 38(6):1132–1139
Galioto A, Dominguez LJ, Pineo A, Ferlisi A, Putignano E, Belvedere M, Costanza G, Barbagallo M (2008) Cardiovascular risk factors in centenarians. Exp Gerontol 43(2):106–113. doi:10.1016/j.exger.2007.06.009
Gibbs CL, Gibson WR (1972) Energy production of rat soleus muscle. Am J Physiol 223(4):864–871
Gulati M, Black HR, Shaw LJ, Arnsdorf MF, Merz CN, Lauer MS, Marwick TH, Pandey DK, Wicklund RH, Thisted RA (2005) The prognostic value of a nomogram for exercise capacity in women. N Engl J Med 353(5):468–475. doi:10.1056/NEJMoa044154
Haseler LJ, Lin AP, Richardson RS (2004) Skeletal muscle oxidative metabolism in sedentary humans: 31P-MRS assessment of O2 supply and demand limitations. J Appl Physiol 97(3):1077–1081. doi:10.1152/japplphysiol.01321.2003
Hollenberg M, Yang J, Haight TJ, Tager IB (2006) Longitudinal changes in aerobic capacity: implications for concepts of aging. J Gerontol A Biol Sci Med Sci 61(8):851–858
Hunter GR, Newcomer BR, Larson-Meyer DE, Bamman MM, Weinsier RL (2001) Muscle metabolic economy is inversely related to exercise intensity and type II myofiber distribution. Muscle Nerve 24(5):654–661. doi:10.1002/mus.1051
Janssen I, Heymsfield SB, Wang ZM, Ross R (2000) Skeletal muscle mass and distribution in 468 men and women aged 18-88 yr. J Appl Physiol 89(1):81–88
Jette M, Sidney K, Blumchen G (1990) Metabolic equivalents (METS) in exercise testing, exercise prescription, and evaluation of functional capacity. Clin Cardiol 13(8):555–565
Johnson BD, Badr MS, Dempsey JA (1994) Impact of the aging pulmonary system on the response to exercise. Clin Chest Med 15(2):229–246
Jones NL (1997) Clinical exercise testing, 4th edn. Saunders, Philadelphia
Jones PR, Pearson J (1969) Anthropometric determination of leg fat and muscle plus bone volumes in young male and female adults. J Physiol 204(2):63P–66P
Kamon E, Metz KF, Pandolf KB (1973) Climbing and cycling with additional weights on the extremities. J Appl Physiol 35(3):367–370
Knudson RJ, Lebowitz MD, Holberg CJ, Burrows B (1983) Changes in the normal maximal expiratory flow-volume curve with growth and aging. Am Rev Respir Dis 127(6):725–734
Levy ML, Quanjer PH, Booker R, Cooper BG, Holmes S, Small I (2009) Diagnostic spirometry in primary care: proposed standards for general practice compliant with American Thoracic Society and European Respiratory Society recommendations. Prim Care Respir J 18(3):130–147. doi:10.4104/pcrj.2009.00054
Lexell J (1995) Human aging, muscle mass, and fiber type composition. J Gerontol A Biol Sci Med Sci 50 Spec No:11–16
Lexell J, Taylor CC, Sjostrom M (1988) What is the cause of the ageing atrophy? Total number, size and proportion of different fiber types studied in whole vastus lateralis muscle from 15- to 83-year-old men. J Neurol Sci 84(2–3):275–294
Mahoney FI, Barthel DW (1965) Functional evaluation: the Barthel Index. Md State Med J 14:61–65
McClaran SR, Babcock MA, Pegelow DF, Reddan WG, Dempsey JA (1995) Longitudinal effects of aging on lung function at rest and exercise in healthy active fit elderly adults. J Appl Physiol 78(5):1957–1968
Murias JM, Spencer MD, Kowalchuk JM, Paterson DH (2011) Influence of phase I duration on phase II VO2 kinetics parameter estimates in older and young adults. Am J Physiol Regul Integr Comp Physiol 301(1):R218–R224. doi:10.1152/ajpregu.00060.2011
Narici MV, Maffulli N (2010) Sarcopenia: characteristics, mechanisms and functional significance. Br Med Bull. doi:10.1093/bmb/ldq008
Paterson DH, Govindasamy D, Vidmar M, Cunningham DA, Koval JJ (2004) Longitudinal study of determinants of dependence in an elderly population. J Am Geriatr Soc 52(10):1632–1638. doi:10.1111/j.1532-5415.2004.52454.x
Perls T, Terry D (2003a) Genetics of exceptional longevity. Exp Gerontol 38(7):725–730
Perls T, Terry D (2003b) Understanding the determinants of exceptional longevity. Ann Intern Med 139(5 Pt 2):445–449
Poole DC, Gaesser GA, Hogan MC, Knight DR, Wagner PD (1992) Pulmonary and leg VO2 during submaximal exercise: implications for muscular efficiency. J Appl Physiol 72(2):805–810
Rantanen T, Guralnik JM, Foley D, Masaki K, Leveille S, Curb JD, White L (1999) Midlife hand grip strength as a predictor of old age disability. JAMA 281(6):558–560
Roca J, Agusti AG, Alonso A, Poole DC, Viegas C, Barbera JA, Rodriguez-Roisin R, Ferrer A, Wagner PD (1992) Effects of training on muscle O2 transport at VO2max. J Appl Physiol 73(3):1067–1076
Stessman J, Hammerman-Rozenberg R, Cohen A, Ein-Mor E, Jacobs JM (2009) Physical activity, function, and longevity among the very old. Arch Intern Med 169(16):1476–1483. doi:10.1001/archinternmed.2009.248
Woo J, Leung J, Sham A, Kwok T (2009) Defining sarcopenia in terms of risk of physical limitations: a 5-year follow-up study of 3,153 Chinese men and women. J Am Geriatr Soc 57(12):2224–2231. doi:10.1111/j.1532-5415.2009.02566.x
Acknowledgments
The authors greatly appreciate the time and effort of the subjects that participated in this study.
This work was supported in part by the PPG (PO1 HL, 09830) the VA Merit grant, and Mons Mazzali Foundation.
Author information
Authors and Affiliations
Corresponding author
About this article
Cite this article
Venturelli, M., Schena, F., Scarsini, R. et al. Limitations to exercise in female centenarians: evidence that muscular efficiency tempers the impact of failing lungs. AGE 35, 861–870 (2013). https://doi.org/10.1007/s11357-011-9379-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11357-011-9379-1