Advertisement

European Radiology

, Volume 25, Issue 7, pp 2163–2175 | Cite as

Adipose tissue compartments, muscle mass, muscle fat infiltration, and coronary calcium in institutionalized frail nonagenarians

  • Fernando Idoate
  • Eduardo L. Cadore
  • Alvaro Casas-Herrero
  • Fabricio Zambom-Ferraresi
  • Teresa Marcellán
  • Ana Ruiz de Gordoa
  • Leocadio Rodriguez-Mañas
  • Gorka Bastarrika
  • Mário C. Marques
  • Nicolas Martínez-Velilla
  • Davinia Vicente-Campos
  • Mikel IzquierdoEmail author
Musculoskeletal

Abstract

Objective

to compare the different adipose tissue (AT) compartments, muscle mass, muscle fat infiltration, coronary calcium, as well as associations among changes in different AT compartments between frail and robust nonagenarians.

Materials and Methods

Forty-two elderly subjects took part in this study: 29 institutionalized frail elderly (92.0 ± 8 years) and 13 robust elderly (88.2 ± 4.1 years). All patients underwent helical thoracic, abdominal and thigh computed tomography (CT). In addition, a non-enhanced prospectively ECG-triggered cardiac CT was performed to quantify the amount of coronary artery calcification and measure pericardial AT.

Results

The robust group presented significantly greater pericardial and abdominal AT volume, as well as greater axial and appendicular muscle size and high-density muscle tissue (greater muscle quality) than the frail group (P < 0.001), whereas no differences between groups were observed in coronary calcium. There were positive correlations between pericardial AT with visceral and subcutaneous AT values, as well as between pericardial AT and quadriceps, hamstrings, psoas and paravertebral low-density muscle tissues in the frail and robust groups (r = 0.57 to 0.91,P < 0.05).

Conclusions

Robust group presented greater muscle size and quality in the axial and appendicular muscles, as well as pericardial and abdominal AT area than the frail group.

Key Points

Robust nonagenarians presented more pericardial and abdominal AT volume than frail.

Frailty is associated with lower muscle size and high-density muscle tissue.

Muscle-fat infiltration shares analogous pattern of visceral and pericardial AT distribution.

Keywords

Adipose tissue Frailty Muscle quality Coronary calcium Muscle fat infiltration 

Notes

Acknowledgments

The scientific guarantor of this publication is Mikel Izquierdo, Head of Department of Health Sciences, Public University of Navarra. This study has received funding by the Spanish Department of Health and Institute Carlos III of the Government of Spain [Spanish Net on Aging and frailty; (RETICEF)], and Economy and Competitivity Department of the Government of Spain, under grants numbered RD12/043/0002, and DEP2011-24105, respectively. Institutional Review Board approval was obtained. Written informed consent was obtained from all subjects (patients) in this study. Methodology: retrospective, cross-sectional study, observational multicenter study, performed at one institution.

References

  1. 1.
    Theou O, Jones GR, Vandervoort AA et al (2010) Daily muscle activity and quiescence in non-frail, pre-frail, and frail older women. Exp Gerontol 45:909–917CrossRefPubMedGoogle Scholar
  2. 2.
    Clegg A (2001) The frailty syndrome. Clin Med 11:72–75CrossRefGoogle Scholar
  3. 3.
    Fiatarone MA, Marks EC, Ryan ND et al (1990) High-intensity strength training in nonagenarians. Effects on skeletal muscle. JAMA 262:2029–3034Google Scholar
  4. 4.
    Heuberger RA (2011) The frailty syndrome: a comprehensive review. J Nutr Gerontol Geriatr 30:315–368CrossRefPubMedGoogle Scholar
  5. 5.
    Goodpaster BH, Kelley DE, Thaete FL et al (2000) Skeletal muscle attenuation determined by computed tomography is associated with skeletal muscle lipid content. J Appl Physiol 89:104–110PubMedGoogle Scholar
  6. 6.
    Goodpaster BH, Chomentowski P, Ward BK et al (2008) Effects of physical activity on strength and skeletal muscle fat infiltration in older adults: a randomized controlled trial. J Appl Physiol 105:1498–1503PubMedCentralCrossRefPubMedGoogle Scholar
  7. 7.
    Cadore EL, Casas-Herrero A, Zambom-Ferraresi F et al (2014) Multicomponent exercises including muscle power training enhance muscle mass, power output, and functional outcomes in institutionalized frail nonagenarians. Age (Dordr) 36(2):773–785Google Scholar
  8. 8.
    Taffe DR, Henwood TR, Nalls MA et al (2009) Alterations in muscle attenuation following detraining and retraining resistance trained older adults. Gerontology 55:217–223CrossRefGoogle Scholar
  9. 9.
    Ross R (2003) Advances in the application of imaging methods in applied and clinical physiology. Acta Diabetol 40:45–50CrossRefGoogle Scholar
  10. 10.
    Visser M, Goodpaster BH, Kritchevsky SB et al (2005) Muscle mass, muscle strength, and muscle fat infiltration as predictors of incident mobility limitations in well-functioning older persons. J Gerontol A Biol Sci Med Sci 60:324–333CrossRefPubMedGoogle Scholar
  11. 11.
    Visser M, Kritchevsky SB, Goodpaster BH et al (2002) Leg muscle mass and composition in relation to lower extremity performance in men and womed aged 70 to 79: the health, aging and body composition study. J Am Geriatr Soc 50:897–904CrossRefPubMedGoogle Scholar
  12. 12.
    Casas-Herrero A, Cadore EL, Zambom-Ferraresi F et al (2013) Functional capacity, muscle fat infiltration, power output and cognitive impairment in institutionalized frail oldest-old. Rejuvenation Res 16:396–403PubMedCentralCrossRefPubMedGoogle Scholar
  13. 13.
    Garcia-Garcia FJ, Gutierrez Avila G, Alfaro-Acha A et al (2011) The prevalence of frailty syndrome in an older population from Spain. The Toledo study for healthy aging. J Nutr Health Aging 15:852–865CrossRefPubMedGoogle Scholar
  14. 14.
    Miao C, Chen S, Ding J et al (2011) The association of pericardial fat with coronary artery plaque index at MR imaging: the multi-ethnic study of atherosclerosis (MESA). Radiology 261:109–115PubMedCentralCrossRefPubMedGoogle Scholar
  15. 15.
    Xie X, Zhao Y, de Bock GH et al (2013) Validation and prognosis of coronary artery calcium scoring in nontriggered thoracic computed tomography: systematic review and meta-analysis. Circ Cardiovasc Imaging 6:514–521CrossRefPubMedGoogle Scholar
  16. 16.
    Bertoni AG, Whitt-Glover MC, Chung H et al (2009) The association between physical activity and subclinical atherosclerosis: the Multi-ethnic study of atherosclerosis. Am J Epidemiol 169:444–454PubMedCentralCrossRefPubMedGoogle Scholar
  17. 17.
    Hamer M, Venuraju SM, Lahiri A et al (2012) Objectively assessed physical activity, sedentary time, and coronary artery calcification in healthy older adults. Arterioscler Thromb Vasc Biol 32:500–505CrossRefPubMedGoogle Scholar
  18. 18.
    Fried LP, Tangen CM, Waltson J et al (2001) Cardiovascular health study collaborative research group. Frailty in older adults: evidence for a phenotype. J Gerontol A Biol Sci Med Sci 56:146–155CrossRefGoogle Scholar
  19. 19.
    Baracos VE, Reiman T, Mourtzakis M et al (2010) Body composition in patients with non-small cell lung cancer: a contemporary view of cáncer cachexia with the use of computed tomography image analysis. Am J Clin Nutr 91:1133–1137CrossRefGoogle Scholar
  20. 20.
    Shen W, Punyanitya M, Wang Z et al (2004) Total body skeletal muscle and adipose tissue volumes: estimation from a single abdominal cross-sectional image. J Appl Physiol 97:2333–2339CrossRefPubMedGoogle Scholar
  21. 21.
    Demerath EW, Sun SS, Rogers N et al (2007) Anatomical patterning of visceral adipose tissue: race, sex, and age variation. Obesity (Silver Spring) 15:2984–2993CrossRefGoogle Scholar
  22. 22.
    Ruan XY, Gallagher D, Harris T, Albu J, Heymsfield S, Kuznia P, Heshka S (2007) Estimating whole body intermuscular adipose tissue from single cross-sectional magnetic resonance images. J Appl Physiol 102:748–754PubMedCentralCrossRefPubMedGoogle Scholar
  23. 23.
    Lee SJ, Janssen I, Heymsfield SB, Ross R (2004) Relation between whole-body and regional measures of human skeletal muscle. Am J Clin Nutr 80:1215–1221PubMedGoogle Scholar
  24. 24.
    Divers J, Wagenknecht LE, Bownden DW et al (2010) Regional adipose tissue associations with calcified atherosclerotic plaque: African American-diabetes heart study. Obesity (Silver Spring) 18:2004–2009CrossRefGoogle Scholar
  25. 25.
    Yoon DH, Choi SH, Yu JH et al (2012) The relationship between visceral adiposity and cognitive performance in older adults. Age Ageing 41:456–461CrossRefPubMedGoogle Scholar
  26. 26.
    Boettcher M, Machann J, Stefan N et al (2009) Intermuscular adipose tissue (IMAT): association with other adipose tissue compartments and insulin sensitivity. J Magn Reson Imaging 29:1340–1345CrossRefPubMedGoogle Scholar
  27. 27.
    Santanasto AJ, Glynn NW, Newman MA et al (2011) Impact of weight loss on physical function with changes in strength, muscle mass, and muscle fat infiltration in overweight to moderately obese older adults: a randomized clinical trial. J Obes. doi: 10.1155/2011/516576 PubMedCentralPubMedGoogle Scholar
  28. 28.
    Muñoz J, Gower B (2003) Relationship between serum leptin concentration and low-density muscle in postmenopausal women. J Clin Endocrinol Metab 88:1157–1161CrossRefPubMedGoogle Scholar
  29. 29.
    Morie M, Reid KF, Miciek R et al (2010) Habitual physical activity levels are associated with performance in measures of physical function and mobility in older men. J Am Geriatr Soc 58:1727–1733PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.
    Lang T, Cauley JA, Tylavsky F et al (2010) Computed tomographic measurements of thigh muscle cross-sectional area and attenuation coefficient predict hip fracture: the health, aging, and body composition study. J Bone Miner Res 25:513–519PubMedCentralCrossRefPubMedGoogle Scholar
  31. 31.
    Prior SJ, Joseph LJ, Brandauer J et al (2007) Reduction in midthigh low-density muscle with aerobic exercise training and weight loss impacts glucose tolerance in older men. J Clin Endocrinol Metab 92:880–886CrossRefPubMedGoogle Scholar
  32. 32.
    Lim SC, Tan BY, Chew SK et al (2002) The relationship between insulin resistance and cardiovascular risk factors in overweight/obese non-diabetic Asian adults: the 1992 Singapore National Health Survey. Int J Obes Relat Metab Disord 26:1511–1516CrossRefPubMedGoogle Scholar
  33. 33.
    Campbell AJ, Buchner DM (1997) Unstable disability and the fluctuations of frailty. Age Ageing 26:315–318CrossRefPubMedGoogle Scholar
  34. 34.
    Rodríguez Mañas L, Féart C, Mann G et al (2012) On behalf of the FOD-CC group. Searching for an operational definition of frailty: a Delphi method based consensus statement. The frailty operative definition-consensus conference project. J Gerontol A Biol Sci Med Sci 68:62–67PubMedCentralCrossRefPubMedGoogle Scholar
  35. 35.
    Thomas F, Pannier B, Benetos A et al (2013) Viceral obesity is not an independent risk factor of mortality in subjects over 65 years. Vasc Health Risk Manag 9:739–745PubMedCentralCrossRefPubMedGoogle Scholar
  36. 36.
    De Schutter A, Lavie CJ, Kachur S et al (2014) Body composition and mortality in a large cohort with preserved ejection fraction: untangling the obesity paradox. Mayo Clin Proc 89:1072–1079CrossRefPubMedGoogle Scholar
  37. 37.
    Hong ES, Khang AR, Roh E et al (2014) Counterintuitive relationship between viceral fat and all-cause mortality in an elderly Asian population. Obesity. doi: 10.1002/0by.20914 Google Scholar
  38. 38.
    Lavie CJ, De Schutter A, Alpert MA et al (2014) Obesity paradox, cachexia, frailty, and heart failure. Heart Fail Clin 10:319–326CrossRefPubMedGoogle Scholar
  39. 39.
    Strandberg TE, Stenholm S, Strandberg AY et al (2013) The “obesity paradox”, frailty, disability, and mortality in older men: a prospective, longitudinal cohort study. Am J Epidemiol 178:1452–1460CrossRefPubMedGoogle Scholar
  40. 40.
    Hong NS, Kim KS, Lee IK et al (2012) The association between obesity paradox and mortality in the elderly differs by serum concentrations of persistent organic pollutants: a possible explanation for the obesity paradox. Int J Obes 36:1170–1175CrossRefGoogle Scholar
  41. 41.
    Mazurek T, Zhang L, Zalewski A et al (2003) Human epicardial adipose tissue is a source of inflammatory mediators. Circulation 108:2460–2466CrossRefPubMedGoogle Scholar
  42. 42.
    Sacks HS, Fain JN (2007) Human epicardial adipose tissue: a review. Am Heart J 153:907–917CrossRefPubMedGoogle Scholar
  43. 43.
    Nasir K, Clouse M (2012) Role of nonenhanced multidetector CT coronary artery calcium testing in asymptomatic and symptomatic individuals. Radiology 264:637–649CrossRefPubMedGoogle Scholar
  44. 44.
    Issever AS, Kentenich M, Köhlitz T et al (2013) Osteoporosis and atherosclerosis: a post-mortem MDCT study of an elderly cohort. Eur Radiol 23:2823–2829CrossRefPubMedGoogle Scholar

Copyright information

© European Society of Radiology 2014

Authors and Affiliations

  • Fernando Idoate
    • 1
  • Eduardo L. Cadore
    • 2
  • Alvaro Casas-Herrero
    • 3
  • Fabricio Zambom-Ferraresi
    • 2
  • Teresa Marcellán
    • 4
  • Ana Ruiz de Gordoa
    • 4
  • Leocadio Rodriguez-Mañas
    • 5
  • Gorka Bastarrika
    • 6
  • Mário C. Marques
    • 7
  • Nicolas Martínez-Velilla
    • 3
  • Davinia Vicente-Campos
    • 8
  • Mikel Izquierdo
    • 9
    Email author
  1. 1.Radiology DepartmentClínica San MiguelPamplonaSpain
  2. 2.Exercise Research Laboratory, Physical Education SchoolFederal University of Rio Grande do SulPorto AlegreBrazil
  3. 3.Division of Geriatric MedicineComplejo Hospitalario de NavarraPamplonaSpain
  4. 4.Casa de MisericordiaPamplonaSpain
  5. 5.Division of Geriatric MedicineUniversity Hospital of GetafeMadridSpain
  6. 6.Radiology at the University of Toronto and Section Head of Cardiac MRI Division at Sunnybrook Health Sciences CentreTorontoCanada
  7. 7.Department of Sport SciencesUniversity of Beira Interior (UBI)CovilhãPortugal
  8. 8.Universidad Francisco de VitoriaMadridSpain
  9. 9.Department of Health SciencesPublic University of NavarraTudelaSpain

Personalised recommendations