Download PDF
Int J Sports Med 2018; 39(03): 225-231
DOI: 10.1055/s-0043-123649
Clinical Sciences
© Georg Thieme Verlag KG Stuttgart · New York

Muscular Strength is Independently Associated with Cystatin C: The KORA-Age Study

Konstantinos Volaklis
1   Department of Prevention and Sports Medicine, Cardiac Rehabilitation Center, Augsburg, Munich, Germany
,
Barbara Thorand
2   Institute of Epidemiology II, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Munich, Germany
,
Anette Peters
2   Institute of Epidemiology II, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Munich, Germany
,
Martin Halle
3   Sports Medicine, Technical University, Munich, Germany
,
Heier Margot
2   Institute of Epidemiology II, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Munich, Germany
,
Ute Amann
4   Institute of Epidemiology II, 3Institute of Epidemiology II, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Munich, Germany
,
Karl Heinz Ladwig
2   Institute of Epidemiology II, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Munich, Germany
,
Holger Schulz
5   Institute of Epidemiology I, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Munich, Germany
,
Wolfgang Koenig
6   Department of Internal Medicine II-Cardiology, University of Ulm, Ulm, Germany
,
Christa Meisinger
2   Institute of Epidemiology II, Helmholtz Zentrum München, German Research Center for Environmental Health, Neuherberg, Munich, Germany
› Author Affiliations
Further Information

Publication History



accepted after revision 06 November 2017

Publication Date:
07 March 2018 (online)

Also available at
    Permissions and Reprints

Abstract

The purpose of this study was to investigate if there is a link between muscular strength (MS) and markers of chronic kidney disease (CKD) among older adults. The cross-sectional analysis based on 1041 men and women, aged 65–94 years, who participated in the KORA-Age study. Participants underwent an interview and extensive examinations including anthropometric measurements, diseases and drug intake registration, determination of health-related behaviors, collection of blood samples for measurements of cystatin C and maximal muscle strength evaluation. One-Way ANOVA revealed significant differences in both mean cystatin C (1.16±0.37 vs. 1.03±0.29 vs. 0.93±0.24 mg/L, p<0.001) and mean eGFRcysC (63.61±18.61 vs. 72.14±18.92 vs. 79.87±18.19 ml/min/1.73 m2, p<0.05) across thirds of maximal muscular strength (from lowest to highest). MS in the lowest third was significantly associated with increased odds of having elevated cystatin C (OR: 1.70, 95% CI: 1.01–2.85, p=0.043) after controlling for age, gender, fat mass, fat-free mass, alcohol intake, smoking status, number of regularly used medications, multimorbidity status, hs-CRP, telomere length and levels of physical activity. Lower levels of MS are independently associated with higher concentrations of cystatin C and lower eGFRcysC in older individuals. Increasing the levels of muscular strength may be useful to prevent the age-related CKD disease of older adults.

Key words

muscular strength - chronic kidney disease - cystatin C - older adults
 

  • References

  • 1 Baxmann AC, Ahmed MS, Marques NC, Menon VB, Pereira AB, Kirsztajn GM, Heilberg IP. Influence of muscle mass and physical activity on serum and urinary creatinine and serum cystatin C. Clin J Am Soc Nephrol 2008; 3: 348-354
    CrossrefPubMedGoogle Scholar
  • 2 Brandt C, Pedersen BK. The role of exercise-induced myokines in muscle homeostasis and the defense against chronic diseases. J Biomed Biotechnol 2010; 520-528
    PubMedGoogle Scholar
  • 3 Cawthon RM. Telomere measurement by quantitative PCR. Nucleic Acids Res 2002; 30: e47
    CrossrefPubMedGoogle Scholar
  • 4 Chang YT, Wu HL, Guo HR, Cheng YY, Tseng CC, Wang MC, Lin CY, Sung JM. Handgrip strength is an independent predictor of renal outcomes in patients with chronic kidney diseases. Nephrol Dial Transplant 2011; 26: 3588-3595
    CrossrefPubMedGoogle Scholar
  • 5 Chaudhry S, Jin L, Meltzer D. Use of a self-report-generated Charlson Comorbidity Index for predicting mortality. Med Care 2005; 43: 607-615
    CrossrefPubMedGoogle Scholar
  • 6 Chauveau P, Moreau K, Lasseur C, Fouque D, Combe C, Aparicio M. Sarcopenia or uremic myopathy in CKD patients. Nephrol Ther 2016; 12: 71-75
    CrossrefPubMedGoogle Scholar
  • 7 Coresh J, Selvin E, Stevens LA, Manzi J, Kusek JW, Eggers P, Van Lente F, Levey AS. Prevalence of chronic kidney disease in the United States. JAMA 2007; 298: 2038-2047
    CrossrefPubMedGoogle Scholar
  • 8 Filler G, Boekankamp A, Hofmann W, Le Bricon T, Martínez-Brú C, Grubb A. Cystatin C as a marker of GFR: History, indications and future research. Clin Biochem 2005; 38: 1-8
    CrossrefPubMedGoogle Scholar
  • 9 Fried LF, Lee JS, Shlipak M, Chertow GM, Green C, Ding J, Harris T, Newman AB. Chronic kidney disease and functional limitation in older people: Health, aging and body composition study. J Am Geriatr Soc 2006; 54: 750-756
    CrossrefPubMedGoogle Scholar
  • 10 Forti LN, an Roie E, Njemini R, Coudyzer W, Beyer I, Delecluse C, Bautmans I. Effects of resistance training at different loads on inflammatory markers in young adults. Eur J Appl Physiol 2017; 117: 511-519
    CrossrefPubMedGoogle Scholar
  • 11 Grontved A, Pan A, Mekary R, Stampfer M, Willett WC, Manson JE, Hu FB. Muscle-strengthening and conditioning activities and risk of type 2 diabetes: A prospective study in two cohorts of US Women. PLOS Medicine 2014; 11: e1001587
    CrossrefPubMedGoogle Scholar
  • 12 Guo VY, Brage S, Ekelund U, Griffin SJ, Simmons RK. the ADDITION-Plus study team. Objectively measured sedentary time, physical activity and kidney function in people with recently diagnosed Type 2 diabetes: A prospective cohort analysis. Diabetes Med 2016; 33: 1222-1229
    CrossrefPubMedGoogle Scholar
  • 13 Harriss DJ, Macsween A, Atkinson G. Standards for Ethics in Sport and Exercise Science Research: 2018 Update. Int J Sports Med 2017; 38: 1126-1131
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Helbig AK, Döring A, Heier M, Emeny RT, Zimmermann AK, Autenrieth CS, Ladwig KH, Grill E, Meisinger C. Association between sleep disturbances and falls among the elderly: Results from the German Cooperative Health Research in the Region of Augsburg-Age study. Sleep Med 2013; 14: 1356-1363
    CrossrefPubMedGoogle Scholar
  • 15 Isoyama N, Qureshi AR, Avesani CM, Lindholm B, Barany P, Heimbuerger O, Cederholm T. Comparative associations of muscle mass and muscle strength with mortality in dialysis patients. Clin J Am Soc Nephrol 2014; 9: 1720-1728
    CrossrefPubMedGoogle Scholar
  • 16 Kim H, Suzuki T, Kim M, Kojima N, Yoshida Y, Hirano H, Saito K, Iwasa H, Shimada H, Hosoi E, Yoshida H. Incidence and predictors of sarcopenia onset in community-dwelling elderly Japanese women: 4-year follow-up study. J Am Med Dir Assoc 2015; 16: 85e1-88e
    CrossrefPubMedGoogle Scholar
  • 17 Kirchberger L, Meisinger C, Heuler M, Zimmermann AK, Thorand B, Autenrieth CS, Peters A, Ladwig KH, Döring A. Patterns of multimorbidity in the aged population. PLoS One 2012; 7: e30556
    CrossrefPubMedGoogle Scholar
  • 18 Löwel H, Döring A, Schneider A, Heier M, Thorand B, Meisinger C. The MONICA Augsburg surveys–basis for prospective cohort studies. Gesundheitswesen 2005; (Suppl. 01) S13-S18
    PubMedGoogle Scholar
  • 19 Mühlberger N, Behrend C, Stark R, Holle R. Datenbankgestützte Online-Erfassung von Arzneimitteln im Rahmen gesundheitswissenschaftlicher Studien – Erfahrungen mit der IDOM-Software. Informatik, Biometrie und Epidemiologie in Medizin und Biologie 2003; 34: 601-611
    PubMedGoogle Scholar
  • 20 Odden M, Chertow GM, Fried L, Newman AB, Connelly S, Angleman S, Harris TB, Simonsick EM, Shlipak MG. the HABC Study. Cystatin C and measures of physical function in elderly adults. The Health, Aging and Body Composition Study. Am J Epidemiol 2006; 1674: 1180-1189
    PubMedGoogle Scholar
  • 21 Odutayo A, Cherney D. Cystatin C and acute changes in glomerular filtration rate. Clin Nephrol 2012; 78: 64-75
    CrossrefPubMedGoogle Scholar
  • 22 Pedersen B. Muscles and their myokines. J Exp Biol 2011; 214: 337-346
    CrossrefPubMedGoogle Scholar
  • 23 Robinson-Cohen C, Littman AJ, Duncan GE, Weiss NS, Sachs MC, Ruzinski J, Kundzins J, Rock D, de Boer IH, Ikizler TA, Himmelfarb J, Kestenbaum BR. Physical activity and change in estimated GFR among persons with CKD. J Am Soc Nephrol 2014; 25: 399-406
    CrossrefPubMedGoogle Scholar
  • 24 Roubenoff R, Parise H, Payette HA, Abad LW, D'Agostino R, Jacques PF, Wilson PW, Dinarello CA, Harris TB. Cytokines, insulin-like growth factor 1, sarcopenia and mortality in very old community-dwelling men and women: the Framingham Heart Study. Am J Med 2003; 115: 429-435
    CrossrefPubMedGoogle Scholar
  • 25 Sarnak MJ, Leez AS, Scholwerth AC, Coresh J, Culleton B, Hamm LL, McCullough PA, Kasiske BL, Kelepouris E, Klag MJ, Parfrey P, Pfeffer M, Raij L, Spinosa DJ, Wilson PW. Kidney disease as a risk factor for development of cardiovascular disease: A statement from the American Heart Association. Circulation 2003; 108: 2154-2169
    CrossrefPubMedGoogle Scholar
  • 26 Schuit A, Schouten A, Westerterp K, Saris W. Validity of the physical activity scale for the elderly (PASE): According to energy expenditure assessed by the doubly labeled water method. J Clin Epidemiol 1997; 5: 541-546
    PubMedGoogle Scholar
  • 27 Segal KR, Van Loan M, Fitzgerald PI, Hodgdon JA, Van Italie TB. Lean body mass estimation by bioelectrical impedance analysis: A four-site cross-validation study. Am J Clin Nutrition 1988; 47: 7-14
    PubMedGoogle Scholar
  • 28 Shlipak MG, Katz R, Cushman M, Sarnak MJ, Stehman-Breen C, Psaty BM, Siscovick D, Tracy RP, Newman A, Fried L. Cystatin-C and inflammatory markers in the ambulatory elderly. Am J Med 2005; 118: 1416-1421
    PubMedGoogle Scholar
  • 29 Shlipak MG, Sarnak MJ, Katz R, Fried LF, Seliger SL, Newman AB, Siscovick DS, Stehman-Breen C. Cystatin C and the risk of death and cardiovascular events among elderly persons. N Engl J Med 2005; 352: 2049-2060
    CrossrefPubMedGoogle Scholar
  • 30 Shlipak MG, Cystatin C. research priorities targeted to clinical decision-making. Am J Kidney Dis 2008; 51: 358-361
    CrossrefPubMedGoogle Scholar
  • 31 Silventoinen K, Magnusson P, Tynelius P, Batty GD, Rasmussen F. Association of body size and muscle strength with incidence of coronary heart disease and cerebrovascular diseases: A population-based cohort study of one million Swedish men. Int J Epidemiol 2009; 38: 110-118
    CrossrefPubMedGoogle Scholar
  • 32 Stevens LA, Coresh J, Schmid CH, Feldman HI, Froissart M, Kusek J, Rossert J, Van Lente F, Bruce R, Zhang YL, Greene T, Levey AS. Estimating GFR using serum Cystatin C alone and in combination with serum creatinine: A pooled analysis of 3418 individuals with CKD. Am J Kidney Dis 2008; 51: 396-406
    PubMedGoogle Scholar
  • 33 Svensson-Faerbom P, Ohlson-Anderson M, Almgren P, Hedblad B, Engstroem G, Persson M, Hedblad B, Engström G, Persson M, Christensson A, Melander O. Cystatin-C identifies cardiovascular risk better that creatinine-based estimates of glomerular filtration in middle-aged individuals without a history of cardiovascular disease. J Intern Med 2014; 275: 506-521
    CrossrefPubMedGoogle Scholar
  • 34 Taglieri N, Koenig W, Kaski JC. Cystatin C and cardiovascular risk. Clin Chem 2009; 55: 1932-1943
    CrossrefPubMedGoogle Scholar
  • 35 Tufan A, Tufan F, Akpinar TS, Ilhan B, Bahat G, Karan MA. Low glomerular filtration rate as an associated risk factor for sarcopenic muscle strength: Is creatinine or cystatin C-based estimation more relevant?. Aging Male 2017; 20: 110-114
    CrossrefPubMedGoogle Scholar
  • 36 Volaklis KA, Halle M, Meisinger C. Muscular strength as a strong predictor of mortality: A narrative review. Eur J Intern Med 2015; 26: 303-310
    CrossrefPubMedGoogle Scholar
  • 37 Volaklis K, Halle M, Koenig W, Oberhoffer R, Grill E, Peters A, Strasser B, Heier M, Emeny R, Schulz H, Ladwig KH, Meisinger C, Thorand B. Association between muscular strength and inflammatory markers among elderly persons with cardiac disease: Results from the KORA-Age Study. Clin Res Cardiol 2015; 104: 982-989
    CrossrefPubMedGoogle Scholar
  • 38 Volaklis KA, Halle M, Thorand B, Peters A, Ladwig KH, Schulz H, Koenig W, Meisinger C. Handgrip strength is inversely and independently associated with multimorbidity among older women: Results from the KORA-Age study. Eur J Intern Med 2016; 31: 35-40
    CrossrefPubMedGoogle Scholar
  • 39 Washburn RA, Smith KW, Jette AM, Janney CA. The Physical Activity Scale for the Elderly (PASE): development and evaluation. J Clin Epidemiol 1993; 46: 153-162
    CrossrefPubMedGoogle Scholar
  • 40 Zelle DM, Klaassen G, van Adrichem E, Bakker SJ, Corpeleijn E, Navis G. Physical inactivity: A risk factor and target for intervention in renal care. Nat Rev Nephrol 2017; 13: 152-168
    CrossrefPubMedGoogle Scholar