Display options
Share it on

J Cachexia Sarcopenia Muscle. 2021 Dec;12(6):1818-1831. doi: 10.1002/jcsm.12785. Epub 2021 Sep 15.

Inflammatory markers are associated with quality of life, physical activity, and gait speed but not sarcopenia in aged men (40-79 years).

Journal of cachexia, sarcopenia and muscle

Jolan Dupont, Leen Antonio, Lenore Dedeyne, Terence W O'Neill, Dirk Vanderschueren, Giulia Rastrelli, Mario Maggi, György Bártfai, Felipe F Casanueva, Aleksander Giwercman, Jolanta Słowikowska-Hilczer, Margus Punab, Ilpo T Huhtaniemi, Frederick C W Wu, Jos Tournoy, Katrien Koppo, Evelien Gielen

Affiliations

  1. Geriatrics and Gerontology, Department of Public Health and Primary Care, KU Leuven, Leuven, Belgium.
  2. Department of Geriatric Medicine, UZ Leuven, Leuven, Belgium.
  3. Clinical and Experimental Endocrinology, Department of Chronic Diseases and Metabolism, KU Leuven, Leuven, Belgium.
  4. Centre for Epidemiology Versus Arthritis, The University of Manchester, NIHR Manchester Biomedical Research Centre, Manchester University NHS Foundation Trust, Manchester, UK.
  5. Andrology, Women's Endocrinology and Gender Incongruence Unit, Mario Serio 'Department of Experimental and Clinical Biomedical Sciences', University of Florence, Florence, Italy.
  6. Endocrinology Unit, Mario Serio 'Department of Experimental and Clinical Biomedical Sciences', University of Florence, Florence, Italy.
  7. Department of Obstetrics, Gynaecology and Andrology, Albert Szent-Györgyi Medical University, Szeged, Hungary.
  8. Department of Medicine, Santiago de Compostela University, Complejo Hospitalario Universitario de Santiago (CHUS), Santiago, Spain.
  9. CIBER de Fisiopatología Obesidad y Nutricion (CB06/03), Instituto Salud Carlos III, Santiago de Compostela, Santiago, Spain.
  10. Department of Translational Medicine, Lund University, Malmö, Sweden.
  11. Department of Andrology and Reproductive Endocrinology, Medical University of Lodz, ?ód?, Poland.
  12. Andrology Unit, United Laboratories of Tartu University Clinics, Tartu, Estonia.
  13. Department of Metabolism, Digestion and Reproduction, Institute of Reproductive and Developmental Biology, Imperial College London, London, UK.
  14. Institute of Biomedicine, Research Centre for Integrative Physiology and Pharmacology, University of Turku, Turku, Finland.
  15. Department of Endocrinology, Manchester Royal Infirmary, The University of Manchester, Manchester, UK.
  16. Exercise Physiology Research Group, Department of Movement Sciences, KU Leuven, Leuven, Belgium.

PMID: 34523822 DOI: 10.1002/jcsm.12785

Abstract

BACKGROUND: Age-related chronic low-grade inflammation (inflammaging) is one of the proposed mechanisms behind sarcopenia. However, findings regarding inflammatory markers in sarcopenic older adults are conflicting. This study aimed to determine the association between inflammatory markers, prevalent as well as incident sarcopenia, sarcopenia-defining parameters, quality of life (QoL), and physical activity in middle-aged and older men.

METHODS: Men aged 40-79 years (mean 59.66 ± 11.00y) were recruited from population registers in eight European centres for participation in the European Male Aging study (EMAS). Subjects were assessed at baseline (2003-2005) and again after a median follow-up of 4.29 years. In 2577 participants, associations between baseline inflammatory markers [high-sensitive C-reactive protein (hs-CRP), white blood cell count (WBC), albumin] and baseline physical activity (PASE) and QoL (SF-36) were analysed. In the Leuven and Manchester cohort (n = 447), data were available on muscle mass (whole-body dual X-ray absorptiometry) and strength. In this subgroup, cross-sectional associations between baseline inflammatory markers and sarcopenia-defining parameters (handgrip strength, chair stand test, appendicular lean mass, and gait speed) and prevalent sarcopenia were examined. In a further subgroup (n = 277), associations with knee extensor strength were explored. Longitudinally, predictive value of baseline inflammation on functional decline, physical activity, QoL, and incident sarcopenia was examined. Subgroup analyses were performed in subgroups with chronic inflammation and stratified by age. Linear and logistic regressions were used, adjusted for age, body mass index, centre, and smoking.

RESULTS: At baseline, hs-CRP and WBC were negatively associated with PASE score (hs-CRP: β = -7.920, P < 0.001; and WBC: β = -4.552, P < 0.001) and the physical component score of SF-36 (hs-CRP: β = -1.025, P < 0.001; and WBC: β = -0.364, P < 0.001). Baseline WBC levels were negatively associated with gait speed (β = -0.013; P = 0.025), quadriceps isometric 90° (β = -5.983; P = 0.035) and isokinetic 60°/s peak torque/body weight (β = -5.532; P = 0.027). The prevalence of sarcopenia at baseline was 18.1% (n = 81). Of those without sarcopenia at baseline, 64 (18.6%) satisfied criteria for sarcopenia at follow-up. There were no significant associations between baseline inflammatory markers and either prevalent or incident sarcopenia, or change in level of sarcopenia-defining parameters between baseline and follow-up.

CONCLUSIONS: In middle-aged and older men, hs-CRP and WBC were negatively associated with QoL and PASE scores, while WBC was negatively associated with gait speed and knee strength. Associations with hs-CRP remained significant in all ages, whereas WBC levels were only associated with PASE, gait speed and knee strength in older adults (60-79 years). Baseline inflammatory markers (hs-CRP, WBC and albumin) did not predict functional decline, decline in physical activity, decreased QoL or incident sarcopenia.

© 2021 The Authors. Journal of Cachexia, Sarcopenia and Muscle published by John Wiley & Sons Ltd on behalf of Society on Sarcopenia, Cachexia and Wasting Disorders.

Keywords: Ageing; Inflammaging; Inflammation; Muscle strength; Older adult; Sarcopenia

References

  1. Cruz-Jentoft AJ, Baeyens JP, Bauer JM, Boirie Y, Cederholm T, Landi F, et al. Sarcopenia: European consensus on definition and diagnosis: Report of the European Working Group on Sarcopenia in Older People. Age Ageing 2010;39:412-423. - PubMed
  2. Cruz-Jentoft AJ, Landi F, Schneider SM, Zuniga C, Arai H, Boirie Y, et al. Prevalence of and interventions for sarcopenia in ageing adults: a systematic review. Report of the International Sarcopenia Initiative (EWGSOP and IWGS). Age Ageing 2014;43:748-759. - PubMed
  3. McLeod M, Breen L, Hamilton DL, Philp A. Live strong and prosper: the importance of skeletal muscle strength for healthy ageing. Biogerontology 2016;17:497-510. - PubMed
  4. Dalle S, Rossmeislova L, Koppo K. The role of inflammation in age-related sarcopenia. Front Physiol 2017;8:1045. - PubMed
  5. Bano G, Trevisan C, Carraro S, Solmi M, Luchini C, Stubbs B, et al. Inflammation and sarcopenia: a systematic review and meta-analysis. Maturitas 2017;96:10-15. - PubMed
  6. Bian AL, Hu HY, Rong YD, Wang J, Wang JX, Zhou XZ. A study on relationship between elderly sarcopenia and inflammatory factors IL-6 and TNF-alpha. Eur J Med Res 2017;22:25. - PubMed
  7. Rong YD, Bian AL, Hu HY, Ma Y, Zhou XZ. Study on relationship between elderly sarcopenia and inflammatory cytokine IL-6, anti-inflammatory cytokine IL-10. BMC Geriatr 2018;18:308. - PubMed
  8. van Atteveld VA, Van Ancum JM, Reijnierse EM, Trappenburg MC, Meskers CGM, Maier AB. Erythrocyte sedimentation rate and albumin as markers of inflammation are associated with measures of sarcopenia: a cross-sectional study. BMC Geriatr 2019;19:233. - PubMed
  9. Cabrerizo S, Cuadras D, Gomez-Busto F, Artaza-Artabe I, Marín-Ciancas F, Malafarina V. Serum albumin and health in older people: review and meta analysis. Maturitas 2015;81:17-27. - PubMed
  10. Cheong M, Chew STH, Oliver J, Baggs G, Low YL, How CH, et al. Nutritional biomarkers and associated factors in community-dwelling older adults: findings from the SHIELD study. Nutrients 2020;12. - PubMed
  11. Cruz-Jentoft AJ, Bahat G, Bauer J, Boirie Y, Bruyere O, Cederholm T, et al. Sarcopenia: revised European consensus on definition and diagnosis. Age Ageing 2019;48:16-31. - PubMed
  12. Steffl M, Bohannon RW, Sontakova L, Tufano JJ, Shiells K, Holmerova I. Relationship between sarcopenia and physical activity in older people: a systematic review and meta-analysis. Clin Interv Aging 2017;12:835-845. - PubMed
  13. Lee SY, Tung HH, Liu CY, Chen LK. Physical activity and sarcopenia in the geriatric population: a systematic review. J Am Med Dir Assoc 2018;19:378-383. - PubMed
  14. Nicklas BJ, Beavers DP, Mihalko SL, Miller GD, Loeser RF, Messier SP. Relationship of objectively-measured habitual physical activity to chronic inflammation and fatigue in middle-aged and older adults. J Gerontol A Biol Sci Med Sci 2016;71:1437-1443. - PubMed
  15. Garvin P, Nilsson E, Ernerudh J, Kristenson M. The joint subclinical elevation of CRP and IL-6 is associated with lower health-related quality of life in comparison with no elevation or elevation of only one of the biomarkers. Quality of life research: an international journal of quality of life aspects of treatment, care and rehabilitation 2016;25:213-221. - PubMed
  16. Tait JL, Duckham RL, Milte CM, Main LC, Daly RM. Associations between inflammatory and neurological markers with quality of life and well-being in older adults. Exp Gerontol 2019;125:110662. - PubMed
  17. Lee DM, O'Neill TW, Pye SR, Silman AJ, Finn JD, Pendleton N, et al. The European Male Ageing Study (EMAS): design, methods and recruitment. Int J Androl 2009;32:11-24. - PubMed
  18. Ware JE Jr, Sherbourne CD. The MOS 36-item short-form health survey (SF-36). I. Conceptual framework and item selection. Med Care 1992;30:473-483. - PubMed
  19. 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. - PubMed
  20. Gielen E, O'Neill TW, Pye SR, Adams JE, Wu FC, Laurent MR, et al. Endocrine determinants of incident sarcopenia in middle-aged and elderly European men. J Cachexia Sarcopenia Muscle 2015;6:242-252. - PubMed
  21. Roberts HC, Denison HJ, Martin HJ, Patel HP, Syddall H, Cooper C, et al. A review of the measurement of grip strength in clinical and epidemiological studies: towards a standardised approach. Age Ageing 2011;40:423-429. - PubMed
  22. Reuben DB, Siu AL. An objective measure of physical function of elderly outpatients. The Physical Performance Test. J Am Geriatr Soc 1990;38:1105-1112. - PubMed
  23. Verschueren S, Gielen E, O'Neill TW, Pye SR, Adams JE, Ward KA, et al. Sarcopenia and its relationship with bone mineral density in middle-aged and elderly European men. Osteoporos Int 2013;24:87-98. - PubMed
  24. Boonen S, Lesaffre E, Dequeker J, Aerssens J, Nijs J, Pelemans W, et al. Relationship between baseline insulin-like growth factor-I (IGF-I) and femoral bone density in women aged over 70 years: potential implications for the prevention of age-related bone loss. J Am Geriatr Soc 1996;44:1301-1306. - PubMed
  25. Willis EA, Shearer JJ, Matthews CE, Hofmann JN. Association of physical activity and sedentary time with blood cell counts: National Health and Nutrition Survey 2003-2006. PloS one. 2018;13:e0204277. - PubMed
  26. Vagetti GC, Barbosa Filho VC, Moreira NB, Oliveira V, Mazzardo O, Campos W. Association between physical activity and quality of life in the elderly: a systematic review, 2000-2012. Rev Bras Psiquiatr (Sao Paulo, Brazil: 1999) 2014;36:76-88. - PubMed
  27. Christian LM, Glaser R, Porter K, Malarkey WB, Beversdorf D, Kiecolt-Glaser JK. Poorer self-rated health is associated with elevated inflammatory markers among older adults. Psychoneuroendocrinology 2011;36:1495-1504. - PubMed
  28. Schaap LA, Pluijm SM, Deeg DJ, Harris TB, Kritchevsky SB, Newman AB, et al. Higher inflammatory marker levels in older persons: associations with 5-year change in muscle mass and muscle strength. J Gerontol A Biol Sci Med Sci 2009;64:1183-1189. - PubMed
  29. Schaap LA, Pluijm SM, Deeg DJ, Visser M. Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am J Med 2006;119:526.e9-526.e17. - PubMed
  30. Puzianowska-Kuźnicka M, Owczarz M, Wieczorowska-Tobis K, Nadrowski P, Chudek J, Slusarczyk P, et al. Interleukin-6 and C-reactive protein, successful aging, and mortality: the PolSenior study. Immunity & ageing: I & A 2016;13:21. - PubMed
  31. Moreno-Gonzalez R, Corbella X, Mattace-Raso F, Tap L, Sieber C, Freiberger E, et al. Prevalence of sarcopenia in community-dwelling older adults using the updated EWGSOP2 definition according to kidney function and albuminuria: the Screening for CKD among Older People across Europe (SCOPE) study. BMC Geriatr 2020;20:327. - PubMed
  32. Custodero C, Anton SD, Beavers DP, Mankowski RT, Lee SA, McDermott MM, et al. The relationship between interleukin-6 levels and physical performance in mobility-limited older adults with chronic low-grade inflammation: The ENRGISE Pilot study. Arch Gerontol Geriatr 2020;90:104131. - PubMed
  33. Zembron-Lacny A, Dziubek W, Wolny-Rokicka E, Dabrowska G, Wozniewski M. The relation of inflammaging with skeletal muscle properties in elderly men. Am J Mens Health 2019;13:1557988319841934. - PubMed
  34. Haynes EMK, Neubauer NA, Cornett KMD, O'Connor BP, Jones GR, Jakobi JM. Age and sex-related decline of muscle strength across the adult lifespan: a scoping review of aggregated data. Appl Physiol, Nutr Metab = Physiol Appl, Nutr Metab 2020;45:1185-1196. - PubMed
  35. Dodds RM, Syddall HE, Cooper R, Benzeval M, Deary IJ, Dennison EM, et al. Grip strength across the life course: normative data from twelve British studies. PloS one 2014;9:e113637. - PubMed
  36. von Haehling S, Morley JE, Anker SD. An overview of sarcopenia: facts and numbers on prevalence and clinical impact. J Cachexia Sarcopenia Muscle 2010;1:129-133. - PubMed
  37. Cooper R, Hardy R, Aihie Sayer A, Ben-Shlomo Y, Birnie K, Cooper C, et al. Age and gender differences in physical capability levels from mid-life onwards: the harmonisation and meta-analysis of data from eight UK cohort studies. PloS one. 2011;6:e27899. - PubMed
  38. Patel HP, Syddall HE, Jameson K, Robinson S, Denison H, Roberts HC, et al. Prevalence of sarcopenia in community-dwelling older people in the UK using the European Working Group on Sarcopenia in Older People (EWGSOP) definition: findings from the Hertfordshire Cohort Study (HCS). Age Ageing 2013;42:378-384. - PubMed
  39. Payette H, Roubenoff R, Jacques PF, Dinarello CA, Wilson PW, Abad LW, et al. Insulin-like growth factor-1 and interleukin 6 predict sarcopenia in very old community-living men and women: the Framingham Heart Study. J Am Geriatr Soc 2003;51:1237-1243. - PubMed
  40. von Haehling S, Morley JE, Coats AJS, Anker SD. Ethical guidelines for publishing in the Journal of Cachexia, Sarcopenia and Muscle: update 2019. J Cachexia Sarcopenia Muscle 2019;10:1143-1145. - PubMed

Publication Types