Skip to main content

Advertisement

SpringerLink
Log in

Inflammatory cytokine responses to progressive resistance training and supplementation with fortified milk in men aged 50+ years: an 18-month randomized controlled trial

  • Original Article
  • Published:
European Journal of Applied Physiology Aims and scope Submit manuscript

Abstract

We examined the effects of progressive resistance training (PRT) and supplementation with calcium-vitamin D3 fortified milk on markers of systemic inflammation, and the relationship between inflammation and changes in muscle mass, size and strength. Healthy men aged 50–79 years (n = 180) participated in this 18-month randomized controlled trial that comprised a factorial 2 × 2 design. Participants were randomized to (1) PRT + fortified milk supplement, (2) PRT, (3) fortified milk supplement, or (4) a control group. Participants assigned to PRT trained 3 days per week, while those in the supplement groups consumed 400 ml day−1 of milk containing 1,000 mg calcium plus 800 IU vitamin D3. We collected venous blood samples at baseline, 12 and 18 months to measure the serum concentrations of IL-6, TNF-α and hs-CRP. There were no exercise × supplement interactions, but serum IL-6 was 29% lower (95% CI, −62, 0) in the PRT group compared with the control group after 12 months. Conversely, IL-6 was 31% higher (95% CI, −2, 65) in the supplement group compared with the non-supplemented groups after 12 and 18 months. These between-group differences did not persist after adjusting for changes in fat mass. In the PRT group, mid-tibia muscle cross-sectional area increased less in men with higher pre-training inflammation compared with those men with lower inflammation (net difference ~2.5%, p < 0.05). In conclusion, serum IL-6 concentration decreased following PRT, whereas it increased after supplementation with fortified milk concomitant with changes in fat mass. Furthermore, low-grade inflammation at baseline restricted muscle hypertrophy following PRT.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • Abramson JL, Vaccarino V (2002) Relationship between physical activity and inflammation among apparently healthy middle-aged and older US adults. Arch Intern Med 162:1286–1292

    Article  PubMed  Google Scholar 

  • American College of Sports Medicine (2000) ACSM guidelines for exercise testing and prescription. Lippincott & Williams, Philadelphia

  • Beavers KM, Hsu FC, Isom S, Kritchevsky SB, Church T, Goodpaster B, Pahor M, Nicklas BJ (2010) Long-term physical activity and inflammatory biomarkers in older adults. Med Sci Sports Exerc 42:2189–2196

    Article  PubMed  CAS  Google Scholar 

  • Brinkley TE, Leng X, Miller ME, Kitzman DW, Pahor M, Berry MJ, Marsh AP, Kritchevsky SB, Nicklas BJ (2009) Chronic inflammation is associated with low physical function in older adults across multiple comorbidities. J Gerontol A Biol Sci Med Sci 64:455–461

    Article  PubMed  Google Scholar 

  • Bruun J, Helge J, Richelsen B, Stallknecht B (2006) Diet and exercise reduce low-grade inflammation and macrophage infiltration in adipose tissue but not in skeletal muscle in severely obese subjects. Am J Physiol Endocrinol Metab 290:E961–E967

    Article  PubMed  CAS  Google Scholar 

  • Bruunsgaard H, Bjerregaard E, Schroll M, Pedersen BK (2004) Muscle strength after resistance training is inversely correlated with baseline levels of soluble tumor necrosis factor receptors in the oldest old. J Am Geriatr Soc 52:237–241

    Article  PubMed  Google Scholar 

  • Castaneda C, Gordon PL, Parker RC, Uhlin KL, Roubenoff R, Levey AS (2004) Resistance training to reduce the malnutrition-inflammation complex syndrome of chronic kidney disease. Am J Kidney Dis 43:607–616

    Article  PubMed  Google Scholar 

  • Cauley JA, Danielson ME, Boudreau RM, Forrest KY, Zmuda JM, Pahor M, Tylavsky FA, Cummings SR, Harris TB, Newman AB (2007) Inflammatory markers and incident fracture risk in older men and women: the Health Aging and Body Composition Study. J Bone Miner Res 22:1088–1095

    Article  PubMed  CAS  Google Scholar 

  • Church TS, Barlow CE, Earnest CP, Kampert JB, Priest EL, Blair SN (2002) Associations between cardiorespiratory fitness and C-reactive protein in men. Arterioscler Thromb Vasc Biol 22:1869–1876

    Article  PubMed  CAS  Google Scholar 

  • Dawson-Hughes B (2008) Serum 25-hydroxyvitamin D and functional outcomes in the elderly. Am J Clin Nutr 88:537S–540S

    PubMed  CAS  Google Scholar 

  • Dekker MJ, Lee S, Hudson R, Kilpatrick K, Graham TE, Ross R, Robinson LE (2007) An exercise intervention without weight loss decreases circulating interleukin-6 in lean and obese men with and without type 2 diabetes mellitus. Metabolism 56:332–338

    Article  PubMed  CAS  Google Scholar 

  • Donges CE, Duffield R, Drinkwater EJ (2010) Effects of resistance or aerobic exercise training on interleukin-6, C-reactive protein, and body composition. Med Sci Sports Exerc 42:304–313

    PubMed  CAS  Google Scholar 

  • Ferrucci L, Corsi A, Lauretani F, Bandinelli S, Bartali B, Taub DD, Guralnik JM, Longo DL (2005) The origins of age-related proinflammatory state. Blood 105:2294–2299

    Article  PubMed  CAS  Google Scholar 

  • Gielen S, Adams V, Mobius-Winkler S, Linke A, Erbs S, Yu J, Kempf W, Schubert A, Schuler G, Hambrecht R (2003) Anti-inflammatory effects of exercise training in the skeletal muscle of patients with chronic heart failure. J Am Coll Cardiol 42:861–868

    Article  PubMed  CAS  Google Scholar 

  • Greiwe JS, Cheng B, Rubin DC, Yarasheski KE, Semenkovich CF (2001) Resistance exercise decreases skeletal muscle tumor necrosis factor alpha in frail elderly humans. FASEB J 15:475–482

    Article  PubMed  CAS  Google Scholar 

  • Grey A, Gamble G, Ames R, Horne A, Mason B, Reid IR (2006) Calcium supplementation does not affect CRP levels in postmenopausal women—a randomized controlled trial. Osteoporos Int 17:1141–1145

    Article  PubMed  CAS  Google Scholar 

  • Kapasi ZF, Ouslander JG, Schnelle JF, Kutner M, Fahey JL (2003) Effects of an exercise intervention on immunologic parameters in frail elderly nursing home residents. J Gerontol A Biol Sci Med Sci 58:636–643

    Article  PubMed  Google Scholar 

  • Klimcakova E, Polak J, Moro C, Hejnova J, Majercik M, Viguerie N, Berlan M, Langin D, Stich V (2006) Dynamic strength training improves insulin sensitivity without altering plasma levels and gene expression of adipokines in subcutaneous adipose tissue in obese men. J Clin Endocrinol Metab 91:5107–5112

    Article  PubMed  CAS  Google Scholar 

  • Kohut ML, McCann DA, Russell DW, Konopka DN, Cunnick JE, Franke WD, Castillo MC, Reighard AE, Vanderah E (2006) Aerobic exercise, but not flexibility/resistance exercise, reduces serum IL-18, CRP, and IL-6 independent of beta-blockers, BMI, and psychosocial factors in older adults. Brain Behav Immun 20:201–209

    Article  PubMed  CAS  Google Scholar 

  • Kukuljan S, Nowson CA, Bass SL, Sanders K, Nicholson GC, Seibel MJ, Salmon J, Daly RM (2008) Effects of a multi-component exercise program and calcium-vitamin-D3-fortified milk on bone mineral density in older men: a randomised controlled trial. Osteoporos Int 20:1241–1251

    Article  PubMed  Google Scholar 

  • Kukuljan S, Nowson CA, Sanders K, Daly RM (2009) Effects of resistance exercise and fortified milk on skeletal muscle mass, size and function in middle aged and older men: An 18-month RCT. J Appl Physiol 107:1864–1873

    Article  PubMed  CAS  Google Scholar 

  • Lambert CP, Wright NR, Finck BN, Villareal DT (2008) Exercise but not diet-induced weight loss decreases skeletal muscle inflammatory gene expression in frail obese elderly persons. J Appl Physiol 105:473–478

    Article  PubMed  CAS  Google Scholar 

  • Leger B, Derave W, De Bock K, Hespel P, Russell AP (2008) Human sarcopenia reveals an increase in SOCS-3 and myostatin and a reduced efficiency of Akt phosphorylation. Rejuvenation Res 11:163B–175B

    Google Scholar 

  • Louis E, Raue U, Yang Y, Jemiolo B, Trappe S (2007) Time course of proteolytic, cytokine, and myostatin gene expression after acute exercise in human skeletal muscle. J Appl Physiol 103:1744–1751

    Article  PubMed  CAS  Google Scholar 

  • Nicklas BJ, Brinkley TE (2009) Exercise training as a treatment for chronic inflammation in the elderly. Exerc Sport Sci Rev 37:165–170

    PubMed  Google Scholar 

  • Nicklas BJ, Ambrosius W, Messier SP, Miller GD, Penninx BW, Loeser RF, Palla S, Bleecker E, Pahor M (2004) Diet-induced weight loss, exercise, and chronic inflammation in older, obese adults: a randomized controlled clinical trial. Am J Clin Nutr 79:544–551

    PubMed  CAS  Google Scholar 

  • Nicklas BJ, Hsu FC, Brinkley TJ, Church T, Goodpaster BH, Kritchevsky SB, Pahor M (2008) Exercise training and plasma C-reactive protein and interleukin-6 in elderly people. J Am Geriatr Soc 56:2045–2052

    Article  PubMed  Google Scholar 

  • Olson TP, Dengel DR, Leon AS, Schmitz KH (2007) Changes in inflammatory biomarkers following one-year of moderate resistance training in overweight women. Int J Obes (Lond) 31:996–1003

    Article  CAS  Google Scholar 

  • Peake JM, Della Gatta P, Cameron-Smith D (2010) Aging and its effects on inflammation in skeletal muscle at rest and following exercise-induced muscle injury. Am J Physiol Regul Integr Comp Physiol 298:R1485–R1495

    Article  PubMed  CAS  Google Scholar 

  • Pearson TA, Mensah GA, Alexander RW, Anderson JL, Cannon RO 3rd, Criqui M, Fadl YY, Fortmann SP, Hong Y, Myers GL, Rifai N, Smith SC Jr, Taubert K, Tracy RP, Vinicor F (2003) Markers of inflammation and cardiovascular disease: application to clinical and public health practice: A statement for healthcare professionals from the Centers for Disease Control and Prevention and the American Heart Association. Circulation 107:499–511

    Article  PubMed  Google Scholar 

  • Penninx BW, Kritchevsky SB, Newman AB, Nicklas BJ, Simonsick EM, Rubin S, Nevitt M, Visser M, Harris T, Pahor M (2004) Inflammatory markers and incident mobility limitation in the elderly. J Am Geriatr Soc 52:1105–1113

    Article  PubMed  Google Scholar 

  • Phillips MD, Flynn MG, McFarlin BK, Stewart LK, Timmerman KL (2010) Resistance training at eight-repetition maximum reduces the inflammatory milieu in elderly women. Med Sci Sports Exerc 42:314–325

    PubMed  CAS  Google Scholar 

  • Schaap LA, Pluijm SM, Deeg DJ, Visser M (2006) Inflammatory markers and loss of muscle mass (sarcopenia) and strength. Am J Med 119:526 e529–e517

    Google Scholar 

  • Schaap LA, Pluijm SM, Deeg DJ, Harris TB, Kritchevsky SB, Newman AB, Colbert LH, Pahor M, Rubin SM, Tylavsky FA, Visser M (2009) 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 64:1183–1189

    Article  PubMed  Google Scholar 

  • Schleithoff SS, Zittermann A, Tenderich G, Berthold HK, Stehle P, Koerfer R (2006) Vitamin D supplementation improves cytokine profiles in patients with congestive heart failure: a double-blind, randomized, placebo-controlled trial. Am J Clin Nutr 83:754–759

    PubMed  CAS  Google Scholar 

  • Shi H, Norman A, Okamura W, Sen A, Zemel M (2001) 1a,25-Dihydroxyvitamin D3 modulates human adipocyte metabolism via nongenomic action. FASEB J 15:2751–2753

    PubMed  CAS  Google Scholar 

  • Stewart AL, Mills KM, King AC, Haskell WL, Gillis D, Ritter PL (2001) CHAMPS physical activity questionnaire for older adults: outcomes for interventions. Med Sci Sports Exerc 33:1126–1141

    PubMed  CAS  Google Scholar 

  • Stewart LK, Flynn MG, Campbell WW, Craig BA, Robinson JP, McFarlin BK, Timmerman KL, Coen PM, Felker J, Talbert E (2005) Influence of exercise training and age on CD14 + cell-surface expression of toll-like receptor 2 and 4. Brain Behav Immun 19:389–397

    Article  PubMed  CAS  Google Scholar 

  • Stewart LK, Flynn MG, Campbell WW, Craig BA, Robinson JP, Timmerman KL, McFarlin BK, Coen PM, Talbert E (2007) The influence of exercise training on inflammatory cytokines and C-reactive protein. Med Sci Sports Exerc 39:1714–1719

    Article  PubMed  CAS  Google Scholar 

  • Teegarden D, White KM, Lyle RM, Zemel MB, Van Loan MD, Matkovic V, Craig BA, Schoeller DA (2008) Calcium and dairy product modulation of lipid utilization and energy expenditure. Obesity (Silver Spring) 16:1566–1572

    Article  CAS  Google Scholar 

  • Tiainen K, Hurme M, Hervonen A, Luukkaala T, Jylha M (2010) Inflammatory markers and physical performance among nonagenarians. J Gerontol A Biol Sci Med Sci 65:658–663

    Article  PubMed  Google Scholar 

  • Timmerman KL, Flynn MG, Coen PM, Markofski MM, Pence BD (2008) Exercise training-induced lowering of inflammatory (CD14+CD16+) monocytes: a role in the anti-inflammatory influence of exercise? J Leukoc Biol 84:1271–1278

    Article  PubMed  CAS  Google Scholar 

  • Van den Berghe G, Van Roosbroeck D, Vanhove P, Wouters PJ, De Pourcq L, Bouillon R (2003) Bone turnover in prolonged critical illness: effect of vitamin D. J Clin Endocrinol Metab 88:4623–4632

    Article  PubMed  Google Scholar 

  • Zemel MB, Richards J, Milstead A, Campbell P (2005) Effects of calcium and dairy on body composition and weight loss in African-American adults. Obes Res 13:1218–1225

    Article  PubMed  CAS  Google Scholar 

  • Zemel MB, Sun X, Sobhani T, Wilson B (2010) Effects of dairy compared with soy on oxidative and inflammatory stress in overweight and obese subjects. Am J Clin Nutr 91:16–22

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This study was financially supported by a grant from the Australian Research Council (ARC) Linkage Scheme. Professor Robin Daly is supported by a National Health and Medical Research Council (NHMRC) Career Development Award (ID 425849). Presented at the American College of Sport Medicine Annual Meeting, Seattle, Washington, May 29, 2009. We thank Tiana Mahncke for analysing the QCT scans. We also thank Murray Goulburn Co-operative Co Ltd for providing the calcium-vitamin D3 low fat UHT fortified milk used in the study, and the City of Greater Geelong and Ocean View Health Club for their generous provision of the gymnasium facilities used throughout the study. The authors also thank the following people for contributions to this study: Shona Bass, Nicole Petrass, Joanne Daly and Sam Korn.

Author information

Authors and Affiliations

  1. The University of Queensland, School of Human Movement Studies, Brisbane, Australia

    Jonathan M. Peake

  2. The University of Queensland, Centre for Military and Veterans’ Health, Brisbane, Australia

    Jonathan M. Peake

  3. Centre for Physical Activity and Nutrition Research, School of Exercise and Nutrition Sciences, Deakin University, 221 Burwood Highway, Melbourne, Burwood, 3125, Australia

    Sonja Kukuljan, Caryl A. Nowson & Robin M. Daly

  4. Department of Clinical and Biomedical Sciences, Barwon Health, The University of Melbourne, Geelong, Australia

    Kerrie Sanders

Authors
  1. Jonathan M. Peake
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sonja Kukuljan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Caryl A. Nowson
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Kerrie Sanders
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Robin M. Daly
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Robin M. Daly.

Additional information

Communicated by William J. Kraemer.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 74 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Peake, J.M., Kukuljan, S., Nowson, C.A. et al. Inflammatory cytokine responses to progressive resistance training and supplementation with fortified milk in men aged 50+ years: an 18-month randomized controlled trial. Eur J Appl Physiol 111, 3079–3088 (2011). https://doi.org/10.1007/s00421-011-1942-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00421-011-1942-z

Keywords

Search

Navigation