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Breast Cancer Research and Treatment

, Volume 155, Issue 3, pp 471–482 | Cite as

The effect of resistance training on markers of immune function and inflammation in previously sedentary women recovering from breast cancer: a randomized controlled trial

  • Amanda D. Hagstrom
  • Paul W. M. Marshall
  • Chris Lonsdale
  • Shona Papalia
  • Birinder S. Cheema
  • Catherine Toben
  • Bernhard T. Baune
  • Maria A. Fiatarone Singh
  • Simon Green
Clinical trial

Abstract

The purpose of this randomized controlled trial was to determine the effects of resistance training (RT) on markers of inflammation and immune function in breast cancer survivors. Thirty-nine breast cancer survivors were randomly assigned to a RT (n = 20) or control (n = 19) group. RT performed supervized exercise three times per week. Natural killer cell (NK) and natural killer T-cell (NKT) function, and markers of inflammation (serum TNF-α, IL-6, IL-10, and CRP) were measured before and after training. Changes in NK and NKT cell function were analyzed using ANCOVA, with the change score the dependent variable, and the baseline value of the same variable the covariate. Effect sizes (ES) were calculated via partial eta-squared. We found a significant reduction, and large associated ESs, in the RT group compared to the control group for change in NK cell expression of TNF-α (p = 0.005, ES = 0.21) and NKT cell expression of TNF-α (p = 0.04, ES = 0.12). No differences were observed in any serum marker. Significant improvements in all measurements of strength were found in RT compared to control (p < 0.001; large ESs ranging from 0.32 to 0.51). These data demonstrate that RT has a beneficial effect on the NK and NKT cell expression of TNF-α indicating that RT may be beneficial in improving the inflammatory profile in breast cancer survivors.

Keywords

Resistance training Immune function Inflammation Breast cancer survivors 

Notes

Acknowledgments

This study was supported by a grant from Western Sydney University, Australia.

Conflict of interest

All authors acknowledge that there are no conflicts of interest.

References

  1. 1.
    Garcia M, Jemal A, Ward E (2007) Global cancer facts and figures 2007. American Cancer Society, AtlantaGoogle Scholar
  2. 2.
    Cunningham-Rundles S, Filippa DA, Braun DW Jr, Antonelli P, Ashikari H (1981) Natural cytotoxicity of peripheral blood lymphocytes and regional lymph node cells in breast cancer in women. J Natl Cancer Inst 67(3):585–590PubMedGoogle Scholar
  3. 3.
    Tsavaris N, Kosmas C, Vadiaka M, Kanelopoulos P, Boulamatsis D (2002) Immune changes in patients with advanced breast cancer undergoing chemotherapy with taxanes. Br J Cancer 87(1):21–27PubMedCentralCrossRefPubMedGoogle Scholar
  4. 4.
    White D, Jones DB, Cooke T, Kirkham N (1982) Natural killer (NK) activity in peripheral blood lymphocytes of patients with benign and malignant breast disease. Br J Cancer 46(4):611–616PubMedCentralCrossRefPubMedGoogle Scholar
  5. 5.
    Whiteside TL, Vujanovic NL, Herberman RB (1998) Natural killer cells and tumor therapy. Curr Top Microbiol Immunol 230:221–244PubMedGoogle Scholar
  6. 6.
    Whiteside TL, Herberman RB (1995) The role of natural killer cells in immune surveillance of cancer. Curr Opin Immunol 7(5):704–710CrossRefPubMedGoogle Scholar
  7. 7.
    Dewan MZ, Terunuma H, Takada M, Tanaka Y, Abe H, Sata T, Toi M, Yamamoto N (2007) Role of natural killer cells in hormone-independent rapid tumor formation and spontaneous metastasis of breast cancer cells in vivo. Breast Cancer Res Treat 104(3):267–275CrossRefPubMedGoogle Scholar
  8. 8.
    Gorelik E, Wiltrout RH, Okumura K, Habu S, Herberman RB (1982) Role of NK cells in the control of metastatic spread and growth of tumor cells in mice. Int J Cancer 30(1):107–112CrossRefPubMedGoogle Scholar
  9. 9.
    Perussia B (1991) Lymphokine-activated killer cells, natural killer cells and cytokines. Curr Opin Immunol 3(1):49–55CrossRefPubMedGoogle Scholar
  10. 10.
    Trapani JA, Smyth MJ (2002) Functional significance of the perforin/granzyme cell death pathway. Nat Rev Immunol 2(10):735–747CrossRefPubMedGoogle Scholar
  11. 11.
    Robertson MJ (2002) Role of chemokines in the biology of natural killer cells. J Leukoc Biol 71(2):173–183PubMedGoogle Scholar
  12. 12.
    Szlosarek P, Charles KA, Balkwill FR (2006) Tumour necrosis factor-alpha as a tumour promoter. Eur J Cancer 42(6):745–750CrossRefPubMedGoogle Scholar
  13. 13.
    Arai KI, Lee F, Miyajima A, Miyatake S, Arai N, Yokota T (1990) Cytokines: coordinators of immune and inflammatory responses. Annu Rev Biochem 59:783–836CrossRefPubMedGoogle Scholar
  14. 14.
    Smyth MJ, Godfrey DI (2000) NKT cells and tumor immunity–a double-edged sword. Nat Immunol 1(6):459–460CrossRefPubMedGoogle Scholar
  15. 15.
    Godfrey DI, Hammond KJ, Poulton LD, Smyth MJ, Baxter AG (2000) NKT cells: facts, functions and fallacies. Immunol Today 21(11):573–583CrossRefPubMedGoogle Scholar
  16. 16.
    Bauernhofer T, Kuss I, Henderson B, Baum AS, Whiteside TL (2003) Preferential apoptosis of CD56dim natural killer cell subset in patients with cancer. Eur J Immunol 33(1):119–124CrossRefPubMedGoogle Scholar
  17. 17.
    Blomgren H, Baral E, Edsmyr F, Strender LE, Petrini B, Wasserman J (1980) Natural killer activity in peripheral lymphocyte population following local radiation therapy. Acta Radiol Oncol 19(2):139–143CrossRefPubMedGoogle Scholar
  18. 18.
    Whiteside TL, Herberman RB (1994) Role of human natural killer cells in health and disease. Clin Diagn Lab Immunol 1(2):125–133PubMedCentralPubMedGoogle Scholar
  19. 19.
    Garner WL, Minton JP, James AG, Hoffmann CC (1983) Human breast cancer and impaired NK cell function. J Surg Oncol 24(1):64–66CrossRefPubMedGoogle Scholar
  20. 20.
    Blomgren H, Baral E, Edsmyr F, Strender L, Petrini B, Wasserman J (1980) Natural killer activity in peripheral lymphocyte population following local radiation therapy. Acta Radiol Oncol 19:139–143CrossRefPubMedGoogle Scholar
  21. 21.
    Levy S, Herberman R, Lippman M, d’Angelo T (1987) Correlation of stress factors with sustained depression of natural killer cell activity and predicted prognosis in patients with breast cancer. J Clin Oncol 5(3):348–353PubMedGoogle Scholar
  22. 22.
    Garner WL, Minton JP, James AG, Hoffman CC (1983) Human breast cancer and impaired NK cell function. J Surg Oncol 24:64–66CrossRefPubMedGoogle Scholar
  23. 23.
    Beitsch P, Lotzova E, Hortobagyi G, Pollock R (1994) Natural immunity in breast cancer patients during neoadjuvant chemotherapy and after surgery. Surg Oncol 3(4):211–219CrossRefPubMedGoogle Scholar
  24. 24.
    Mock V, Pickett M, Ropka ME, Muscari Lin E, Stewart KJ, Rhodes VA, McDaniel R, Grimm PM, Krumm PM, McCorkle R (2001) Fatigue and quality of life outcomes of exercise during cancer treatment. Cancer Pract 9(3):119–127CrossRefPubMedGoogle Scholar
  25. 25.
    Sewell HF, Halbert CF, Robins RA, Galvin A, Chan S, Blamey RW (1993) Chemotherapy-induced differential changes in lymphocyte subsets and natural-killer-cell function in patients with advanced breast cancer. Int J Cancer 55(5):735–738CrossRefPubMedGoogle Scholar
  26. 26.
    Solomayer EF, Feuerer M, Bai L, Umansky V, Beckhove P, Meyberg GC, Bastert G, Schirrmacher V, Diel IJ (2003) Influence of adjuvant hormone therapy and chemotherapy on the immune system analysed in the bone marrow of patients with breast cancer. Clin Cancer Res 9(1):174–180PubMedGoogle Scholar
  27. 27.
    Szlosarek PW, Balkwill FR (2003) Tumour necrosis factor alpha: a potential target for the therapy of solid tumours. Lancet Oncol 4(9):565–573CrossRefPubMedGoogle Scholar
  28. 28.
    Leek RD, Landers R, Fox SB, Ng F, Harris AL, Lewis CE (1998) Association of tumour necrosis factor alpha and its receptors with thymidine phosphorylase expression in invasive breast carcinoma. Br J Cancer 77(12):2246–2251PubMedCentralCrossRefPubMedGoogle Scholar
  29. 29.
    Hanahan D, Weinberg RA (2000) The hallmarks of cancer. Cell 100(1):57–70CrossRefPubMedGoogle Scholar
  30. 30.
    Hagemann T, Wilson J, Kulbe H, Li NF, Leinster DA, Charles K, Klemm F, Pukrop T, Binder C, Balkwill FR (2005) Macrophages induce invasiveness of epithelial cancer cells via NF-kappa B and JNK. J Immunol 175(2):1197–1205CrossRefPubMedGoogle Scholar
  31. 31.
    Fairey AS, Courneya KS, Field CJ, Bell GJ, Jones LW, Mackey JR (2005) Randomized controlled trial of exercise and blood immune function in postmenopausal breast cancer survivors. J Appl Physiol 98(4):1534–1540CrossRefPubMedGoogle Scholar
  32. 32.
    Galvao DA, Taaffe DR, Spry N, Joseph D, Newton RU (2010) Combined resistance and aerobic exercise program reverses muscle loss in men undergoing androgen suppression therapy for prostate cancer without bone metastases: a randomized controlled trial. J Clin Oncol 28(2):340–347CrossRefPubMedGoogle Scholar
  33. 33.
    Gomez AM, Martinez C, Fiuza-Luces C, Herrero F, Perez M, Madero L, Ruiz JR, Lucia A, Ramirez M (2011) Exercise training and cytokines in breast cancer survivors. Int J Sports Med 32(6):461–467CrossRefPubMedGoogle Scholar
  34. 34.
    Na YM, Kim MY, Kim YK, Ha YR, Yoon DS (2000) Exercise therapy effect on natural killer cell cytotoxic activity in stomach cancer patients after curative surgery. Arch Phys Med Rehabil 81(6):777–779CrossRefPubMedGoogle Scholar
  35. 35.
    Peters C, Lotzerich H, Niemeier B, Schule K, Uhlenbruck G (1994) Influence of a moderate exercise training on natural killer cytotoxicity and personality traits in cancer patients. Anticancer Res 14(3A):1033–1036PubMedGoogle Scholar
  36. 36.
    Nieman DC, Cook VD, Henson DA, Suttles J, Rejeski WJ, Ribisl PM, Fagoaga OR, Nehlsen-Cannarella SL (1995) Moderate exercise training and natural killer cell cytotoxic activity in breast cancer patients. Int J Sports Med 16(5):334–337CrossRefPubMedGoogle Scholar
  37. 37.
    Hutnick N, Williams N, Kraemer W, Osega-Smith E, Dixon R, Bleznak A, Mastro A (2005) Exercise and lymphocyte activation following chemotherapy for breast cancer. Med Sci Sports Exerc 37(11):1827–1835CrossRefPubMedGoogle Scholar
  38. 38.
    Galvao DA, Nosaka K, Taaffe DR, Peake J, Spry N, Suzuki K, Yamaya K, McGuigan MR, Kristjanson LJ, Newton RU (2008) Endocrine and immune responses to resistance training in prostate cancer patients. Prostate Cancer Prostatic Dis 11(2):160–165CrossRefPubMedGoogle Scholar
  39. 39.
    Chung HY, Cesari M, Anton S, Marzetti E, Giovannini S, Seo AY, Carter C, Yu BP, Leeuwenburgh C (2009) Molecular inflammation: underpinnings of aging and age-related diseases. Ageing Res Rev 8(1):18–30PubMedCentralCrossRefPubMedGoogle Scholar
  40. 40.
    Cordova C, Lopes ESF Jr, Pires AS, Souza VC, Brito CJ, Moraes CF, Sposito AC, Nobrega OT (2011) Long-term resistance training is associated with reduced circulating levels of IL-6, IFN-gamma and TNF-alpha in elderly women. Neuroimmunomodulation 18(3):165–170CrossRefPubMedGoogle Scholar
  41. 41.
    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(2):475–482CrossRefPubMedGoogle Scholar
  42. 42.
    McFarlin BK, Flynn MG, Phillips MD, Stewart LK, Timmerman KL (2005) Chronic resistance exercise training improves natural killer cell activity in older women. J Gerontol A Biol Sci Med Sci 60(10):1315–1318CrossRefPubMedGoogle Scholar
  43. 43.
    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(2):314–325CrossRefPubMedGoogle Scholar
  44. 44.
    Pedersen B, Steensberg A, Fischer C, Keller C, Keller P, Plomgaard P, Febbraio M, Saltin B (2003) Searching for the exercise factor: is IL-6 a candidate? J Muscle Res Cell Motil 24(2–3):113–119CrossRefPubMedGoogle Scholar
  45. 45.
    Petersen AMW, Pedersen BK (2005) The anti-inflammatory effect of exercise. J Appl Physiol 98(4):1154–1162CrossRefPubMedGoogle Scholar
  46. 46.
    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(3):201–209CrossRefPubMedGoogle Scholar
  47. 47.
    Heled Y, Dror Y, Moran DS, Rosenzweig T, Sampson SR, Epstein Y, Meyerovitch J (2005) Physical exercise increases the expression of TNFalpha and GLUT 1 in muscle tissue of diabetes prone Psammomys obesus. Life Sci 77(23):2977–2985CrossRefPubMedGoogle Scholar
  48. 48.
    Visser M, Pahor M, Taaffe DR, Goodpaster BH, Simonsick EM, Newman AB, Nevitt M, Harris TB (2002) Relationship of interleukin-6 and tumor necrosis factor-alpha with muscle mass and muscle strength in elderly men and women: the Health ABC Study. J Gerontol A Biol Sci Med Sci 57(5):M326–M332CrossRefPubMedGoogle Scholar
  49. 49.
    Ohira T, Schmitz KH, Ahmed RL, Yee D (2006) Effects of weight training on quality of life in recent breast cancer survivors: the weight training for breast cancer survivors (WTBS) study. Cancer 106(9):2076–2083CrossRefPubMedGoogle Scholar
  50. 50.
    Schmitz KH, Ahmed RL, Hannan PJ, Yee D (2005) Safety and efficacy of weight training in recent breast cancer survivors to alter body composition, insulin, and insulin-like growth factor axis proteins. Cancer Epidemiol Biomark Prev 14(7):1672–1680CrossRefGoogle Scholar
  51. 51.
    Cheema B, Gaul C (2006) Full-body exercise training improves fitness and quality of life in survivors of breast cancer. J Strength Cond Res 20(1):14–21PubMedGoogle Scholar
  52. 52.
    Schmitz K, Ahmed R, Troxel A, Cheville A, Smith R, Lewis-Grant L, Bryan C, Williams-Smith C, Greene Q (2009) Weight lifting in women with breast-cancer-related lymphedema. N Engl J Med 361:664–673CrossRefPubMedGoogle Scholar
  53. 53.
    Musanti R (2012) A study of exercise modality and physical self-esteem in breast cancer survivors. Med Sci Sports Exerc 44:352–361CrossRefPubMedGoogle Scholar
  54. 54.
    Waltman NL, Twiss JJ, Ott CD, Gross GJ, Lindsey AM, Moore TE, Berg K, Kupzyk K (2010) The effect of weight training on bone mineral density and bone turnover in postmenopausal breast cancer survivors with bone loss: a 24-month randomized controlled trial. Osteoporos Int 21(8):1361–1369CrossRefPubMedGoogle Scholar
  55. 55.
    Winters-Stone KM, Dobek J, Nail L, Bennett JA, Leo MC, Naik A, Schwartz A (2011) Strength training stops bone loss and builds muscle in postmenopausal breast cancer survivors: a randomized, controlled trial. Breast Cancer Res Treat 127(2):447–456PubMedCentralCrossRefPubMedGoogle Scholar
  56. 56.
    Hagstrom AD, Marshall PW, Lonsdale C, Cheema BS, Fiatarone Singh MA, Green S (2015) Resistance training improves fatigue and quality of life in previously sedentary breast cancer survivors: a randomised controlled trial. Eur J Cancer Care. doi: 10.1111/ecc.12422
  57. 57.
    Shimano T, Kraemer WJ, Spiering BA, Volek JS, Hatfield DL, Silvestre R, Vingren JL, Fragala MS, Maresh CM, Fleck SJ et al (2006) Relationship between the number of repetitions and selected percentages of one repetition maximum in free weight exercises in trained and untrained men. J Strength Cond Res 20(4):819–823PubMedGoogle Scholar
  58. 58.
    Hodge G, Hodge S, Li-Liew C, Reynolds PN, Holmes M (2012) Increased natural killer T-like cells are a major source of pro-inflammatory cytokines and granzymes in lung transplant recipients. Respirology 17(1):155–163CrossRefPubMedGoogle Scholar
  59. 59.
    Hodge G, Hodge S, Reynolds P, Holmes M (2005) Intracellular cytokines in blood T cells in lung transplant patients—a more relevant indicator of immunosuppression than drug levels. Clin Exp Immunol 139(1):159–164PubMedCentralCrossRefPubMedGoogle Scholar
  60. 60.
    Marfell-Jones M, Olds T, Stewart A, Carter L (2007) International Standards for Anthropometric AssessmentGoogle Scholar
  61. 61.
    Yuhasz MS (1974) Physical fitness and sports appraisal laboratory manual. University of Western Ontario, LondonGoogle Scholar
  62. 62.
    Pallant J (2013) SPSS survival manual. McGraw-Hill International, New YorkGoogle Scholar
  63. 63.
    Fairey AS, Courneya KS, Field CJ, Bell GJ, Jones LW, Martin BS, Mackey JR (2005) Effect of exercise training on C-reactive protein in postmenopausal breast cancer survivors: a randomized controlled trial. Brain Behav Immun 19(5):381–388CrossRefPubMedGoogle Scholar
  64. 64.
    Rifai N, Ridker PM (2001) High-sensitivity C-reactive protein: a novel and promising marker of coronary heart disease. Clin Chem 47(3):403–411PubMedGoogle Scholar
  65. 65.
    Kraemer WJ, Staron RS, Hagerman FC, Hikida RS, Fry AC, Gordon SE, Nindl BC, Gothshalk LA, Volek JS, Marx JO et al (1998) The effects of short-term resistance training on endocrine function in men and women. Eur J Appl Physiol Occup Physiol 78(1):69–76CrossRefPubMedGoogle Scholar
  66. 66.
    Lu SS, Lau CP, Tung YF, Huang SW, Chen YH, Shih HC, Tsai SC, Lu CC, Wang SW, Chen JJ et al (1996) Lactate stimulates progesterone secretion via an increase in cAMP production in exercised female rats. Am J Physiol 271(5 Pt 1):E910–E915PubMedGoogle Scholar
  67. 67.
    Lu SS, Lau CP, Tung YF, Huang SW, Chen YH, Shih HC, Tsai SC, Lu CC, Wang SW, Chen JJ et al (1997) Lactate and the effects of exercise on testosterone secretion: evidence for the involvement of a cAMP-mediated mechanism. Med Sci Sports Exerc 29(8):1048–1054CrossRefPubMedGoogle Scholar
  68. 68.
    Kast RE, Altschuler EL (2005) Anti-apoptosis function of TNF-alpha in chronic lymphocytic leukemia: lessons from Crohn’s disease and the therapeutic potential of bupropion to lower TNF-alpha. Arch Immunol Ther Exp 53(2):143–147Google Scholar
  69. 69.
    Toth MJ, Matthews DE, Tracy RP, Previs MJ (2005) Age-related differences in skeletal muscle protein synthesis: relation to markers of immune activation. Am J Physiol Endocrinol Metab 288(5):E883–E891CrossRefPubMedGoogle Scholar
  70. 70.
    Li Q, Morimoto K, Nakadai A, Qu T, Matsushima H, Katsumata M, Shimizu T, Inagaki H, Hirata Y, Hirata K et al (2007) Healthy lifestyles are associated with higher levels of perforin, granulysin and granzymes A/B-expressing cells in peripheral blood lymphocytes. Prev Med 44(2):117–123CrossRefPubMedGoogle Scholar
  71. 71.
    Staats R, Balkow S, Sorichter S, Northoff H, Matthys H, Luttmann W, Berg A, Virchow JC (2000) Change in perforin-positive peripheral blood lymphocyte (PBL) subpopulations following exercise. Clin Exp Immunol 120(3):434–439PubMedCentralCrossRefPubMedGoogle Scholar
  72. 72.
    Peng YP, Zhu Y, Zhang JJ, Xu ZK, Qian ZY, Dai CC, Jiang KR, Wu JL, Gao WT, Li Q et al (2013) Comprehensive analysis of the percentage of surface receptors and cytotoxic granules positive natural killer cells in patients with pancreatic cancer, gastric cancer, and colorectal cancer. J Transl Med 11:262PubMedCentralCrossRefPubMedGoogle Scholar
  73. 73.
    Grossman WJ, Verbsky JW, Tollefsen BL, Kemper C, Atkinson JP, Ley TJ (2004) Differential expression of granzymes A and B in human cytotoxic lymphocyte subsets and T regulatory cells. Blood 104(9):2840–2848CrossRefPubMedGoogle Scholar
  74. 74.
    Bratke K, Kuepper M, Bade B, Virchow JC Jr, Luttmann W (2005) Differential expression of human granzymes A, B, and K in natural killer cells and during CD8+ T cell differentiation in peripheral blood. Eur J Immunol 35(9):2608–2616CrossRefPubMedGoogle Scholar
  75. 75.
    Bade B, Boettcher HE, Lohrmann J, Hink-Schauer C, Bratke K, Jenne DE, Virchow JC Jr, Luttmann W (2005) Differential expression of the granzymes A, K and M and perforin in human peripheral blood lymphocytes. Int Immunol 17(11):1419–1428CrossRefPubMedGoogle Scholar
  76. 76.
    Ahmed R, Thomas W, Yee D, Schmitz K (2006) Randomized controlled trial of weight training and lymphedema in breast cancer survivors. J Clin Oncol 24(18):2765–2772CrossRefPubMedGoogle Scholar
  77. 77.
    Courneya K, Segal R, Mackey J, Gelmon K, Reid R, Friedenreich C, Ladha A, Proulx C, Vallance J, Lane K et al (2007) Effects of aerobic and resistance exercise in breast cancer patients receiving adjuvant chemotheraphy: a multicenter randomized controlled trial. J Clin Oncol 25(28):4396–4404CrossRefPubMedGoogle Scholar
  78. 78.
    Schmitz KH, Troxel AB, Cheville A, Grant LL, Bryan CJ, Gross CR, Lytle LA, Ahmed RL (2009) Physical activity and lymphedema (the PAL trial): assessing the safety of progressive strength training in breast cancer survivors. Contemp Clin Trials 30(3):233–245PubMedCentralCrossRefPubMedGoogle Scholar
  79. 79.
    Schwartz AL, Winters-Stone K, Gallucci B (2007) Exercise effects on bone mineral density in women with breast cancer receiving adjuvant chemotherapy. Oncol Nurs Forum 34(3):627–633CrossRefPubMedGoogle Scholar
  80. 80.
    Winters-Stone KM, Dobek J, Bennett JA, Nail LM, Leo MC, Schwartz A (2012) The effect of resistance training on muscle strength and physical function in older, postmenopausal breast cancer survivors: a randomized controlled trial. J Cancer Surviv 6(2):189–199PubMedCentralCrossRefPubMedGoogle Scholar
  81. 81.
    American College of Sports Medicine position stand (2009) Progression models in resistance training for healthy adults. Med Sci Sports Exerc 41(3):687–708CrossRefGoogle Scholar
  82. 82.
    Nakashima J, Tachibana M, Ueno M, Miyajima A, Baba S, Murai M (1998) Association between tumor necrosis factor in serum and cachexia in patients with prostate cancer. Clin Cancer Res 4(7):1743–1748PubMedGoogle Scholar
  83. 83.
    Gratacos J, Collado A, Filella X, Sanmarti R, Canete J, Llena J, Molina R, Ballesta A, Munoz-Gomez J (1994) Serum cytokines (IL-6, TNF-alpha, IL-1 beta and IFN-gamma) in ankylosing spondylitis: a close correlation between serum IL-6 and disease activity and severity. Br J Rheumatol 33(10):927–931CrossRefPubMedGoogle Scholar
  84. 84.
    Winkler G, Lakatos P, Salamon F, Nagy Z, Speer G, Kovacs M, Harmos G, Dworak O, Cseh K (1999) Elevated serum TNF-alpha level as a link between endothelial dysfunction and insulin resistance in normotensive obese patients. Diabet Med 16(3):207–211CrossRefPubMedGoogle Scholar
  85. 85.
    Beutler BA, Milsark IW, Cerami A (1985) Cachectin/tumor necrosis factor: production, distribution, and metabolic fate in vivo. J Immunol 135(6):3972–3977PubMedGoogle Scholar
  86. 86.
    Selby P, Hobbs S, Viner C, Jackson E, Jones A, Newell D, Calvert AH, McElwain T, Fearon K, Humphreys J et al (1987) Tumour necrosis factor in man: clinical and biological observations. Br J Cancer 56(6):803–808PubMedCentralCrossRefPubMedGoogle Scholar
  87. 87.
    Allgayer H, Nicolaus S, Schreiber S (2004) Decreased interleukin-1 receptor antagonist response following moderate exercise in patients with colorectal carcinoma after primary treatment. Cancer Detect Prev 28(3):208–213CrossRefPubMedGoogle Scholar
  88. 88.
    Battaglini CL, Hackney AC, Garcia R, Groff D, Evans E, Shea T (2009) The effects of an exercise program in leukemia patients. Integr Cancer Ther 8(2):130–138CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2016

Authors and Affiliations

  • Amanda D. Hagstrom
    • 1
    • 2
  • Paul W. M. Marshall
    • 2
  • Chris Lonsdale
    • 3
  • Shona Papalia
    • 2
  • Birinder S. Cheema
    • 2
    • 4
  • Catherine Toben
    • 5
  • Bernhard T. Baune
    • 5
  • Maria A. Fiatarone Singh
    • 6
    • 7
  • Simon Green
    • 2
    • 8
  1. 1.School of Science and TechnologyUniversity New EnglandArmidaleAustralia
  2. 2.School of Science and HealthWestern Sydney UniversityCampbelltownAustralia
  3. 3.Institute for Positive Psychology and EducationAustralian Catholic UniversityStrathfieldAustralia
  4. 4.The National Institute of Complementary Medicine (NICM)Western Sydney UniversityCampbelltownAustralia
  5. 5.School of MedicineUniversity of AdelaideAdelaideAustralia
  6. 6.Exercise, Health and Performance Research Group and Sydney Medical SchoolUniversity of SydneySydneyAustralia
  7. 7.Hebrew Senior-Life and Jean Mayer USDA Human Nutrition Center on Aging at Tufts UniversityBostonUSA
  8. 8.School of MedicineWestern Sydney UniversityCampbelltownAustralia

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