The effect of exercise intensity on the inflammatory profile of cancer survivors: A randomised crossover study.


Journal

European journal of clinical investigation
ISSN: 1365-2362
Titre abrégé: Eur J Clin Invest
Pays: England
ID NLM: 0245331

Informations de publication

Date de publication:
Jul 2023
Historique:
revised: 06 03 2023
received: 15 01 2023
accepted: 11 03 2023
medline: 13 6 2023
pubmed: 16 3 2023
entrez: 15 3 2023
Statut: ppublish

Résumé

Systemic inflammation has been clearly linked to poorer health outcomes from cancer diagnosis through to survivorship. There is accumulating evidence that exercise can reduce inflammation. However, the optimal intensity of exercise to reduce systemic inflammation is unknown. The aim of this randomised crossover study was to identify the difference between high- and low-intensity aerobic exercise on the inflammatory profile of cancer survivors after a single exercise session (acute) and a short training period (six sessions over 2 weeks). Participants (n = 20) were randomised to either low- or high-intensity exercise. They underwent 2 weeks of stationary cycling at their assigned intensity and then underwent a 6-week washout period of no exercise before returning to complete 2 weeks of exercise at the remaining intensity. Twenty participants with a mean age of 56.4 (±9.4) years were enrolled and completed the intervention. There was no effect of exercise intensity after a single exercise session. After 2 weeks of training, there was a significant effect of intensity on chemokines CCL2 (mean difference ± SEM; 13.2 pg/mL ± 5.0, p = .04) and CXCL12 (150.3 pg/mL ± 51.8, p = .02), where CCL2 was decreased after low-intensity exercise and CXCL12 decreased after high-intensity exercise. Our data suggest that while exercise intensity may impact different cell types in the circulation, both low- and high-intensity exercise can positively modulate inflammatory markers. The potential to scale up low-intensity exercise over time is likely to be more broadly applicable and achievable for cancer survivor cohorts while still eliciting beneficial effects on systemic inflammation.

Sections du résumé

BACKGROUND BACKGROUND
Systemic inflammation has been clearly linked to poorer health outcomes from cancer diagnosis through to survivorship. There is accumulating evidence that exercise can reduce inflammation. However, the optimal intensity of exercise to reduce systemic inflammation is unknown.
AIMS OBJECTIVE
The aim of this randomised crossover study was to identify the difference between high- and low-intensity aerobic exercise on the inflammatory profile of cancer survivors after a single exercise session (acute) and a short training period (six sessions over 2 weeks).
METHOD METHODS
Participants (n = 20) were randomised to either low- or high-intensity exercise. They underwent 2 weeks of stationary cycling at their assigned intensity and then underwent a 6-week washout period of no exercise before returning to complete 2 weeks of exercise at the remaining intensity.
RESULTS RESULTS
Twenty participants with a mean age of 56.4 (±9.4) years were enrolled and completed the intervention. There was no effect of exercise intensity after a single exercise session. After 2 weeks of training, there was a significant effect of intensity on chemokines CCL2 (mean difference ± SEM; 13.2 pg/mL ± 5.0, p = .04) and CXCL12 (150.3 pg/mL ± 51.8, p = .02), where CCL2 was decreased after low-intensity exercise and CXCL12 decreased after high-intensity exercise.
DISCUSSION CONCLUSIONS
Our data suggest that while exercise intensity may impact different cell types in the circulation, both low- and high-intensity exercise can positively modulate inflammatory markers.
CONCLUSION CONCLUSIONS
The potential to scale up low-intensity exercise over time is likely to be more broadly applicable and achievable for cancer survivor cohorts while still eliciting beneficial effects on systemic inflammation.

Identifiants

pubmed: 36920320
doi: 10.1111/eci.13984
doi:

Types de publication

Randomized Controlled Trial Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

e13984

Informations de copyright

© 2023 The Authors. European Journal of Clinical Investigation published by John Wiley & Sons Ltd on behalf of Stichting European Society for Clinical Investigation Journal Foundation.

Références

Pierce BL, Ballard-Barbash R, Bernstein L, et al. Elevated biomarkers of inflammation are associated with reduced survival among breast cancer patients. J Clin Oncol. 2009;27(21):3437-3444.
Nie D, Gong H, Mao X, Li Z. Systemic immune-inflammation index predicts prognosis in patients with epithelial ovarian cancer: a retrospective study. Gynecol Oncol. 2019;152(2):259-264.
Zhang Y, Shi SM, Yang H, et al. Systemic inflammation score predicts survival in patients with intrahepatic cholangiocarcinoma undergoing curative resection. J Cancer. 2019;10(2):494-503.
Salgado R, Junius S, Benoy I, et al. Circulating interleukin-6 predicts survival in patients with metastatic breast cancer. Int J Cancer. 2003;103(5):642-646.
Watanabe T, Konishi T, Kishimoto J, et al. Ulcerative colitis-associated colorectal cancer shows a poorer survival than sporadic colorectal cancer: a nationwide Japanese study. Inflamm Bowel Dis. 2011;17(3):802-808.
Cleeland CS, Bennett GJ, Dantzer R, et al. Are the symptoms of cancer and cancer treatment due to a shared biologic mechanism? A cytokine-immunologic model of cancer symptoms. Cancer. 2003;97(11):2919-2925.
Bellastella G, Scappaticcio L, Esposito K, Giugliano D, Maiorino MI. Metabolic syndrome and cancer: the common soil hypothesis. Diabetes Res Clin Pract. 2018;143:389-397.
Giza DE, Iliescu G, Hassan S, Marmagkiolis K, Iliescu C. Cancer as a risk factor for cardiovascular disease. Curr Oncol Rep. 2017;19(6):39.
Orre IJ, Reinertsen KV, Aukrust P, et al. Higher levels of fatigue are associated with higher CRP levels in disease-free breast cancer survivors. J Psychosom Res. 2011;71(3):136-141.
Schmitz KH, Speck RM. Risks and benefits of physical activity among breast cancer survivors who have completed treatment. Womens Health. 2010;6(2):221-238.
Irwin ML, Cartmel B, Gross CP, et al. Randomized exercise trial of aromatase inhibitor-induced arthralgia in breast cancer survivors. J Clin Oncol. 2015;33(10):1104-1111.
Sandler C, Goldstein D, Horsfield S, et al. TOPS: a randomised controlled trial of a multidisciplinary intervention for post-cancer fatigue. J Clin Oncol. 2015;33(15_suppl):9571.
Meneses-Echavez JF, Gonzalez-Jimenez E, Ramirez-Velez R. Supervised exercise reduces cancer-related fatigue: a systematic review. J Physiother. 2015;61(1):3-9.
Meneses-Echavez JF, Gonzalez-Jimenez E, Ramirez-Velez R. Effects of supervised multimodal exercise interventions on cancer-related fatigue: systematic review and meta-analysis of randomized controlled trials. Biomed Res Int. 2015;2015:328636.
Ballard-Barbash R, Friedenreich CM, Courneya KS, Siddiqi SM, McTiernan A, Alfano CM. Physical activity, biomarkers, and disease outcomes in cancer survivors: a systematic review. J Natl Cancer Inst. 2012;104(11):815-840.
Gleeson M, Bishop NC, Stensel DJ, Lindley MR, Mastana SS, Nimmo MA. The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol. 2011;11(9):607-615.
Murphy EA, Enos RT, Velazquez KT. Influence of exercise on inflammation in cancer: direct effect or innocent bystander? Exerc Sport Sci Rev. 2015;43(3):134-142.
Kruijsen-Jaarsma M, Révész D, Bierings MB, Buffart LM, Takken T. Effects of exercise on immune function in patients with cancer: a systematic review. Exerc Immunol Rev. 2013;19:120-143.
Ostrowski K, Schjerling P, Pedersen BK. Physical activity and plasma interleukin-6 in humans-effect of intensity of exercise. Eur J Appl Physiol. 2000;83(6):512-515.
Scott JP, Sale C, Greeves JP, Casey A, Dutton J, Fraser WD. Effect of exercise intensity on the cytokine response to an acute bout of running. Med Sci Sports Exerc. 2011;43(12):2297-2306.
Clifford BK, Mizrahi D, Sandler CX, et al. Barriers and facilitators of exercise experienced by cancer survivors: a mixed methods systematic review. Support Care Cancer. 2018;26(3):685-700.
Duncan M, Moschopoulou E, Herrington E, et al. Review of systematic reviews of non-pharmacological interventions to improve quality of life in cancer survivors. BMJ Open. 2017;7(11):e015860.
Tang MF, Liou TH, Lin CC. Improving sleep quality for cancer patients: benefits of a home-based exercise intervention. Support Care Cancer. 2010;18(10):1329-1339.
Simera I, Moher D, Hoey J, Schulz KF, Altman DG. A catalogue of reporting guidelines for health research. Eur J Clin Invest. 2010;40(1):35-53.
Beekley MD, Brechue WF, Dehoyos DV, Garzarella L, Werber-Zion G, Pollock* ML. Cross-validation of the YMCA submaximal cycle ergometer test to predict VO2max. Res Q Exerc Sport. 2004;75(3):337-342.
Borg G. Ratings of perceived exertion and heart rates during short-term cycle exercise and their use in a new cycling strength test. Int J Sports Med. 1982;3(3):153-158.
Schell J, Leelarthaepin B. Physical Fitness Assessment in Exercise and Sport Science. 2nd ed. Leelar Biomediscience Services; 1994.
Karvonen MJ, Kentala E, Mustala O. The effects of training on heart rate; a longitudinal study. Ann Med Exp Biol Fenn. 1957;35(3):307-315.
Davis JA, Convertino VA. A comparison of heart rate methods for predicting endurance training intensity. Med Sci Sports. 1975;7(4):295-298.
Viana JL, Kosmadakis GC, Watson EL, et al. Evidence for anti-inflammatory effects of exercise in CKD. J Am Soc Nephrol. 2014;25(9):2121-2130.
Perandini LA, Sales-de-Oliveira D, Mello S, et al. Inflammatory cytokine kinetics to single bouts of acute moderate and intense aerobic exercise in women with active and inactive systemic lupus erythematosus. Exerc Immunol Rev. 2015;21:174-185.
Fritz CO, Morris PE, Richler JJ. Effect size estimates: current use, calculations, and interpretation. J Exp Psychol Gen. 2012;141(1):2-18.
Anderson MJ, Gorley RN, Clarke KR. PERMANOVA+ for PRIMER: Guide to Software and Statistical Methods. PRIMER-E; 2008:214.
Arend WP, Malyak M, Guthridge CJ, Gabay C. Interleukin-1 receptor antagonist: role in biology. Annu Rev Immunol. 1998;16:27-55.
Docherty S, Harley R, McAuley JJ, et al. The effect of exercise on cytokines: implications for musculoskeletal health: a narrative review. BMC Sports Sci Med Rehabil. 2022;14(1):5.
Pedersen BK, Febbraio MA. Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev. 2008;88(4):1379-1406.
Meneses-Echávez JF, Correa-Bautista JE, González-Jiménez E, et al. The effect of exercise training on mediators of inflammation in breast cancer survivors: a systematic review with meta-analysis. Cancer Epidemiol Biomarkers Prev. 2016;25(7):1009-1017.
Deshmane SL, Kremlev S, Amini S, Sawaya BE. Monocyte chemoattractant protein-1 (MCP-1): an overview. J Interferon Cytokine Res. 2009;29(6):313-326.
Metzemaekers M, Gouwy M, Proost P. Neutrophil chemoattractant receptors in health and disease: double-edged swords. Cell Mol Immunol. 2020;17(5):433-450.
Cerqueira É, Marinho DA, Neiva HP, Lourenço O. Inflammatory effects of high and moderate intensity exercise-a systematic review. Front Physiol. 2019;10:1550.
Nieman DC, Wentz LM. The compelling link between physical activity and the body's defense system. J Sport Health Sci. 2019;8(3):201-217.
Rose GL, Skinner TL, Mielke GI, Schaumberg MA. The effect of exercise intensity on chronic inflammation: a systematic review and meta-analysis. J Sci Med Sport. 2021;24(4):345-351.
Kleckner IR, Kamen C, Cole C, et al. Effects of exercise on inflammation in patients receiving chemotherapy: a nationwide NCORP randomized clinical trial. Support Care Cancer. 2019;27(12):4615-4625.
Krishnan U, Singh H, Tedla N, Leach ST, Kaakoush NO. Presence of gastric pepsinogen in the trachea is associated with altered inflammation and microbial composition. Infect Immun. 2020;88(12):e00455-20.
Sardeli AV, Tomeleri CM, Cyrino ES, Fernhall B, Cavaglieri CR, Chacon-Mikahil MPT. Effect of resistance training on inflammatory markers of older adults: a meta-analysis. Exp Gerontol. 2018;111:188-196.
Tran B, Vajdic CM, Webber K, et al. Self-reported health, lifestyle and social circumstances of Australian adult cancer survivors: a propensity score weighted cross-sectional study. Cancer Epidemiol. 2020;67:101773.

Auteurs

Briana K Clifford (BK)

School of Health Sciences, UNSW, Sydney, New South Wales, Australia.
School of Nursing, Midwifery and Social Work, University of Queensland, Brisbane, Queensland, Australia.

Nadeem O Kaakoush (NO)

School of Biomedical Sciences, UNSW, New South Wales, Sydney, Australia.

Nicodemus Tedla (N)

School of Biomedical Sciences, UNSW, New South Wales, Sydney, Australia.

David Goldstein (D)

School of Clinical Medicine, UNSW, New South Wales, Sydney, Australia.
Prince of Wales Hospital, Randwick, New South Wales, Australia.

David Simar (D)

School of Health Sciences, UNSW, Sydney, New South Wales, Australia.

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