Abstract
Purpose
Type 2 diabetes has been associated with an increase in inflammatory and endothelial biomarkers, which are associated with an increased risk of cardiovascular disease and diabetes-related complications. This study examined the effects of high-intensity progressive resistance training (PRT) with moderate weight loss (WL) versus WL alone on inflammatory and endothelial biomarkers in older overweight adults with type 2 diabetes.
Methods
This was a 12-month randomized controlled trial in which 36 inactive, overweight adults aged 60–80 years with poorly controlled type 2 diabetes were randomized to 6 months of supervised PRT + WL or stretching (sham) exercise plus WL followed by 6 months of home-training without dietary modification. Fasted blood samples were collected at baseline and subsequent 3-month intervals with the following inflammatory [interleukin (IL)-10, IL-6, tumor necrosis factor (TNF)-α, adiponectin] and endothelial markers [resistin and intercellular adhesion molecule (ICAM)-1)] assessed.
Results
No significant within-group changes or between-group differences were detected for any inflammatory or endothelial biomarker following the 6-month supervised exercise and WL phase. There was a greater reduction in IL-10 at 9 months in the PRT + WL relative to WL group (P = 0.033). There was also a greater reduction in TNF-α at 9 and 12 months in the PRT + WL relative to WL group (P = 0.026 and P = 0.024, respectively). Serum adiponectin increased in the PRT + WL relative to WL group after 12 months (P = 0.036). All results were adjusted for baseline values, age, weight, sex, diabetes duration, medication use and any change in medication.
Conclusions
Long-term participation in PRT, independent of change in weight, can result in some improvements in certain inflammatory markers in older overweight adults with type 2 diabetes.
Similar content being viewed by others
Abbreviations
- HbA1c :
-
Glycated hemoglobin
- hs-CRP:
-
High sensitive C-reactive protein
- IL-6:
-
Interleukin-6
- IL-10:
-
Interleukin-10
- TNF-α:
-
Tumor necrosis factor-alpha
- ICAM-1:
-
Intercellular adhesion molecule-1
- PRT:
-
Progressive resistance training
- WL:
-
Weight loss
References
Albertini J, Valensi P, Lormeau B, Aurousseau M, Ferrière F, Attali J, Gattegno L (1998) Elevated concentrations of soluble E-selectin and vascular cell adhesion molecule-1 in NIDDM. Effect of intensive insulin treatment. Diabetes Care 21:1008–1013
Balducci S, Zanuso S, Nicolucci A, Fernando F et al (2010) Anti-inflammatory effect of exercise training in subjects with type 2 diabetes and the metabolic syndrome is dependent on exercise modalities and independent of weight loss. Nutr Metab Cardiovasc Dis 20:608–617
Barone Gibbs B, Dobrosielski DA, Bonekamp S, Stewart KJ, Clark JM (2012) A randomized trial of exercise for blood pressure reduction in type 2 diabetes: effect on flow-mediated dilation and circulating biomarkers of endothelial function. Atherosclerosis 224:446–453
Bastard JP, Maachi M, Lagathu C, Kim MJ, Caron M, Vidal H, Capeau J, Feve B (2006) Recent advances in the relationship between obesity, inflammation, and insulin resistance. Eur Cytokine Netw 17:4–12
Beavers KM, Ambrosius WT, Nicklas BJ, Rejeski WJ (2013) Independent and combined effects of physical activity and weight loss on inflammatory biomarkers in overweight and obese older adults. J Am Geriatr Soc 61:1089–1094
Brinkworth GD, Noakes M, Buckley JD, Keogh JB, Clifton PM (2009) Long-term effects of a very-low-carbohydrate weight loss diet compared with an isocaloric low-fat diet after 12 mo. Am J Clin Nutr 90:23–32
Capel F, Klimcakova E, Viguerie N, Roussel B et al (2009) Macrophages and adipocytes in human obesity: adipose tissue gene expression and insulin sensitivity during calorie restriction and weight stabilization. Diabetes 58:1558–1567
Cardinal J, Pretorius CJ, Ungerer JP (2010) Biological and diurnal variation in glucocorticoid sensitivity detected with a sensitive in vitro dexamethasone suppression of cytokine production assay. J Clin Endocrinol Metab 95:3657–3663
Cesari M, Penninx BW, Pahor M, Lauretani F, Corsi AM, Rhys Williams G, Guralnik JM, Ferrucci L (2004) Inflammatory markers and physical performance in older persons: the InCHIANTI study. J Gerontol A Biol Sci Med Sci 59:242–248
Chae JS, Paik JK, Kang R, Kim M, Choi Y, Lee SH, Lee JH (2013) Mild weight loss reduces inflammatory cytokines, leukocyte count, and oxidative stress in overweight and moderately obese participants treated for 3 years with dietary modification. Nutr Res 33:195–203
Chatterjee S, Khunti K, Davies MJ (2017) Type 2 diabetes. Lancet. doi:10.1016/s0140-6736(17)30058-2
Cooper JH, Collins BE, Adams DR, Robergs RA, Donges CE (2016) Limited effects of endurance or interval training on visceral adipose tissue and systemic inflammation in sedentary middle-aged men. J Obes. doi:10.1155/2016/2479597
Daly RM, O'Connell SL, Mundell NL, Grimes CA, Dunstan DW, Nowson CA (2014) Protein-enriched diet, with the use of lean red meat, combined with progressive resistance training enhances lean tissue mass and muscle strength and reduces circulating IL-6 concentrations in older women: a cluster randomized controlled trial. Am J Clin Nutr 99(4):899–901
de Jager W, Bourcier K, Rijkers GT, Prakken BJ, Seyfert-Margolis V (2009) Prerequisites for cytokine measurements in clinical trials with multiplex immunoassays. BMC Immunol 10:1–11
Dunstan D, Daly R, Owen N, Jolley D, De Courten M, Shaw J, Zimmet P (2002) High-intensity resistance training improves glycemic control in older patients with type 2 diabetes. Diabetes Care 25:1729–1736
Dunstan D, Daly R, Owen N, Jolley D, Vulikh E, Shaw J, Zimmet P (2005) Home-based resistance training is not sufficient to maintain improved glycemic control following supervised training in older individuals with type 2 diabetes. Diabetes Care 28:3–9
Esser N, Legrand-Poels S, Piette J, Scheen AJ, Paquot N (2014) Inflammation as a link between obesity, metabolic syndrome and type 2 diabetes. Diabetes Res Clin Pract 105:141–150
Forsythe LK, Wallace JM, Livingstone MB (2008) Obesity and inflammation: the effects of weight loss. Nutr Res Rev 21:117–133
García-Unciti M, Izquierdo M, Idoate F, Gorostiaga E et al (2012) Weight-loss diet alone or combined with progressive resistance training induces changes in association between the cardiometabolic risk profile and abdominal fat depots. Ann Nutr Metab 61:296–304
Giannopoulou I, Fernhall B, Carhart R, Weinstock RS, Baynard T, Figueroa A, Kanaley JA (2005) Effects of diet and/or exercise on the adipocytokine and inflammatory cytokine levels of postmenopausal women with type 2 diabetes. Metabolism 54:866–875
Hayashino Y, Jackson JL, Hirata T, Fukumori N, Nakamura F, Fukuhara S, Tsujii S, Ishii H (2014) Effects of exercise on C-reactive protein, inflammatory cytokine and adipokine in patients with type 2 diabetes: a meta-analysis of randomized controlled trials. Metabolism 63:431–440
Ho TP, Zhao X, Courville AB, Linderman JD et al (2015) Effects of a 12-month moderate weight loss intervention on insulin sensitivity and inflammation status in nondiabetic overweight and obese subjects. Horm Metab Res 47:289–296
Imayama I, Ulrich CM, Alfano CM, Wang C et al (2012) Effects of a caloric restriction weight loss diet and exercise on inflammatory biomarkers in overweight/obese postmenopausal women: a randomized controlled trial. Cancer Res 72:2314–2326
Karstoft K, Pedersen BK (2016) Exercise and type 2 diabetes: focus on metabolism and inflammation. Immunol Cell Biol 94:146–150
Khoo J, Dhamodaran S, Chen DD, Yap SY, Chen RY, Tian HH (2015) Exercise-induced weight loss is more effective than dieting for improving adipokine profile, insulin resistance, and inflammation in obese men. Int J Sport Nutr Exerc Metab 25:566–575
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
Kolb H, Mandrup-Poulsen T (2009) The global diabetes epidemic as a consequence of lifestyle-induced low-grade inflammation. Diabetologia 53:10–20
Kosteli A, Sugaru E, Haemmerle G, Martin JF, Lei J, Zechner R, Ferrante AW Jr (2010) Weight loss and lipolysis promote a dynamic immune response in murine adipose tissue. J Clin Investig 120:3466–3479
Kwon HR, Min KW, Ahn HJ, Seok HG, Lee JH, Park GS, Han KA (2011) Effects of aerobic exercise vs. resistance training on endothelial function in women with type 2 diabetes mellitus. Diabetes Metab J 35:364–373
Lee SY, Chang HJ, Sung J, Kim KJ, Shin S, Cho IJ, Shim CY, Hong GR, Chung N (2014) The impact of obesity on subclinical coronary atherosclerosis according to the risk of cardiovascular disease. Obesity 22:1762–1768
Liberman K, Forti LN, Beyer I, Bautmans I (2017) The effects of exercise on muscle strength, body composition, physical functioning and the inflammatory profile of older adults: a systematic review. Curr Opin Clin Nutr Metab Care 20:30–53
Madsen EL, Rissanen A, Bruun JM, Skogstrand K, Tonstad S, Hougaard DM, Richelsen B (2008) Weight loss larger than 10% is needed for general improvement of levels of circulating adiponectin and markers of inflammation in obese subjects: a 3-year weight loss study. Eur J Endocrinol 158:179–187
Maiorana A, O’Driscoll G, Cheetham C, Dembo L, Stanton K, Goodman C, Taylor R, Green D (2001) The effect of combined aerobic and resistance exercise training on vascular function in type 2 diabetes. J Am Coll Cardiol 38:860–866
Mavros Y, Kay S, Simpson KA, Baker MK et al (2014) Reductions in C-reactive protein in older adults with type 2 diabetes are related to improvements in body composition following a randomized controlled trial of resistance training. J Cachexia Sarcopenia Muscle 5:111–120
Messier SP, Mihalko SL, Legault C, Miller GD et al (2013) Effects of intensive diet and exercise on knee joint loads, inflammation, and clinical outcomes among overweight and obese adults with knee osteoarthritis: the IDEA randomized clinical trial. JAMA 310:1263–1273
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
Okada S, Hiuge A, Makino H, Nagumo A, Takaki H, Konishi H, Goto Y, Yoshimasa Y, Miyamoto Y (2010) Effect of exercise intervention on endothelial function and incidence of cardiovascular disease in patients with type 2 diabetes. J Atheroscler Thromb 17:828–833
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 31:996–1003
Peake JM, Kukuljan S, Nowson CA, Sanders K, Daly RM (2011) 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(12):3079–3088
Ribeiro F, Alves AJ, Duarte JA, Oliveira J (2010) Is exercise training an effective therapy targeting endothelial dysfunction and vascular wall inflammation? Int J Cardiol 141:214–221
Samaras K, Viardot A, Lee PN, Jenkins A, Botelho NK, Bakopanos A, Lord RV, Hayward CS (2013) Reduced arterial stiffness after weight loss in obese type 2 diabetes and impaired glucose tolerance: the role of immune cell activation and insulin resistance. Diabetes Vasc Dis Res 10:40–48
Sixt S, Beer S, Bluher M, Korff N et al (2010) Long- but not short-term multifactorial intervention with focus on exercise training improves coronary endothelial dysfunction in diabetes mellitus type 2 and coronary artery disease. Eur Heart J 31:112–119
Snel M, van Diepen JA, Stijnen T, Pijl H, Romijn JA, Meinders AE, Voshol P, Jazet IM (2011) Immediate and long-term effects of addition of exercise to a 16-week very low calorie diet on low-grade inflammation in obese, insulin-dependent type 2 diabetic patients. Food Chem Toxicol 49:3104–3111
Strasser B, Arvandi M, Siebert U (2012) Resistance training, visceral obesity and inflammatory response: a review of the evidence. Obes Rev 13:578–591
Strasser B, Berger K, Fuchs D (2015) Effects of a caloric restriction weight loss diet on tryptophan metabolism and inflammatory biomarkers in overweight adults. Eur J Nutr 54:101–107
Thompson D, Walhin JP, Batterham AM, Stokes KA, Cooper AR, Andrews RC (2014) Effect of diet or diet plus physical activity versus usual care on inflammatory markers in patients with newly diagnosed type 2 diabetes: the Early ACTivity in Diabetes (ACTID) randomized, controlled trial. J Am Heart Assoc. doi:10.1161/jaha.114.000828
Tilg H, Moschen AR (2008) Inflammatory mechanisms in the regulation of insulin resistance. Mol Med 14:222–231
Tonjes A, Scholz M, Fasshauer M, Kratzsch J, Rassoul F, Stumvoll M, Bluher M (2007) Beneficial effects of a 4-week exercise program on plasma concentrations of adhesion molecules. Diabetes Care 30:e1
Trussardi Fayh AP, Lopes AL, Fernandes PR, Reischak-Oliveira A, Friedman R (2013) Impact of weight loss with or without exercise on abdominal fat and insulin resistance in obese individuals: a randomised clinical trial. Br J Nutr 110:486–492
Van Gaal LF, Mertens IL, De Block CE (2006) Mechanisms linking obesity with cardiovascular disease. Nature 444:875–880
van Gemert WA, May AM, Schuit AJ, Oosterhof BY, Peeters PH, Monninkhof EM (2016) Effect of weight loss with or without exercise on inflammatory markers and adipokines in postmenopausal women: the SHAPE-2 trial, a randomized controlled trial. Cancer Epidemiol Biomark Prev 25:799–806
Wycherley TP, Brinkworth GD, Noakes M, Buckley JD, Clifton PM (2008) Effect of caloric restriction with and without exercise training on oxidative stress and endothelial function in obese subjects with type 2 diabetes. Diabetes Obes Metab 10:1062–1073
You T, Nicklas BJ (2006) Chronic inflammation: role of adipose tissue and modulation by weight loss. Curr Diabetes Rev 2:29–37
You T, Arsenis NC, Disanzo BL, Lamonte MJ (2013) Effects of exercise training on chronic inflammation in obesity: current evidence and potential mechanisms. Sports Med 43:243–256
Zhao YF, Feng DD, Chen C (2006) Contribution of adipocyte-derived factors to beta-cell dysfunction in diabetes. Int J Biochem Cell Biol 38:804–819
Acknowledgements
Funds for the purchase of exercise equipment were kindly provided by the Rotary Club of Kew, Victoria, Australia and by Soroptimist International, Brighton Division. We wish to thanks all the volunteers whose cooperation and dedication made this study possible.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Funding
This study was financially supported by a Grant from the Victorian Health Promotion Foundation (VicHealth) (Grant No. 98-0146).
Additional information
Communicated by Fabio Fischetti.
Electronic supplementary material
Below is the link to the electronic supplementary material.
421_2017_3657_MOESM1_ESM.docx
Online Resource 1: Mean baseline values, absolute changes relative to baseline and the net between group differences for the change after 3, 6, 9 and 12 months for the various serum inflammatory markers, adiponectin and the endothelial markers resistin and ICAM-1 for the PRT + WL and WL groups. ‡ P<0.05 vs WL at baseline (DOCX 25 kb)
Rights and permissions
About this article
Cite this article
Miller, E.G., Sethi, P., Nowson, C.A. et al. Effects of progressive resistance training and weight loss versus weight loss alone on inflammatory and endothelial biomarkers in older adults with type 2 diabetes. Eur J Appl Physiol 117, 1669–1678 (2017). https://doi.org/10.1007/s00421-017-3657-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00421-017-3657-2