Download PDF
Int J Sports Med
DOI: 10.1055/a-2502-9854
Physiology & Biochemistry

Twelve-week interval training alters cytokines, adipokines and bone markers in women with obesity

Masumeh Alizadeh Osalou
1   Division of Exercise Nutrition and Metabolism, Faculty of Sport Sciences, Hacettepe University, Ankara, Türkiye
2   Department of Physical Education, Islamic Azad University, Urmia, Iran
,
Muhammed Mustafa Atakan 
1   Division of Exercise Nutrition and Metabolism, Faculty of Sport Sciences, Hacettepe University, Ankara, Türkiye
,
Yasemin Güzel 
1   Division of Exercise Nutrition and Metabolism, Faculty of Sport Sciences, Hacettepe University, Ankara, Türkiye
,
Şükran Nazan Koşar
1   Division of Exercise Nutrition and Metabolism, Faculty of Sport Sciences, Hacettepe University, Ankara, Türkiye
› Author Affiliations
› Further Information
Also available at
   Permissions and Reprints

Abstract

This study aimed to investigate the effects of a 12-week high-intensity interval training on inflammatory cytokines, adipokines, and markers of bone turnover and examine whether high-intensity interval training-induced changes in inflammatory cytokines and adipokines were associated with changes in markers of bone turnover. Twenty-four women with obesity (mean [standard deviation]: age: 36.1 [3.38] years, height: 158.9 [11.9] cm, and body mass index: 31.9 [1.5] kg/m2) were randomly assigned to either control (n=10) or high-intensity interval training (n=14) groups. Body mass (− 2.7%), fat mass (− 15%), and percent body fat (− 6.2%) significantly decreased (p<0.05), while the predicted V̇O2max increased (29.6%; p<0.001) following the high-intensity interval training program. The training program resulted in increased adiponectin (7.6%) and osteocalcin (11.3%; p<0.05) and reduced tumor necrosis factor alpha (66.1%), interleukin-1α (18.6%), C-reactive protein (24.0%), leptin (21.5%), and carboxy-terminal telopeptide cross-linking type one collagen (14%; p<0.05). When high-intensity interval training and control groups were analyzed separately, training-induced changes in inflammatory cytokines and adipokines were not associated with changes in bone turnover markers (p>0.05), whereas significant associations were found when the data of the groups were analyzed together (p<0.05). In conclusion, a 12-week high-intensity interval exercise program improves the inflammatory state, adipokines, markers of bone turnover, cardiorespiratory fitness, and body composition in women with obesity.

Keywords

intermittent training - osteocalcin - leptin - bone alkaline phosphatase - adiponectin

Supplementary Material



Publication History

Received: 26 August 2024

Accepted after revision: 11 December 2024

Article published online:
06 March 2025

© 2025. Thieme. All rights reserved.

Georg Thieme Verlag KG
Oswald-Hesse-Straße 50, 70469 Stuttgart, Germany

 

  • References

  • 1 Bredella MA, Torriani M, Ghomi RH. et al Determinants of bone mineral density in obese premenopausal women. Bone 2011; 48: 748-754
    PubMedSearch in Google Scholar
  • 2 Cao JJ. Effects of obesity on bone metabolism. J Orthop Surg Res 2011; 6: 30
    PubMedSearch in Google Scholar
  • 3 Mundy GR. Osteoporosis and inflammation. Nutr Rev 2007; 65: 147-151
    PubMedSearch in Google Scholar
  • 4 Gkastaris K, Goulis DG, Potoupnis M. et al Obesity, osteoporosis and bone metabolism. J Musculoskelet Neuronal Interact 2020; 20: 372-381
    PubMedSearch in Google Scholar
  • 5 Savvidis C, Tournis S, Dede AD. Obesity and bone metabolism. Hormones 2018; 17: 205-217
    PubMedSearch in Google Scholar
  • 6 Halade GV, El Jamali A, Williams PJ. et al Obesity-mediated inflammatory microenvironment stimulates osteoclastogenesis and bone loss in mice. Exp Gerontol 2011; 46: 43-52
    PubMedSearch in Google Scholar
  • 7 Pedersen BK, Saltin B. Exercise as medicine – evidence for prescribing exercise as therapy in 26 different chronic diseases. Scand J Med Sci Sports 2015; 25: 1-72
    CrossrefPubMedSearch in Google Scholar
  • 8 Atakan MM, Kosar SN, Guzel Y. et al The role of exercise, diet, and cytokines in preventing obesity and improving adipose tissue. Nutrients 2021; 13: 1459
    PubMedSearch in Google Scholar
  • 9 Banfi G, Lombardi G, Colombini A. et al Bone metabolism markers in sports medicine. Sports Med 2010; 40: 697-714
    PubMedSearch in Google Scholar
  • 10 Weston KS, Wisloff U, Coombes JS. High-intensity interval training in patients with lifestyle-induced cardiometabolic disease: a systematic review and meta-analysis. Br J Sports Med 2014; 48: 1227-1234
    PubMedSearch in Google Scholar
  • 11 Atakan MM, Guzel Y, Shrestha N. et al Effects of high-intensity interval training (HIIT) and sprint interval training (SIT) on fat oxidation during exercise: a systematic review and meta-analysis. Br J Sports Med 2022; 56: 988-996
    PubMedSearch in Google Scholar
  • 12 Wewege M, van den Berg R, Ward RE. et al The effects of high-intensity interval training vs. moderate-intensity continuous training on body composition in overweight and obese adults: a systematic review and meta-analysis. Obes Rev 2017; 18: 635-646
    PubMedSearch in Google Scholar
  • 13 Batacan RB, Duncan MJ, Dalbo VJ. et al Effects of high-intensity interval training on cardiometabolic health: a systematic review and meta-analysis of intervention studies. Br J Sports Med 2017; 51: 494-503
    PubMedSearch in Google Scholar
  • 14 Lu M, Li M, Yi L. et al Effects of 8-week high-intensity ınterval training and moderate-intensity continuous training on bone metabolism in sedentary young females. J Exerc Sci Fit 2022; 20: 77-83
    PubMedSearch in Google Scholar
  • 15 Atakan MM, Li Y, Kosar SN. et al Evidence-based effects of high-intensity interval training on exercise capacity and health: A review with a historical perspective. Int J Environ Res Public Health 2021; 18: 7201
    PubMedSearch in Google Scholar
  • 16 Leggate M, Carter WG, Evans MJ. et al Determination of inflammatory and prominent proteomic changes in plasma and adipose tissue after high-intensity intermittent training in overweight and obese males. J Appl Physiol (1985) 2012; 112: 1353-1360
    PubMedSearch in Google Scholar
  • 17 Nikseresht M, Sadeghifard N, Agha-Alinejad H. et al Inflammatory markers and adipocytokine responses to exercise training and detraining in men who are obese. J Strength Cond Res 2014; 28: 3399-3410
    PubMedSearch in Google Scholar
  • 18 Nikseresht M, Agha-Alinejad H, Azarbayjani MA. et al Effects of nonlinear resistance and aerobic interval training on cytokines and insulin resistance in sedentary men who are obese. J Strength Cond Res 2014; 28: 2560-2568
    PubMedSearch in Google Scholar
  • 19 Barry JC, Simtchouk S, Durrer C. et al Short-term exercise training reduces anti-inflammatory action of interleukin-10 in adults with obesity. Cytokine 2018; 111: 460-469
    PubMedSearch in Google Scholar
  • 20 Mezil YA, Allison D, Kish K. et al Response of bone turnover markers and cytokines to high-intensity low-impact exercise. Med Sci Sports Exerc 2015; 47: 1495-1502
    PubMedSearch in Google Scholar
  • 21 Ravnholt T, Tybirk J, Jorgensen NR. et al High-intensity intermittent “5-10-15” running reduces body fat, and increases lean body mass, bone mineral density, and performance in untrained subjects. Eur J Appl Physiol 2018; 118: 1221-1230
    PubMedSearch in Google Scholar
  • 22 Munk PS, Breland UM, Aukrust P. et al High intensity interval training reduces systemic inflammation in post-PCI patients. Eur J Cardiovasc Prev Rehabil 2011; 18: 850-857
    PubMedSearch in Google Scholar
  • 23 Davidovic Cvetko E, Nesic N, Matic A. et al Effects of 8-week increment aerobic exercise program on bone metabolism and body composition in young non-athletes. Eur J Appl Physiol 2022; 122: 1019-1034
    PubMedSearch in Google Scholar
  • 24 Thomas S, Reading J, Shephard RJ. Revision of the physical activity readiness questionnaire (PAR-Q). Can J Sport Sci 1992; 17: 338-345
    PubMedSearch in Google Scholar
  • 25 Bruce RA, Blackmon JR, Jones JW. et al Exercising testing in adult normal subjects and cardiac patients. Pediatrics 1963; 32: 742-756
    PubMedSearch in Google Scholar
  • 26 Howley ET, Bassett DR, Welch HG. Criteria for maximal oxygen uptake: review and commentary. Med Sci Sports Exerc 1995; 27: 1292-1292
    CrossrefPubMedSearch in Google Scholar
  • 27 Tanaka H, Monahan KD, Seals DR. Age-predicted maximal heart rate revisited. J Am Coll Cardiol 2001; 37: 153-156
    CrossrefPubMedSearch in Google Scholar
  • 28 Guzel Y, Atakan MM, Areta JL. et al Ten weeks of low-volume walking training improve cardiometabolic health and body composition in sedentary postmenopausal women with obesity without affecting markers of bone metabolism. Res Sports Med 2024; 32: 331-343
    PubMedSearch in Google Scholar
  • 29 Cohen J. Statistical power analysis for the behavioral sciences. 2nd edn Routledge; 1988
    Search in Google Scholar
  • 30 Benjamini Y, Hochberg Y. Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Series B Stat Methodol 1995; 57: 289-300
    PubMedSearch in Google Scholar
  • 31 Hotamisligil GS. Inflammation and metabolic disorders. Nature 2006; 444: 860-867
    PubMedSearch in Google Scholar
  • 32 Shapses SA, Pop LC, Wang Y. Obesity is a concern for bone health with aging. Nutr Res 2017; 39: 1-13
    PubMedSearch in Google Scholar
  • 33 Khosla S. Minireview: the OPG/RANKL/RANK system. Endocrinology 2001; 142: 5050-5055
    PubMedSearch in Google Scholar
  • 34 Beavers KM, Brinkley TE, Nicklas BJ. Effect of exercise training on chronic inflammation. Clin Chim Acta 2010; 411: 785-793
    PubMedSearch in Google Scholar
  • 35 Gleeson M, Bishop NC, Stensel DJ. et al The anti-inflammatory effects of exercise: mechanisms and implications for the prevention and treatment of disease. Nat Rev Immunol 2011; 11: 607-615
    CrossrefPubMedSearch in Google Scholar
  • 36 Balducci S, Zanuso S, Nicolucci A. et al 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 2010; 20: 608-617
    PubMedSearch in Google Scholar
  • 37 Asle Mohammadi Zadeh M, Kargarfard M, Marandi SM. et al Diets along with interval training regimes improves inflammatory & anti-inflammatory condition in obesity with type 2 diabetes subjects. J Diabetes Metab Disord 2018; 17: 253-267
    PubMedSearch in Google Scholar
  • 38 Hooshmand Moghadam B, Golestani F, Bagheri R. et al The effects of high-intensity interval training vs. moderate-intensity continuous training on inflammatory markers, body composition, and physical fitness in overweight/obese survivors of breast cancer: a randomized controlled clinical trial. Cancers (Basel) 2021; 13: 4386
    PubMedSearch in Google Scholar
  • 39 Wang S, Zhou H, Zhao C. et al Effect of exercise training on body composition and inflammatory cytokine levels in overweight and obese individuals: a systematic review and network meta-analysis. Front Immunol 2022; 13: 921085
    PubMedSearch in Google Scholar
  • 40 Brotto M, Bonewald L. Bone and muscle: Interactions beyond mechanical. Bone 2015; 80: 109-114
    PubMedSearch in Google Scholar
  • 41 Mohammad Rahimi GR, Niyazi A, Alaee S. The effect of exercise training on osteocalcin, adipocytokines, and insulin resistance: a systematic review and meta-analysis of randomized controlled trials. Osteoporos Int 2021; 32: 213-224
    PubMedSearch in Google Scholar
  • 42 Mohammad Rahimi GR, Bijeh N, Rashidlamir A. Effects of exercise training on serum preptin, undercarboxylated osteocalcin and high molecular weight adiponectin in adults with metabolic syndrome. Exp Physiol 2020; 105: 449-459
    PubMedSearch in Google Scholar
  • 43 Hiam D, Landen S, Jacques M. et al Osteocalcin and its forms respond similarly to exercise in males and females. Bone 2021; 144: 115818
    PubMedSearch in Google Scholar
  • 44 Micielska K, Flis M, Kortas JA. et al Nordic walking rather than high intensity interval training reduced myostatin concentration more effectively in elderly subjects and the range of this drop was modified by metabolites of vitamin D. Nutrients 2021; 13: 4393
    PubMedSearch in Google Scholar
  • 45 Alp A. Effects of aerobic exercise on bone-specific alkaline phosphatase and urinary CTX levels in premenopausal women. Turk J Phys Med Rehab 2013; 59: 310-314
    PubMedSearch in Google Scholar
  • 46 Yusni Y, Rahman S. The effect of chronic exercise on a biomarker of bone resorption in healthy adults. Fam Med Prim Care Rev 2019; 21: 270-276
    PubMedSearch in Google Scholar
  • 47 Santos L, Elliott-Sale KJ, Sale C. Exercise and bone health across the lifespan. Biogerontology 2017; 18: 931-946
    PubMedSearch in Google Scholar
  • 48 Park HS, Park JY, Yu R. Relationship of obesity and visceral adiposity with serum concentrations of CRP, TNF-α and IL-6. Diabetes Res Clin Pract 2005; 69: 29-35
    PubMedSearch in Google Scholar
  • 49 Considine RV, Sinha MK, Heiman ML. et al Serum immunoreactive-leptin concentrations in normal-weight and obese humans. N Engl J Med 1996; 334: 292-295
    CrossrefPubMedSearch in Google Scholar
  • 50 Menezes AMB, Oliveira PD, Wehrmeister FC. et al Association between interleukin-6, C-reactive protein and adiponectin with adiposity: findings from the 1993 Pelotas (Brazil) birth cohort at 18 and 22 years. Cytokine 2018; 110: 44-51
    PubMedSearch in Google Scholar
  • 51 Labouesse MA, Gertz ER, Piccolo BD. et al Associations among endocrine, inflammatory, and bone markers, body composition and weight loss induced bone loss. Bone 2014; 64: 138-146
    PubMedSearch in Google Scholar
  • 52 Baker-LePain JC, Nakamura MC, Lane NE. Effects of inflammation on bone: an update. Curr Opin Rheumatol 2011; 23: 389-395
    PubMedSearch in Google Scholar
  • 53 Suh H-s, Hwang I-c, Lee K-s. et al Relationships between serum osteocalcin, leptin and the effect of weight loss by pharmacological treatment in healthy, nonsmoking Korean obese adults. Clinica Chimica Acta 2013; 418: 17-21
    PubMedSearch in Google Scholar
  • 54 Oshima K, Nampei A, Matsuda M. et al Adiponectin increases bone mass by suppressing osteoclast and activating osteoblast. Biochem Biophys Res Commun 2005; 331: 520-526
    PubMedSearch in Google Scholar
  • 55 Ducy P, Amling M, Takeda S. et al Leptin inhibits bone formation through a hypothalamic relay: a central control of bone mass. Cell 2000; 100: 197-207
    PubMedSearch in Google Scholar
  • 56 Sabag A, Little JP, Johnson NA. Low-volume high-intensity interval training for cardiometabolic health. J Physiol 2022; 600: 1013-1026
    PubMedSearch in Google Scholar