Advertisement

The effects of exercise on cardiovascular disease risk factors and cardiovascular physiology in rheumatoid arthritis

  • George S. MetsiosEmail author
  • R. H. Moe
  • M. van der Esch
  • J. J. C. S. Veldhuijzen van Zanten
  • S. A. M. Fenton
  • Y. Koutedakis
  • P. Vitalis
  • N. Kennedy
  • N. Brodin
  • C. Bostrom
  • T. W. Swinnen
  • K. Tzika
  • K. Niedermann
  • E. Nikiphorou
  • G. E. Fragoulis
  • T. P. V. M. Vlieland
  • C. H. M. Van den Ende
  • George D. Kitas
  • The IMPACT-RMD Consortium
Review
First Online:
  • 78 Downloads

Abstract

Cardiovascular disease (CVD) morbidity and mortality is highly prevalent in patients with rheumatoid arthritis (RA) with debilitating effects for the individual as well as significant healthcare impact. Current evidence demonstrates that engaging in aerobic and resistance exercise (i.e. structured physical activity) can significantly improve patient-reported and clinical index-assessed outcomes in RA. In addition to this, engagement in exercise programmes improves, in a dose-dependent manner, the risk of developing CVD as well as CVD symptoms and outcomes. The present narrative review uses evidence from systematic reviews and meta-analyses as well as controlled trials, to synthesize the current state-of-the-art on the potential effects of aerobic and resistance exercise on CVD risk factors as well as on cardiac and vascular function and structure in people with RA. Where there is a lack of evidence in RA to explain potential mechanisms, relevant studies from the general population are also discussed and linked to RA.

Keywords

Exercise Physical activity Rheumatoid arthritis Non-communicable disease Autoimmune disease Cardiovascular disease Inflammation Rehabilitation 
This is a preview of subscription content, log in to check access.

Notes

Author contributions

All authors contributed to the study conception and design. Material preparation, data collection and analysis were performed by GSM, PV and KT. The first draft of the manuscript was written by GSM and GDK and all authors commented on all versions of the manuscript and provided relevant comments for further amending the manuscript and produce the final draft. All authors read and approved the final manuscript.

References

  1. 1.
    Turesson C, O'Fallon WM, Crowson CS, Gabriel SE, Matteson EL (2003) Extra-articular disease manifestations in rheumatoid arthritis: incidence trends and risk factors over 46 years. Ann Rheum Dis 62(8):722–727PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Kitas GD, Gabriel SE (2011) Cardiovascular disease in rheumatoid arthritis: state of the art and future perspectives. Ann Rheum Dis 70(1):8–14PubMedCrossRefPubMedCentralGoogle Scholar
  3. 3.
    Avina-Zubieta JA, Thomas J, Sadatsafavi M, Lehman AJ, Lacaille D (2012) Risk of incident cardiovascular events in patients with rheumatoid arthritis: a meta-analysis of observational studies. Ann Rheum Dis 71(9):1524–1529PubMedCrossRefPubMedCentralGoogle Scholar
  4. 4.
    Khalid U, Egeberg A, Ahlehoff O, Lane D, Gislason GH, Lip GYH et al (2018) Incident heart failure in patients with rheumatoid arthritis: a nationwide cohort study. J Am Heart Assoc 7(2):e007227PubMedPubMedCentralCrossRefGoogle Scholar
  5. 5.
    Agca R, Heslinga SC, Rollefstad S, Heslinga M, McInnes IB, Peters MJ et al (2017) EULAR recommendations for cardiovascular disease risk management in patients with rheumatoid arthritis and other forms of inflammatory joint disorders: 2015/2016 update. Ann Rheum Dis 76(1):17–28PubMedCrossRefPubMedCentralGoogle Scholar
  6. 6.
    Metsios GS, Lahart IM (2015) Exercise as medicine in rheumatoid arthritis. Mediterr J Rheumatol 26(2):54–61Google Scholar
  7. 7.
    Metsios GS, Lemmey A (2015) Exercise as medicine in rheumatoid arthritis: effects on function, body composition, and cardiovascular disease risk. J Clin Exerc Physiol 4(1):14–22CrossRefGoogle Scholar
  8. 8.
    Gasparyan AY, Ayvazyan L, Blackmore H, Kitas GD (2011) Writing a narrative biomedical review: considerations for authors, peer reviewers, and editors. Rheumatol Int 31(11):1409–1417PubMedCrossRefPubMedCentralGoogle Scholar
  9. 9.
    Lee DC, Artero EG, Sui X, Blair SN (2010) Mortality trends in the general population: the importance of cardiorespiratory fitness. J Psychopharmacol 24(Suppl):27–35PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Hurkmans E, van der Giesen FJ, Vliet Vlieland TP, Schoones J, Van den Ende EC (2009) Dynamic exercise programs (aerobic capacity and/or muscle strength training) in patients with rheumatoid arthritis. Cochrane Database Syst Rev.  https://doi.org/10.1002/14651858.CD006853.pub2 CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Osthoff AK, Niedermann K, Braun J, Adams J, Brodin N, Dagfinrud H et al (2018) 2018 EULAR recommendations for physical activity in people with inflammatory arthritis and osteoarthritis. Ann Rheum Dis 77(9):1251–1260PubMedCrossRefPubMedCentralGoogle Scholar
  12. 12.
    Libby P (2002) Inflammation in atherosclerosis. Nature 420(6917):868–874PubMedCrossRefPubMedCentralGoogle Scholar
  13. 13.
    Stevens RJ, Douglas KM, Saratzis AN, Kitas GD (2005) Inflammation and atherosclerosis in rheumatoid arthritis. Expert Rev Mol Med 7(7):1–24PubMedCrossRefPubMedCentralGoogle Scholar
  14. 14.
    Mann S, Beedie C, Jimenez A (2014) Differential effects of aerobic exercise, resistance training and combined exercise modalities on cholesterol and the lipid profile: review, synthesis and recommendations. Sports Med 44(2):211–221PubMedCrossRefPubMedCentralGoogle Scholar
  15. 15.
    Pattyn N, Cornelissen VA, Eshghi SR, Vanhees L (2013) The effect of exercise on the cardiovascular risk factors constituting the metabolic syndrome: a meta-analysis of controlled trials. Sports Med 43(2):121–133PubMedCrossRefPubMedCentralGoogle Scholar
  16. 16.
    Kelley GA, Kelley KS (2006) Aerobic exercise and lipids and lipoproteins in men: a meta-analysis of randomized controlled trials. J Mens Health Gend 3(1):61–70PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Kelley GA, Kelley KS, Tran ZV (2004) Aerobic exercise and lipids and lipoproteins in women: a meta-analysis of randomized controlled trials. J Womens Health (Larchmt) 13(10):1148–1164CrossRefGoogle Scholar
  18. 18.
    Metsios GS, Kalinoglou A, Panoulas VF, Wilson M, Nevill AM, Koutedakis Y et al (2009) Association of physical inactivity with increased cardiovascular risk in patients with rheumatoid arthritis. Eur J Cardiovasc Prev Rehabil 16(2):188–194PubMedCrossRefPubMedCentralGoogle Scholar
  19. 19.
    Metsios GS, Koutedakis Y, Zanten JJ, Kalinoglou A, Vitalis P, Duda JL et al (2015) Cardiorespiratory fitness levels and their association with cardiovascular profile in patients with rheumatoid arthritis: a cross-sectional study. Rheumatology (Oxford) 54(12):2215–2220Google Scholar
  20. 20.
    Kalinoglou A, Metsios GS, Zanten JJ, Nightingale P, Kitas GD, Koutedakis Y (2013) Individualised aerobic and resistance exercise training improves cardiorespiratory fitness and reduces cardiovascular risk in patients with rheumatoid arthritis. Ann Rheum Dis 72(11):1819–1825PubMedCrossRefPubMedCentralGoogle Scholar
  21. 21.
    Earnest CP, Artero EG, Sui X, Lee DC, Church TS, Blair SN (2013) Maximal estimated cardiorespiratory fitness, cardiometabolic risk factors, and metabolic syndrome in the aerobics center longitudinal study. Mayo Clin Proc 88(3):259–270PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Calabresi L, Franceschini G (2010) Lecithin:cholesterol acyltransferase, high-density lipoproteins, and atheroprotection in humans. Trends Cardiovasc Med 20(2):50–53PubMedCrossRefPubMedCentralGoogle Scholar
  23. 23.
    Riedl I, Yoshioka M, Nishida Y, Tobina T, Paradis R, Shono N et al (2010) Regulation of skeletal muscle transcriptome in elderly men after 6 weeks of endurance training at lactate threshold intensity. Exp Gerontol 45(11):896–903PubMedCrossRefPubMedCentralGoogle Scholar
  24. 24.
    Seip RL, Angelopoulos TJ, Semenkovich CF (1995) Exercise induces human lipoprotein lipase gene expression in skeletal muscle but not adipose tissue. Am J Physiol 268(2 Pt 1):E229–E236PubMedPubMedCentralGoogle Scholar
  25. 25.
    Duggan C, Tapsoba JD, Wang CY, Campbell KL, Foster-Schubert K, Gross MD et al (2016) Dietary weight loss, exercise, and oxidative Stress in postmenopausal women: a randomized controlled trial. Cancer Prev Res (Phila) 9(11):835–843CrossRefGoogle Scholar
  26. 26.
    Park JH, Park H, Lim ST, Park JK (2015) Effects of a 12-week healthy-life exercise program on oxidized low-density lipoprotein cholesterol and carotid intima-media thickness in obese elderly women. J Phys Ther Sci 27(5):1435–1439PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    de Sousa CV, Sales MM, Rosa TS, Lewis JE, de Andrade RV, Simoes HG (2017) The antioxidant effect of exercise: a systematic review and meta-analysis. Sports Med 47(2):277–293PubMedCrossRefPubMedCentralGoogle Scholar
  28. 28.
    Wadley AJ, Zanten JJ, Kalinoglou A, Metsios GS, Smith JP, Kitas GD et al (2014) Three months of moderate-intensity exercise reduced plasma 3-nitrotyrosine in rheumatoid arthritis patients. Eur J Appl Physiol 114(7):1483–1492PubMedCrossRefPubMedCentralGoogle Scholar
  29. 29.
    Pedersen BK, Febbraio MA (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88(4):1379–1406CrossRefPubMedGoogle Scholar
  30. 30.
    Metsios GS, Kitas GD (2019) Physical activity, exercise and rheumatoid arthritis: Effectiveness, mechanisms and implementation. Best Practice Res Clin Rheumat.  https://doi.org/10.1016/j.berh.2019.03.013(in press) CrossRefGoogle Scholar
  31. 31.
    Ellulu MS, Patimah I, Khaza'ai H, Rahmat A, Abed Y (2017) Obesity and inflammation: the linking mechanism and the complications. Arch Med Sci 13(4):851–863PubMedCrossRefPubMedCentralGoogle Scholar
  32. 32.
    Saltiel AR, Olefsky JM (2017) Inflammatory mechanisms linking obesity and metabolic disease. J Clin Invest 127(1):1–4PubMedPubMedCentralCrossRefGoogle Scholar
  33. 33.
    Verheggen RJ, Maessen MF, Green DJ, Hermus AR, Hopman MT, Thijssen DH (2016) A systematic review and meta-analysis on the effects of exercise training versus hypocaloric diet: distinct effects on body weight and visceral adipose tissue. Obes Rev 17(8):664–690PubMedCrossRefPubMedCentralGoogle Scholar
  34. 34.
    Hayashino Y, Jackson JL, Hirata T, Fukumori N, Nakamura F, Fukuhara S et al (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(3):431–440PubMedCrossRefPubMedCentralGoogle Scholar
  35. 35.
    Bartlett DB, Willis LH, Slentz CA, Hoselton A, Kelly L, Huebner JL et al (2018) Ten weeks of high-intensity interval walk training is associated with reduced disease activity and improved innate immune function in older adults with rheumatoid arthritis: a pilot study. Arthritis Res Ther 20(1):127PubMedPubMedCentralCrossRefGoogle Scholar
  36. 36.
    de Jong Z, Munneke M, Zwinderman AH, Kroon HM, Jansen A, Ronday KH et al (2003) Is a long-term high-intensity exercise program effective and safe in patients with rheumatoid arthritis? Results of a randomized controlled trial. Arthritis Rheum 48(9):2415–2424PubMedCrossRefGoogle Scholar
  37. 37.
    Baillet A, Vaillant M, Guinot M, Juvin R, Gaudin P (2012) Efficacy of resistance exercises in rheumatoid arthritis: meta-analysis of randomized controlled trials. Rheumatology (Oxford) 51(3):519–527CrossRefGoogle Scholar
  38. 38.
    Panoulas VF, Douglas KM, Milionis HJ, Kalinglou A, Nightingale P, Kita MD et al (2007) Prevalence and associations of hypertension and its control in patients with rheumatoid arthritis. Rheumatology (Oxford) 46(9):1477–1482CrossRefGoogle Scholar
  39. 39.
    Panoulas VF, Metsios GS, Pace AV, John H, Treharne GJ, Banks MJ et al (2008) Hypertension in rheumatoid arthritis. Rheumatology (Oxford) 47(9):1286–1298CrossRefGoogle Scholar
  40. 40.
    Cornelissen VA, Smart NA (2013) Exercise training for blood pressure: a systematic review and meta-analysis. J Am Heart Assoc 2(1):e004473PubMedPubMedCentralCrossRefGoogle Scholar
  41. 41.
    Naci H, Salcher-Konrad M, Dias S, Blum MR, Sahoo SA, Nunan D et al (2019) How does exercise treatment compare with antihypertensive medications? A network meta-analysis of 391 randomised controlled trials assessing exercise and medication effects on systolic blood pressure. Br J Sports Med 53(14):859–869PubMedCrossRefPubMedCentralGoogle Scholar
  42. 42.
    Hamer M (2006) The anti-hypertensive effects of exercise: integrating acute and chronic mechanisms. Sports Med 36(2):109–116PubMedCrossRefPubMedCentralGoogle Scholar
  43. 43.
    Giles JT, Danielides S, Szklo M, Post WS, Blumenthal RS, Petri M et al (2015) Insulin resistance in rheumatoid arthritis: disease-related indicators and associations with the presence and progression of subclinical atherosclerosis. Arthritis Rheumatol 67(3):626–636PubMedPubMedCentralCrossRefGoogle Scholar
  44. 44.
    Colberg SR, Sigal RJ, Yardley JE, Riddell MC, Dunstan DW, Dempsey PC et al (2016) physical activity/exercise and diabetes: a position statement of the american diabetes association. Diabetes Care 39(11):2065–2079PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Richter EA, Hargreaves M (2013) Exercise, GLUT4, and skeletal muscle glucose uptake. Physiol Rev 93(3):993–1017PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Thomas DE, Elliott EJ, Naughton GA (2006) Exercise for type 2 diabetes mellitus. Cochrane Database Syst Rev.  https://doi.org/10.1002/14651858.CD002968.pub2 CrossRefPubMedPubMedCentralGoogle Scholar
  47. 47.
    Kalinoglou A, Metsios GS, Koutedakis Y, Kitas GD (2011) Obesity in rheumatoid arthritis. Rheumatology (Oxford) 50(3):450–462CrossRefGoogle Scholar
  48. 48.
    Nikiphorou E, Fragoulis GE (2018) Inflammation, obesity and rheumatic disease: common mechanistic links. A narrative review. Ther Adv Musculoskelet Dis 10(8):157–67.PubMedPubMedCentralCrossRefGoogle Scholar
  49. 49.
    Metsios GS, Kalinoglou A, Sandoo A, van Zanten JJ, Toms TE, John H et al (2010) Vascular function and inflammation in rheumatoid arthritis: the role of physical activity. Open Cardiovasc Med J 4:89–96PubMedPubMedCentralGoogle Scholar
  50. 50.
    Kalinoglou A, Metsios GS, Panoulas VF, Douglas KM, Nevill AM, Jamurtas AZ et al (2009) Associations of obesity with modifiable risk factors for the development of cardiovascular disease in patients with rheumatoid arthritis. Ann Rheum Dis 68(2):242–245PubMedCrossRefGoogle Scholar
  51. 51.
    Nikiphorou E, Norton S, Young A, Dixey J, Walsh D, Helliwell H et al (2018) The association of obesity with disease activity, functional ability and quality of life in early rheumatoid arthritis: data from the early rheumatoid arthritis study/early rheumatoid arthritis network UK prospective cohorts. Rheumatology (Oxford) 75(7):1194–1202CrossRefGoogle Scholar
  52. 52.
    Kremers HM, Crowson CS, Therneau TM, Roger VL, Gabriel SE (2008) High ten-year risk of cardiovascular disease in newly diagnosed rheumatoid arthritis patients: a population-based cohort study. Arthritis Rheum 58(8):2268–2274PubMedCrossRefPubMedCentralGoogle Scholar
  53. 53.
    Clark JE (2015) Diet, exercise or diet with exercise: comparing the effectiveness of treatment options for weight-loss and changes in fitness for adults (18–65 years old) who are overfat, or obese; systematic review and meta-analysis. J Diabetes Metab Disord 14:31PubMedPubMedCentralCrossRefGoogle Scholar
  54. 54.
    Roubenoff R, Roubenoff RA, Cannon JG, Kehayias JJ, Zhuang H, Dawson-Hughes B et al (1994) Rheumatoid cachexia: cytokine-driven hypermetabolism accompanying reduced body cell mass in chronic inflammation. J Clin Invest 93(6):2379–2386PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Summers GD, Metsios GS, Kalinoglou A, Kitas GD (2010) Rheumatoid cachexia and cardiovascular disease. Nat Rev Rheumatol 6(8):445–451PubMedCrossRefPubMedCentralGoogle Scholar
  56. 56.
    Lecker SH, Solomon V, Mitch WE, Goldberg AL (1999) Muscle protein breakdown and the critical role of the ubiquitin-proteasome pathway in normal and disease states. J Nutr 129(Suppl):227S–S237PubMedCrossRefPubMedCentralGoogle Scholar
  57. 57.
    Guttridge DC, Mayo MW, Madrid LV, Wang CY, Baldwin AS (2000) NF-kappaB-induced loss of MyoD messenger RNA: possible role in muscle decay and cachexia. Science 289(5488):2363–2366PubMedCrossRefPubMedCentralGoogle Scholar
  58. 58.
    Metsios GS, Kalinoglou A, Panoulas VF, Koutedakis Y, Nevill AM, Douglas KM et al (2008) New resting energy expenditure prediction equations for patients with rheumatoid arthritis. Rheumatology (Oxford) 47(4):500–506CrossRefGoogle Scholar
  59. 59.
    Utomi V, Oxborough D, Whyte GP, Somauroo J, Sharma S, Shave R et al (2013) Systematic review and meta-analysis of training mode, imaging modality and body size influences on the morphology and function of the male athlete's heart. Heart 99(23):1727–1733PubMedCrossRefPubMedCentralGoogle Scholar
  60. 60.
    Nakou ES, Parthenakis FI, Kallergis EM, Marketou ME, Nakos KS, Vardas PE (2016) Healthy aging and myocardium: A complicated process with various effects in cardiac structure and physiology. Int J Cardiol 209:167–175PubMedCrossRefPubMedCentralGoogle Scholar
  61. 61.
    Wilson M, O'Hanlon R, Prasad S, Deighan A, Macmillan P, Oxborough D et al (1985) (2011) Diverse patterns of myocardial fibrosis in lifelong, veteran endurance athletes. J Appl Physiol 110(6):1622–1626CrossRefGoogle Scholar
  62. 62.
    Serneri GG, Boddi M, Modesti PA, Cecioni I, Coppo M, Padeletti L et al (2001) Increased cardiac sympathetic activity and insulin-like growth factor-I formation are associated with physiological hypertrophy in athletes. Circ Res 89(11):977–982PubMedCrossRefPubMedCentralGoogle Scholar
  63. 63.
    Weeks KL, Bernardo BC, Ooi JYY, Patterson NL, McMullen JR (2017) The IGF1-PI3K-Akt signaling pathway in mediating exercise-induced cardiac hypertrophy and protection. Adv Exp Med Biol 1000:187–210PubMedCrossRefPubMedCentralGoogle Scholar
  64. 64.
    Cioffi G, Viapiana O, Ognibeni F, Dalbeni A, Gatti D, Adami S, et al (2015) Prevalence and factors related to left ventricular systolic dysfunction in asymptomatic patients with rheumatoid arthritis. A prospective tissue Doppler echocardiography study. Herz 40(7):989–96.PubMedCrossRefPubMedCentralGoogle Scholar
  65. 65.
    Aslam F, Bandeali SJ, Khan NA, Alam M (2013) Diastolic dysfunction in rheumatoid arthritis: a meta-analysis and systematic review. Arthritis Care Res (Hoboken) 65(4):534–543CrossRefGoogle Scholar
  66. 66.
    Liang KP, Myasoedova E, Crowson CS, Davis JM, Roger VL, Karon BL et al (2010) Increased prevalence of diastolic dysfunction in rheumatoid arthritis. Ann Rheum Dis 69(9):1665–1670PubMedPubMedCentralCrossRefGoogle Scholar
  67. 67.
    Corrao S, Argano C, Pistone G, Messina S, Calvo L, Perticone F (2015) Rheumatoid arthritis affects left ventricular mass: systematic review and meta-analysis. Eur J Intern Med 26(4):259–267PubMedCrossRefPubMedCentralGoogle Scholar
  68. 68.
    Corrao S, Messina S, Pistone G, Calvo L, Scaglione R, Licata G (2013) Heart involvement in rheumatoid arthritis: systematic review and meta-analysis. Int J Cardiol 167(5):2031–2038PubMedCrossRefPubMedCentralGoogle Scholar
  69. 69.
    Fine NM, Crowson CS, Lin G, Oh JK, Villarraga HR, Gabriel SE (2014) Evaluation of myocardial function in patients with rheumatoid arthritis using strain imaging by speckle-tracking echocardiography. Ann Rheum Dis 73(10):1833–1839PubMedCrossRefPubMedCentralGoogle Scholar
  70. 70.
    Logstrup BB, Deibjerg LK, -Andersen A, Ellingsen T (2014) Left ventricular function in treatment-naive early rheumatoid arthritis. Am J Cardiovasc Dis 4(2):79–86PubMedPubMedCentralGoogle Scholar
  71. 71.
    Metsios GS, Kalinoglou A, Zanten JJ, Treharne GJ, Panoulas VF, Douglas KM et al (2008) Rheumatoid arthritis, cardiovascular disease and physical exercise: a systematic review. Rheumatology (Oxford) 47(3):239–248CrossRefGoogle Scholar
  72. 72.
    Urman A, Taklalsingh N, Sorrento C, McFarlane IM (2018) Inflammation beyond the Joints: rheumatoid arthritis and cardiovascular disease. Scifed J Cardiol 2(3):1000019PubMedPubMedCentralGoogle Scholar
  73. 73.
    Sandoo A, Zanten JJ, Metsios GS, Carroll D, Kitas GD (2011) Vascular function and morphology in rheumatoid arthritis: a systematic review. Rheumatology (Oxford) 50(11):2125–2139CrossRefGoogle Scholar
  74. 74.
    Sandoo A, van Zanten JJ, Metsios GS, Carroll D, Kitas GD (2010) The endothelium and its role in regulating vascular tone. Open Cardiovasc Med J 4:302–312PubMedPubMedCentralCrossRefGoogle Scholar
  75. 75.
    Ashor AW, Lara J, Siervo M, -Morales C, Oggioni C, Jakovljevic DG et al (2015) Exercise modalities and endothelial function: a systematic review and dose-response meta-analysis of randomized controlled trials. Sports Med 45(2):279–296PubMedCrossRefPubMedCentralGoogle Scholar
  76. 76.
    Hambrecht R, Adams V, Erbs S, Linke A, Krankel N, Shu Y et al (2003) Regular physical activity improves endothelial function in patients with coronary artery disease by increasing phosphorylation of endothelial nitric oxide synthase. Circulation 107(25):3152–3158PubMedCrossRefPubMedCentralGoogle Scholar
  77. 77.
    Rehman J, Li J, Parvathaneni L, Karlsson G, Panchal VR, Temm CJ et al (2004) Exercise acutely increases circulating endothelial progenitor cells and monocyte-/macrophage-derived angiogenic cells. J Am Coll Cardiol 43(12):2314–2318PubMedCrossRefPubMedCentralGoogle Scholar
  78. 78.
    Metsios GS, Kalinoglou A, Zanten JJ, Nightingale P, Sandoo A, Dimitroulas T et al (2014) Individualised exercise improves endothelial function in patients with rheumatoid arthritis. Ann Rheum Dis 73(4):748–751PubMedCrossRefPubMedCentralGoogle Scholar
  79. 79.
    Zanten J, Sandoo A, Metsios GS, Kalinoglou A, Ntoumanis N, Kitas GD (2019) Comparison of the effects of exercise and anti-TNF treatment on cardiovascular health in rheumatoid arthritis: results from two controlled trials. Rheumatol Int 39(2):219–225PubMedCrossRefPubMedCentralGoogle Scholar
  80. 80.
    Nystoriak MA, Bhatnagar A (2018) Cardiovascular effects and benefits of exercise. Front Cardiovasc Med 5:135PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Faculty of Education, Health and WellbeingUniversity of WolverhamptonWalsallUK
  2. 2.Department of RheumatologyRussells Hall Hospital, Dudley Group NHS Foundation TrustDudleyUK
  3. 3.School of Physical Education and Sport ScienceUniversity of ThessalyVolosGreece
  4. 4.Department of RheumatologyNational Resource Centre for Rehabilitation in Rheumatology, Diakonhjemmet HospitalOsloNorway
  5. 5.ACHIEVE-Center of Applied Research, Faculty of Health, Reade, Center for Rehabilitation and Rheumatology/Amsterdam Rehabilitation Research CenterAmsterdam University of Applied SciencesAmsterdamThe Netherlands
  6. 6.School of Sport, Exercise and Rehabilitation SciencesUniversity of BirminghamBirminghamUK
  7. 7.School of Allied Health, Faculty of Education and Health Sciences and Health Research InstituteUniversity of LimerickLimerickIreland
  8. 8.Department of Neurobiology, Care Sciences and Society, Division of PhysiotherapyKarolinska InstitutetHuddingeSweden
  9. 9.Division of RheumatologyUniversity Hospitals LeuvenLeuvenBelgium
  10. 10.School of Health Professions, Institute of PhysiotherapyZurich University of Applied SciencesWinterthurSwitzerland
  11. 11.Department of Academic RheumatologyKing’s College LondonLondonUK
  12. 12.Institute of Infection, Immunity and InflammationUniversity of GlasgowGlasgowUK
  13. 13.Department of Orthopaedics, Rehabilitation and Physical TherapyLeiden University Medical CenterLeidenThe Netherlands
  14. 14.Department of RheumatologySint MaartenskliniekNijmegenThe Netherlands

Personalised recommendations

Cite article

Buy options