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05-06-2018 | Systemic sclerosis | Article

The effects of upper and lower limb exercise on the microvascular reactivity in limited cutaneous systemic sclerosis patients

Journal: Arthritis Research & Therapy

Authors: A. Mitropoulos, A. Gumber, H. Crank, M. Akil, M. Klonizakis

Publisher: BioMed Central

Abstract

Background

Aerobic exercise in general and high-intensity interval training (HIIT) specifically is known to improve vascular function in a range of clinical conditions. HIIT in particular has demonstrated improvements in clinical outcomes, in conditions that have a strong macroangiopathic component. Nevertheless, the effect of HIIT on microcirculation in systemic sclerosis (SSc) patients is yet to be investigated. Therefore, the purpose of the study was to compare the effects of two HIIT protocols (cycle and arm cranking) on the microcirculation of the digital area in SSc patients.

Methods

Thirty-four limited cutaneous SSc patients (65.3 ± 11.6 years old) were randomly allocated in three groups (cycling, arm cranking and control group). The exercise groups underwent a 12- week exercise program twice per week. All patients performed the baseline and post-exercise intervention measurements where physical fitness, functional ability, transcutaneous oxygen tension (ΔTcpO₂), body composition and quality of life were assessed. Endothelial-dependent as well as -independent vasodilation were assessed in the middle and index fingers using LDF and incremental doses of acetylcholine (ACh) and sodium nitroprusside (SNP). Cutaneous flux data were expressed as cutaneous vascular conductance (CVC).

Results

Peak oxygen uptake increased in both exercise groups (p < 0.01, d = 1.36). ΔTcpO₂ demonstrated an increase in the arm-cranking group only, with a large effect, but not found statistically significant,(p = 0.59, d = 0.93). Endothelial-dependent vasodilation improvement was greater in the arm-cranking (p < 0.05, d = 1.07) in comparison to other groups. Both exercise groups improved life satisfaction (p < 0.001) as well as reduced discomfort and pain due to Raynaud’s phenomenon (p < 0.05). Arm cranking seems to be the preferred mode of exercise for study participants as compared to cycling (p < 0.05). No changes were observed in the body composition or the functional ability in both exercise groups.

Conclusions

Our results suggest that arm cranking has the potential to improve the microvascular endothelial function in SSc patients. Also notably, our recommended training dose (e.g., a 12-week HIIT program, twice per week), appeared to be sufficient and tolerable for this population. Future research should focus on exploring the feasibility of a combined exercise such as aerobic and resistance training by assessing individual’s experience and the quality of life in SSc patients.

Trial registration

ClinicalTrials.gov (NCT number): NCT03058887, February 23, 2017.

Gabrielli A, Avvedimento EV, Krieg T. Scleroderma. N Engl J Med. 2009;36:1989–2003.CrossRef

Bolster MBSR. Clinical features of systemic sclerosis. In: Hochberg MC, Silman AJ, Smolen JS, Weinblatt ME, Weisman MH, editors. Rheumatology. 6th ed. Philadelphia: Mosby Elsevier; 2008. p. 1375–85.

Jimenez SA, Derk CT. Following the molecular pathways toward an understanding of the pathogenesis of systemic sclerosis. Ann Intern Med. 2004;140:37–50.CrossRefPubMed

Varga J, Abraham D. Systemic sclerosis: a prototypic multisystem fibrotic disorder. J Clin Invest. 2007;117:557–67.CrossRefPubMedPubMedCentral

Isenberg DA, Black C. ABC of Rheumatology. Raynaud's phenomenon, scleroderma, and overlap syndromes. BMJ. 1995;310:795–8.CrossRefPubMedPubMedCentral

Kavian N, Batteux F. Macro- and microvascular disease in systemic sclerosis. Vasc Pharmacol. 2015;71:16–23.CrossRef

Kahaleh B. Progress in research into systemic sclerosis. Lancet. 2004;364:561–2.CrossRefPubMed

Sunderkötter C, Riemekasten G. Pathophysiology and clinical consequences of Raynaud’s phenomenon related to systemic sclerosis. Rheumatology (Oxford). 2006;45:33–5.CrossRef

Altman RD, Medsger TA Jr, Bloch DA, Michel BA. Predictors of survival in systemic sclerosis (scleroderma). Arthritis Rheum. 1991;34:403–13.CrossRefPubMed

10.

Pope JE. The diagnosis and treatment of Raynaud's phenomenon: a practical approach. Drugs. 2007;67:517–25.CrossRefPubMed

11.

Prescribing & Medicines Team Health and Social Care Information Centre. Prescription Cost Analysis for England 2015. 2016. https://digital.nhs.uk/catalogue/PUB20200. Accessed 07 May 2016.

12.

Ramos JS, Dalleck LC, Tjonna AE, Beetham KS, Coombes JS. The impact of high-intensity interval training versus moderate-intensity continuous training on vascular function: a systematic review and meta-analysis. Sports Med. 2015;45:679–92.CrossRefPubMed

13.

Meyer P, Normandin E, Gayda M, Billon G, Guiraud T, Bosquet L, et al. High-intensity interval exercise in chronic heart failure: protocol optimization. J Card Fail. 2012;18:126–33.CrossRefPubMed

14.

Smith-Ryan A. Enjoyment of high-intensity interval training in an overweight/obese cohort: a short report. Clin Physiol Funct Imaging. 2017;37:89–93.CrossRefPubMed

15.

Guiraud T, Nigam A, Gremeaux V, Meyer P, Juneau M, Bosquet L. High-intensity interval training in cardiac rehabilitation. Sports Med. 2012;42:587–605.CrossRefPubMed

16.

Kessler HS, Sisson SB, Short KR. The potential for high-intensity interval training to reduce cardiometabolic disease risk. Sports Med. 2012;42:489–509.CrossRefPubMed

17.

Hoogen F, Khanna D, Fransen J, Johnson SR, Baron M, Tyndall A, et al. 2013 Classification Criteria for Systemic Sclerosis: An American College of Rheumatology/European League Against Rheumatism Collaborative Initiative. Arthritis Rheum. 2013;65:2737–47.CrossRefPubMedPubMedCentral

18.

Borg GA. Perceived exertion: a note on “history” and methods. Med Sci Sports. 1973;5:90–3.PubMed

19.

Smith PM, Price MJ, Doherty M. The influence of crank rate on peak oxygen consumption during arm crank ergometry. J Sports Sci. 2001;19:955–60.CrossRefPubMed

20.

Smith PM, Doherty M, Price MJ. The effect of crank rate strategy on peak aerobic power and peak physiological responses during arm crank ergometry. J Sports Sci. 2007;25:711–8.CrossRefPubMed

21.

Wasserman K. In: Hansen JE, Sue DY, Stringer WW, Sietsema KE, Sun XG, Whipp BJ, editors. Principles of exercise testing and interpretation : including pathophysiology and clinical applications. London: Wolters Kluwer/Lippincott Williams & Wilkins; 2012. p. 141–2.

22.

Deuschle K, Weinert K, Becker MO, Backhaus M, Huscher D, Riemekasten G. Six-minute walk distance as a marker for disability and complaints in patients with systemic sclerosis. Clin Exp Rheumatol. 2011;29:S53–9.PubMed

23.

Klonizakis M, Tew G, Michaels J, Saxton J. Exercise training improves cutaneous microvascular endothelial function in post- surgical varicose vein patients. Microvasc Res. 2009;78:67–70.CrossRefPubMed

24.

Klonizakis M, Tew G, Michaels J, Saxton J. Impaired microvascular endothelial function is restored by acute lower-limb exercise in post-surgical varicose vein patients. Microvasc Res. 2009;77:158–62.CrossRefPubMed

25.

Wasilewski R, Ubara EO, Klonizakis M. Assessing the effects of a short-term green tea intervention in skin microvascular function and oxygen tension in older and younger adults. Microvasc Res. 2016;107:65–71.CrossRefPubMed

26.

Dolan P. Modeling valuations for EuroQol health states. Med Care. 1997;35:1095–108.CrossRefPubMed

27.

Jung ME, Bourne JE, Little JP. Where does HIT fit? An examination of the affective response to high-intensity intervals in comparison to continuous moderate- and continuous vigorous-intensity exercise in the exercise intensity-affect continuum. PLoS One. 2014;9:e114541.CrossRefPubMedPubMedCentral

28.

Mullineaux DR, Bartlett RM, Bennett S. Research design and statistics in biomechanics and motor control. J Sports Sci. 2001;19:739–60.CrossRefPubMed

29.

Mitropoulos A, Gumber A, Crank H, Klonizakis M. Validation of an arm crank ergometer test for use in sedentary adults. J Sports Sci Med. 2017;16:558–64.PubMedPubMedCentral

30.

Metsios GS, Stavropoulos-Kalinoglou A, Veldhuijzen vZ, Nightingale P, Sandoo A, Dimitroulas T, et al. Individualised exercise improves endothelial function in patients with rheumatoid arthritis. Ann Rheum Dis. 2014;73:748.CrossRefPubMed

31.

Dias I, Farinatti P, De Souza MG, Manhanini DP, Balthazar E, Dantas DL, et al. Effects of resistance training on obese adolescents. Med Sci Sports Exerc. 2015;47:2636–44.CrossRefPubMed

32.

Laughlin M, Newcomer S, Bender S. Importance of hemodynamic forces as signals for exercise-induced changes in endothelial cell phenotype. J Appl Physiol. 2008;104:588.CrossRefPubMed

33.

Busse R, Mülsch A. Induction of nitric oxide synthase by cytokines in vascular smooth muscle cells. FEBS Lett. 1990;275:87–90.CrossRefPubMed

34.

Fukai T, Siegfried MR, Ushio-Fukai M, Cheng Y, Kojda G, Harrison DG. Regulation of the vascular extracellular superoxide dismutase by nitric oxide and exercise training. J Clin Invest. 2000;105:1631.CrossRefPubMedPubMedCentral

35.

Adams V, Linke A, Krankel N, Erbs S, Gummert J, Mohr F, et al. Impact of regular physical activity on the expression of angiotensin II receptors and activity of NADPH oxidase in the left mammarial artery of patients with coronary artery disease. Eur Heart J. 2004;25:224.CrossRef

36.

Wisloff PU, Stoylen MA, Loennechen EJ, Bruvold AM, Rognmo JO, Haram LP, et al. Superior cardiovascular effect of aerobic interval-training versus moderate continuous training in elderly heart failure patients. Med Sci Sports Exerc. 2007;39:S32.CrossRef

37.

Tjønna AE, Lee SJ, Rognmo Ø, Stølen TO, Bye A, Haram PM, et al. Aerobic interval training versus continuous moderate exercise as a treatment for the metabolic syndrome: a pilot study. Circulation. 2008;118:346–54.CrossRefPubMedPubMedCentral

38.

Mitranun W, Deerochanawong C, Tanaka H, Suksom D. Continuous vs interval training on glycemic control and macro- and microvascular reactivity in type 2 diabetic patients. Scand J Med Sci Sports. 2014;24:e69–76.CrossRefPubMed

39.

Laughlin MH, Rubin LJ, Rush JW, Price EM, Schrage WG, Woodman CR. Short-term training enhances endothelium-dependent dilation of coronary arteries, not arterioles. J Appl Physiol. 2003;94:234Y44.

40.

Tronc F, Wassef M, Esposito B, Henrion D, Glagov S, Tedgui A. Role of NO in flow-induced remodeling of the rabbit common carotid artery. Arterioscler Thromb Vasc Biol. 1996;16:1256–62.CrossRefPubMed

41.

Klonizakis M, Winter E. Effects of arm-cranking exercise in cutaneous microcirculation in older, sedentary people. Microvasc Res. 2011;81:331–6.CrossRefPubMed

42.

Sinoway LI, Musch TI, Minotti JR, Zelis R. Enhanced maximal metabolic vasodilatation in the dominant forearms of tennis players. J Appl Physiol (1985). 1986;61:673–8.CrossRef

43.

Green DJ, Cable NT, Fox C, Rankin JM, Taylor RR. Modification of forearm resistance vessels by exercise training in young men. J Appl Physiol (Bethesda, MD: 1985). 1994;77:1829.CrossRef

44.

Green DJ, Fowler DT, O'Driscoll JG, Blanksby BA, Taylor RR. Endothelium-derived nitric oxide activity in forearm vessels of tennis players. J Appl Physiol (Bethesda, MD.: 1985). 1996;81:943.CrossRef

45.

Ribeiro F, Alves AJ, Duarte JA, Oliveira J. Is exercise training an effective therapy targeting endothelial dysfunction and vascular wall inflammation? Int J Cardiol. 2010;141:214–21.CrossRefPubMed

46.

Liu L, Yu B, Chen J, Tang Z, Zong C, Shen D, et al. Different effects of intermittent and continuous fluid shear stresses on osteogenic differentiation of human mesenchymal stem cells. Biomech Model Mechanobiol. 2012;11:391–401.CrossRefPubMed

47.

Mcmahan Z, Wigley F. Raynaud’s phenomenon and digital ischemia: a practical approach to risk stratification, diagnosis and management. Int J Clin Rheumatol. 2010;5:355–70.CrossRef

48.

Ingraham KM, Steen VD. Morbidity of digital tip ulcerations in scleroderma. Arth Rheum. 2006;54:P578.

49.

Vitielo M, Abuchar A, Santana N, Dehesa L, Kerdel FA. An update on the treatment of the cutaneous manifestations of systemic sclerosis: The dermatologist's point of view. J Clin Aesthet Dermatol. 2012;5:33–43.

50.

Pope J, Fenlon D, Thompson A, Shea B, Furst D, Wells GA, et al. Iloprost and cisaprost for Raynaud's phenomenon in progressive systemic sclerosis. Cochrane Database Syst Rev. 2000;2:CD000953.

51.

Wigley FM, Wise RA, Miller R, Needleman BW, Spence RJ. Anticentromere antibody as a predictor of digital ischemic loss in patients with systemic sclerosis. Arthritis Rheum. 1992;35:688–93.CrossRefPubMed

52.

Oliveira NC, Portes LA, Pettersson H, Alexanderson H, Boström C. Aerobic and resistance exercise in systemic sclerosis: state of the art. Musculoskeletal Care. 2017;15:316–23.CrossRefPubMed

53.

Scherr J, Wolfarth B, Christle JW, Pressler A, Wagenpfeil S, Halle M. Associations between Borg's rating of perceived exertion and physiological measures of exercise intensity. Eur J Appl Physiol. 2013;113:147–55.CrossRefPubMed

54.

Blanchard CM, Rodgers WM, Spence JC, Courneya KS. Feeling state responses to acute exercise of high and low intensity. J Sci Med Sport. 2001;4:30–8.CrossRefPubMed

55.

Parfitt G, Hughes S. The exercise intensity–affect relationship: evidence and implications for exercise behavior. J Exerc Sci Fit. 2009;7:S34–41.CrossRef

56.

Allcock RJ, Forrest I, Corris PA, Crook PR, Griffiths ID. A study of the prevalence of systemic sclerosis in northeast England. Rheumatology (Oxford). 2004;43:596–602.CrossRef

57.

Brudin L, Berg S, Ekberg P, Castenfors J. Is transcutaneous PO2 monitoring during exercise a reliable alternative to arterial PO2 measurements? Clin Physiol. 1994;14:47–52.CrossRefPubMed

58.

Planès C, Leroy M, Foray E, Raffestin B. Arterial blood gases during exercise: validity of transcutaneous measurements. Arch Phys Med Rehabil. 2001;82:1686–91.CrossRefPubMed

59.

Carter R, Banham SW. Use of transcutaneous oxygen and carbon dioxide tensions for assessing indices of gas exchange during exercise testing. Respir Med. 2000;94:350–5.CrossRefPubMed