Rheumatology International

, Volume 39, Issue 2, pp 227–238 | Cite as

Supervised walking improves cardiorespiratory fitness, exercise tolerance, and fatigue in women with primary Sjögren’s syndrome: a randomized-controlled trial

  • Samira Tatiyama Miyamoto
  • Valéria Valim
  • Luciana Carletti
  • Wan-Fai Ng
  • Anselmo José Perez
  • Dennis William Lendrem
  • Michael Trennel
  • Raquel Altoé Giovelli
  • Laiza Hombre Dias
  • Érica Vieira Serrano
  • Alice Mendonça Subtil
  • Vanessa Cândido Abreu
  • Jamil NatourEmail author
Clinical Trials



The aim of this study was to evaluate the safety and effectiveness of a supervised walking program in women with primary Sjögren’s syndrome (pSS).


Forty-five sedentary women fulfilling the American European Consensus Criteria for pSS were randomized to a training group (TG, n = 23) or control group (CG, n = 22). Patients in the TG were submitted to supervise walking three times a week for 16 weeks. The patients of the CG were instructed to not perform any kind of regular physical exercise. Physical fitness [maximum oxygen uptake (VO2max) and distance], EULAR Sjögren’s Syndrome Disease Activity Index (ESSDAI), hematological tests, and Medical Outcomes Study 36 (SF-36) were assessed at baseline and week 16. In addition, EULAR Sjögren’s Syndrome Patient Reported Index (ESSPRI), Functional Assessment of Chronic Illness Therapy Fatigue Subscale (FACIT-fatigue), and Beck Depression Inventory (BDI) were measured prior to intervention, after 8 and 16 weeks. Patient global assessment of response to therapy was completed at the final assessment. An intent-to-treat analysis was performed.


After 16 weeks, the mean change of VO2max (ml/kg/min), distance, and FACIT-fatigue were higher in the TG than in the CG (p = 0.016, p = 0.043 and p = 0.030, respectively). Improved cardiorespiratory fitness was associated with improvements in fatigue scores and physical components of quality of life (SF-36). Furthermore, improved fatigue scores were associated with reduced depression and improvements in the physical and mental components of SF-36. Overall, 95.4% of patients in the TG rated themselves as clinically improved versus 62% of the patients in the CG (p = 0.049). There was no flare in disease activity and no serious adverse events with exercise.


This supervised walking program was demonstrated to be feasible and safe with improvements in cardiorespiratory fitness, exercise tolerance, fatigue, and patient perception of improvement in pSS patients.

Trial registration

Clinical ID, number NCT02370225.


Sjögren’s syndrome Fatigue Exercise Rehabilitation 


Author contributions

Study conception and design: STM, VV, JN, LC, and AJP. Acquisition of data: RAG, LHS, EVS, VCA, and AMS. Data analysis and interpretation: STM, JN, VV, LC, AJP, DL, and WN. Writing: STM, JN, DL, and WN.

All authors have read and approved the manuscript.


This work was supported by grants to Samira Tatiyama Miyamoto from the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior-CAPES Foundation [BEX 8831/14-9].

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

All procedures performed in studies involving human participants were in accordance with the ethical standards of the institutional and/or national research committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards.

Informed consent

Informed consent was obtained from all the participants included in the study.

Supplementary material

296_2018_4213_MOESM1_ESM.docx (19 kb)
Supplementary material 1 (DOCX 19 KB)
296_2018_4213_MOESM2_ESM.docx (21 kb)
Supplementary material 2 (DOCX 20 KB)


  1. 1.
    Perandini LA, de Sá-Pinto AL, Roschel H et al (2012) Exercise as a therapeutic tool to counteract inflammation and clinical symptoms in autoimmune rheumatic diseases. Autoimmun Rev 12:218–224. CrossRefGoogle Scholar
  2. 2.
    Colbert LH, Visser M, Simonsick EM et al (2004) Physical activity, exercise, and inflammatory markers in older adults: findings from the health, aging and body composition study. J Am Geriatr Soc 52:1098–1104. CrossRefGoogle Scholar
  3. 3.
    Mathur N, Pedersen BK (2008) Exercise as a mean to control low-grade systemic inflammation. Mediat Inflamm 2008:109502. CrossRefGoogle Scholar
  4. 4.
    Petersen AMW, Pedersen BK (2005) The anti-inflammatory effect of exercise. J Appl Physiol 98:1154–1162. CrossRefGoogle Scholar
  5. 5.
    Roger-van Dartel SAA, Repping-Wuts H, Flendrie M et al (2015) The effect of aerobic exercise training on fatigue in rheumatoid arthritis: a meta-analysis. Arthritis Care Res (Hoboken) 67:1054–1062. CrossRefGoogle Scholar
  6. 6.
    Tench CM, McCarthy J, McCurdie I et al (2003) Fatigue in systemic lupus erythematosus: a randomized controlled trial of exercise. Rheumatology 42:1050–1054. CrossRefGoogle Scholar
  7. 7.
    Carvalho MRP, De Sato EI, Tebexreni AS et al (2005) Effects of supervised cardiovascular training program on exercise tolerance, aerobic capacity, and quality of life in patients with systemic lupus erythematosus. Arthritis Rheum 53:838–844. CrossRefGoogle Scholar
  8. 8.
    Robb-Nicholson LC, Daltroy L, Eaton H et al (1989) Effects of aerobic conditioning in lupus fatigue: a pilot study. Br J Rheumatol 28:500–505CrossRefGoogle Scholar
  9. 9.
    Daltroy LH, Robb-Nicholson C, Iversen MD et al (1995) Effectiveness of minimally supervised home aerobic training in patients with systemic rheumatic disease. Br J Rheumatol 34:1064–1069. CrossRefGoogle Scholar
  10. 10.
    Ramsey-Goldman R, Schilling EM, Dunlop D et al (2000) A pilot study on the effects of exercise in patients with systemic lupus erythematosus. Arthritis Care Res 13:262–269CrossRefGoogle Scholar
  11. 11.
    Verhoeven F, Guillot X, Prati C et al (2018) Aerobic exercise for axial spondyloarthritis—its effects on disease activity and function as compared to standard physiotherapy: a systematic review and meta—analysis. Int J Rheum Dis 1:1–8. Google Scholar
  12. 12.
    Oliveira NC, Santos Sabbag LM dos, Sá Pinto AL de et al (2009) Aerobic exercise is safe and effective in systemic sclerosis. Int J Sports Med 30:728–732. CrossRefGoogle Scholar
  13. 13.
    Pinto ALS, Oliveira NC, Gualano B et al (2011) Efficacy and safety of concurrent training in systemic sclerosis. J strength Cond Res 25:1423–1428. CrossRefGoogle Scholar
  14. 14.
    Strömbeck BE, Theander E, Jacobsson LTH (2007) Effects of exercise on aerobic capacity and fatigue in women with primary Sjogren’s syndrome. Rheumatology 46:868–871. CrossRefGoogle Scholar
  15. 15.
    Bowman SJ, Rao V (2014) Sjögren’s syndrome. Med (Baltim) 42:162–166. CrossRefGoogle Scholar
  16. 16.
    Seror R, Ravaud P, Bowman SJ et al (2010) EULAR Sjögren’s syndrome disease activity index: development of a consensus systemic disease activity index for primary Sjögren’s syndrome. Ann Rheum Dis 69:1103–1109. CrossRefGoogle Scholar
  17. 17.
    Lendrem D, Mitchell S, McMeekin P et al (2014) Health-related utility values of patients with primary Sjögren’s syndrome and its predictors. Ann Rheum Dis 73:1362–1368. CrossRefGoogle Scholar
  18. 18.
    Meijer JM, Meiners PM, Huddleston Slater JJR et al (2009) Health-related quality of life, employment and disability in patients with Sjögren’s syndrome. Rheumatology 48:1077–1082. CrossRefGoogle Scholar
  19. 19.
    Cui Y, Li L, Yin R et al (2018) Depression in primary Sjögren’s syndrome: a systematic review and meta-analysis. Psychol Health Med 23:198–209. CrossRefGoogle Scholar
  20. 20.
    Hackett KL, Gotts ZM, Ellis J et al (2017) An investigation into the prevalence of sleep disturbances in primary Sjögren’s syndrome: a systematic review of the literature. Rheumatology 56:570–580. CrossRefGoogle Scholar
  21. 21.
    Dassouki T, Benatti FB, Pinto AJ et al (2017) Objectively measured physical activity and its influence on physical capacity and clinical parameters in patients with primary Sjögren’s syndrome. Lupus 26:690–697CrossRefGoogle Scholar
  22. 22.
    Ng W-F, Miller A, Bowman JS et al (2017) Physical activity but not sedentary activity is reduced in primary Sjögren’s syndrome. Rheumatol Int 37:623–631. CrossRefGoogle Scholar
  23. 23.
    Strömbeck B, Ekdahl C, Manthorpe R, Jacobsson LTH (2003) Physical capacity in women with primary Sjögren’s syndrome: a controlled study. Arthritis Rheum 49:681–688. CrossRefGoogle Scholar
  24. 24.
    Miyamoto S, Altoé R, Carletti L et al (2015) Oxygen uptake, fatigue and quality of life in primary Sjögren’s syndrome (Abstract). Scand J Rheumatol 81:366–367Google Scholar
  25. 25.
    Wouters EJM, van Leeuwen N, Bossema ER et al (2012) Physical activity and physical activity cognitions are potential factors maintaining fatigue in patients with primary Sjogren’s syndrome. Ann Rheum Dis 71:668–673. CrossRefGoogle Scholar
  26. 26.
    Ng W-F, Bowman SJ (2010) Primary Sjogren’s syndrome: too dry and too tired. Rheumatology 49:844–853. CrossRefGoogle Scholar
  27. 27.
    Vitali C, Bombardieri S, Jonsson R et al (2002) Classification criteria for Sjögren’s syndrome: a revised version of the European criteria proposed by the American–European consensus group. Ann Rheum Dis 61:554–558CrossRefGoogle Scholar
  28. 28.
    Associação Brasileira de Empresas de Pesquisa (ABEP) (2008) Critério de classificação econômica Brasil. Available at:
  29. 29.
    Valim V, Oliveira LM, Suda AL et al (2002) Peak oxygen uptake and ventilatory anaerobic threshold in fibromyalgia. J Rheumatol 29:353–357Google Scholar
  30. 30.
    Keyser RE, Rus V, Mikdashi JA, Handwerger BS (2010) Exploratory study on oxygen consumption on-kinetics during treadmill walking in women with systemic lupus erythematosus. Arch Phys Med Rehabil 91:1402–1409. CrossRefGoogle Scholar
  31. 31.
    Keyser RE, Rus V, Cade WT et al (2003) Evidence for aerobic insufficiency in women with systemic lupus erythematosus. Arthritis Rheum 49:16–22. CrossRefGoogle Scholar
  32. 32.
    Lemos MCD, Valim V, Zandonade E, Natour J (2010) Intensity level for exercise training in fibromyalgia by using mathematical models. BMC Musculoskelet Disord 11:54. CrossRefGoogle Scholar
  33. 33.
    Gaudreault N, Boulay P (2018) Cardiorespiratory fitness among adults with fibromyalgia. Breathe (Shef Engl) 14:e25–e33. CrossRefGoogle Scholar
  34. 34.
    Fairshter RD, Walters J, Salness K et al (1983) A comparison of incremental exercise tests during cycle and treadmill ergometry. Med Sci Sports Exerc 15:549–554CrossRefGoogle Scholar
  35. 35.
    Glass SGB (2007) ACSM’s Metabolic Calculations Handbook. Lippincott Williams & Wilkins, BaltimoreGoogle Scholar
  36. 36.
    Hall C, Figueroa A, Fernhall B, Kanaley JA (2004) Energy expenditure of walking and running: comparison with prediction equations. Med Sci Sports Exerc 36:2128–2134CrossRefGoogle Scholar
  37. 37.
    Serrano ÉV, Valim V, Miyamoto S et al (2013) Transcultural adaptation of the “EULAR sjögren’s syndrome disease activity index (ESSDAI)” into Brazilian Portuguese. Rev Bras Reumatol. Google Scholar
  38. 38.
    Webster K, Odom L, Peterman A et al (1999) The functional assessment of chronic illness therapy (FACIT) measurement system: validation of version 4 of the core questionnaire. Qual Life Res 8:604Google Scholar
  39. 39.
    Seror R, Ravaud P, Mariette X et al (2011) EULAR Sjogren’s syndrome patient reported index (ESSPRI): development of a consensus patient index for primary Sjogren’s syndrome. Ann Rheum Dis 70:968–972. CrossRefGoogle Scholar
  40. 40.
    Paganotti MA, Valim V, Serrano EV et al (2015) Validation and psychometric properties of the EULAR Sjögren’s syndrome patient reported index (ESSPRI) into Brazilian Portuguese. Rev Bras Reumatol. Google Scholar
  41. 41.
    Gorenstein C, Andrade L (1996) Validation of a Portuguese version of the beck depression inventory and the state-trait anxiety inventory in Brazilian subjects. Brazilian J Med Biol Res 29:453–457Google Scholar
  42. 42.
    Ciconelli R, Ferraz M, Santos W et al (1999) Brazilian–Portuguese version of the SF-36 questionnaire: a reliable and valid quality of life outcome measure. Rev Bras Reumatol 39:143–150Google Scholar
  43. 43.
    Jacobsson LTH, Stro B (2007) The role of exercise in the rehabilitation of patients with systemic lupus erythematosus and patients with primary Sjögren’s syndrome. Curr Opin Rheumatol 19:197–203CrossRefGoogle Scholar
  44. 44.
    Valim V, Oliveira L, Suda A et al (2003) Aerobic fitness effects in fibromyalgia. J Rheumatol 30:1060–1069Google Scholar
  45. 45.
    Assis MR, Silva LE, Alves AMB et al (2006) A randomized controlled trial of deep water running: clinical effectiveness of aquatic exercise to treat fibromyalgia. Arthritis Rheum 55:57–65. CrossRefGoogle Scholar
  46. 46.
    Franklin BA, Whaley MH, Howley ET et al (2000) ACMS’s guidelines for exercise testing and prescription, 6th edn. Lippincott Williams & Wilkins, PhiladelphiaGoogle Scholar
  47. 47.
    Seror R, Theander E, Brun JG et al (2015) Validation of EULAR primary Sjogren’s syndrome disease activity (ESSDAI) and patient indexes (ESSPRI). Ann Rheum Dis 74:859–866. CrossRefGoogle Scholar
  48. 48.
    Dey S, Singh RH, Dey PK (1992) Exercise training: Significance of regional alterations in serotonin metabolism of rat brain in relation to antidepressant effect of exercise. Physiol Behav 52:1095–1099. CrossRefGoogle Scholar
  49. 49.
    Kasapis C, Thompson PD (2005) The effects of physical activity on serum C-reactive protein and inflammatory markers: a systematic review. J Am Coll Cardiol 45:1563–1569. CrossRefGoogle Scholar
  50. 50.
    Hackett KL, Newton JL, Frith J et al (2012) Impaired functional status in primary Sjögren’s syndrome. Arthritis Care Res (Hoboken) 64:1760–1764. CrossRefGoogle Scholar

Copyright information

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

Authors and Affiliations

  1. 1.Department of Integrated Education in HealthUniversidade Federal do Espírito SantoVitoriaBrazil
  2. 2.Department of RheumatologyUniversidade Federal de São Paulo-Escola Paulista de MedicinaSão PauloBrazil
  3. 3.Rheumatology Outpatient Clinic-Hospital Universitário Cassiano Antônio de Moares (HUCAM)Universidade Federal do Espírito SantoVitoriaBrazil
  4. 4.Department of Medical ClinicUniversidade Federal do Espírito SantoVitoriaBrazil
  5. 5.Exercise Physiology Laboratory (LAFEX)Universidade Federal do Espírito SantoVitoriaBrazil
  6. 6.Musculoskeletal Research Group, Institute of Cellular MedicineNewcastle UniversityNewcastle upon TyneUK
  7. 7.MoveLab, Physical Activity and Exercise Research, Institute of Cellular MedicineNewcastle UniversityNewcastle upon TyneUK

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