Prevalence and factors associated with disturbed sleep in patients with ankylosing spondylitis and non-radiographic axial spondyloarthritis: a systematic review

Abstract

This review explores the prevalence and factors associated with disturbed sleep for patients with ankylosing spondylitis and non-radiographic axial spondyloarthritis in order to clarify consistent findings in this otherwise disparate research field. The association of physical, demographic and psychological factors correlating with poor sleep was explored, and the effectiveness of interventions assessed. Ten electronic databases were searched: AMED, CINAHL, Embase, Medline, PsycINFO, PubMed, Scopus, Web of Science, OpenGrey and BASE. Following application of inclusion and exclusion criteria, 29 articles were critically assessed on the basis of methodology, experimental design, ethics and quality of sleep data, leading to the selection of 15 studies for final review. Poor sleep was reported in 35–90% of patients with axial spondyloarthritis and is more prevalent within this clinical population compared to healthy control subjects. Disturbed sleep is an important aspect of disease for patients and reflects the severity of disease activity, pain, fatigue and functional disability. However, the direction of this relationship is undetermined. Associations with age, gender, years spent in education, quality of life and depression have also been demonstrated. Anti-TNF medication is effective in reducing poor sleep, and exercise has also produced beneficial results. Future research into poor sleep should take account of its multifactorial nature. There is also a current lack of research investigating non-pharmacological interventions or combination therapies. A standardised, validated measurement of poor sleep, appropriate for regular patient screening, would be a useful first step for future research.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2

References

  1. 1.

    Kiltz U, Baraliakos X, Karakostas P, Igelmann M, Kalthoff L, Klink C, Krause D, Schmitz-bortz E, Flörecke M, Bollow M, Braun J (2012) Do patients with non-radiographic axial spondylarthritis differ from patients with ankylosing spondylitis? Arthritis Care Res 64:1415–1422

    Article  Google Scholar 

  2. 2.

    Boonen A, Sieper J, van der Heijde D, Dougados M, Bukowski JF, Valluri S, Vlahos B, Kotak S (2015) The burden of non-radiographic axial spondyloarthropathy. Semin Arthritis Rheum 44:556–562

    Article  PubMed  Google Scholar 

  3. 3.

    Dalyan M, Güner A, Tuncer S, Bilgiç A, Arasil T (1999) Disability in ankylosing spondylitis. Disabil Rehabil 21:74–79

    CAS  Article  PubMed  Google Scholar 

  4. 4.

    Bostan E, Borman P, Bodur H, Barca N (2003) Functional disability and quality of life in patients with ankylosing spondylitis. Rheumatol Int 23:121–126

    PubMed  Google Scholar 

  5. 5.

    Rudwaleit M, Metter A, Listing J, Sieper J, Braun J (2006) Inflammatory back pain in ankylosing spondylitis: a reassessment of the clinical history for application as classification and diagnostic criteria. Arthritis Rheum 54:569–578

    Article  PubMed  Google Scholar 

  6. 6.

    Hart F, Taylor R, Huskisson E (1970) Pain at night. Lancet 295:881–884

    Article  Google Scholar 

  7. 7.

    Tanfield M (1978) Ankylosing spondylitis and sleep. Lancet 311:944–945

    Article  Google Scholar 

  8. 8.

    Sengupta R, Stone MA (2007) The assessment of ankylosing spondylitis in clinical practice. Nat Clin Pract Rheumatol 3:496–503

    CAS  Article  PubMed  Google Scholar 

  9. 9.

    Callis Duffin K, Wong B, Horn EJ, Krueger GG (2009) Psoriatic arthritis is a strong predictor of sleep interference in patients with psoriasis. J Am Acad Dermatol 60:604–608

    Article  PubMed  Google Scholar 

  10. 10.

    Duruöz MT, Sari Sürmeli Z, Uçar Ü, Topçu E, Duruöz E (2013) Evaluation of sleep quality in psoriatic arthritis patients. Ann Rheum Dis 72:A682

    Google Scholar 

  11. 11.

    Taylor-Gjevre R, Gjevre JA, Skomro R, Nair BV (2011) Assessment of sleep health in patients with rheumatic disease. Int J Clin Rheumatol 6:207–218

    CAS  Article  Google Scholar 

  12. 12.

    Kinnucan JA, Rubin DT, Ali T (2013) Sleep and inflammatory bowel disease: exploring the relationship between sleep disturbances and inflammation. Gastroenterol Hepatol 9:718–727

    Google Scholar 

  13. 13.

    Wolfe F, Michaud K, Li T (2006) Sleep disturbance in patients with rheumatoid arthritis: evaluation by medical outcomes study and visual analog sleep scales. J Rheumatol 33:1942–1951

    PubMed  Google Scholar 

  14. 14.

    Ananthakrishnan AN, Long MD, Martin CF, Sandler RS, Kappelman MD (2013) Sleep disturbance and risk of active disease in patients with Crohn’s disease and ulcerative colitis. Clin Gastroenterol Hepatol 1:965–971

    Article  Google Scholar 

  15. 15.

    Da Costa D, Zummer M, Fitzcharles MA (2009) Determinants of sleep problems in patients with spondyloarthropathy. Musculoskelet Care 7:143–161

    Article  Google Scholar 

  16. 16.

    Heiberg T, Lie E, van Der Heijde D, Kvien TK (2011) Sleep problems are of higher priority for improvement for patients with ankylosing spondylitis than for patients with other inflammatory arthropathies. Ann Rheum Dis 70:872

    Article  PubMed  Google Scholar 

  17. 17.

    Ward MM (1999) Health-related quality of life in ankylosing spondylitis: a survey of 175 patients. Arthritis Care Res 12:247–255

    CAS  Article  PubMed  Google Scholar 

  18. 18.

    Eilertsen G, Ormstad H, Kirkevold M, Mengshoel A, Söderberg S, Olsson M (2015) Similarities and differences in the experience of fatigue among people living with fibromyalgia, multiple sclerosis, ankylosing spondylitis and stroke. J Clin Nurs 24:2023–2034

    Article  PubMed  Google Scholar 

  19. 19.

    Deshpande K, Wininger K (2009) Spinal cord stimulation for pain management in ankylosing spondylitis: a case report. Neuromodulation 12:54–59

    Article  PubMed  Google Scholar 

  20. 20.

    Moher D, Liberati A, Tetzlaff J, Altman DG (2009) PRISMA Group: preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement. Ann Intern Med 151:264–269

    Article  PubMed  Google Scholar 

  21. 21.

    Abdulaziez O, Asaad T (2012) Sleep problems in ankylosing spondylitis: polysomnographic pattern and disease related variables. Egypt Rheumatol 34:59–65

    Article  Google Scholar 

  22. 22.

    Altan L, Bingöl U, Aslan M, Yurtkuran M (2006) The effect of balneotherapy on patients with ankylosing spondylitis. Scand J Rheumatol 35:283–289

    CAS  Article  PubMed  Google Scholar 

  23. 23.

    Aydin E, Bayraktar K, Turan Y, Kurt Omurlu I, Tastaban E, Sendur O (2015) Sleep quality in patients with ankylosing spondylitis. Rev Bras Reumatol 55:340–345

    Article  PubMed  Google Scholar 

  24. 24.

    Bao C, Huang F, Khan M, Fei K, Wu Z, Zhuang Y, Gathany T, Han C, Hsia E (2014) Safety and efficacy of golimumab in Chinese patients with active ankylosing spondylitis: 1-year results of a multicentre, randomized, double-blind, placebo-controlled phase III trial. Rheumatol 53:1654–1663

    Article  Google Scholar 

  25. 25.

    Batmaz I, Sariyildiz M, Dilek B, Bez Y, Karakoc M, Cevik R (2013) Sleep quality and associated factors in ankylosing spondylitis: relationship with disease parameters, psychological status and quality of life. Rheumatol Int 33:1039–1045

    Article  PubMed  Google Scholar 

  26. 26.

    Deodhar A, Braun J, Inman R, Mack M, Parasuraman S, Buchanan J, Hsu B, Gathany T, van der Heijde D (2010) Golimumab reduces sleep disturbance in patients with active ankylosing spondylitis: results from a randomized, placebo-controlled trial. Arthritis Care Res 62:1266–1271

    Article  Google Scholar 

  27. 27.

    Dougados M, Tsai WC, Saaibi DL, Bonin R, Bukowski J, Pedersen R, Vlahos B, Kotak S (2015) Evaluation of health outcomes with etanercept treatment in patients with early nonradiographic axial spondyloarthritis. J Rheumatol 42:1835–1841

    CAS  Article  PubMed  Google Scholar 

  28. 28.

    Hultgren S, Broman J, Gudbjörnsson B, Hetta J, Lindqvist U (2000) Sleep disturbances in outpatients with ankylosing spondylitis a questionnaire study with gender implications. Scand J Rheumatol 29:365–369

    CAS  Article  PubMed  Google Scholar 

  29. 29.

    Jiang Y, Yang M, Wu H, Song H, Zhan F, Liu S, Gao G, Liu Z, Hu Z, He P, Zhang S, Hu Z, Lin Z, Zhang Y, Li Y, Shen L, Huang A, Liao Z, Cao S, Wei Y, Li L, Li Q, Lv Q, Qi J, Huang J, Li T, Jin O, Pan Y (2015) The relationship between disease activity measured by the BASDAI and psychological status, stressful life events, and sleep quality in ankylosing spondylitis. Clin Rheumatol 34:503–510

    Article  PubMed  Google Scholar 

  30. 30.

    Karadağ O, Nakas D, Kalyoncu U, Akdoğan A, Kiraz S, Ertenli I (2012) Effect of anti-TNF treatment on sleep problems in ankylosing spondylitis. Rheumatol Int 32:1909–1913

    Article  PubMed  Google Scholar 

  31. 31.

    Karapolat H, Akkoc Y, Sari I, Eyigor S, Akar S, Kirazli Y, Akkoc N (2008) Comparison of group-based exercise versus home-based exercise in patients with ankylosing spondylitis: effects on Bath Ankylosing Spondylitis Indices, quality of life and depression. Clin Rheumatol 27:695–700

    Article  PubMed  Google Scholar 

  32. 32.

    Li Y, Zhang S, Zhu J, Du X, Huang F (2012) Sleep disturbances are associated with increased pain, disease activity, depression, and anxiety in ankylosing spondylitis: a case-control study. Arthritis Res Ther 14:R215

    Article  PubMed  PubMed Central  Google Scholar 

  33. 33.

    Rudwaleit M, Gooch K, Michel B, Herold M, Thörner A, Wong R, Kron M, Chen N, Kupper H (2011) Adalimumab improves sleep and sleep quality in patients with active ankylosing spondylitis. J Rheumatol 38:79–86

    Article  PubMed  Google Scholar 

  34. 34.

    Sieper J, Kivitz A, Van Tubergen A, Deodhar A, Coteur G, Woltering F, Landewe R (2015) Impact of certolizumab pegol on patient-reported outcomes in patients with axial spondyloarthritis. Arthritis Care Res 67:1475–1480

    CAS  Article  Google Scholar 

  35. 35.

    Solak Ö, Fidan F, Dündar Ü, Türel A, Ayçiçek A, Kavuncu V, Unlü M (2009) The prevalence of obstructive sleep apnoea syndrome in ankylosing spondylitis patients. Rheumatol 48:433–435

    Article  Google Scholar 

  36. 36.

    Critical Appraisal Skills Programme (2014) CASP checklists. CASP, Oxford. http://www.casp.uk/net. Accessed 8 Oct 2015

  37. 37.

    Doward LC, Spoorenberg A, Cook SA, Whalley D, Helliwell PS, Kay LJ, McKenna SP, Tennant A, van der Heijde D, Chamberlain MA (2003) The development of the ASQOL: a quality of life instrument specific to ankylosing spondylitis. Ann Rheum Dis 62:20–26

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  38. 38.

    Johns MW (1991) A new method for measuring daytime sleepiness: the Epworth sleepiness scale. Sleep 14:540–545

    CAS  PubMed  Google Scholar 

  39. 39.

    Jenkins CD, Stanton B-A, Niemcryk SJ, Rose RM (1988) A scale for the estimation of sleep problems in clinical research. J Clin Epidemiol 41:313–321

    CAS  Article  PubMed  Google Scholar 

  40. 40.

    Hays R, Stewart A (1992) Sleep measures. In: Ware JE Jr, Sherbourne CD (1992) The MOS 36-item short-form health survey (SF-36): I. Conceptual framework and item selection. Med Care 30(6):473–483

  41. 41.

    Hunt S, McEwan J, McKenna S (1985) Measuring health status: a new tool for clinicians and epidemiologists. J R Coll Gen Pract 35 (273):185–188

  42. 42.

    Buysse DJ, Reynolds CF, Monk TH, Berman SR, Kupfer DJ (1989) The Pittsburgh Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res 28:193–213

    CAS  Article  PubMed  Google Scholar 

  43. 43.

    Hetta J, Almqvist M, Ågren H, Hambert G, Liljenberg B, Roos BE (1985) Prevalence of sleep disturbances and related symptoms in a middle-aged Swedish population. In: Koella WP, Ruther E, Schulz H (eds) Sleep ‘84. Gustav Fischer Verlag, Stuttgart, pp 373–376

    Google Scholar 

  44. 44.

    Tekatas A, Pamuk ON (2015) Increased frequency of restless leg syndrome in patients with ankylosing spondylitis. Int J Rheum Dis 18:58–62

    Article  PubMed  Google Scholar 

  45. 45.

    Weinstock LB, Walters AS, Paueksakon P (2012) Restless legs syndrome—theoretical roles of inflammatory and immune mechanisms. Sleep Med Rev 6:341–354

    Article  Google Scholar 

  46. 46.

    Yamamoto J, Okamoto Y, Shibuya E, Nishimura M, Kawakami Y (2000) Obstructive sleep apnea syndrome induced by ossification of the anterior longitudinal ligament with ankylosing spondylitis. Nihon Kokyuki Gakkai Zasshi 38:413–416

    CAS  PubMed  Google Scholar 

  47. 47.

    Ohayon MM, Carskadon MA, Guilleminault C, Vitiello MV (2004) Metaanalysis of quantitative sleep parameters from childhood to old age in healthy individuals: developing normative sleep values across the human lifespan. Sleep 27:1255–1273

    PubMed  Google Scholar 

  48. 48.

    Sivertsen B, Krokstad S, Øverland S, Mykletun A (2009) The epidemiology of insomnia: associations with physical and mental health. The HUNT-2 study. J Psychosom Res 67:109–116

    Article  PubMed  Google Scholar 

  49. 49.

    Sivertsen B, Lallukka T, Salo P, Pallesen S, Hysing M, Krokstad S, Øverland S (2014) Insomnia as a risk factor for ill health: results from the large population-based prospective HUNT Study in Norway 2014. J Sleep Res 23:124–132

    Article  PubMed  Google Scholar 

  50. 50.

    López-Medina C, Schiotis RE, Font-Ugalde P, Castro-Villegas MC, Calvo-Gutiérrez J, Ortega-Castro R, Jiménez-Gasco R, Escudero-Contreras A, Collantes-Estévez E (2016) Assessment of fatigue in spondyloarthritis and its association with disease activity. J Rheumatol 43:751–757

    Article  PubMed  Google Scholar 

  51. 51.

    Abad V, Guilleminault C (2014) Sleep deprivation and rheumatologic disease. Sleep deprivation and disease: effects on the body, brain and behavior. Springer, New York, pp 149–170

    Google Scholar 

  52. 52.

    Ruof J, Stucki G (1999) Validity aspects of erythrocyte sedimentation rate and C-reactive protein in ankylosing spondylitis: a literature review. J Rheumatol 26:966–970

    CAS  PubMed  Google Scholar 

  53. 53.

    Günaydin R, Göksel Karatepe A, Ceşmeli N, Kaya T (2009) Fatigue in patients with ankylosing spondylitis: relationships with disease-specific variables, depression, and sleep disturbance. Clin Rheumatol 28:1045–1051

    Article  PubMed  Google Scholar 

  54. 54.

    Da Costa D, Zummer M, Fitzcharles M (2011) Biopsychosocial determinants of physical and mental fatigue in patients with spondyloarthropathy. Rhematol Int 31(4):473–480

    Article  Google Scholar 

  55. 55.

    Missaoui B, Revel M (2006) Fatigue in ankylosing spondylitis. Ann Readapt Med Phys 49:389–391

    Article  Google Scholar 

  56. 56.

    Spath-Schwalbe E, Hansen K, Schmidt F, Schrezenmeier H, Marshall L, Burger K, Fehm HL, Born J (1998) Acute effects of recombinant human interleukin-6 on endocrine and central nervous sleep functions in healthy men. J Clin Endocrinol Metab 83:1573–1579

    CAS  PubMed  Google Scholar 

  57. 57.

    Vgontzas A, Zoumakis M, Papanicolaou D, Bixler E, Prolo P, Lin HM, Vela-Bueno A, Kales A, Chrousos GP (2002) Chronic insomnia is associated with a shift of interleukin-6 and tumor necrosis factor secretion from nighttime to daytime. Metabolism 51:887–892

    CAS  Article  PubMed  Google Scholar 

  58. 58.

    Smith MT, Haythornthwaite JA (2004) How do sleep disturbance and chronic pain inter-relate? Insights from the longitudinal and cognitive-behavioral clinical trials literature. Sleep Med Rev 8:119–132

    Article  PubMed  Google Scholar 

  59. 59.

    Kundermann B, Krieg JC, Schreiber W, Lautenbacher S (2004) The effect of sleep deprivation on pain. Pain Res Manag 9:25–32

    Article  PubMed  Google Scholar 

  60. 60.

    Moore AR (2013) What works for whom? Determining the efficacy and harm of treatments for pain. Pain 154:S77–S86

    Article  Google Scholar 

  61. 61.

    Moldofsky H (2001) Sleep and pain. Sleep Med Rev 5:387–398

    Article  Google Scholar 

  62. 62.

    Jeong HJ, Lee TH, Lee JM, Choi G, Son CN, Kim JM, Cho YW, Kim SH (2014) Sleep disturbances in Korean patients with ankylosing spondylitis are associated with increased disease activity. J Rheum Dis 21:241–247

    Article  Google Scholar 

  63. 63.

    Irwin M (2002) Effects of sleep and sleep loss on immunity and cytokines. Brain Behav Immunol 16:503–512

    CAS  Article  Google Scholar 

  64. 64.

    Koh WH, Pande I, Samuels A, Jones SD, Calin A (1997) Low dose amitriptyline in ankylosing spondylitis: a short term, double blind, placebo controlled study. J Rheumatol 24(11):2158–2161

    CAS  PubMed  Google Scholar 

  65. 65.

    Koltyn KF (2000) Analgesia following exercise. A review. Sports Med 29:85–98

    CAS  Article  PubMed  Google Scholar 

  66. 66.

    Masiero S, Bonaldo L, Pigatto M, Nigro AL, Ramonda R, Punzi L (2011) Rehabilitation treatment in patients with ankylosing spondylitis stabilized with tumor necrosis factor inhibitor therapy. A randomized controlled trial. J Rheumatol 38(7):1335–1342

    CAS  Article  PubMed  Google Scholar 

  67. 67.

    Mease P, Rao S, Joshi A, Clifford S, Vernon C, Cifaldi M (2013) Quality of life, physical function and symptoms in non-radiographic axial spondyloarthritis: The patient perspective. Arthritis Rheumatol 65:S1053

    Google Scholar 

  68. 68.

    Takahashi S, Kapas L, Fang J, Krueger JM (1999) Somnogenic relationships between tumor necrosis factor and interleukin-1. Am J Physiol 276(4):R1132–R1140

    CAS  PubMed  Google Scholar 

  69. 69.

    Born J, Lange T, Hansen K, Molle M, Fehm HL (1997) Effects of sleep and circadian rhythm on human circulating immune cells. J Immunol 158:4454–4464

    CAS  PubMed  Google Scholar 

  70. 70.

    Everson CA (1993) Sustained sleep deprivation impairs host defense. Am J Physiol 265(5):R1148–R1154

    CAS  PubMed  Google Scholar 

  71. 71.

    Brophy S, Calin A (2002) Definition of disease flare in ankylosing spondylitis: the patients’ perspective. J Rheumatol 29:954–958

    PubMed  Google Scholar 

  72. 72.

    Ranjbaran Z, Keefer L, Stepanski E, Farhadi A, Keshavarzian A (2007) The relevance of sleep abnormalities to chronic inflammatory conditions. Inflamm Res 56:51–57

    CAS  Article  PubMed  Google Scholar 

  73. 73.

    Hsiao Y, Chen Y, Tseng C, Wu L, Lin W, Su V, Perng D, Chang S, Chen Y, Chen T, Lee Y, Chou K (2015) Sleep disorders and increased risk of autoimmune diseases in individuals without sleep apnea. Sleep 38:581–586

    PubMed  PubMed Central  Google Scholar 

  74. 74.

    Kang J, Lin H (2012) Obstructive sleep apnea and the risk of autoimmune diseases: a longitudinal population based study. Sleep Med 13:583–588

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

We would like to offer a special acknowledgement to the following for support of their time and expertise during the research and writing of this project: Dr. Alison Lee, Coordinator of Graduate Studies in Psychology; Dr Robert Irwin, Senior Lecturer at Bath Spa University; Charles Jenkins, Producer at BBC Bristol.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Raj Sengupta.

Ethics declarations

Conflict of interest

Shaaron Leverment declares that she has no conflict of interest. Alison Wadeley declares that she has no conflict of interest. Emily Clarke declares that she has no conflict of interest. Dr. Raj Sengupta has received research grants from Abbvie and Pfizer, speaker honoraria from Abbvie, Pfizer, UCB, Novartis, Roche, MSD and is a member of BSR Biologics guideline group, Advisor to NICE Guideline TA383.

Ethical standard

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.

Human and animal rights

This article does not contain any studies with animals performed by any of the authors.

Electronic supplementary material

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Leverment, S., Clarke, E., Wadeley, A. et al. Prevalence and factors associated with disturbed sleep in patients with ankylosing spondylitis and non-radiographic axial spondyloarthritis: a systematic review. Rheumatol Int 37, 257–271 (2017). https://doi.org/10.1007/s00296-016-3589-x

Download citation

Keywords

  • Spondyloarthritis
  • Insomnia
  • BASDAI
  • ASQoL
  • Anti-TNF
  • Inflammation