Abstract
Objective
The aim of the study was to determine which disease-related factors and non-disease features can explain the presence of systemic lupus erythematosus (SLE)-related fatigue in Turkish patients.
Methods
This cross-sectional study was carried out with 99 SLE patients and 71 healthy controls. To assess fatigue and health-related quality of life (HRQoL) the participants were asked to complete two questionnaires: the short form-36 health survey (SF-36) and the multidimensional assessment of fatigue (MAF) scale. Anxiety and depression of participants were assessed by the hospital anxiety and depression scale (HADS).
Results
A total of 99 patients (female/male 95/4) and 71 controls (female/male 40/31) were studied. The mean age and standard deviation (±SD) of patients and controls were 43.3 ± 12.2 years and 43.2 ± 12.1 years, respectively. The mean (SD) disease duration was 7.8 ± 5.3 years and median SLE disease activity index (SLEDAI) score was 0 (range = 0–16). The level of fatigue was higher in patients compared to controls with mean MAF scores of 24.7 ± 12.2 and 12.8 ± 9.9 (p < 0.001), respectively. The HADS-D and HADS-A scores were also significantly higher in SLE patients (6.6 ± 4.3 vs. 3.6 ± 2.9, p < 0.001 and 7.2 ± 4 vs. 4.9 ± 4, p = 0.007, respectively). There were no significant associations between the MAF and SLEDAI scores (r = 0.05, p = 0.63) but MAF scores positively correlated with age, HADS-A and HADS-D scores and negatively correlated with physical component summary (PCS), mental component summary (MCS) and each domain of SF-36 except role emotional in SLE patients.
Conclusion
Fatigue is an important factor influencing patient daily life independent from disease activity in our study. The SLE patients with severe fatigue should also be assessed for other possible underlying causes such as anxiety, depression and poor quality of life.
Zusammenfassung
Ziel
Ziel der Studie war es zu bestimmen, durch welche krankheitsbedingten Faktoren und nicht krankheitsbedingten Merkmale das Vorliegen einer durch Lupus erythematodes (SLE) hervorgerufenen Fatigue bei türkischen Patienten erklärt werden kann.
Methoden
Diese Querschnittsstudie wurde mit 99 SLE-Patienten und 71 gesunden Kontrollpersonen durchgeführt. Um Fatigue und gesundheitsbedingte Lebensqualität (HRQoL) zu untersuchen, wurden die Teilnehmer gebeten, 2 Fragebögen auszufüllen: den Short-Form(SF)-36 Fragebogen zum Gesundheitszustand und die Multidimensional Assessment of Fatigue (MAF) Scale. Angst und Depression der Teilnehmer wurden mittels der Hospital Anxiety and Depression Scale (HADS) untersucht.
Ergebnisse
Insgesamt wurden 99 Patienten (95 weiblich, 4 männlich) und 71 Kontrollpersonen (40 weiblich, 31 männlich) untersucht. Das mittlere Alter (± Standardabweichung [SD]) der Patienten und Kontrollpersonen betrug 43,3 ± 12,2 bzw. 43,2 ± 12,1 Jahre. Die mittlere (± SD) Krankheitsdauer lag bei 7,8 ± 5,3 Jahren und der mediane Score des SLE-Krankheitsaktivitätsindex („SLE disease activity index“, SLEDAI) betrug 0 (Range: 0–16). Der Fatigue-Wert war bei den Patienten höher als bei der Kontrollgruppe mit einem mittleren MAF-Score von 24,7 ± 12,2 bzw. 12,8 ± 9,9 (p < 0,001). Die HADS-D- und HADS-A-Scores waren ebenfalls signifikant höher bei SLE-Patienten (6,6 ± 4,3 vs. 3,6 ± 2,9 [p < 0,001] bzw. 7,2 ± 4 vs. 4,9 ± 4, [p = 0,007]). Es gab keine signifikante Assoziation zwischen den MAF- und SLEDAI-Scores (r = 0,05; p = 0,63), jedoch korrelierten die MAF-Scores positiv mit dem Alter, den HADS-A- und HADS-D-Scores sowie negativ mit der Physical Component Summary (PCS), der Mental Component Summary (MCS) und jeder Domäne des SF-36-Fragebogens mit Ausnahme der emotionalen Rollenfunktion.
Schlussfolgerung
Fatigue ist ein wichtiger Faktor, der das Alltagsleben der Patienten in unserer Studie unabhängig von der Krankheitsaktivität beeinflusst. SLE-Patienten mit schwerer Fatigue sollten auch auf andere möglicherweise zugrunde liegenden Ursachen wie Angst, Depression oder schlechte Lebensqualität untersucht werden.
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References
Petri M, Genovese M, Engle E, Hochberg M (1991) Definition, incidence, and clinical description of flare in systemic lupus erythematosus. A prospective cohort study. Arthritis Rheum 34:937–944
Yilmaz-Oner S, Oner C, Dogukan FM, Moses TF, Demir K, Tekayev N, Yilmaz N, Tuglular S, Direskeneli H (2015) Anxiety and depression predict quality of life in Turkish patients with systemic lupus erythematosus. Clin Exp Rheumatol 33:360–365
McElhone K, Abbott J, Teh LS (2006) A review of health related quality of life in systemic lupus erythematosus. Lupus 15:633–643
Jolly M (2005) How does quality of life of patients with systemic lupus erythematosus compare with that of other common chronic illnesses? J Rheumatol 32:1706–1708
McElhone K, Abbott J, Shelmerdine J, Bruce IN, Ahmad Y, Gordon C, Peers K, Isenberg D, Ferenkeh-Koroma A, Griffiths B, Akil M, Maddison P, Teh LS (2007) Development and validation of a disease-specific health-related quality of life measure, the LupusQol, for adults with systemic lupus erythematosus. Arthritis Rheum 57:972–979
Thumboo J, Strand V (2007) Health-related quality of life in patients with systemic lupus erythematosus: an update. Ann Acad Med Singap 36:115–122
Cleanthous S, Tyagi M, Isenberg DA, Newman SP (2012) What do we know about self-reported fatigue in systemic lupus erythematosus? Lupus 21:465–476. doi:10.1177/0961203312436863
Zonana-Nacach A, Roseman JM, McGwin G Jr, Friedman AW, Baethge BA, Reveille JD, Alarcón GS (2009) Systemic lupus erythematosus in three ethnic groups. VI: Factors associated with fatigue within 5 years of criteria diagnosis. LUMINA Study Group. LUpus in MInority populations: NAture vs Nurture. Lupus 9:101–109
Omdal R, Sjöholm H, Koldingsnes W, Sundsfjord JA, Jacobsen EA, Husby G, Mellgren SI (2005) Fatigue in patients with lupus is not associated with disturbances in cerebral blood flow as detected by SPECT. J Neurol 252:78–83
Wang B, Gladman DD, Urowitz MB (1998) Fatigue in lupus is not correlated with disease activity. J Rheumatol 25:892–895
Wysenbeek AJ, Leibovici L, Weinberger A, Guedj D (1993) Fatigue in systemic lupus erythematosus. Prevalence and relation to disease expression. Br J Rheumatol 32:633–635
Da Costa D, Dritsa M, Bernatsky S, Pineau C, Ménard HA, Dasgupta K, Keschani A, Rippen N, Clarke AE (2006) Dimensions of fatigue in systemic lupus erythematosus: relationship to disease status and behavioral and psychosocial factors. J Rheumatol 33:1282–1288
Jump RL, Robinson ME, Armstrong AE, Barnes EV, Kilbourn KM, Richards HB (2005) Fatigue in systemic lupus erythematosus: contributions of disease activity, pain, depression, and perceived social support. J Rheumatol 32:1699–1705
Mancuso CA, Perna M, Sargent AB, Salmon JE (2011) Perceptions and measurements of physical activity in patients with systemic lupus erythematosus. Lupus 20:231–242. doi:10.1177/0961203310383737
Mackay M (2015) Lupus brain fog: a biologic perspective on cognitive impairment, depression, and fatigue in systemic lupuserythematosus. Immunol Res 63:26–37. doi:10.1007/s12026-015-8716-3
Morris G, Maes M (2013) Myalgic encephalomyelitis/chronic fatigue syndrome and encephalomyelitis disseminata/multiple sclerosis show remarkable levels of similarity in phenomenology and neuroimmune characteristics. BMC Med 11:205. doi:10.1186/1741-7015-11-205
Lucas K, Maes M (2013) Role of the Toll Like receptor (TLR) radical cycle in chronic inflammation: possible treatments targeting the TLR4 pathway. Mol Neurobiol 48:190–204. doi:10.1007/s12035-013-8425-7
Moses N, Wiggers J, Nicholas C, Cockburn J (2005) Prevalence and correlates of perceived unmet needs of people with systemic lupus erythematosus. Patient Educ Couns 57:30–38
Danoff-Burg S, Friedberg F (2009) Unmet needs of patients with systemic lupus erythematosus. Behav Med 35:5–13. doi:10.3200/BMED.35.1.5-13
Krupp LB, LaRocca NG, Muir-Nash J, Steinberg AD (1989) The fatigue severity scale. Application to patients with multiple sclerosis and systemic lupus erythematosus. Arch Neurol 46:1121–1123
Belza BL, Henke CJ, Yelin EH, Epstein WV, Gilliss CL (1993) Correlates of fatigue in older adults with rheumatoid arthritis. Nurs Res 42:93–99
Mortada M, Abdul-Sattar A, Gossec L (2015) Fatigue in Egyptian patients with rheumatic diseases: a qualitative study. Health Qual Life Outcomes 13:134. doi:10.1186/s12955-015-0304-7
Hifinger M, Putrik P, Ramiro S, Keszei AP, Hmamouchi I, Dougados M, Gossec L, Boonen A (2016) In rheumatoid arthritis, country of residence has an important influence on fatigue: results from the multinational COMORA study. Rheumatology (Oxford) 55:735–744. doi:10.1093/rheumatology
Burgos PI, Alarcón GS, McGwin G Jr, Crews KQ, Reveille JD, Vilá LM (2009) Disease activity and damage are not associated with increased levels of fatigue in systemic lupus erythematosus patients from a multiethnic cohort: LXVII. Arthritis Rheum 61:1179–1186. doi:10.1002/art.24649
Hochberg MC (1997) Updating the American College of Rheumatology revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum 40:1725
Bombardier C, Gladman DD, Urowitz MB, Caron D, Chang CH (1992) Derivation of the SLEDAI. A disease activity index for lupus patients. The Committee on Prognosis Studies in SLE. Arthritis Rheum 35:630–640
Zigmond AS, Snaith RP (1983) The hospital anxiety and depression scale. Acta Psychiatr Scand 67:361–370
Sterling K, Gallop K, Swinburn P, Flood E, French A, Al Sawah S, Iikuni N, Naegeli A, Nixon A (2014) Patient-reported fatigue and its impact on patients with systemic lupus erythematosus. Lupus 23:124–132. doi:10.1177/0961203313511554
Overman CL, Kool MB, Da Silva JA, Geenen R (2016) The prevalence of severe fatigue in rheumatic diseases: an international study. Clin Rheumatol 35:409–415. doi:10.1007/s10067-015-3035-6
Godaert GL, Hartkamp A, Geenen R, Garssen A, Kruize AA, Bijlsma JW, Derksen RH (2002) Fatigue in daily life in patients with primary Sjögren’s syndrome and systemic lupus erythematosus. Ann N Y Acad Sci 966:320–326
Thyberg I, Dahlström O, Thyberg M (2009) Factors related to fatigue in women and men with early rheumatoid arthritis: the Swedish TIRA study. J Rehabil Med 41:904–912. doi:10.2340/16501977-0444
Kozora E, Ellison MC, West S (2006) Depression, fatigue, and pain in systemic lupus erythematosus (SLE): relationship to the American College of Rheumatology SLE neuropsychological battery. Arthritis Rheum 55:628–635
Kozora E, Arciniegas DB, Zhang L, West S (2007) Neuropsychological patterns in systemic lupus erythematosus patients with depression. Arthritis Res Ther 9:R48
Pettersson S, Moller S, Svenungsson E, Gunnarsson I, Welin Henriksson E (2010) Women’s experience of SLE-related fatigue: a focus group interview study. Rheumatology (Oxford) 49:1935–1942. doi:10.1093/rheumatology/keq174
Pettersson S, Boström C, Eriksson K, Svenungsson E, Gunnarsson I, Henriksson EW (2015) Lifestyle habits and fatigue among people with systemic lupus erythematosus and matched population controls. Lupus 24:955–965. doi:10.1177/0961203315572716
Mattsson M, Möller B, Lundberg IE, Gard G, Boström C (2008) Reliability and validity of the Fatigue Severity Scale in Swedish for patients with systemic lupus erythematosus. Scand J Rheumatol 37:269–277. doi:10.1080/03009740801914868
Skapinakis P, Lewis G, Mavreas V (2004) Temporal relations between unexplained fatigue and depression: longitudinal data from an international study in primary care. Psychosom Med 66:330–335
Gilboe IM, Kvien TK, Husby G (1999) Health status in systemic lupus erythematosus compared to rheumatoid arthritis and healthy controls. J Rheumatol 26:1694–1700
Schwartzberg JG, Cowett A, VanGeest J, Wolf MS (2007) Communication techniques for patients with low health literacy: a survey of physicians, nurses, and pharmacists. Am J Health Behav 31:96–104
Fonseca R, Bernardes M, Terroso G, de Sousa M, Figueiredo-Braga M (2014) Silent burdens in disease: fatigue and depression in SLE. Autoimmune Dis 2014:790724. doi:10.1155/2014/790724
The American College of Rheumatology (1999) nomenclature and case definitions for neuropsychiatric lupus syndromes. Arthritis Rheum 42:599–608
Bruce IN, Mak VC, Hallett DC, Gladman DD, Urowitz MB (1999) Factors associated with fatigue in patients with systemic lupus erythematosus. Ann Rheum Dis 58:379–381
Tench CM, McCurdie I, White PD, D’Cruz DP (2000) The prevalence and associations of fatigue in systemic lupus erythematosus. Rheumatology (Oxford) 39:1249–1254
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S. Yilmaz-Oner, B. Ilhan, M. Can, F. Alibaz-Oner, O. Polat-Korkmaz, G. Ozen, G. Mumcu, H.M. Kremers, S. Tuglular and H. Direskeneli state that they have no competing interest.
All studies on humans described in this manuscript were carried out with the approval of the responsible ethics committee and in accordance with national law and the Helsinki Declaration of 1975 (in its current revised form). Informed consent was obtained from all patients included in the study.
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U. Müller-Ladner, Bad Nauheim
U. Lange, Bad Nauheim
S. Yilmaz-Oner and B. Ilhan contributed equally to the study
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Yilmaz-Oner, S., Ilhan, B., Can, M. et al. Fatigue in systemic lupus erythematosus. Z Rheumatol 76, 913–919 (2017). https://doi.org/10.1007/s00393-016-0185-0
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DOI: https://doi.org/10.1007/s00393-016-0185-0