Fatigue in ANCA-associated vasculitis (AAV) and systemic sclerosis (SSc): similarities with Myalgic encephalomyelitis/Chronic Fatigue Syndrome (ME/CFS). A critical review of the literature

Figures & data

Figure 1. Comparison of the pathophysiological features of ME/CFS, SSc and AAV.

Table 1. IOM 2015 criteria for the diagnosis of ME/CFS [122].

Required Symptoms	A substantial reduction or impairment in the ability to engage in pre-illness levels of activity	Duration > 6 months Presence of fatigue that is: profound and of new onset not the result of ongoing or unusual excessive exertion not substantially alleviated by rest
	Post-exertional malaise (PEM)	Worsening of symptoms after physical, mental, or emotional exertion that would not have caused a problem before the illness. Symptoms usually worsen 12 to 48 hours after the activity or exposure and can last for days or even weeks.
	Unrefreshing sleep	Patients may not feel better or less tired even after a full night of sleep.
At least one of the following two additional manifestations must be present	Cognitive impairment	Patients have problems with thinking, memory, executive function, and information processing, as well as attention deficit and impaired psychomotor functions. Can be exacerbated by exertion and effort.
	Orthostatic intolerance	Orthostatic symptoms including lightheadedness, fainting, increased fatigue, cognitive worsening, headaches, or nausea are worsened with quiet upright posture (either standing or sitting) that are improved with lying down.

Figure 2. Flow charts summarizing search strategy for both the SSc and PSV reviews.

Table 2. Summary of papers describing fatigue prevalence, correlates and interventions in systemic sclerosis.

Author	Year	Type of Study	Populations	Fatigue Measures	Findings	Findings, Control group	Ref
Kesikburun et al.	2015	Cross-sectional	33 SSc patients 34 Healthy controls	FSS SF-36 vitality	63% of patients experienced severe fatigue. Dyspnea correlated with fatigue, pulmonary function did not. Mean FSS score in SSc patients (4.8 ± 1.8). Mean SF-36 vitality score in SSc (41.3 ± 11.9).	Mean FSS score in healthy controls (1.3 ± 0.5). Mean SF-36 vitality score in SSc (56.5 ± 7.3).	[132]
Sierakowska et al.	2016	Cross-sectional diagnostic survey	140 SSc patients* 277 RA patients	VAS Fatigue	33% of SSc patients reported having fatigue. Fatigue correlated with age, disease duration and Pol-ENAT (educational needs). Mean VAS fatigue score (46.6 ± 29.5)	19% of RA patients reported having fatigue. Fatigue correlated with age and disease duration but not with Pol-ENAT. Mean VAS fatigue score (52.9 ± 22)	[140]
Justo et al.	2017	Cross-sectional	26 SSc patients 26 Healthy controls	FACIT FIS	Mean FACIT score 29.5 (21.8–33.8). Mean FIS score 45 (26–66). Fatigue did not correlate with isokinetic parameters	Mean FACIT score 44 (40–46.3). Mean FIS score 20 (17–24.3). Fatigue did not correlate with isokinetic parameters	[139]
Gok et al.	2018	Cross-sectional	50 SSc patients 51 RA patients	FSS, VAS MAF SF-36 vitality	Fatigue similar in SSc and RA, fatigue correlated with SF-36 physical function and mental health scores and well as quality of life (HAQ). Mean FFS (4.7 ± 1.8) Mean VAS (6.0 ± 2.7) Mean MAF-GFI (27.8 ± 12.2) Mean SF-36 vitality score (48.4 ± 20.3)	Fatigue similar in SSc and RA, fatigue correlated with SF-36 physical function and mental health scores and well as quality of life (HAQ). Mean FFS (4.4 ± 1.9) Mean VAS (5.1 ± 2.8) Mean MAF-GFI (25.3 ± 12.8) Mean SF-36 vitality score (51.8 ± 21.5)	[141]
Peytrignet et al.	2018	Prospective, longitudinal Study	326 edSSc patients	FACIT	35.8% of patients quite a bit or very much fatigued. Fatigue correlated with current and previous corticosteroid use, organ involvement (renal, cardiac, and pulmonary), skin thickening, lower hemoglobin and higher CRP and ESR. Fatigue also correlated with SF-36 physical function and mental health scores and well as quality of life (sHAQ). Fatigue did not correlate with age or presence of autoantibodies. Worsening HAQ-DI over a 12-month period was associated with increasing fatigue. Mean FACIT score (31.0 (20.0–41.0)		[133]
Sierakowska et al.	2018	Cross-sectional	140 SSc patients*	VAS	Fatigue correlated with Pol-ENAT (educational needs). Fatigue correlated with increasing age, lower level of education and disease duration. Mean VAS fatigue 50 (25–70)		[146]
Horsley-Silva et al.	2019	Cross-sectional	287 SSc patients	FSS	Patients with poor sleep quality had higher fatigue scores than those that did not (44.6 vs 33.15). Patients with moderate to severe heartburn had worse fatigue scores (45.2 vs 38.4)		[144]
March et al.	2019	Cross-sectional	94 SSc patients	BFI	BFI indicated a moderate level of fatigue in SSc patients. Depressed patients had higher fatigue values than those without (33.6 vs 1.76). Fatigue also correlated with higher depression scores. Mean BFI score (39.6 ± 21.0)		[143]
Sierakowska et al.	2019	Cross-sectional	231 SSc patients	VAS	Fatigue higher in dSSc. Fatigue correlated with quality of life (SScQoL), though lost significance in final multivariate analysis. Mean VAS fatigue score 43.00 (29.04), in lSSc 38.56 (30.20) and in dSSc 47.33 (27.30).		[138]
Cetin et al.	2020	Randomized controlled trial	28 dSSc patients (14 per group)	FSS FIS	Tai Chi group: Significant improvement in fatigue after 10 weeks of Tai Chi exercise. Mean Baseline FSS (5.53 ± 1.32). Mean Baseline FIS (80.92 ± 45.41). Mean FFS score after 10 weeks (3.68 ± 1.14) Mean FIS score after 10 weeks (45.42 ± 22.33)	Home-Exercise group: No improvement in fatigue after 10 weeks. Mean Baseline FFS (5.27 ± 1.67). Mean Baseline FIS (55.07 ± 37.26). Mean FFS score after 10 weeks (5.02 ± 1.44). Mean FIS score after 10 weeks (54.42 ± 35.14).	[134]
Murphy et al	2021	Cross-sectional	267 SSc patients^#	PROMIS-29	Fatigue rated as one of most severe symptoms, T score 0.87 SD above US population (58.7 (10.4)). Fatigue was associated with ability to participate in social role, physical function and quality of life in all models tested. Fatigue not difference between lSSc (58.4 ± 10.4) and dSSc (57.5 ± 10.1) subtypes.		[136]
Murphy et al	2021	Post-Hoc analysis	267 SSc patients^#	PROMIS-29	Fatigue rated as one of most severe symptoms, T score 0.87 SD above US population (58.7 (10.4)). Fatigue remained constant over 16-week period. Fatigue at baseline predicative of worse social participation at 16 weeks. Fatigue was not a predictor of worse physical functioning or quality of life.		[142]
Santiago et al	2021	Cross-sectional	142 SSc patients	FACIT	Fatigue correlated negatively with disease severity, body image and quality of life. Fatigue correlated positively with social perceptions, happiness and positive personality traits. No difference in fatigue observed between the SSc subtypes. Mean FACIT score (34.0 ± 18.3).		[137]
Yakut et al	2021	Randomized controlled trial	40 SSc patients (20 per group)	FIS	Supervised exercise group: Significant improvement in fatigue levels after 12 weeks of supervised exercise. Mean Baseline FIS score 70 (48–99). Mean FIS after 12 weeks 25 (14–50).	Home exercise group: No improvement in fatigue after 12 weeks of home exercise. Man Baseline FIS score (76.5 (40.5–100). Mean FIS after 12 weeks 72.5 (37–91.25).	[145]
Yakut et al	2021	Cross-sectional	35 SSc patients 35 Healthy controls	FIS	80% of SSc patients reported having fatigue. Fatigue in SSc patients was significantly associated with age, dyspnea severity, pulmonary function, diffusion capacity, respiratory-peripheral muscle strength, functional capacity, and health-related quality of life. Mean FIS score (74.62 ± 31.54).	17.1% of healthy controls reported having fatigue. Mean FIS score (11.05 ± 10.20)	[135]

*Same patients in both studies

^#Same patients in both studies

Table 3. Summary of papers describing fatigue prevalence, correlates and interventions in primary systemic vasculitis.

Author	Year	Type of Study	Populations	Fatigue Measures	Findings	Findings, Control Group	Ref
Basu N. et al.	2010	Case-control	90 AAV patients 781 Healthy controls	CFS	38.4% of patients reported having moderate to severe fatigue. Fatigue varied between subtypes with higher rates of fatigue in MPA. Fatigue was associated with a history of renal involvement, depression and chronic pain (fibromyalgia). Fatigue was not associated with disease activity, disease damage, disease duration, cyclophosphamide exposure, ANCA positivity or eGFR.	26.1% of healthy controls reported having moderate to severe fatigue.	[162]
Basu N. et al. (The characterization … ANCA-associated vasculitis.)	2014	Case-control	410 AAV patients* 380 Chronic disease controls 470 Healthy controls	CFS	Fatigue was associated with both the physical and metal component of the SF36. Fatigue was the greatest contributor to impaired QoL in AAV.		[174]
Basu N, et al. (Explaining fatigue in ANCA-associated vasculitis)	2013	Cross-sectional	410 AAV patients*	CFS	74.8% of patients reported a high level of fatigue. Sleep disturbances and pain explained the highest variance in fatigue. Other significant factors included, elevated CRP, being female, unemployment, anxiety, depression, dysfunctional coping strategies, MPO subtype, eGFR and chest involvement. Factors not associated with fatigue included age, smoking, disease activity, disease duration, steroid use, and ANCA positivity.		[163]
Basu N. et al. (Fatigue-related … with polyangiitis.)	2013	Case-control	14 GPA patients 14 Healthy controls	CFS	MRI investigation into white matter changes in fatigued GPA patients with fatigue, showed no differences between cases and controls in macroscopic damage. Patients did show a greater structural connectivity in fornix and cingulum nerve bundles (p < 0.05).		[176]
Basu N. et al. (Neural correlates … imaging study)	2014	Case-control	12 GPA with fatigue 14 GPA without fatigue 13 CFS controls	CFS	Fatigue in GPA appears to involve the striato-thalamo-frontal structures of the brain.		[177]
Can Sandikci et al.	2018	Cross-sectional	155 Behcet’s disease 107 Healthy controls	MAF	Patients with active disease had significantly higher MAF scores (26.8 ± 9.7) than those with inactive disease (20.4 ± 9.4). Fatigue was correlated anxiety, depression, disease activity, QoL. No correlation was observed between fatigue, age, gender, education level, or major organ involvement and disease duration.	Healthy controls Mean MAF score 19.2 (7.3–44.2)	[168]
Grayson PC. et al.	2013	Cross-sectional	48 Behcet’s Disease^# 12 CNS 121 CS 32 GCA 332 GPA 12 HS 42 MPA 36 PAN 57 TA	MFI-20	Mean MFI score for all patient groups 16.0 (4–20), with 76% of patients having a score above 13. Illness perceptions were significantly associated with fatigue in vasculitis patients.		[166]
Grayson et al.	2014	Cross-sectional	48 Behcet’s Disease TIGR_A_211402112 CNS TIGR_A_2114021121 CS TIGR_A_211402132 Giant cell arthritis TIGR_A_2114021332 GPA TIGR_A_211402112 HS TIGR_A_211402142 MPA TIGR_A_211402136 PAN TIGR_A_211402157 TA	MFI-20	Fatigue at onset: Correlated with psychological factors, pollution in the environment and bad luck. Fatigue did not correlate with medical risk factors, infectious, hereditary or altered immune factors.	Fatigue at relapse: Correlated with psychological factors, medication factors and changes in the weather. Fatigue did not correlate with medical risk factors, pollution in the environment, infectious, hereditary, or altered immunity factors, or bad luck.	[179]
Hajj-Ali et al.	2011	Cross-sectional	55 GPA patients	VAS fatigue	76.4% of patients experienced fatigue. Fatigue correlated with depression, sleep disturbances and Fibromyalgia. Fatigue correlated with symptom intensity, but not with disease duration, vasculitis damage index or BVAS/GPA. Fatigue did not correlate with glucocorticoid use.		[165]
Ilhan et al.	2016	Cross-sectional	123 Behcet’s syndrome 71 Healthy controls	MAF	Mean MAF score (20.6 ± 14.7) Increased anxiety, depression and Physical dysfunction as well as active disease were risk factors for elevated MAF scores in BS patients. Immunosuppressive treatment and major organ involvement were not associated with fatigue. Fatigue correlated with anxiety, depression, both the physical and mental components of the SF-36, and disease activity. Fatigue did not correlate with disease duration or age.	Mean MAF score (12.8 ± 9.9) Smoking and anxiety were significantly associated with increased fatigued scores in healthy controls. Anxiety, depression, and the physical and metal components of the SF-36 were correlated with fatigue in healthy controls.	[173]
Koutanji et al.	2003	Cross-sectional	31 WG patients 9 MPA patients 11 CSS patients	SF-36 vitality VAS fatigue	SF-36 vitality and VAS fatigue were associated with pain (VAS). SF-36 vitality was associated with steroid treatment. SF-36 vitality correlated with disability (HAQ), and pain, symptom severity, sleep and fatigue as measured by VAS. SF-36 vitality score all patients (40.10 ± 21.37) SF-36 vitality scores WG (42.26 ± 22.80), CSS (38.64 ± 16.29) and MPA (34.44 ± 22.70). VAS fatigue score were significantly different between the disease groups; WG (35.32 ± 23.31), CCS (60.57 ± 29.70) and MPA (70.00 ± 36.74).		[170]
Macfarlane et al.	2013	Case-control	166 AAV patients 225 Commercial database controls 182 NHS registry control group	CFS	69.9% of AAV patients reported high levels of fatigue. Patients reported significantly higher fatigue scores than controls from both groups; however, these measures were increased when compared to the less fatigued commercial control group.	NHS control group 53.3% reported high levels of fatigue Commercial database control group reported 40% high fatigue.	[164]
Mayor & Reidy	2018	Cross-sectional	249 PSV patients	MFI-20,	91.2% of the patients reported significant fatigue. Pain, sleep disturbances and disease activity were significantly associated with fatigue.		[167]
McClean et al.	2016	Cross-sectional	48 AAV patients 41 Healthy controls	MFI-20	Mean MFI score 13 (8–16) SF-36 vitality 50 (30–60) No correlation between fatigue, disease type, lung or renal involvement or hemoglobin level, cardiovascular fitness, but fatigue was significantly associated with physical fatigue (MFI) and VDI (Vasculitis damage index) scores. There was a strong correlation between anxiety, depression, pain, sleep disturbances, muscle endurance time and physical fatigue in the patient group	Mean MFI score 5.5 (4–8) SF-36 vitality 80 (70–85)	[169]
O’Malley et al.	2020	2 clinical trials MYCYC and RITUXVAS	150 AAV patients 470 Healthy Controls	SF-36 Vitality	Baseline SF-36 vitality score median and IGR 70 (55–80) in AAV patients. On average patients fatigue improved following treatment, though they did not return to normal and a subset of patients showed no improvement at all.	Baseline SF-36 vitality score median and IGR 30 (10–48) in healthy controls	[182]
Rimland et al.	2020	Prospective observational cohort	56 GCA patients 56 TAK patients	MFI	Median MFI scores were similar between GCA and TAK, with a combined score of 14 (12–17). Fatigue correlated with illness perception, the physical and mental components of the SF-36, patient global assessment and vascular FDG-PET activity. Fatigue did not correlate with CRP or ESR. Fatigue levels did not change significantly between active and remission state of disease (±7 months).		[172]
Strand et al.	2019	Randomized control trial	GCA patients 100 on TCZ-QW +Pred-26 50 on TCZ-Q2W+Pred 50 on PBO + Pred-26 51 on PBO + Pred-52	FACIT	Baseline mean FACIT scores: TCZ-QW +Pred-26: 36.1 (11.1) Least squares mean change after 52 weeks: 5.30 Patients receiving tocilizumab (TCZ) had significant and clinically relevant improvement in their symptoms of fatigue.	Baseline mean FACIT scores: PBO + Pred-26: 35.0 (12.8) PBO + Pred-52: 31.4 (13.6) Least squares mean change after 52 weeks: PBO + Pred-26: 0.09 PBO + Pred-52: −0.42	[183]
Tomasson et al.	2019	Feasibility and Construct Validation Study	PSV (n = 973)	PROMIS SF-36 vitality	Mean baseline PROMIS fatigue score: 54.3 (9.5) Fatigue scores were similar between disease subtypes. Fatigue correlated with all subclasses of the SF-36 and patient derived disease activity scores.		[171]
Tuin J et al.	2013	Case-control	AAV patients 33 with androgen deficiency 37 without androgen deficiency	MFI-20	Mean general fatigue MFI score all patients: 11.93 (4.8) Mean general fatigue MFI score androgen deficient patients 13.0 (4.3) Age, lower testosterone levels, VDI and CRP were predictive of increased fatigue in AAV patients.	Mean general fatigue MFI score androgen non-deficient patients 11.0 (5.2)	[175]
Harper et al.	2021	Randomized control feasibility study	43 AAV patients 22 in intervention group 21 in standard care group		Intervention Group MFI Baseline: 16.3 12 wks: 14.2 24 wks: 13.4 52 wks: 13.8 Adjusted mean differences favored intervention group	Standard Care Group MFI Baseline: 16.9 12 wks: 15.5 24 wks: 14.3 52 wks: 14.7	[184]

*Same patients

^#Same patients

Figure 3. Factors associated with fatigue in SSc and AAV. Factors were weighted by how many times they were found to be associated with fatigue within each respective review.

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