Recommendation n 1
Recommendation #1: Patient assessment
In addition to the standard care of non-lupus patients of the same age and sex, the assessment of the SLE patient must include the evaluation of: disease activity by a validated index at each visit, organ damage annually, general quality of life by patient history and/or by a 0 to 10 Visual Analogue Scale (VAS- patient global) at each visit, comorbidities and drug toxicity.
The clinical picture of SLE is extremely variable and may be related to disease activity, organ damage, drug toxicity and quality of life. Many studies have documented poor correlations between activity, damage, and quality of life, suggesting that these measures assess different aspects of patient status (1-9). Activity and damage assessment have important prognostic significance as studies have shown a significant correlation between the degree of activity and the subsequent development of damage and between early damage accrual and the development of damage and mortality.
Therefore, many authors have suggested that the assessment of SLE patients should include measures of disease activity, disease damage, quality of life and drug toxicity (3-5).
In recent years, indices have been developed and validated to measure these parameters (1-34). The most frequently used activity indices are the British Isles Lupus Assessment Group (BILAG), the European Consensus Lupus Activity Measurement (ECLAM), the Lupus Activity Index (LAI), the Systemic Lupus Activity Measure (SLAM), the SIS (SLE Index Score) and the SLE Disease Activity Index (SLEDAI), and revised versions as SLEDAI-2K and Safety of Estrogen in Lupus Erythematosus National Assessment (SELENA) SLEDAI. The Systemic Lupus International Collaborating Clinics (SLICC/ACR) Damage Index has been developed to assess irreversible damage in SLE patients occurring after disease onset. Recently, SLE- specific indices to assess patient’s quality of life have been developed and validated as well, although the SF-36 is most widely used to assess quality of life.
Indeed the assessment of activity, damage and quality of life is a part of the routine clinical evaluation. However, it relies on the physician’s experience and therefore may be subject to significant inter- as well as intra-rater variability in the absence of appropriate training. Despite their prognostic role and their use in observational studies and randomized controlled trials, the limited data available suggest that validated indices are used in a small number of centres in clinical practice. This might be attributed to issues of feasibility (particularly time required to calculate indices, not always available during routine assessments) and the need to perform tests which are not always part of the routine patient assessment (e.g. immunological tests, eye examination etc). However, the use of validated indices might greatly improve the collection of data, and therefore the quality, of the assessment made during routine evaluations, and few studies show the feasibility of performing validated disease activity indices in routine clinical practice (35). Therefore, the Committee agreed upon recommending the routine assessment of disease activity using any validated index (global or organ specific) and/or a physician global assessment on a scale from 0 to 3, and an annual assessment of damage with the SLICC/ACR damage index.
In randomized controlled trials, the assessment of quality of life is usually based on the use of the short form 36 (SF36), and recently SLE- specific indices have been developed (2-8,36-39). These tools allow a comparison of QoL among patients and centres and therefore their use should be considered when performing observational studies. However, it was felt that the administration of these questionnaires in routine clinical practice was unlikely to be feasible, and therefore the Committee agreed on the routine evaluation of patient’s quality of life based on the patient’s history or with a 0 to 10 VAS (patient global) at each visit.
Recommendation # 2: Cardiovascular risk factors
At baseline and during follow up at least once a year*:
• Assess: smoking, vascular events (cerebral/cardiovascular), physical activity, oral contraceptives, hormonal therapies, and family history of cardiovascular disease.
• Blood tests: blood cholesterol, glucose.
• Examination: Blood pressure, body mass index (and/or waist circumference).
*Some patients may need more frequent follow-up (i.e. patients on glucocorticoids).
Premature atherosclerosis and increased incidence of cardiovascular disease (CVD) among patients with SLE are well established (40-89). CVD is an important cause of morbidity and a leading cause of death of SLE patients (43-51,53). Many authors have reported a higher prevalence of traditional risk factors among SLE patients. In 1992, Petri et al reported that the prevalence of all CV risk factors was significantly higher among SLE patients versus age-sex and race matched non-SLE subjects (general population) (40).
The systematic literature review (SLR) found an increased prevalence of hypertension and dyslipidemia among SLE patients. The reported prevalence of hypertension among SLE patients ranges from 14% to 52%, with half of the examined studies reporting a prevalence ≥ 40%. In all the studies comparing SLE patients with healthy controls, the prevalence of hypertension was significantly higher in SLE patients (33-52% SLE patients vs 6-35% healthy controls) (40-42, 44-50, 54, 57, 59-71).
Published data on lipid profiles agree on a high prevalence (ranging from 11.5 to 75%) of dyslipidemia (most frequently assessing cholesterol levels) in SLE patients. Current prednisone dose and cumulative prednisone dose have been correlated with total cholesterol levels in different studies (72-80).
Fewer data are available on whether the prevalence of diabetes (prevalence ranging from 0.9 to 11.2%) or obesity is increased, as only a few studies have shown a higher prevalence among SLE patients (81-83). No differences have been reported with respect to the general population as far as smoking habits are concerned (84). It might be expected that SLE patients have a more sedentary life-style; indeed one study reported a 70% of prevalence of sedentary life-style according to the American Heart Association Guidelines.
Data from the literature have shown that the increased incidence of CVD and premature atherosclerosis in SLE cannot be fully explained by the traditional CVD risk factors. In fact, it has been shown that population screening based on Framingham risk equations, when applied to SLE patients, does not fully explain the cardiovascular risk (90-91). On this basis, SLE could be included in the group of conditions in which the use of these predictive charts is insufficient. For this reason, some authors have proposed that SLE should be considered as a coronary heart disease high risk state (much like diabetes mellitus) and have suggested different targets for risk factor modification specifically tailored to SLE patients (91-94).
However, at present, agreement exists on the need for monitoring traditional cardiovascular (CV) risk factors and treating modifiable risk factors according to the existing guidelines.
Based on these data, the assessment of traditional CV risk factors in routine clinical practice is recommended and should be performed with patient history, patient examination and laboratory exams (i.e. blood cholesterol and blood glucose).
As far as obesity is concerned, an alternative to body mass index (BMI) might be the measurement of waist circumference, which appears to be associated with the risk of death (95).
In view of the potential of drugs to affect the occurrence of CV risk factors, more frequent assessments may be required in certain situations, e.g glucocorticoids therapy (30, 34, 52, 92, 96).
Recommendation # 3: Other comorbidities
1. Osteoporosis.
All SLE patients
• should be assessed for adequate calcium and Vitamin D intake, regular exercise, and smoking habit,
• should be screened and followed for osteoporosis according to existing guidelines
o for postmenopausal women
o for patients on glucocorticoids, or on any other medication that may reduce BMD
2. Cancer. Cancer screening is recommended according to the guidelines for the general population, including PAP smears..
SLE patients are at increased risk of comorbidities, among which osteoporosis and cancer have been considered in the present recommendations due to their frequency (97-121).
In the majority of the studies included in our SLR, osteoporosis was assessed by DXA according to WHO definitions. The prevalence of fractures, when evaluated, was done by radiographs. The majority of data refer to women with SLE, either premenopausal or postmenopausal. The prevalence of osteoporosis among SLE patients varied from 4 to 24% (spine 7-23%, femur 3-23%). When only premenopausal patients were evaluated, the prevalence of osteoporosis ranged between 10-20%. Vertebral fractures had a prevalence ranging between 7.6% and 37% (98, 104, 110,114,117).
In SLE patients, additional risk factors for osteoporosis include treatment with glucocorticoids as well as other medications that may impact bone mass (such as anticoagulant therapy or immunosuppressive drugs) and by reduced levels of vitamin D related to the avoidance of sun exposure or ethnicity (African, African- Caribbean, African- Americans) (97, 104, 105, 108, 113, 118, 119).
Osteoporosis is a well established side effect of chronic glucocorticoids use; although the incidence of osteoporosis is time and dose dependent, there is no consensus about a ‘‘safe’’ dose. Indeed, data suggest that bone loss is observed in patients exposed to 7.5 mg of prednisolone daily. According to the EULAR- based recommendations on the management of systemic glucocorticoid therapy in rheumatic diseases, “If a patient is started on prednisone >7.5 mg daily and continues on prednisone for more than 3 months, calcium and vitamin D supplementation should be prescribed” (118). Therefore, it is recommended that SLE patients be assessed for adequate calcium and Vitamin D intake. In addition, assessment of modifiable risk factors for osteoporosis, such as smoking habits and physical exercise are also recommended.
It is recommended that SLE patients should be screened according to the existing guidelines for postmenopausal women (120, 121) and/or for patients treated with medications that may affect bone mass (Table 1).
Table 1. Drugs that may affect bone mass
|Glucocorticoids |
|Immunosuppressive drugs |
|Cyclosporine |
|Tacrolimus |
|Methotrexate |
|Heparin |
|Thyroxine |
|Aromatase inhibitors |
|Longterm anticonvulsants (phenytoin, phenobarbital, carbamazepine, piramidone) |
|Gonadotropin releasing hormone antagonists |
|Proton pump inhibitors (omeprazole) |
|Loop diuretics |
|Antidepressants (particularly selective serotonin reuptake inhibitors- SSRIs) |
The SLR found that cancer incidence is increased in SLE patients, particularly haematological malignancies (non-Hodgkin lymphoma), cervical cancer (cervical intraepithelial neoplasm), breast cancer and lung cancer (122-140).
In addition, an abnormal cervico-vaginal cytology is reported in up to 16% of examined patients, with an OR ranging between 1.8 and 28 compared with the general population (Table 2) (135, 138- 140).
Table 2. Standardized incidence rate of cancer in SLE patients
|Type of cancer |Standardized incidence rate of cancer |
|All cancers |1.15- 1.59 |
|Breast cancer |0.89- 2.1 |
|Hematologic cancers |1.31- 2.75 |
|Hodgkin lymphoma |2.4- 17.82 |
|Non Hodgkin lymphoma |3.47- 11.63 |
|Cervical cancer |3.08- 8.15 |
|Lung cancer |1.31- 5.55 |
With the exception of cervical intraepithelial neoplasm, the existing studies fail to clearly show an association between the development of cancer and treatment with immunosuppressive drugs (140).
No increased incidence of bladder cancer was reported, not even in association with cyclophosphamide therapy, independent of the protocol (NIH protocol, Eurolupus protocol, or oral administration) (141-143). The association between bladder cancer and cyclophoshamide use described among patients with haematological malignancies and with vasculitis appears to be related to the cumulative dose of cyclophosphamide and is significant for cumulative doses over 25 gr (144, 145).
Additionally, Bernatsky et al have found that SLE patients undergo cancer screening (mammogram, fecal occult blood and PAP test) even less frequently than the general population (146).
Based on these data, it is recommended that patients with SLE undergo cancer screening at least according to the guidelines for the general population (e.g, the American Cancer Society Guidelines for the Early Detection of Cancer relative to breast cancer, cervical cancer and colon and rectal cancer). However, taking in consideration the epidemiological and clinical characteristics of SLE patients, the development of SLE specific guidelines might be considered.
As far as cervical intraepithelial neoplasm is concerned, literature data show that HPV (Human Papillomavirus) DNA testing may improve the specificity of the diagnosis and therefore should be considered (147-150).
Recommendation #4: Infection risk
# 4.1 Screening
We recommend that patients should be screened for:
– Human Immunodeficiency virus (HIV) based on patient’s risk factors,
– Hepatitis C virus (HCV), hepatitis B virus (HBV) based on patient’s risk factors, particularly before immunosuppressive (IS) drugs including high dose glucocorticoids are started,
– Tuberculosis, according to local guidelines, especially before IS drugs including high dose glucocorticoids are started,
– Cytomegalovirus (CMV) testing should be considered during treatment in selected patients.
# 4.2 Vaccination
SLE patients are at high risk of infections and prevention should be recommended. The administration of inactivated vaccines (especially influenza and pneumococcus), following the Centers for Disease Control (CDC) guidelines for immunosuppressed patients, should be strongly considered in SLE patients on IS drugs, preferably administered when the SLE is inactive. For other vaccinations, an individual risk/benefit analysis is recommended.
# 4.3 Monitoring
At follow up visits, continuous assessment of the risk of infection by taking into consideration the presence of:
– severe neutropenia ( 50 mg/l).
Recommendation #7 : Mucocutaneous involvement
Mucocutaneous lesions should be characterized, according to the existing classification systems, as to whether they may be:
- Lupus erythematosus (LE)-specific.
- LE-nonspecific.
- LE mimickers.
- Drug-related.
Lesions should be assessed for activity and damage, using validated indices (i.e. CLASI).
Cutaneous manifestations occur often during the course of the disease, being observed in over 80% of patients. They include LE-specific and LE-nonspecific skin lesions, primarily based on histopathologic criteria (292- 303). The LE-specific cutaneous findings encompass the various subtypes of cutaneous lupus erythematosus (CLE), which are subdivided into four different categories as defined by constellations of clinical features, histological changes, laboratory abnormalities, and average duration of skin lesions: acute CLE (ACLE), subacute CLE (SCLE), chronic CLE (CCLE), and intermittent CLE (ICLE). In contrast, skin lesions, such as urticarial vasculitis and livedo reticularis, are some of the most common LE-nonspecific cutaneous lesions and are mostly associated with SLE.
However, the diagnosis of cutaneous manifestations in LE may be difficult, as many conditions may mimic LE (Table 3) and therefore the diagnosis may require evaluation by an experienced dermatologist and a skin biopsy for histological analysis.
Data from the Cutaneous Lupus Disease Area and Severity index (CLASI) study confirm this difficulty, showing the presence of misdiagnosis among specialists (specificity of diagnosis of 0.46 for the rheumatology group versus 0.74 for the dermatology group). In addition, three out of the 11 patients enrolled in the first CLASI were excluded because findings from repeated biopsies showed the presence of confounding conditions that made the diagnosis of CLE impossible (304- 306).
Follow-up re-biopsy is recommended if there is a change in the clinical morphology of the lesions or if there is a lack of response to treatment.
The CLASI index has been recently developed to assess patients with CLE. The index has two scores, one describing activity of the disease and the second damage; the index has been validated and its reliability has been shown. Recent data have confirmed its reliability when used by dermatologists and also by rheumatologists. Although this index was developed to create a measure of consensus in trials of CLE, its use in clinical practice might be considered at least in SLE patients with prevalent cutaneous manifestations, as this might improve the quality of the physician judgment on activity and response to therapy (304-305).
Table 3. Most frequent lupus mimickers
|Subtype |LE mimickers |
|ACLE |Localized form: |
| |Dermatomyositis, rosacea, seborrhea, eczema , tinea facei, erysipelas, perioral dermatitis |
| | |
| |Generalized form: |
| |Virus exanthema, drug eruption, erythema multiforme, toxic epidermal necrolysis, dermatomyositis |
|SCLE |Tinea corporis, psoriasis, mycosis fungoides, erythema multiforme/toxic epidermal necrolysis, erythema annulare |
| |centrifugum, erythema gyratum repens, drug eruption, nummular eczema, seborrhea, eczema, actinic keratosis |
|DLE |Tinea faciei, actinic keratosis, lupus vulgaris, sarcoidosis |
|LEP |Different forms of panniculitis, subcutaneous sarcoidosis, polyarteritis nodosa, malignant lymphoma (in particular |
| |subcutaneous panniculitic-like T-cell lymphoma), morphea profunda, subcutaneouss granuloma anulare |
|CHLE |Pernio, lupus pernio, vasculitis/vasculopathy |
|LET |Lymphocytic infiltration of Jessner-Kanof, polymorphic light eruption, pseudolymphoma, B-cell lymphoma, plaque-like |
| |cutaneous mucinosis, solar urticaria |
ACLE, acute cutaneous lupus erythematosus; SCLE, subacute cutaneous lupus erythematosus; DLE, discoid lupus erythematosus; LEP, lupus erythematosus profundus/panniculitis; CHLE, chilblain lupus erythematosus; LET, lupus erythematosus tumidus
Recommendation #8: Kidney
- Patients with a persistently abnormal urinalysis or raised serum creatinine should have urine protein/creatinine ratio (or 24 h proteinuria), urine microscopy, renal ultrasound and be considered for referral for biopsy.
- Patients with established nephropathy should have protein/creatinine ratio (or 24 h proteinuria) and immunological tests (C3, C4, anti-dsDNA), urinary sediment microscopy and blood pressure at least every 3 months for the first 2-3 years.
- Patients with established chronic renal disease (eGFR < 60 ml or stable proteinuria > 0.5 mg/24 hrs) should be followed according to the National Kidney Foundation guidelines for chronic kidney disease.
Kidney involvement is common in SLE patients and is an important cause of morbidity and mortality. Despite all therapies, up to 25% of patients treated with cyclophosphamide (CYC) protocols may develop renal insufficiency and end stage renal disease (ESRD). Treatment discontinuation is associated with the occurrence of flares - up to 50% - independent of the type of treatment protocol used (307- 312).
The SLR found that serum creatinine, urine sediment analysis, proteinuria (either as 24 hours proteinuria or urine protein/creatinine ratio) and blood pressure have a predictive value for the presence and outcome of kidney involvement and the occurrence of flares. Urinary infection should be excluded in presence of abnormal microscopy (270-285, 307- 317).
According to recently published Recommendations, renal biopsy has a role in diagnosing lupus nephritis as well as defining prognosis and treatment and should therefore be considered (241).
Serum creatinine, urine sediment analysis, proteinuria and blood pressure have a predictive value for the presence and outcome of kidney involvement and the occurrence of flares. Relapses of kidney disease are common, being observed in up to 45%. The SLR found that the relapse rate increases over time, being 6-9% at 1 year, around 24% at 2 years, 21-28% at three years and 25-45% at 5 years. At 10 years, relapse rate is 45%. The estimate flare rate is 0.1-0.2 flares per patient and year (284, 308-314).
The renal outcome has been variably defined as doubling serum creatinine or reaching end stage renal disease (ESRD). The risk of doubling serum creatinine ranges between 7.4 and 8.5% at 5 years and between 14.3 and 18.2% at 10 years. The risk of developing ESRD ranges between 3 and 36%. The percentage of patients without ESRD ranges between 66 and 97%. Black patients have a higher risk of developing ESRD (52% at 5 years). The following variables have been associated with renal survival at 5 years: age (< 30=79%; >30=48%), ethnicity (Black= 49-59%, Others= 76-82%), serum creatinine (2.4=31% or 2=49%), hypertension (present= 69%, absent=87%), C3 complement, nephritic flares, kidney biopsy, activity index, and chronicity index. Reduction of proteinuria after six months combination IS/stetroid therapy, i.e. renal response is associated with a lower risk of doubling serum creatinine or ESRD (275- 280, 284, 285, 317).
Guidelines have been published for the monitoring of patients with chronic kidney disease ().
Recommendation #9: Neuropsychiatric manifestations
- SLE patients should be monitored for the presence of neuropsychological symptoms (seizures, paresthesiae, numbness, weakness, headache, epilepsy, depression, etc) by focused history.
- Cognitive impairment may be assessed by evaluating attention, concentration, word finding and memory difficulties (i.e. by asking the patient about problems with multitasking, with household tasks, or memory). If there is a suspicion of any cognitive impairment, then the patient should be assessed in further detail.
Neurological involvement (central, peripheral, or autonomic) occurs frequently in SLE. A wide range of prevalence from 14 to 80 % has been reported in the literature (318- 326). The most frequent syndromes observed are headache, mood disorders, seizures, cognitive impairement (CI) and cerebrovascular disease.
The assessment of neurological symptoms is difficult and no specific instrument has been evaluated in clinical practice. Therefore it has been suggested that patients should be monitored by clinical history and examination.
As far as CI is considered, the tests evaluating CI in SLE are various and differ between studies. The majority of studies report a high prevalence of CI; 7 out of the 30 studies examined reported a very high prevalence (>50% of all patients evaluated), 8 studies reported a prevalence ranging between 20 and 50%, and 6 a low prevalence (< 20%) with CI. In few studies, a comparison with control groups was performed, either with patients with rheumatoid arthritis or with the general population. In four studies, CI in control groups was much less prevalent than in SLE.
CI may be assessed by evaluating memory, attention, concentration, and word finding difficulties (i.e. by asking the patient whether he can multitask, or whether she has difficulties with household tasks, or whether he is forgetting things) (321- 326).
Recommendation #10: Eye assessment
In patients treated with glucocorticoids or antimalarials, a baseline eye examination is recommended according to standard guidelines.
An eye examination during follow up is recommended:
• in selected patients taking glucocorticoids (high risk of glaucoma or cataracts),
• in patients on antimalarial drugs and
o low risk -> no further testing is required until 5 years after baseline; after the first 5 years of treatment, eye assessment is recommended yearly,
o high risk -> eye assessment is recommended yearly.
The incidence of retinopathy among SLE patients treated with antimalarial drugs is relatively low. In a recent study of 400 patients with rheumatoid arthritis (RA) and SLE treated for more than 6 years, the prevalence of retinopathy was 0.5% (328- 331).
Risk factors for the development of retinopathy are age (above 60 years), presence of macular degeneration, retinal dystrophy, obesity, liver disease, renal insufficiency, duration of therapy > 5 years, daily dose of hydroxychloroquine above 6.5 mg/kg, or chloroquine above 3 mg/kg. Few cases are observed among patients treated for less than 5 years and with daily dose of hydroxychloroquine of less than 6.5 mg/kg, or of chloroquine of less than 3 mg/kg (332- 334).
In 2002, recommendations on screening for chloroquine and hydroxychloroquine retinopathy were published which included the need for a baseline eye assessment before starting therapy. Thereafter, in low risk patients, no further testing is required for the next 5 years; after the first 5 years of treatment, eye assessment is recommended yearly. In high-risk patients, an eye assessment is recommended yearly (332- 335). According with published Recommendations, the baseline examination should include a complete ophthalmologic examination including best-correcter viasual acuity and dilated examination of the cornea and retina, a baseline field testing (Amsler grid or Humphrey 10-2 field).
Glucocorticoids-induced cataracts occur among patients treated with glucocorticoids; some studies suggest that 10-15 mg of prednisone daily for a year may be sufficient to cause cataracts. Data available on SLE patients confirm a significant association between cumulative prednisone dose (36.5 g) and development of cataracts with a RR: 1.9 (CI 1.4-2.5) (336- 337).
The EULAR evidence-based recommendations on the management of systemic glucocorticoid therapy in rheumatic diseases indicate cataract or glaucoma as comorbidities based on a level of evidence of IV (expert committee reports/opinions and/or clinical opinion of respected authorities) and a strength of recommendation of 92 (CI: 87-96) (118, 339).
Systemic glucocorticoids increase the risk of glaucoma by raising the intraocular pressure. Authors have reported the development of glaucoma in 19% of subjects with rheumatic diseases treated with > 7.5 mg/day of prednisone vs 3% of those treated with 7.5 mg/day. In the general population, 18-36% of those exposed to glucocorticoids had an increase in intraocular pressure. Risk factors for glaucoma development are family history of glaucoma, age (over 40 years), ethnic background (African-Americans are six to eight times more likely to develop glaucoma than are Caucasians), diabetes mellitus, hypertension, hypothyroidism, great myopia, pre-existing glaucoma, chronic uveitis, and iritis.
In addition eye assessment is required if there are symptoms suggesting eye involvement by lupus.
Eye assessment could be performed by an optician in countries were opticians are trained in recognizing complex eye disease.
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