CYC is the treatment of choice for severe neuropsychiatric NP involvement in SLE and is also reserved for the treatment of any severe organ-threatening disease manifestations [ 25 ]. Sirolimus, an inhibitor of the mammalian target of rapamycin mTOR , a serine-threonine kinase involved in T-cell proliferation, has recently emerged as a promising therapy in patients with clinically active SLE, particularly in those presenting musculoskeletal involvement [ 26 , 27 ].
IS drugs are also burdened by their association to side effects, such as severe infections, malignancies, teratogenity and infertility, potentially leading to additional organ damage and mortality. In recent years, a better understanding of SLE etiopathogenesis has led to the introduction of a number of biologic agents that specifically target disease pathways underlying the development and progression of lupus.
Some of these therapies, such as rituximab RTX and belimumab, are available in clinical practice, while others are being tested in ongoing clinical trials. Despite the lack of trial evidence, the efficacy of RTX in the treatment of refractory LN and in severe non-renal SLE manifestations has been shown in many observational studies [ 30 , 31 ].
Belimumab takes into account the pathophysiological significance of BAFF in autoimmune diseases. Its central role in autoimmunity is well established. Elevated levels of BAFF correlate with autoimmune disease in humans, mice and dogs [ 35 ]. A significant improvement of disease activity was achieved in the treatment arm compared with the placebo arm, and the trials thus met the primary endpoint.
Belimumab also resulted in a reduction of flares and steroid use, as well as an improvement in HRQoL and levels of fatigue [ 36 ]. This led in to the approval of the use of belimumab to treat SLE [ 37 , 38 ]. The efficacy and safety of belimumab administered subcutaneously were confirmed in another trial [ 39 ].
Based on the results of randomized clinical trials RCTs and real-life experience, belimumab is particularly effective in patients with active disease, serological activity and high PDN intake, with earlier use achieving a better clinical response [ 40 , 41 ].
In this context, a pooled post hoc analysis of the BLISS studies, with the aim to determine the effect of belimumab on patients with renal involvement, showed a greater improvement in renal disease in patients with serologic activity at baseline or receiving MMF, as has been confirmed in the real-life setting [ 42 , 43 ]. The finding of renal tubular epithelial cell-derived BAFF expression that mediated kidney damage and correlated with LN activity in the mouse and humans further supports the efficacy of belimumab in LN [ 44 ].
Indeed, as the authors of these studies stated, the selection of patients suitable for belimumab therapy based on serological activity could be troublesome as these patients may be at high risk of developing LN. Regarding conventional IS, combination therapies designed to target two or more complementary pathways could be an effective strategy for the treatment of lupus, even with biologics.
There is a strong rationale for this combined therapeutic approach. First, treatment with belimumab leads to the mobilization of memory B cells from tissues despite an overall decrease in peripheral B-cell levels, making tissue-resident B cells more susceptible to depletion by RTX. Second, blocking the effects of high BAFF levels in the serum might have favorable effects on B-cell reconstitution after depletion.
The synergistic or additive effects of such a combination have been demonstrated in preclinical studies in lupus-prone mice and in case reports [ 50 , 51 ]. Intravenous immunoglobulins IVIGs , which are purified from the plasma of healthy human donors, represent a valid therapeutic option for those patients with SLE with concomitant infections or for those who have contraindications or are refractory to conventional therapies.
In some cases, for example in cases of neurological or hematological involvement, IVIGs can be given as first-line therapy [ 52 ]. Despite being used since the s, IVIG therapy is still considered to be experimental without any clear indications.
A systematic review of observational studies highlighted the association of IVIG administration with significant improvement in disease activity scores and complement levels [ 53 ]. Therapeutic plasma exchange TPE is a blood purification technique used for the removal of pathological substances, such as monoclonal para-proteins and auto-Ab, as well as for the replacement of deficient plasma components. This therapeutic option is helpful when treatment with other agents fails or in presence of leucopenia and psychosis, but it has been profiled as an effective therapeutic option especially for patients with SLE with thrombotic thrombocytopenic purpura and catastrophic antiphospholipid syndrome [ 54 ].
In contrast with plasma exchange, immunoadsorption IAS , a more specific form of extracorporeal treatment, leads to a specific and nearly complete clearance of circulating IgG and ICs, while neither removing other plasma proteins or necessitating substitution with fresh frozen plasma or albumin.
In the past two decades IAS has emerged as a valuable option in the treatment of SLE, showing beneficial effects in patients with refractory disease or contraindications to standard immunosuppression, or during pregnancy [ 55 ].
Available studies have shown that short-term use of IAS reduces proteinuria and improves global disease activity, enabling GC dosages to be lowered [ 56 ]. In addition, prolonged IAS treatment has been shown to provide additional therapeutic benefits and to maintain an acceptable safety profile [ 55 ]. In the context of a holistic approach to lupus patients, there is an emerging body of evidence supporting the importance of correct lifestyle habits in the management of the disease, with particular attention to smoking cessation, physical activity and vitamin D supplementation [ 57 ].
According to the results of a recent meta-analysis, tobacco smoking, in addition to its well-known adverse effects, significantly reduces the effectiveness of HCQ and belimumab in cutaneous lesions and systemic manifestations. Cigarette smoking also appears to be a risk factor of SLE, negatively influencing the course of the disease [ 58 ]. Physical activity is emerging as pivotal in the reduction of cardiovascular risk and has also been shown to have positive effects on fatigue and mental health [ 59 ].
Vitamin D deficiency is common in patients with SLE, and a large body of evidence supports the negative impact of vitamin D deficiency on disease activity, fatigue and risk of thrombosis [ 57 ]. There are currently registered studies on SLE that are recruiting participants; these include studies on targeting B cells, plasma cells, co-stimulation, cytokines and their receptors, chemokines and their receptors and complement factors or interferons.
Obinutuzumab OBZ , a new-generation, glycoengineered type II anti-CD20 monoclonal Ab, induced superior B-cell cytotoxicity in patients with lupus in vitro, as demonstrated in whole blood assays [ 64 ], so further investigations on OBZ are ongoing. B-cell receptor BCR signaling is believed to play a pivotal role in the development and maintenance of autoimmunity. The decrease of Lyn tyrosine kinase and spleen tyrosine kinase Syk in response to BCR stimulation in patients with active SLE further supports the hypothesis that B cells are under constant activation through BCR signaling [ 65 ].
Since it was thought that CD22 engagement would impose negative regulation of BCR signaling, epratuzumab, an anti-CD22 monoclonal antibody, was tested in SLE, but with negative results [ 66 ]. Long-lived plasma cells producing auto-Ab appear to be an interesting target of lupus research.
As a consequence, a proteasome blocker, such as bortezomib, was used in a RCT, showing a good response [ 70 ]. However, there was a substantial rate of side effects [ 71 ]. Further clinical studies with other less toxic proteasome blockers are ongoing e. The safety profile was consistent with that reported in previous studies, and serious infections were observed in a dose-dependent manner [ 73 ]. Baricitinib is currently under investigation in a phase III trial.
The accumulation of evidence showing that IFN-activated genes play a significant role in the pathophysiology of SLE has led to the testing of different therapeutic approaches. Mitochondrial dysfunction recently emerged as a pivotal factor in the immune dysregulation and development of organ damage in SLE.
Idebenone, a coenzyme Q10 synthetic quinone analog, has been found to ameliorate disease activity and the severity of organ damage, including glomerular inflammation and fibrosis in a murin model of SLE, suggesting a potential therapeutic role in humans [ 78 ].
Oxidative stress is increased in SLE, contributing to immune system dysregulation and comorbidities [ 79 ]. Reversal of glutathione depletion by application of its amino acid precursor, N -acetylcysteine, safely improves disease activity in lupus patients by blocking mTOR in T lymphocytes, but further research is needed [ 80 ]. The loss of tolerance to self-antigens in SLE patients is associated with dysregulation of T-cell signaling, including the depletion of total levels of lymphocyte-specific protein kinase from sphingolipid-cholesterol-enriched membrane microdomains lipid rafts.
Atorvastatin has emerged as an effective therapy by targeting lipid raft-associated signaling abnormalities in autoreactive T cells [ 81 ]. Chimeric antigen receptor CAR T-cell therapy is an emergent approach in cancer immunotherapy and has shown efficacy in the treatment of B-cell malignancies through specific targeting of the B-cell surface antigen CD19 [ 82 , 83 ]. CARs are fusion proteins consisting of a single-chain fragment from a monoclonal Ab specific for the target antigen of interest and T-cell receptor intracellular signaling domains.
The treatment involves the isolation of a patient's autologous T cells, the genetic modification of these cells to express the antigen-specific CARs, cell expansion, and finally re-infusion of the modified cells into the patient [ 84 ]. Interleukin-2 IL-2 is involved in the expansion of immune tolerance by increasing regulatory T cells and suppressing effector T cells, including T helper 17 and T follicular helper cells.
When used at high doses, IL-2 demonstrated efficacy in certain types of solid tumors, also contributing to the establishment of the concept of its use in cancer immunotherapy, while at low doses it was found to increase anti-infectious immune response [ 86 ]. A double-blind and placebo-controlled trial recently displayed the efficacy of low-dose IL-2 in the treatment of SLE, with a lower rate of infections, although not statistically significant, recorded in the IL-2 group compared to placebo [ 87 ].
The most relevant SLE therapies according to their different mechanisms of action are shown in Fig. Main mechanisms of systemic lupus erythematosus lupus pathogenesis with related targeted therapies. Advances in the treatment of SLE have been made in recent decades, leading to an increase in patient survival worldwide.
Nevertheless, lupus currently is associated with a 2. Patients with SLE have a higher risk of cardiovascular disease CVD compared to the general population due to a complex interplay between traditional cardiovascular risk factors and SLE-specific conditions.
CVD still represents the major cause of premature mortality in patients with SLE [ 5 ], but its effect remains underestimated among clinicians and treatment requires an interdisciplinary approach. Patients with SLE also present a higher risk of infections, both as a consequence of their disease and of the therapies used in their clinical management.
The risk of lupus flare deriving from vaccination has never been never confirmed, but vaccination rates remain low [ 88 ]. Further efforts are therefore needed to reinforce the immunization coverage of patients with SLE. Lupus is known to cause a significant and sometimes severe neurological involvement, resulting in a number of diverse symptoms, referred to as NP-SLE.
This heterogeneity in neurological and psychiatric symptoms occurring in SLE poses both diagnostic and therapeutic challenges with a substantial risk of either over- or under-treatment. It is well known that lupus patients with CNS involvement often present a more significant impairment of HRQoL when compared with those who have other serious manifestations of the disease e.
No decisive treatments for NP-SLE are as yet available, and there is only weak evidence on which to base recommendations [ 32 ]. It is the result of a multifactorial etiology and leads to a strong reduction of the HRQoL [ 89 ] and work productivity [ 90 ].
The relationship between several psychosocial factors, mainly pain, mood and sleep disorders, and comorbidities, such as fibromyalgia, anemia and vitamin D deficiency, is well established and can explain why fatigue is detectable even in patients in remission or with low disease activity. However, the relationship between fatigue and disease activity is still a matter of debate. We recently reported a significant correlation between the titer of the anti-NR2 Ab, severity of fatigue, disease activity and anti-double stranded DNA Ab—independently from the presence of NP lupus manifestations.
In addition, treatment with belimumab for at least 6 months affected both the severity of fatigue and the levels of anti-NR2 Ab [ 91 ]. Physical activity and vitamin D supplementation [ 92 ] have also been shown to improve fatigue levels in patients with SLE. Despite these findings, relieving fatigue remains an unmet need for lupus patients and a challenge for their physicians, and new effective approaches are needed.
Over the last 30 years, advances in treatment have improved the life expectancy and HRQoL of SLE patients, but much more remains to be done. The heterogeneity of SLE, the different forms of progression and the concomitant medications have limited the approval of new therapies, despite major efforts of the scientific community and associated industries.
A more precise characterization of disease phenotypes based on molecular and clinical features is expected to lead to the development of more effective and less toxic regimens in the management of SLE. Tsokos GC. Systemic lupus erythematosus. N Engl J Med. Epigenetic aspects of systemic lupus erythematosus. Rheumatol Ther. Role of human leukocyte antigens HLA in autoimmune diseases.
Ann Rheum Dis. PubMed Google Scholar. Surviving the butterfly and the wolf: mortality trends in systemic lupus erythematosus. Autoimmun Rev. The majority of Swedish systemic lupus erythematosus patients are still affected by irreversible organ impairment: factors related to damage accrual in two regional cohorts.
Remission in systemic lupus erythematosus: durable remission is rare. Remission and low disease activity in systemic lupus erythematosus: an achievable goal even with fewer steroids? Real-life data from a monocentric cohort. Lupus Sci Med. Association of the lupus low disease activity state LLDAS with health-related quality of life in a multinational prospective study. Arthritis Res Ther. Morand EF, Mosca M.
Treat to target, remission and low disease activity in SLE. Best Pract Res Clin Rheumatol. The role of antimalarial agents in the treatment of SLE and lupus nephritis. Nat Rev Nephrol. Controlled trial with chloroquine diphosphate in systemic lupus erythematosus. Ponticelli C, Moroni G. Hydroxychloroquine in systemic lupus erythematosus SLE. Expert Opin Drug Saf. Damage in systemic lupus erythematosus and its association with corticosteroids.
Arthritis Rheum. Accrual of organ damage over time in patients with systemic lupus erythematosus. J Rheumatol. Prednisone, lupus activity, and permanent organ damage. Apostolopoulos D, Morand EF. It hasn't gone away: the problem of glucocorticoid use in lupus remains. Rheumatology Oxford. CAS Google Scholar. Methylprednisolone and cyclophosphamide, alone or in combination, in patients with lupus nephritis.
A randomized, controlled trial. Ann Intern Med. Immunosuppressive therapy in lupus nephritis: The Euro-Lupus Nephritis Trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide. Update on lupus nephritis: Core Curriculum Am J Kidney Dis. Multitarget therapy for induction treatment of lupus nephritis: a randomized trial.
A randomized, controlled double-blind study comparing the efficacy and safety of dose-ranging voclosporin with placebo in achieving remission in patients with active lupus nephritis. Kidney Int. Systemic lupus erythematosus: a therapeutic challenge for the XXI century. Clin Rheumatol. Clinical experience of sirolimus regarding efficacy and safety in systemic lupus erythematosus.
Front Pharmacol. Efficacy and safety of rituximab in patients with active proliferative lupus nephritis: the Lupus Nephritis Assessment with Rituximab study. Short-term efficacy and safety of rituximab therapy in refractory systemic lupus erythematosus: results from the British Isles Lupus Assessment Group Biologics Register. Mice transgenic for BAFF develop lymphocytic disorders along with autoimmune manifestations.
J Exp Med. BAFF, a novel ligand of the tumor necrosis factor family, stimulates B cell growth. BAFF and innate immunity: new therapeutic targets for systemic lupus erythematosus. Immunol Cell Biol. Improvements in health-related quality of life with belimumab, a B-lymphocyte stimulator-specific inhibitor, in patients with autoantibody-positive systemic lupus erythematosus from the randomised controlled BLISS trials.
Efficacy and safety of belimumab in patients with active systemic lupus erythematosus: a randomised, placebo-controlled, phase 3 trial. A phase III, randomized, placebo-controlled study of belimumab, a monoclonal antibody that inhibits B lymphocyte stimulator, in patients with systemic lupus erythematosus.
Efficacy and safety of subcutaneous belimumab in systemic lupus erythematosus: a fifty-two-week randomized, double-blind placebo-controlled study. Arthritis Rheumatol. Clinical predictors of response and discontinuation of belimumab in patients with systemic lupus erythematosus in real life setting. Results of a large, multicentric, nationwide study. J Autoimmun. First real-world insights into belimumab use and outcomes in routine clinical care of systemic lupus erythematosus in Germany: Results from the OBSErve Germany study.
Effect of belimumab treatment on renal outcomes: results from the phase 3 belimumab clinical trials in patients with SLE. Belimumab and low-doses of mycophenolate mofetil as induction therapy of class IV lupus nephritis: case series and literature review.
BMC Nephrol. Renal tubular epithelial cell-derived BAFF expression mediates kidney damage and correlates with activity of proliferative lupus nephritis in mouse and men. Poor responders to steroids and patients with particular manifestations of SLE benefit with a combination of steroids and other immunosuppressive drugs. Prednisolone may be indicated in women with a desire to conceive, during pregnancy or lactation.
Hydroxychloroquine HCQ has been noticed to have immunomodulatory properties that are used to treat arthritis and cutaneous flares, protect against ultraviolet UV rays, improve sicca symptoms, treat milder disease, and improve the cardiovascular profile of a patient by reducing cholesterol, the risk of diabetes, and carotid plaque development; it also has antithrombotic properties.
Furthermore, it can also be indicated during pregnancy or lactation. There are case reports of cardiotoxicity, which is a serious but very rare adverse event. There is also a rare risk of retinal toxicity. Immunosuppressive agents are frequently indicated to reduce the risk of long-term damage accrual, control active disease, and as steroid-sparing agents [ 3 ]. Azathioprine is the most commonly used cytotoxic agent in lupus, and it is usually initiated for the control moderate activity of lupus, the prevention of flares, maintenance therapy after remission, and steroid dose reduction.
Also, it is the preferred drug for fertility preservation and during pregnancy. Cyclophosphamide is primarily used in the treatment of GI, muscle, and pulmonary manifestations. While mycophenolate mofetil MMF was shown to be a good induction agent as effective as cyclophosphamide , when combined with steroids, it can reduce moderate and severe lupus disease activity, reduce renal and non-renal flares; it also aids in steroid dose reduction and is well tolerated.
It is more effective than azathioprine and less toxic than cyclophosphamide. Cyclophosphamide and MMF are both contraindicated during pregnancy and lactation. In refractory cases, other drugs can be used. Cyclosporin and tacrolimus inhibit calcineurin which in turn inhibits the production of cytokines and lymphocyte proliferation—especially T-helper cells [ 25 ].
Cyclosporin is useful as a steroid-sparing agent in patients with normal renal function. There is some evidence to suggest that tacrolimus can be used in case of induction of LN. Direct B cell elimination or inhibition of B cell survival agents leading to B cell depletion has been the most widely used and logical biological option in SLE [ 3 ].
Atacicept is a fully human recombinant fusion protein that blocks the activity of both A proliferation-inducing ligand APRIL and B-lymphocyte stimulator BLyS — B cell activating factors, which according to some studies have the property of preventing flares and reducing the activity of the disease. However, a more extensive investigation is necessary to demonstrate its efficacy and safety profile. It was even more beneficial in moderate—severe seropositive lupus mostly musculoskeletal and cutaneous disease.
In the United Kingdom, the only biological agent approved for SLE is belimumab, and further studies are required. Rituximab acts against CD20 on the surface of pre-B cells maturing to memory B cells. This binding leads to apoptosis of B cells and does not prevent stem cell regeneration. Its properties have been amply demonstrated in the reduction of disease activity in lupus of moderate to severe severity in refractory non-renal cases, in addition to its role in the reduction of steroid doses.
In many open-label studies, rituximab has shown efficacy in arthritis, fatigue, renal disease, and serositis and skin involvement in SLE. It is safe and tolerated well either as an alone agent or in combination with cyclophosphamide.
Another monoclonal antibody against the CD20 antigen, ofatumumab unlike rituximab, it is fully humanized , has been demonstrated in case studies to be effective in treating SLE. It promises to be a useful therapy in SLE patients who cannot tolerate rituximab. Rontalizumab was evaluated in phase II randomized trial and was not effective enough in its primary outcome. Treat to Target for SLE is an international initiative established to give recommendations to treat each patient based on a unique target.
This novel approach contributes to the improvement of the clinical management of the disease, for which the measurement of results and therapeutic options must be made available. In SLE, the studies on remission have used various terms to define remission, including the absence of serological and clinical activity, clinically quiescent but serologically active, and whether the state was achieved on or off treatment.
Definitions of Remission in SLE DORIS , a large international task force, has published eight key statements and three principles for defining remission due to a lack of consensus in its definition. The aim is to harmonize efforts in research. According to this consensus, remission is defined as the clinical absence of the disease, given by absence of disease activity in a clinical and organ-based laboratory test, ignoring serum complement and anti-dsDNA antibodies.
Absence or presence of treatment needs to be mentioned while defining remission. With the recent advancements in understanding the pathogenetic mechanisms and immunopathogenesis of SLE, the focus has shifted toward the control of disease activity, flares control, management of comorbidities e. The introduction of corticosteroids and immunosuppressive agents has improved the prognosis of those affected.
However, SLE poses a significant impact for the mortality and morbidity of the patients. We still need new research and randomized controlled trials aiming at devising targeted treatment protocols for this multisystemic disease. Cureus is not responsible for the scientific accuracy or reliability of data or conclusions published herein. All content published within Cureus is intended only for educational, research and reference purposes. Additionally, articles published within Cureus should not be deemed a suitable substitute for the advice of a qualified health care professional.
Do not disregard or avoid professional medical advice due to content published within Cureus. The authors have declared that no competing interests exist. National Center for Biotechnology Information , U. Journal List Cureus v. Published online Sep Author information Article notes Copyright and License information Disclaimer. Corresponding author. Neha Waqas moc. Received Aug 29; Accepted Sep This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
See Cureus. This article has been cited by other articles in PMC. Abstract Systemic lupus erythematosus SLE is a chronic autoimmune disease with varied natural history and multisystemic involvement. Keywords: auto-antibodies, autoimmune disease, multisystemic, biological agents, immunosuppressives, neuropsychiatric systemic lupus erythematosus, remission, inflammatory, therapeutic, immunology.
Introduction and background Systemic lupus erythematosus SLE is a chronic autoimmune inflammatory disease with a wide spectrum of clinical and serological manifestations caused by autoantibody production, complement activation, and immune complex deposition.
Epidemiology SLE is a rare disease with an incidence of approximately 1—10 per , person-years and a prevalence of 20— per , person-years. Pathogenesis The pathogenesis of SLE is characterized by the formation of autoantibodies and a breakdown in the immune milieu of the body leading to an unregulated inflammatory response. Classification criteria In , the Systemic Lupus International Collaborating Clinics SLICC group introduced a set of validated criteria with higher sensitivity than the revised American College of Rheumatology criteria which had been in vogue since Review Pathology and management The clinician should have a proper understanding of pathogenesis, immunology, laboratory evaluation, and updated treatment options when diagnosing and treating SLE [ 17 ].
Treatment The treatment for this malady depends on the organs and systems involved as well as the severity. Remission Treat to Target for SLE is an international initiative established to give recommendations to treat each patient based on a unique target.
Conclusions With the recent advancements in understanding the pathogenetic mechanisms and immunopathogenesis of SLE, the focus has shifted toward the control of disease activity, flares control, management of comorbidities e. Footnotes The authors have declared that no competing interests exist. References 1. Genetic susceptibility to SLE: new insights from fine mapping and genome-wide association studies. Nat Rev Genet. The genetic basis of systemic lupus erythematosus-knowledge of today and thoughts for tomorrow.
Prokunina L, Alarcon-Riquelme M. Hum Mol Genet. The revised criteria for the classification of systemic lupus erythematosus. Arthritis Rheum. Efficacy of mycophenolate mofetil in patients with diffuse proliferative lupus nephritis. N Engl J Med. Understanding the role of environmental factors in the development of systemic lupus erythematosus. Best Pract Res Clin Rheumatol. Drivers of the immunopathogenesis in systemic lupus erythematosus.
Collaboration, genetic associations, and lupus erythematosus. Crow MK. Clinical features of systemic lupus erythematosus. Petri M. Curr Opin Rheumatol. Serum interferon levels in patients with systemic lupus erythematosus. Pathogenesis and potential therapeutic targets in systemic lupus erythematosus: from bench to bedside. Auto Immun Highlights. Immunosuppressive therapy in lupus nephritis: the Euro-Lupus Nephritis Trial, a randomized trial of low-dose versus high-dose intravenous cyclophosphamide.
Systemic lupus erythematosus and lupus nephritis. Koutsokeras T, Healy T. Nat Rev Drug Discov. Global natural regulatory T cell depletion in active systemic lupus erythematosus. J Immunol. Treatment for lupus nephritis.
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