Abstract
Synopsis
Cyclosporin is a lipophilic cyclic polypeptide which produces calcium-dependent, specific, reversible inhibition of transcription of interleukin-2 and several other cytokines, most notably in T helper lymphocytes. This reduces the production of a range of cytokines, inhibiting the activation and/or maturation of various cell types, including those involved in cell-mediated immunity. Thus, cyclosporin has immunosuppressive properties, and has a proven place as first line therapy in the prophylaxis and treatment of transplant rejection.
Cyclosporin has also been evaluated in a large range of disorders where immunoregulatory dysfunction is a suspected or proven aetiological factor, and this is the focus of the present review. In patients with severe disease refractory to standard treatment, oral cyclosporin is an effective therapy in acute ocular Behçet’s syndrome, endogenous uveitis, psoriasis, atopic dermatitis, rheumatoid arthritis, active Crohn’s disease and nephrotic syndrome. Concomitant low dose corticosteroid therapy may improve response rates in some disorders. The drug can be considered as a first line therapy in patients with moderate or severe aplastic anaemia who are ineligible for bone marrow transplantation, with the additional benefit of reducing platelet alloantibody titres. It may also be of considerable therapeutic benefit in patients with primary biliary cirrhosis, particularly those with less advanced disease. Limited evidence suggests cyclosporin is effective in patients with intractable pyoderma gangrenosum, polymyositis/dermatomyositis or severe, corticosteroid-de-pendent asthma. Indeed, the steroid-sparing effect of cyclosporin is a significant advantage in a number of indications. Furthermore, the drug has shown some efficacy in a wide range of other, generally uncommon disorders in which controlled clinical trials are lacking and/or are unlikely to be performed. Cyclosporin does not appear to be effective in patients with allergic contact dermatitis, multiple sclerosis or amyotrophic lateral sclerosis. It is only temporarily effective in patients with type I (insulin-dependent) diabetes mellitus and should not be used in this indication.
To avoid relapse after control of active disease, patients should receive cyclosporin maintenance therapy at the lowest effective dosage. However, maintenance therapy appears to be of no benefit in patients with Crohn’s disease and cyclosporin should be discontinued in these patients once active disease is controlled.
Hypertrichosis, gingival hyperplasia, and neurological and gastrointestinal effects are the most common adverse events in cyclosporin recipients, but are Usually mild to moderate and resolve on dosage reduction. Changes in laboratory variables indicating renal dysfunction are relatively common, although serious irreversible damage is rare. However, renal function monitoring is recommended, and cyclosporin dosage should be reduced by 25 to 50% if serum creatinine increases > 30% above baseline, with treatment discontinuation if creatinine does not return to within 30% of baseline levels within 1 month. A large number of interactions between cyclosporin and other agents have been identified.
In the treatment of immunoregulatory disorders, cyclosporin has generally been reserved for use in patients with severe refractory disease and patients who have become steroid-dependent or, in patients with aplastic anaemia, those with moderate or severe disease who are ineligible for bone marrow transplantation. Despite these limitations, cyclosporin appears to be a very effective agent in a number of recalcitrant disorders where achieving adequate disease control is a major advance. This merits a trial of cyclosporin in these patients despite the careful monitoring required.
Pharmacodynamic Properties
Cyclosporin is a lipophilic cyclic polypeptide of 11 amino acids with unique immunosuppressive properties. It acts specifically and reversibly on lymphocytes (in particular T helper cells), producing selective suppression of cell-mediated immunity. This suppression is contingent on the mode of activation and is calcium-dependent.
Cyclosporin forms a complex with cyclophilin in the cytoplasm, which then binds to calcineurin, a calcium- and calmodulin-dependent phosphatase, in a calcium-dependent manner. Inhibition of calcineurin activity is implicated in the activation and/or translocation of a nuclear factor which binds to the interleukin-2 enhancer allowing the interleukin-2 gene to be transcribed. The transcription of several other cytokines, including interferon-7, and several other interleukins, is also inhibited by cyclosporin.
Interleukin-2 production by T helper cells is a pivotal step in the evolution of the immune response. It is required for the activation and clonal expansion of T helper and T cytotoxic cells, and the maturation of various other cell types. Thus, inhibition of interleukin-2 expression by cyclosporin reduces the production of a wide range of other cytokines, producing indirect effects on other cells involved in the immune response.
Prophylaxis or treatment with cyclosporin has shown efficacy in induced animal models of human disorders with a presumed or proven immune component including asthma, haemolytic anaemia, nephritis, Graves’ and Hashimotos’ thyroiditis, Guillain-Barré syndrome, inflammatory bowel disease, multiple sclerosis, myasthenia gravis, pancreatitis, psoriasis, rheumatoid arthritis and uveitis. However, disease recurred after treatment discontinuation in some models, while others were not considered to correlate well with human disease. Cyclosporin was effective as both prophylaxis and treatment in a genetic animal model of systemic lupus erythematosus/arteritis/arthritis, as treatment in genetic models of alopecia areata and keratoconjunctivitis sicca/Sjögren’s syndrome, and as prophylaxis in models of vitiligo and type I diabetes mellitus. It was ineffective as treatment in genetic models of type I diabetes mellitus, and as treatment or prophylaxis in Hashimotos’ thyroiditis.
Cyclosporin has an indirect vasoconstrictor effect which has been associated with hypertension and renal dysfunction. In the kidney, cyclosporin produces structural and functional changes affecting predominantly the proximal tubule and the afferent arteriole. These effects result in impaired renal function which is usually reversible and, less often, structural renal damage. The mechanism of cyclosporin nephrotoxicity remains to be established and more than one effect may be involved. Increased thromboxane A2 levels causing renal vasoconstriction and proliferation of vascular smooth muscle cells into the intima, reduced release of vasodilatory kinins, and altered calcium responses producing exaggerated arteriolar smooth muscle and mesangial cell responses with a resultant decrease in glomerular filtration rate, have been proposed.
Cyclosporin has also been shown to modify the multi-drug resistance phenotype of cancer cells, enhancing intracellular antineoplastic drug accumulation. This effect does not appear to be associated with the immunosuppressive activity of cyclosporin.
Pharmacokinetic Properties
The pharmacokinetic properties of cyclosporin show wide interpatient variation. The drug is poorly absorbed after oral administration, primarily in the small intestine, and has a bioavailability of about 30% (range 5 to 70%) in healthy volunteers. Maximum blood concentrations of cyclosporin are usually observed 1 to 8 hours after oral administration, and a second peak may be noted in some patients. This second peak may be due to enhanced absorption following a meal, as bile increases cyclosporin absorption, or may represent excretion of cyclosporin as a sulphate conjugate in the bile, which is then degraded to the parent compound and reabsorbed.
Cyclosporin is rapidly (within about 10 minutes) distributed between blood cells (60 to 70%) and plasma. Most of the cyclosporin in blood cells is taken up by erythrocytes (41 to 58%), whereas most of the drug in plasma is bound to lipoproteins (≈ 34%). Cyclosporin has a large apparent volume of distribution of 4 to 8 L/kg. Tissue drug concentrations appear to correlate with tissue levels of cyclophilin and lipids, being highest in leucocyte-rich organs, and in fat and fatty organs. Cyclosporin does not cross the blood-brain barrier or enter the cerebrospinal fluid to any significant extent, but does cross the blood-retinal barrier in patients with severe ocular disease where this barrier is compromised. The drug crosses the placenta and is found in amniotic fluid and fetal blood; it is also present in breast milk.
Cyclosporin is metabolised by cytochrome P-450IIIA enzymes, predominantly in the liver, but some presystemic metabolism by P-450IIIA enzymes in the gastrointestinal mucosa may also occur. There is no single major metabolic pathway and more than 30 metabolites have been observed. The most active metabolites show only 10 to 20% of the immunosuppressive activity of cyclosporin and do not appear to act synergistically with the parent compound. Cyclosporin exhibits linear elimination with a clearance rate of 0.38 to 3 L/h/kg. The elimination half-life has been measured as about 19 hours but this is probably an underestimate. Following oral administration, 90% of a dose is excreted in the bile (< 1% unchanged) and 6% in the urine (< 0.1% unchanged).
Cyclosporin metabolism is age-dependent with an increased clearance and decreased elimination half-life in children, who may have increased dosage requirements. Clearance is decreased in patients with hepatic impairment or reduced low density lipoprotein levels in serum, and possibly also in the elderly. Reduced distribution to blood cells in patients with aplastic anaemia, reduced absorption in patients with inflammatory bowel disorders, and decreased tissue distribution in patients with hyperlipoproteinaemia, might also be expected.
It is recommended that cyclosporin concentrations be measured in whole blood using an assay method specific for the parent compound. Routine monitoring of metabolites is not considered necessary.
Therapeutic Efficacy
The therapeutic efficacy of cyclosporin has been evaluated in an extensive range of disorders where immunoregulatory dysfunction is a presumed or proven aetiological factor.
Ophthalmological disorders: Oral cyclosporin is effective therapy in patients with severe endogenous posterior uveitis, with improvements in visual parameters being maintained during long term therapy. The beneficial effects were particularly marked in patients with acute ocular manifestations of Behçet#x2019;s syndrome, where cyclosporin appeared at least as effective as standard therapies in comparative trials. Small trials indicate cyclosporin 2% eye drops are also useful in patients with severe refractory vernal conjunctivitis.
Dermatological disorders: Cyclosporin has a dose-proportional effect in patients with severe psoriasis vulgaris, with relatively rapid therapeutic benefit when dosage is titrated to effect. In a comparison with etretinate, cyclosporin provided more rapid lesion clearance and, unlike etretinate, therapeutic effect was maintained during tapering of the dosage. Relapse occurs when cyclosporin is reduced below a minimum effective dosage. Concurrent topical steroid therapy appears to be of additional benefit in cyclosporin recipients. Intralesional cyclosporin administration is effective but unlikely to be of practical use, whereas evaluation of topical cyclosporin therapy for psoriasis has been limited by the lack of a vehicle providing sufficient percutaneous absorption of the drug. Cyclosporin has also shown efficacy in patients with palmoplantar pustulosis (pustular psoriasis).
Oral and topical cyclosporin have demonstrated short term efficacy compared with placebo in patients with atopic dermatitis, and had a steroid-sparing effect. Although evidence is limited, cyclosporin shows significant therapeutic activity in patients with pyoderma gangrenosum, producing complete ulcer healing in patients who failed conventional therapy. Similarly, oral cyclosporin therapy seems to be effective in patients with refractory bullous skin disorders and has a steroid-sparing effect. Low dose topical or oral cyclosporin has shown efficacy in severe refractory lichen planus, particularly in patients with oral disease manifestations. However, topical cyclosporin appears largely ineffective in patients with alopecia areata, and although oral cyclosporin has shown some efficacy, it seems unlikely to be used in this essentially cosmetic disorder. Allergic contact dermatitis does not appear to be responsive to cyclosporin.
Haematological disorders: Cyclosporin was at least as effective as standard therapy with anti-lymphocyte (including antithymocyte) globulin plus steroid therapy in patients with aplastic anaemia. Furthermore, the addition of cyclosporin to standard treatment regimens significantly improved response rates and cyclosporin appears effective in patients refractory to antilymphocyte globulin therapy. It also reduces alloantibody titres in patients with aplastic anaemia refractory to platelet transfusion. Thus, cyclosporin alone or in combination with antilymphocyte or antithymocyte globulin should be considered a first-line therapy in patients with moderate to severe aplastic anaemia not eligible for bone marrow transplantation.
Gastroenterological disorders: Oral cyclosporin was an effective therapy in a subgroup of patients with active Crohn’s disease resistant to or intolerant of conventional therapy. However, relapse is common during maintenance therapy or after cyclosporin discontinuation. A large double-blind 18-month study found cyclosporin was less effective than placebo for maintaining remission in patients with low disease activity initially, being associated with a significant worsening of symptoms. Thus, while cyclosporin is a useful alternative, with a potential steroid-sparing effect in patients with severe active disease, current evidence indicates it should not be used as long term maintenance therapy. Preliminary data suggest that intravenous cyclosporin can abrogate the need for colectomy in patients with severe active refractory ulcerative colitis.
Liver disorders: Cyclosporin reduces both disease-related deaths and the need for transplantation compared with placebo, in patients with primary biliary cirrhosis. Beneficial effects on metabolic bone status have also been noted with cyclosporin therapy in these patients. Limited data also indicate some efficacy in patients with autoimmune chronic active hepatitis, but viral chronic active disease has generally not responded to cyclosporin therapy.
Neurological disorders: Cyclosporin therapy has produced improvements in patients with myasthenia gravis similar to those observed with azathioprine or prednisone. However, these results require confirmation in the long term. Neurological deterioration following surgery after subarachnoid haemorrhage was reduced in cyclosporin recipients compared with controls in a small study. Large studies in patients with amyotrophic lateral sclerosis or multiple sclerosis found cyclosporin therapy was associated with no significant additional benefit compared with placebo.
Nephrotic syndrome: Cyclosporin has significant activity in both adults and children with nephrotic syndrome including minimal change disease, focal segmental glomerular sclerosis and membranous nephropathy. It has a significant steroid-sparing effect in steroid-dependent patients and shows efficacy in patients with steroid-resistant disease. While maintenance therapy is required by most patients, response is maintained in some patients following cyclosporin discontinuation. Additional benefit is obtained with the use of cyclosporin in combination with low dose steroids. However, results of a 2-year study indicate chlorambucil therapy should be tried before cyclosporin therapy is considered. Furthermore, cyclosporin should not be used in patients with established renal insufficiency, particularly those with focal segmental glomerular sclerosis.
Rheumatoid arthritis: Oral cyclosporin therapy is more effective than placebo, and at least as effective as azathioprine, chloroquine, methotrexate or penicillamine in patients with severe refractory rheumatoid arthritis of long duration. Significant improvements in functional assessments of disease occur but significant changes in laboratory measures of disease are infrequent. While associated with a slower rate of disease improvement than higher dosages, it is recommended that low doses of cyclosporin be used initially, with slow titration to effect, as patients with rheumatoid arthritis seem particularly susceptible to the renal adverse effects of this drug. Limited data indicate cyclosporin is also beneficial in patients with recent disease onset and in severe refractory juvenile rheumatoid arthritis.
Type I (insulin-dependent) diabetes mellitus: While cyclosporin therapy produces an initial reduction or abolition of insulin requirements in patients with recently diagnosed type I diabetes mellitus, all patients eventually relapse, and cyclosporin is not currently recommended in this indication.
Other immunoregulatory disorders: Cyclosporin has shown therapeutic activity in a large number of other disorders where immunoregulatory dysfunction is a known or suspected component. The most notable of these are severe corticosteroid-dependent asthma and polymyositis/dermatomyositis, and to a lesser extent, steroid-dependent systemic lupus erythematosus and Sjögren’s syndrome.
Tolerability
Cyclosporin therapy is associated with a considerable incidence of adverse events, the most common of which are hypertrichosis, gingival hyperplasia, and neurological and gastrointestinal effects. These are usually of mild to moderate severity and resolve on dosage reduction.
Changes in laboratory variables indicating dose-proportional renal dysfunction are relatively common during cyclosporin therapy but serious irreversible damage is rare, with values returning to near baseline on dosage reduction or discontinuation. Nevertheless, regular monitoring of renal function is considered mandatory in cyclosporin recipients. Older patients, and patients with existing renal impairment or hypertension also appear to be more at risk of cyclosporin nephrotoxicity. The most common findings on renal biopsy in cyclosporin recipients have been striped interstitial fibrosis, tubular atrophy and arteriolar changes including hyalinosis. In non-transplant indications, avoidance of increases in serum creatinine > 30% above baseline by dose titration and a cyclosporin dosage < 5 mg/kg/day reduces, but does not completely abolish, the risk of serious structural kidney damage.
While hypertension may occur, it is usually controlled with antihypertensive therapy. The incidence of malignancy and infection is possibly less in patients receiving cyclosporin therapy compared with other potent immunosuppressive agents. An increased risk of skin cancer is suspected in patients with psoriasis receiving cyclosporin after other therapies, particularly photochemotherapy (PUVA). Cyclosporin has also been associated with hypomagnesaemia, hepatic dysfunction, and increased fasting triglyceride levels. The frequency of patient withdrawal because of adverse events was usually similar between treatment arms in comparisons of cyclosporin with other active therapies.
Acute oral cyclosporin overdosage is associated with few clinical symptoms but acute parenteral overdosage may be life-threatening, particularly in premature neonates. Gastric lavage and administration of activated charcoal is recommended for oral overdosage. Cyclosporin is not removed by haemodialysis, nor is total blood transfusion likely to be effective. The effects of chronic cyclosporin overdosage have not been reported.
Drug Interactions
Three clinically important types of drug interaction with cyclosporin have been identified. Concomitant administration of agents slowing the rate of cyclosporin metabolism (e.g. macrolide antibiotics, azole antifungals, high dose corticosteroids, some calcium channel antagonists, H2histamine receptor antagonists, oral anticoagulants and sex hormones) may result in increased trough cyclosporin concentrations. Concomitant administration of agents increasing the rate of cyclosporin metabolism (e.g. anticonvulsants, antitubercular antibiotics) may result in decreased trough cyclosporin concentrations. The third possible outcome is increased or additive nephrotoxicity and appears to involve agents with known nephrotoxic potential such as aminoglycoside antibiotics, diuretics and rarely, nonsteroidal anti-inflammatory drugs.
Various other interactions including increased gingival hyperplasia with nifedipine, increased myopathy with lovastatin, seizures with aluminium-containing medications or ketoconazole plus methylprednisolone, and a protective renal effect with enalapril, prazosin and calcium channel antagonists have been reported.
Dosage and Administration
Patients with endogenous uveitis (including Behçet’s syndrome) should receive oral cyclosporin 5 mg/kg/day to achieve remission of acute disease, increased to 7 mg/kg for a short time and/or in conjunction with low dose corticosteroid therapy if required. In psoriasis, a dosage of 2.5 mg/kg/day should be used initially, gradually increased after 1 month in 0.5 to 1 mg/kg/day increments if response is inadequate, to a maximum of 5 mg/kg/day. Cyclosporin should be discontinued in patients not responding sufficiently after 6 weeks at 5 mg/kg/day. Maintenance therapy in patients with endogenous uveitis or psoriasis should utilise the lowest effective dosage of cyclosporin and should not exceed 5 mg/kg/day.
Cyclosporin 3 to 7 mg/kg/day may be used in patients with moderate to severe aplastic anaemia, titrated according to response and renal function. Treatment should be continued for at least 3 months and until peripheral blood cell counts have stabilised for at least 1 month, then slowly tapered. Concomitant antilymphocyte globulin and/or steroid therapy may be used.
Cyclosporin 5 mg/kg/day (adults) or 6 mg/kg/day (children) is recommended for the induction of remission in nephrotic syndrome, although this should be reduced to 2.5 mg/kg/day in patients with impairment of renal function other than proteinuria. Dosage should be titrated according to response and renal function, but should not exceed the recommended initial starting dosage. Low dose corticosteroid therapy may be added in patients with an insufficient response to cyclosporin monotherapy but cyclosporin should be discontinued in patients not responding after 3 months of therapy. The lowest effective cyclosporin dosage should be used for maintenance of remission.
In patients with rheumatoid arthritis an initial dosage of 3 to 3.5 mg/kg/day is recommended in recognition that some of these patients may be very sensitive to the renal effects of cyclosporin. In other disorders an initial dosage of 5 mg/kg/day or less should probably be used, with gradual dose-escalation, if required, to a maximum of 5 mg/kg/day. Downward titration to the lowest effective dosage should be undertaken once remission is obtained. Low dose corticosteroid therapy may be added, where appropriate, if response to cyclosporin monotherapy is insufficient.
Blood pressure and renal function should be monitored every 2 weeks in the first 3 months of therapy, then every 2 months, although monthly assessment is recommended in patients receiving cyclosporin > 2.5 mg/kg/day long term or those particularly at risk of nephrotoxicity. Cyclosporin dosage should be reduced by 25 to 50% if serum creatinine increases by more than 30% above baseline, with therapy discontinued if creatinine level does not return to within 30% of baseline within 1 month. Therapy should also be discontinued in patients developing hypertension uncontrolled by appropriate therapy. Cyclosporin is contraindicated in patients with uncontrolled infection, any malignancy other than skin cancer, or a glomerular filtration rate < 2.4 L/h/1.73m2.
Cyclosporin should be administered twice daily, orally if at all possible. The recommended intravenous dose is approximately one-third of the oral dose and may be considered for initial treatment of patients with inflammatory bowel disease with an accelerated gut transit time.
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Various sections of the manuscript reviewed by: R. Assan, Service de Diabétologie, Hôpital Bichat, Paris, France; C.G. Barnes, Department of Rheumatology, Royal London Hospital, Whitechapel, London, England; D. BenEzra, Department of Ophthalmology, Hadassah University Hospital, Jerusalem, Israel; G.P. Bray, Institute of Liver Studies, King’s College Hospital of Medicine and Dentistry, Denmark Hill, London, England; J. Brynskov, Department of Medical Gastroenterology F, Glostrup University Hospital, Glostrup, Copenhagen, Denmark; N. Frickhofen, Abteilung Innere Medizin III, Universität Ulm, Ulm, Federal Republic of Germany; D.W. Holt, Analytical Unit, St George’s Hospital Medical School, London, England; T.E. Mandel, Walter and Eliza Hall Institute of Medical Research, Royal Melbourne Hospital, Melbourne, Victoria, Australia; M.J. Mihatsch, Department of Pathology, University of Basel, Basel, Switzerland; U. Mrowietz, Klinik für Dermatologie, Venerologie und Allergologie, Universität zu Kiel, Kiel, Federal Republic of Germany; P. Niaudet, Département de Pédiatrie Médicale, Hôpital Necker-Enfants Malades, Paris, France; C. Ponticelli, Divisione di Nefrologia e Dialisi, Ospedale Maggiore di Milano, Milano, Italy; J.A. Vale, West Midlands Poisons Unit, Dudley Road Hospital, Birmingham, England; M. Yamamoto, Division of Tumor Immunology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, Massachusetts, USA; G.C. Yee, Department of Pharmacy Practice, College of Pharmacy, University of Florida, Gainesville, Florida, USA; D.E. Yocum, Department of Medicine, Section of Rheumatology/Allergy and Immunology, University of Arizona Health Sciences Center, Tucson, Arizona, USA.
An erratum for this article can be found at http://dx.doi.org/10.1007/BF03259110
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Faulds, D., Goa, K.L. & Benfield, P. Cyclosporin. Drugs 45, 953–1040 (1993). https://doi.org/10.2165/00003495-199345060-00007
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DOI: https://doi.org/10.2165/00003495-199345060-00007