Transfusion and Apheresis Science xxx (2014) xxx–xxx
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Review
Miscellaneous indications for extracorporeal photochemotherapy (ECP) Heidrun Andreu-Ullrich ⇑ Head of Dijon Blood Transfusion Centre and Blood Collection Department, Etablissement Français du Sang Bourgogne Franche-Comté, site de Dijon, 2, rue Angélique Ducoudray, BP 47834, 21078 Dijon Cedex, France
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Article history: Available online xxxx Keywords: Photopheresis Autoimmune disease Extracorporeal photochemotherapy ECP
a b s t r a c t Extracorporeal photochemotherapy (ECP) has been applied to many T-cell mediated diseases where immunosuppressive drugs are insufficient or not tolerated. As ECP is mainly used in rare indications after failure of other therapies, controlled studies are hardly possible. In addition, the importance of the extracorporeal circuit imposes ethical doubts in organising sham ECP procedure, which explains the rarity of controlled double-blind studies. However, encouraging and even successful results have been reported in newly developed diabetes mellitus, erosive lichen planus, Crohn’s disease, systemic sclerosis, nephrogenic fibrosing dermopathy, atopic dermatitis, rheumatoid arthritis, systemic lupus erythematodes, psoriasis arthritis, cutaneous mucinosis, scleromyxoedema, pemphigus vulgaris, multiple sclerosis, eosinophilic fasciitis and in the prevention of percutaneous transluminal coronary angioplasty (PTCA) restenosis. This article discusses the various levels of evidence in the above cited indications. Ó 2014 Elsevier Ltd. All rights reserved.
Contents 1. 2.
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Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Literature analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Type II hypersensitivity autoimmune diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.1. Pemphigus vulgaris and pemphigus foliaceus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Type IV hypersensitivity autoimmune diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.1. Crohn’s disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.2. Type 1 diabetes in children . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.3. Multiple sclerosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.4. Psoriasis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.5. Rheumatoid arthritis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.6. Lupus erythematosus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Other T-dependent autoimmune diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.1. Systemic sclerosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.2. Ankylosing spondylitis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.3. Erosive cutaneous lichen planus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Other highly probable autoimmune diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
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Please cite this article in press as: Andreu-Ullrich H. Miscellaneous indications for extracorporeal photochemotherapy (ECP). Transf Apheres Sci (2014), http://dx.doi.org/10.1016/j.transci.2014.04.007
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4. 5.
3.1. Eosinophilic fasciitis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Nephrogenic systemic fibrosis (NSF) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Atopic dermatitis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Scleromyxoedema . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Febrile ulceronecrotic Mucha–Habermann disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6. Epidermolysis bullosa acquisita . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Other . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction As shown by many authors, ECP is a highly efficient therapy through its immunomodulatory effects. Initial side effects due to oral application of 8-Methoxypsoralen (8-MOP) and utilisation of cell separators with a large extracorporeal volume have been almost fully abrogated: the use of 8-MOP either IV or in the UV exposure phase as well as the development of new devices adapted to ECP with reduced extra-corporeal volumes [1,2] has shown to be at least as efficient as the initially proposed technique [3] and lead to an important reduction of ECP side effects, thus making the use of this technique possible in children. In particular heparin side effects can today be completely avoided by using citric acid, citrate and dextrose A (ACD-A) anticoagulation. Moreover, during the last thirty years it has been shown that ECP is not associated with an increased incidence of infections and malignancy and thus may be a good candidate to replace immunosuppressive drugs in many diseases, when patients become resistant to and/or dependent on them. Its mechanism of action on normalising immunity in many different diseases is described in another article of this journal. ECP can safely be combined to other therapies. ECP has been applied to many T-cell mediated diseases where immunosuppressive drugs are insufficient or not tolerated. As ECPC is mainly used in rare indications after failure of other therapies, controlled studies are hardly possible. In addition, the importance of the extracorporeal circuit imposes ethical doubts in organising sham ECP procedure, which explains the rarity of controlled double-blind studies. Encouraging and even successful results have been reported in various diseases as described below. However, it should be stressed that most guidelines and recommendations are not dealing at all with these rare diseases as most studies consist in isolated or small cohort clinical cases in heterogeneous conditions: The American Society for Apheresis has given recommendations on the use of apheresis [4]. But for ECP, they only take into account the Therakos system, thus excluding many European studies. As these recommendations propose manly established therapies mainly based on randomised controlled studies, most rescue therapies are not mentioned. In a report of a workshop of the British Photodermatology Group McKenna et al. evaluated study results of ECP on various diseases [5]. They limited the evaluation on the Therakos system and concentrated on controlled studies and reports on successful rescue treatments.
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The recommendations of the German society of transfusion medicine give comparisons between ASFA guidelines and an own rating summarised in comparable categories from strength I (apheresis as acknowledged first line therapy alone or in combination) to IV (apheresis treatment not recommended), studies under way and no rating. Most diseases and clinical conditions described in this article are either classified as expecting study results or category III accepting ECP in single cases after failure of other therapies [6]. 2. Literature analysis 2.1. Type II hypersensitivity autoimmune diseases 2.1.1. Pemphigus vulgaris and pemphigus foliaceus In pemphigus, antibodies against desmosomes (intercellular adhesion molecules) cause blisters on skin and mucous membranes that lead to painful erosions followed by dehydration and weight loss, bleedings, secondary infections and death in up to 10% of patients. In pemphigus vulgaris anti-desmoglein 3 antibodies lead to intra-epidermal, supra-basilar acantholysis. In pemphigus foliaceus antidesmoglein 1 antibodies are associated with sub-corneal acantholysis. IgG with or without C3 deposition in the intercellular spaces is observed. Glucocorticoids, immunosuppressing drugs, iv IgG and monoclonal antibodies are used to induce remission. In severe refractory cases plasma exchange, immuno-adsorption and ECP have been successfully combined to these treatments to reduce drug side effects [7–10]. 2.2. Type IV hypersensitivity autoimmune diseases 2.2.1. Crohn’s disease Crohn’s disease is a chronic relapsing inflammatory disease that is usually treated with steroids, mesalamine, antibiotics and other immunosuppressants like antitumour necrosis factor (TNF) agents. Steroid dependency is reported in up to 36% of patients after the first steroid cycle and even higher later in the course of the disease. Two controlled studies in steroid dependent Crohn’s disease in adults have shown advantages of ECP. The pilot study was a prospective open monocentric trial [11]. Twenty-four patients were included; the first phase consisted of steroid tapering to a maintenance dose of at least 10 mg/day prednisolone, ECP was started in parallel to steroid withdrawal in 10 patients, four of whom achieved remission while four others showed partial response. In phase 3 this remission remained stable in three out of four
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patients and 8-MOP photo-adducts could be observed in three colonic biopsy monocyte samples. These encouraging results led to an open-label, multicentre prospective trial [12]: 31 patients with steroid-dependent Crohn’s disease in remission (Crohn’s disease activity index (CDAI) score of 91 and inflammatory bowel disease questionnaire (IBDQ) of 172.5, were treated with ECP for 24 weeks, 65% of them were refractory to anti-TNF agents or immunosuppressants. After 24 weeks 7 of 31 patients discontinued steroids at a CDAI below 150. The steroid dose of the other patients at the same time point was 10 mg/day with a CDAI of 110. Three patients remained in steroid-free remission following maintenance treatment. Ten patients receiving ECP at week 48 had a steroid dose of 3.5 mg/day with a CDAI of 40 and an IBDQ of 188. In conclusion, ECP permitted discontinuation or important reduction of steroids in this population of steroid-dependent Crohn’s disease. In children the use of steroids and immunosuppressive drugs are feared not only for their immediate side effects but also for their long term complications. Cushingoid problems, opportunistic infections and secondary tumours (lymphoma) may be the consequence. Cheerva et al. [13] reported a case of Crohn’s disease in an 11-year-old boy refractory to steroids, antibiotics and liquid nutrition, poor response to infliximab and azathioprine for one year. He was then treated by 31 ECP procedures for 27 weeks. Prednisone could be weaned during ECP while infliximab and azathioprine remained stable. Overall he improved significantly and remained stable for 16 months after the end of ECP treatment. 2.2.2. Type 1 diabetes in children Type 1 diabetes develops over years with increasing autoimmunity and defective beta-cell function involving CD4- and CD8-lymphocytes, APCs and B-lymphocytes. Preservation of beta-cell function is the main goal of early onset immune-modulatory therapy such as anti-CD3 antibodies or ECP. Forty-nine children with recent onset type 1 diabetes (day 5–6 after diagnosis) were included into a randomised, double blind, placebo controlled study [14]. Forty patients completed the treatment period with ECP or sham treatment. The treatment group patients needed lower insulin doses to reach satisfactory HbA1c values and secreted significantly more C-peptide in their urine at the end of the study. The positive effect of ECP was shown as a weak but significant effect for the 3 years follow up period. Other studies on the same patients highlighted ECP effects on the preservation of regulatory T-cell function [15] and an increase of activated CD4- and CD8-lymphocytes in the control group [16]. The patients received oral 8-MOP which has been shown to be inferior to direct injection of the exact drug dose into the cell concentrate at a dose of 50 ng/ml cell solution, the treatment arm patients received 5 cycles of 2 ECP on consecutive days in a regular way for three months. The oral 8-MOP administration and less performing cell separators as compared to more recent devices accounted for some study withdrawals and could easily be avoided
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in a new study. The authors proposed more intensive ECP schemes to increase ECP effects. Three months seem too short to prevent islet cell loss on the long term. Although recent experimental ECP underlines its benefit in early therapy of diabetes type 1 [17] no new clinical studies have been undertaken on this promising subject. 2.2.3. Multiple sclerosis Multiple sclerosis is an autoimmune T-cell disorder with widely varying evolution. That is one of the reasons why the advantage of any treatment is very difficult to determine. Here, randomisation is ethically problematic and technically difficult to carry out. ECP effects can only be observed after weeks and if used at the right intensity. Animal models show advantages and some authors propose ECP in individual cases [18]. A safety and tolerability study proposes ECP in refractory relapsing remitting multiple sclerosis. Reduction in relapse rate and stabilisation of the Expanded Disability Status Scale (EDSS) was shown in the five treated patients as compared to the pre-treatment phase [19,20]. Several other studies have been conducted in severe and in long-lasting progressive multiple sclerosis without proving a benefit of ECP [21,22]. 2.2.4. Psoriasis Refractory psoriasis and psoriatic arthritis can be treated by ECP. In several non-controlled studies good results were observed [23–26]. 2.2.5. Rheumatoid arthritis Rheumatoid arthritis was one of the very first autoimmune diseases where ECP was used. Positive results were reported in patients with the severe refractory form [27–31]. Today it is only used if all drug therapies fail or are contraindicated. However, no controlled studies have been carried out. [32]. 2.2.6. Lupus erythematosus Lupus erythematosus is treated with steroids, immunosuppression, anti-malarials and iv IgG. Several cases of improvement of severe lupus erythematosus refractory to drugs or with contraindications to drugs have been reported [33,34]. 2.3. Other T-dependent autoimmune diseases 2.3.1. Systemic sclerosis Diffuse systemic sclerosis (SSc) was one of the first indications where ECP was used [35]. This chronic autoimmune disorder is characterised by collagen deposition and fibrosis of skin and internal organs (heart, lungs, kidney). In the limited cutaneous form, fibrosis is localised and slowly progressing. The diffuse cutaneous form is marked by rapid progression with the lowest survival rates among connective tissue diseases. Methotrexate, cyclophosphamide and other immunosuppressants are usually insufficient to stop disease progression and cause multiple side effects. The above mentioned multicentre randomized, prospective, single blind parallel group study showed significant benefit of ECP after six months, but not at ten months follow up. Many patients in the d-penicillamin
Please cite this article in press as: Andreu-Ullrich H. Miscellaneous indications for extracorporeal photochemotherapy (ECP). Transf Apheres Sci (2014), http://dx.doi.org/10.1016/j.transci.2014.04.007
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treatment arm had dropped out due to side effects, thus reducing the power of the study. Another double blind placebo-controlled study on 64 diffuse SSc patients showed improved skin severity scores and joint involvement after ECP treatment [36]. In another study by Papp et al. [37], 16 patients with diffuse SSc and a disease duration between 0.5 and 7 years received a one year treatment with only amlodipine and pentoxyphyllin and then 6 ECP treatment cycles on two following days every six weeks each. Dermal thickness reduced, mobility of joints improved and internal organ involvement did not deteriorate during the observation period. A positive correlation between reduction of Il-17 levels and skin thickness could be observed. The authors conclude that ECP reduces autoimmunity and decelerates the fibrotic process. The absence of side effects advocates this treatment. Other authors stress the importance of monitoring deterioration of internal organ function during ECP because restoration of immune function seems to act primarily on skin and joints and only to a lesser extent on internal organ involvement. Since the advent of ACE inhibitors in the treatment of renal failure survival has improved. [38,39] Some older studies did not show superiority of ECP over control therapy [40,41]. 2.3.2. Ankylosing spondylitis Ankylosing spondylitis is an autoimmune disorder characterised by pain and increasing stiffness that reduces quality of life over years. It is classically treated by nonsteroidal anti-inflammatory drugs (NSAIDs), sulfasalazine and steroids and anti-TNF-agents. Surgery may be an option. A case report describes successful treatment of ankylosing spondylitis in a patient treated by ECP for his concurrent cutaneous T-cell lymphoma (CTCL). The patient improved after 3 months, pain stopped completely and he did not need any more nonsteroidal anti-inflammatory as well as disease modifying anti-rheumatic drugs were withdrawn after 12 months of therapy [42]. 2.3.3. Erosive cutaneous lichen planus Erosive cutaneous lichen planus causes painful erythematous ulcerative lesions of mucosal membranes and skin erosions. If topical immune suppressive therapies are insufficient systemic steroids are applied with the accompanying side effects. Several case reports have published successful treatment of severe refractory erosive cutaneous lichen planus by ECP [43–47]. One study describes a three-year follow up of 12 patients with oral lichen planus treated by photopheresis in decreasing frequency. All improved, nine showed complete and the three others partial remission. When ECP frequency was reduced too much, relapse occurred. Partial or complete remission was re-established by increasing frequency of ECP [48]. 3. Other highly probable autoimmune diseases 3.1. Eosinophilic fasciitis Eosinophilic fasciitis is a rare connective tissue disorder with thickening of the skin and fasciae by a chronic
inflammatory infiltrate with eosinophils. It is classified and treated like systemic sclerosis. Several reports of improvement by ECP have been described [49,50].
3.2. Nephrogenic systemic fibrosis (NSF) Nephrogenic systemic fibrosis (NSF) is a T-cell disorder where gadolinium based dyes are observed in renal disease patients with slowly progressing fibrosis of the skin and less often internal organs [51]. Gadolinium-containing contrast agents in combination with systemic inflammation or tissue and vascular injury seem to be initiating factors. NSF (also called nephrogenic fibrosing dermopathy) is treated by steroids and immunomodulating drugs similarly to systemic sclerosis therapy, but also by ECP and plasma exchange. Successful ECP treatment has been reported in several case reports [52–57]. However, Kreuter reported insufficient response of two NSF patients treated by ECP without other therapies who received ECP after one year of disease progression [51].
3.3. Atopic dermatitis Like many chronic cutaneous autoimmune diseases atopic dermatitis is treated initially by topical steroids, immune modulators and phototherapy, second line therapy consists of oral application of the same drugs. ECP has been applied in patients with severe atopic dermatitis refractory to these treatments. A small but significant effect was observed in a study with 10 patients treated by ECP as systemic monotherapy for 20 weeks [58]. Other studies showed significant improvement of disease score and quality of life [59–63]. A retrospective follow-up of 6 severe refractory atopic dermatitis patients on ECP for more than one year showed clinical improvement without side effects [64].
3.4. Scleromyxoedema Scleromyxoedema is a rare connective tissue disease of unknown aetiology showing papular eruptions, dermal fibroblast proliferation and monoclonal proteinemia. Single cases of successful treatment with ECP have been described and a combination with steroids, immunosuppression and bath PUVA was recommended [65–68]. A case of successful treatment of a patient with scleredema, a similar disease, has also been reported with a follow up of 41 months [69].
3.5. Febrile ulceronecrotic Mucha–Habermann disease Febrile ulceronecrotic Mucha–Habermann disease is very rare and a subtype of pityriasis lichenoides with ulcero-necrotic skin lesions, high fever and severe constitutional symptoms. It is treated by steroids and methotrexate. Marenco [70] describes the successful treatment of a patient with refractory Mucha–Habermann disease with iv IgG and ECP maintenance therapy.
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3.6. Epidermolysis bullosa acquisita Epidermolysis bullosa acquisita is a disease caused by tissue-bound and circulating antibodies against collagen type VII that hinder attachment of epidermis to dermis resulting in skin fragility, blisters, erosions, scars and milia. First line therapy with colchicine is often insufficient and success has been achieved by combination with other therapies like dapsone, plasma exchange, infliximab and iv IgG. Several publications report improvement by long term ECP [31,9,71–73].
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operating cell separators and oral application of 8-MOP. The important blood volume changes during the procedure and drug intolerance are great obstacles for the use in children with a small blood volume, while continuously operating cell separators and the addition of 8-MOP directly into the cell concentrate are much better adapted to treatment of children. A new randomized trial using modern ECP technology and sufficient treatment intensity should be done in this frequent disease, to identify if ECP helps in preventing its full development, thus improving many patients’ quality of life and reducing long-term therapy costs.
4. Other Prevention of restenosis after percutaneous transluminal coronary angioplasty. Bisaccia et al. published a study on 41 control and 37 ECP patients with single-vessel coronary artery disease with or without stent deployment. Clinical restenosis occurred significantly less frequently in the ECP group. Further studies should better determine the use of ECP in this group of patients [74]. 5. Conclusion Several controlled studies and many case reports prove the important role of ECP in normalising immune mediated problems in various disorders without side effects. The only drawbacks are its availability and costs. In diseases where controlled studies can be carried out they should prove the advantages of ECP in achieving improvement and reducing other drug therapies and their important long-term side effects. This is typically the case for ECP use in graft versus host GvH disease after allogeneic hematopoietic stem cell transplantation. ECP has been used as a rescue therapy in patients with rare chronic diseases related to various immunological disorders that were not controlled with conventional therapy. Drug reduction is particularly important in young patients and ECP should be used early in children for its steroid sparing capacity. In many diseases, ECP will probably continue to be used in the future despite incomplete evidence of efficacy, as the very limited number of patients does not enable large clinical studies. Case reports should be encouraged however, including those without success, in order to better document the role of ECP in the management of these patients. Conversely, some indications may be more completely investigated in frequent diseases. Prevention of restenosis after percutaneous transluminal coronary angioplasty by ECP as well as Crohn disease are two fields where prospective randomised studies should be undertaken. Another example which is far from being a rare disease is diabetes type 1 in its recent onset phase : although several trials have been reported, there is at present no universally recognised management to try to control the auto-immune process. ECP is a good candidate, due to the fact that it does not show the usual side effects of immunosuppressive drugs. The first trial to try to delay or event prevent the onset of diabetes type 1 has been done with the first generation of ECP technology, using discontinuously
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Review
Miscellaneous indications for extracorporeal photochemotherapy (ECP) Heidrun Andreu-Ullrich ⇑ Head of Dijon Blood Transfusion Centre and Blood Collection Department, Etablissement Français du Sang Bourgogne Franche-Comté, site de Dijon, 2, rue Angélique Ducoudray, BP 47834, 21078 Dijon Cedex, France
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Article history: Available online xxxx Keywords: Photopheresis Autoimmune disease Extracorporeal photochemotherapy ECP
a b s t r a c t Extracorporeal photochemotherapy (ECP) has been applied to many T-cell mediated diseases where immunosuppressive drugs are insufficient or not tolerated. As ECP is mainly used in rare indications after failure of other therapies, controlled studies are hardly possible. In addition, the importance of the extracorporeal circuit imposes ethical doubts in organising sham ECP procedure, which explains the rarity of controlled double-blind studies. However, encouraging and even successful results have been reported in newly developed diabetes mellitus, erosive lichen planus, Crohn’s disease, systemic sclerosis, nephrogenic fibrosing dermopathy, atopic dermatitis, rheumatoid arthritis, systemic lupus erythematodes, psoriasis arthritis, cutaneous mucinosis, scleromyxoedema, pemphigus vulgaris, multiple sclerosis, eosinophilic fasciitis and in the prevention of percutaneous transluminal coronary angioplasty (PTCA) restenosis. This article discusses the various levels of evidence in the above cited indications. Ó 2014 Elsevier Ltd. All rights reserved.
Contents 1. 2.
3.
Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Literature analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1. Type II hypersensitivity autoimmune diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.1.1. Pemphigus vulgaris and pemphigus foliaceus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2. Type IV hypersensitivity autoimmune diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.1. Crohn’s disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.2. Type 1 diabetes in children . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.3. Multiple sclerosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.4. Psoriasis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.5. Rheumatoid arthritis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.2.6. Lupus erythematosus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3. Other T-dependent autoimmune diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.1. Systemic sclerosis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.2. Ankylosing spondylitis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 2.3.3. Erosive cutaneous lichen planus . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Other highly probable autoimmune diseases . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
00 00 00 00 00 00 00 00 00 00 00 00 00 00 00 00
⇑ Tel.: +33 380706043; fax: +33 380706005. E-mail address: [email protected] http://dx.doi.org/10.1016/j.transci.2014.04.007 1473-0502/Ó 2014 Elsevier Ltd. All rights reserved.
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4. 5.
3.1. Eosinophilic fasciitis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.2. Nephrogenic systemic fibrosis (NSF) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.3. Atopic dermatitis. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.4. Scleromyxoedema . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.5. Febrile ulceronecrotic Mucha–Habermann disease . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 3.6. Epidermolysis bullosa acquisita . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Other . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction As shown by many authors, ECP is a highly efficient therapy through its immunomodulatory effects. Initial side effects due to oral application of 8-Methoxypsoralen (8-MOP) and utilisation of cell separators with a large extracorporeal volume have been almost fully abrogated: the use of 8-MOP either IV or in the UV exposure phase as well as the development of new devices adapted to ECP with reduced extra-corporeal volumes [1,2] has shown to be at least as efficient as the initially proposed technique [3] and lead to an important reduction of ECP side effects, thus making the use of this technique possible in children. In particular heparin side effects can today be completely avoided by using citric acid, citrate and dextrose A (ACD-A) anticoagulation. Moreover, during the last thirty years it has been shown that ECP is not associated with an increased incidence of infections and malignancy and thus may be a good candidate to replace immunosuppressive drugs in many diseases, when patients become resistant to and/or dependent on them. Its mechanism of action on normalising immunity in many different diseases is described in another article of this journal. ECP can safely be combined to other therapies. ECP has been applied to many T-cell mediated diseases where immunosuppressive drugs are insufficient or not tolerated. As ECPC is mainly used in rare indications after failure of other therapies, controlled studies are hardly possible. In addition, the importance of the extracorporeal circuit imposes ethical doubts in organising sham ECP procedure, which explains the rarity of controlled double-blind studies. Encouraging and even successful results have been reported in various diseases as described below. However, it should be stressed that most guidelines and recommendations are not dealing at all with these rare diseases as most studies consist in isolated or small cohort clinical cases in heterogeneous conditions: The American Society for Apheresis has given recommendations on the use of apheresis [4]. But for ECP, they only take into account the Therakos system, thus excluding many European studies. As these recommendations propose manly established therapies mainly based on randomised controlled studies, most rescue therapies are not mentioned. In a report of a workshop of the British Photodermatology Group McKenna et al. evaluated study results of ECP on various diseases [5]. They limited the evaluation on the Therakos system and concentrated on controlled studies and reports on successful rescue treatments.
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The recommendations of the German society of transfusion medicine give comparisons between ASFA guidelines and an own rating summarised in comparable categories from strength I (apheresis as acknowledged first line therapy alone or in combination) to IV (apheresis treatment not recommended), studies under way and no rating. Most diseases and clinical conditions described in this article are either classified as expecting study results or category III accepting ECP in single cases after failure of other therapies [6]. 2. Literature analysis 2.1. Type II hypersensitivity autoimmune diseases 2.1.1. Pemphigus vulgaris and pemphigus foliaceus In pemphigus, antibodies against desmosomes (intercellular adhesion molecules) cause blisters on skin and mucous membranes that lead to painful erosions followed by dehydration and weight loss, bleedings, secondary infections and death in up to 10% of patients. In pemphigus vulgaris anti-desmoglein 3 antibodies lead to intra-epidermal, supra-basilar acantholysis. In pemphigus foliaceus antidesmoglein 1 antibodies are associated with sub-corneal acantholysis. IgG with or without C3 deposition in the intercellular spaces is observed. Glucocorticoids, immunosuppressing drugs, iv IgG and monoclonal antibodies are used to induce remission. In severe refractory cases plasma exchange, immuno-adsorption and ECP have been successfully combined to these treatments to reduce drug side effects [7–10]. 2.2. Type IV hypersensitivity autoimmune diseases 2.2.1. Crohn’s disease Crohn’s disease is a chronic relapsing inflammatory disease that is usually treated with steroids, mesalamine, antibiotics and other immunosuppressants like antitumour necrosis factor (TNF) agents. Steroid dependency is reported in up to 36% of patients after the first steroid cycle and even higher later in the course of the disease. Two controlled studies in steroid dependent Crohn’s disease in adults have shown advantages of ECP. The pilot study was a prospective open monocentric trial [11]. Twenty-four patients were included; the first phase consisted of steroid tapering to a maintenance dose of at least 10 mg/day prednisolone, ECP was started in parallel to steroid withdrawal in 10 patients, four of whom achieved remission while four others showed partial response. In phase 3 this remission remained stable in three out of four
Please cite this article in press as: Andreu-Ullrich H. Miscellaneous indications for extracorporeal photochemotherapy (ECP). Transf Apheres Sci (2014), http://dx.doi.org/10.1016/j.transci.2014.04.007
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patients and 8-MOP photo-adducts could be observed in three colonic biopsy monocyte samples. These encouraging results led to an open-label, multicentre prospective trial [12]: 31 patients with steroid-dependent Crohn’s disease in remission (Crohn’s disease activity index (CDAI) score of 91 and inflammatory bowel disease questionnaire (IBDQ) of 172.5, were treated with ECP for 24 weeks, 65% of them were refractory to anti-TNF agents or immunosuppressants. After 24 weeks 7 of 31 patients discontinued steroids at a CDAI below 150. The steroid dose of the other patients at the same time point was 10 mg/day with a CDAI of 110. Three patients remained in steroid-free remission following maintenance treatment. Ten patients receiving ECP at week 48 had a steroid dose of 3.5 mg/day with a CDAI of 40 and an IBDQ of 188. In conclusion, ECP permitted discontinuation or important reduction of steroids in this population of steroid-dependent Crohn’s disease. In children the use of steroids and immunosuppressive drugs are feared not only for their immediate side effects but also for their long term complications. Cushingoid problems, opportunistic infections and secondary tumours (lymphoma) may be the consequence. Cheerva et al. [13] reported a case of Crohn’s disease in an 11-year-old boy refractory to steroids, antibiotics and liquid nutrition, poor response to infliximab and azathioprine for one year. He was then treated by 31 ECP procedures for 27 weeks. Prednisone could be weaned during ECP while infliximab and azathioprine remained stable. Overall he improved significantly and remained stable for 16 months after the end of ECP treatment. 2.2.2. Type 1 diabetes in children Type 1 diabetes develops over years with increasing autoimmunity and defective beta-cell function involving CD4- and CD8-lymphocytes, APCs and B-lymphocytes. Preservation of beta-cell function is the main goal of early onset immune-modulatory therapy such as anti-CD3 antibodies or ECP. Forty-nine children with recent onset type 1 diabetes (day 5–6 after diagnosis) were included into a randomised, double blind, placebo controlled study [14]. Forty patients completed the treatment period with ECP or sham treatment. The treatment group patients needed lower insulin doses to reach satisfactory HbA1c values and secreted significantly more C-peptide in their urine at the end of the study. The positive effect of ECP was shown as a weak but significant effect for the 3 years follow up period. Other studies on the same patients highlighted ECP effects on the preservation of regulatory T-cell function [15] and an increase of activated CD4- and CD8-lymphocytes in the control group [16]. The patients received oral 8-MOP which has been shown to be inferior to direct injection of the exact drug dose into the cell concentrate at a dose of 50 ng/ml cell solution, the treatment arm patients received 5 cycles of 2 ECP on consecutive days in a regular way for three months. The oral 8-MOP administration and less performing cell separators as compared to more recent devices accounted for some study withdrawals and could easily be avoided
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in a new study. The authors proposed more intensive ECP schemes to increase ECP effects. Three months seem too short to prevent islet cell loss on the long term. Although recent experimental ECP underlines its benefit in early therapy of diabetes type 1 [17] no new clinical studies have been undertaken on this promising subject. 2.2.3. Multiple sclerosis Multiple sclerosis is an autoimmune T-cell disorder with widely varying evolution. That is one of the reasons why the advantage of any treatment is very difficult to determine. Here, randomisation is ethically problematic and technically difficult to carry out. ECP effects can only be observed after weeks and if used at the right intensity. Animal models show advantages and some authors propose ECP in individual cases [18]. A safety and tolerability study proposes ECP in refractory relapsing remitting multiple sclerosis. Reduction in relapse rate and stabilisation of the Expanded Disability Status Scale (EDSS) was shown in the five treated patients as compared to the pre-treatment phase [19,20]. Several other studies have been conducted in severe and in long-lasting progressive multiple sclerosis without proving a benefit of ECP [21,22]. 2.2.4. Psoriasis Refractory psoriasis and psoriatic arthritis can be treated by ECP. In several non-controlled studies good results were observed [23–26]. 2.2.5. Rheumatoid arthritis Rheumatoid arthritis was one of the very first autoimmune diseases where ECP was used. Positive results were reported in patients with the severe refractory form [27–31]. Today it is only used if all drug therapies fail or are contraindicated. However, no controlled studies have been carried out. [32]. 2.2.6. Lupus erythematosus Lupus erythematosus is treated with steroids, immunosuppression, anti-malarials and iv IgG. Several cases of improvement of severe lupus erythematosus refractory to drugs or with contraindications to drugs have been reported [33,34]. 2.3. Other T-dependent autoimmune diseases 2.3.1. Systemic sclerosis Diffuse systemic sclerosis (SSc) was one of the first indications where ECP was used [35]. This chronic autoimmune disorder is characterised by collagen deposition and fibrosis of skin and internal organs (heart, lungs, kidney). In the limited cutaneous form, fibrosis is localised and slowly progressing. The diffuse cutaneous form is marked by rapid progression with the lowest survival rates among connective tissue diseases. Methotrexate, cyclophosphamide and other immunosuppressants are usually insufficient to stop disease progression and cause multiple side effects. The above mentioned multicentre randomized, prospective, single blind parallel group study showed significant benefit of ECP after six months, but not at ten months follow up. Many patients in the d-penicillamin
Please cite this article in press as: Andreu-Ullrich H. Miscellaneous indications for extracorporeal photochemotherapy (ECP). Transf Apheres Sci (2014), http://dx.doi.org/10.1016/j.transci.2014.04.007
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treatment arm had dropped out due to side effects, thus reducing the power of the study. Another double blind placebo-controlled study on 64 diffuse SSc patients showed improved skin severity scores and joint involvement after ECP treatment [36]. In another study by Papp et al. [37], 16 patients with diffuse SSc and a disease duration between 0.5 and 7 years received a one year treatment with only amlodipine and pentoxyphyllin and then 6 ECP treatment cycles on two following days every six weeks each. Dermal thickness reduced, mobility of joints improved and internal organ involvement did not deteriorate during the observation period. A positive correlation between reduction of Il-17 levels and skin thickness could be observed. The authors conclude that ECP reduces autoimmunity and decelerates the fibrotic process. The absence of side effects advocates this treatment. Other authors stress the importance of monitoring deterioration of internal organ function during ECP because restoration of immune function seems to act primarily on skin and joints and only to a lesser extent on internal organ involvement. Since the advent of ACE inhibitors in the treatment of renal failure survival has improved. [38,39] Some older studies did not show superiority of ECP over control therapy [40,41]. 2.3.2. Ankylosing spondylitis Ankylosing spondylitis is an autoimmune disorder characterised by pain and increasing stiffness that reduces quality of life over years. It is classically treated by nonsteroidal anti-inflammatory drugs (NSAIDs), sulfasalazine and steroids and anti-TNF-agents. Surgery may be an option. A case report describes successful treatment of ankylosing spondylitis in a patient treated by ECP for his concurrent cutaneous T-cell lymphoma (CTCL). The patient improved after 3 months, pain stopped completely and he did not need any more nonsteroidal anti-inflammatory as well as disease modifying anti-rheumatic drugs were withdrawn after 12 months of therapy [42]. 2.3.3. Erosive cutaneous lichen planus Erosive cutaneous lichen planus causes painful erythematous ulcerative lesions of mucosal membranes and skin erosions. If topical immune suppressive therapies are insufficient systemic steroids are applied with the accompanying side effects. Several case reports have published successful treatment of severe refractory erosive cutaneous lichen planus by ECP [43–47]. One study describes a three-year follow up of 12 patients with oral lichen planus treated by photopheresis in decreasing frequency. All improved, nine showed complete and the three others partial remission. When ECP frequency was reduced too much, relapse occurred. Partial or complete remission was re-established by increasing frequency of ECP [48]. 3. Other highly probable autoimmune diseases 3.1. Eosinophilic fasciitis Eosinophilic fasciitis is a rare connective tissue disorder with thickening of the skin and fasciae by a chronic
inflammatory infiltrate with eosinophils. It is classified and treated like systemic sclerosis. Several reports of improvement by ECP have been described [49,50].
3.2. Nephrogenic systemic fibrosis (NSF) Nephrogenic systemic fibrosis (NSF) is a T-cell disorder where gadolinium based dyes are observed in renal disease patients with slowly progressing fibrosis of the skin and less often internal organs [51]. Gadolinium-containing contrast agents in combination with systemic inflammation or tissue and vascular injury seem to be initiating factors. NSF (also called nephrogenic fibrosing dermopathy) is treated by steroids and immunomodulating drugs similarly to systemic sclerosis therapy, but also by ECP and plasma exchange. Successful ECP treatment has been reported in several case reports [52–57]. However, Kreuter reported insufficient response of two NSF patients treated by ECP without other therapies who received ECP after one year of disease progression [51].
3.3. Atopic dermatitis Like many chronic cutaneous autoimmune diseases atopic dermatitis is treated initially by topical steroids, immune modulators and phototherapy, second line therapy consists of oral application of the same drugs. ECP has been applied in patients with severe atopic dermatitis refractory to these treatments. A small but significant effect was observed in a study with 10 patients treated by ECP as systemic monotherapy for 20 weeks [58]. Other studies showed significant improvement of disease score and quality of life [59–63]. A retrospective follow-up of 6 severe refractory atopic dermatitis patients on ECP for more than one year showed clinical improvement without side effects [64].
3.4. Scleromyxoedema Scleromyxoedema is a rare connective tissue disease of unknown aetiology showing papular eruptions, dermal fibroblast proliferation and monoclonal proteinemia. Single cases of successful treatment with ECP have been described and a combination with steroids, immunosuppression and bath PUVA was recommended [65–68]. A case of successful treatment of a patient with scleredema, a similar disease, has also been reported with a follow up of 41 months [69].
3.5. Febrile ulceronecrotic Mucha–Habermann disease Febrile ulceronecrotic Mucha–Habermann disease is very rare and a subtype of pityriasis lichenoides with ulcero-necrotic skin lesions, high fever and severe constitutional symptoms. It is treated by steroids and methotrexate. Marenco [70] describes the successful treatment of a patient with refractory Mucha–Habermann disease with iv IgG and ECP maintenance therapy.
Please cite this article in press as: Andreu-Ullrich H. Miscellaneous indications for extracorporeal photochemotherapy (ECP). Transf Apheres Sci (2014), http://dx.doi.org/10.1016/j.transci.2014.04.007
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3.6. Epidermolysis bullosa acquisita Epidermolysis bullosa acquisita is a disease caused by tissue-bound and circulating antibodies against collagen type VII that hinder attachment of epidermis to dermis resulting in skin fragility, blisters, erosions, scars and milia. First line therapy with colchicine is often insufficient and success has been achieved by combination with other therapies like dapsone, plasma exchange, infliximab and iv IgG. Several publications report improvement by long term ECP [31,9,71–73].
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operating cell separators and oral application of 8-MOP. The important blood volume changes during the procedure and drug intolerance are great obstacles for the use in children with a small blood volume, while continuously operating cell separators and the addition of 8-MOP directly into the cell concentrate are much better adapted to treatment of children. A new randomized trial using modern ECP technology and sufficient treatment intensity should be done in this frequent disease, to identify if ECP helps in preventing its full development, thus improving many patients’ quality of life and reducing long-term therapy costs.
4. Other Prevention of restenosis after percutaneous transluminal coronary angioplasty. Bisaccia et al. published a study on 41 control and 37 ECP patients with single-vessel coronary artery disease with or without stent deployment. Clinical restenosis occurred significantly less frequently in the ECP group. Further studies should better determine the use of ECP in this group of patients [74]. 5. Conclusion Several controlled studies and many case reports prove the important role of ECP in normalising immune mediated problems in various disorders without side effects. The only drawbacks are its availability and costs. In diseases where controlled studies can be carried out they should prove the advantages of ECP in achieving improvement and reducing other drug therapies and their important long-term side effects. This is typically the case for ECP use in graft versus host GvH disease after allogeneic hematopoietic stem cell transplantation. ECP has been used as a rescue therapy in patients with rare chronic diseases related to various immunological disorders that were not controlled with conventional therapy. Drug reduction is particularly important in young patients and ECP should be used early in children for its steroid sparing capacity. In many diseases, ECP will probably continue to be used in the future despite incomplete evidence of efficacy, as the very limited number of patients does not enable large clinical studies. Case reports should be encouraged however, including those without success, in order to better document the role of ECP in the management of these patients. Conversely, some indications may be more completely investigated in frequent diseases. Prevention of restenosis after percutaneous transluminal coronary angioplasty by ECP as well as Crohn disease are two fields where prospective randomised studies should be undertaken. Another example which is far from being a rare disease is diabetes type 1 in its recent onset phase : although several trials have been reported, there is at present no universally recognised management to try to control the auto-immune process. ECP is a good candidate, due to the fact that it does not show the usual side effects of immunosuppressive drugs. The first trial to try to delay or event prevent the onset of diabetes type 1 has been done with the first generation of ECP technology, using discontinuously
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