Impact of extracorporeal photopheresis on skin scores and quality of life in patients with steroid-refractory chronic GVHD
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1 Bone Marrow Transplantation (214) 49, & 214 Macmillan Publishers Limited All rights reserved /14 ORIGINAL ARTICLE Impact of extracorporeal photopheresis on skin scores and quality of life in patients with steroid-refractory chronic GVHD FL Dignan 1,2,3, S Aguilar 1, JJ Scarisbrick 4, BE Shaw 2,3, MN Potter 2, J Cavenagh 5, JF Apperley 6, AK Fielding 7, A Pagliuca 8,KRaj 8, DI Marks 9, A Peniket 1, C Crawley 11, MB Koh 12 and FJ Child 1 There are few prospective studies evaluating the role of extracorporeal photopheresis (ECP) in chronic GVHD (cgvhd) and only occasional reports of the effect of ECP on patients quality of life (QoL). We report a single-centre prospective study of patients undergoing fortnightly ECP for moderate or severe cgvhd. Response was assessed after 6 months of treatment using NIH scoring criteria and reduction in immunosuppression. QoL assessments were undertaken at baseline and at 6 months using the chronic GVHD symptom scale (cgvhd SS) and dermatology life quality index (DLQI). An intention-to-treat analysis showed that 19/38 (5%) of patients had a complete or partial response. Twenty-seven out of 38 patients completed 6 months of ECP treatment and 7% (19/27) had a complete or partial response. Eighty per cent of patients who completed 6 months of ECP treatment had a reduction in immunosuppression dose. A subset of patients completed QoL questionnaires. Seventeen out of 18 patients (94%) showed an improvement in scores. The mean cgvhd SS and mean DLQI score were both significantly lower after 6 months of ECP (22 compared with 36, P ¼.12 and 3.4 compared with 6.9, P ¼.9, respectively). This study confirms that ECP can lead to objective clinical responses and, in addition, may lead to an improvement in QoL in cgvhd. Bone Marrow Transplantation (214) 49, 74 78; doi:1.138/bmt ; published online 24 February 214 Keywords: GVHD; extracorporeal photopheresis; quality of life INTRODUCTION Extracorporeal photopheresis (ECP) is a cell-based immunemodulatory therapy, which was first reported by Edelson et al. 1 for the treatment of erythrodermic cutaneous T-cell lymphoma. Our group and others have previously reported the efficacy of ECP in the management of cgvhd in retrospective studies. 2 5 To date, there are only a few prospective studies of ECP for this condition 6 9 and one randomised prospective trial. 1 In addition, there are few data on the effect of ECP on quality of life (QoL) in patients with cgvhd. In a retrospective study, we have previously shown that a fortnightly regimen of ECP improved the clinical signs and symptoms of cgvhd. 2 The aim of the current report was to prospectively assess the effect of a fortnightly schedule of ECP on the clinical signs and symptoms of cgvhd. The secondary aims were to assess the effect of ECP on health-related QoL and to assess response in terms of change in immunosuppression dose at 6 months. SUBJECTS AND METHODS Patient population From 1 October 21 to 1 December 211, a total of 52 consecutive patients commenced ECP treatment for GVHD at St John s Institute of Dermatology, St Thomas Hospital in London, UK. Six patients were excluded from the study, as they were 18 years of age, did not give written informed consent or completed less than one cycle of treatment. Four patients were excluded, as they had received ECP for acute GVHD elsewhere prior to referral and, at the time of initial clinic assessment, had no clinical signs of cgvhd. Four patients with isolated hepatic or gastrointestinal GVHD were excluded, as they had persistent acute GVHD and did not fulfil the National Institutes of Health (NIH) diagnostic criteria for cgvhd. Thirty-eight patients were eligible for the study. Referrals were made to the ECP unit at the discretion of the transplant physicians from centres in southern England, and the decision to offer treatment was made by the ECP unit. Patients had steroid-refractory or steroid-dependent disease or were intolerant of corticosteroids. All patients gave written informed consent to data collection and study participation. The study was approved by the Kent Research Ethics Committee (1/H111/21). The clinical assessment of the symptoms and signs of cgvhd was based on the NIH consensus development project on criteria for clinical trials in cgvhd. 11 The extent of cutaneous involvement was measured by the percentage of body surface area involved. This measurement was subdivided to include the percentage of erythema and the percentage of movable and non-movable sclerosis. The percentage of oral mucosa involved with lichenoid change or erythema was documented, and the number of ulcers or mucoceles in the mouth was also recorded. These findings were used to assign an oral score between and 12. Patients were also asked to give an oral pain score between and 1 and an ocular pain score between and 1. Response criteria Response was assessed after 6 months of ECP treatment using NIH criteria. 11 Response was primarily assessed by one dermatologist to avoid inter-observer variation. A complete overall response was defined as a complete resolution of all symptoms and signs of cgvhd. A partial overall 1 St John s Institute of Dermatology, St Thomas Hospital, London, UK; 2 Section of Haemato-oncology, The Royal Marsden Hospital, Sutton, UK; 3 University College London, Cancer Institute, London, UK; 4 Department of Dermatology, Queen Elizabeth Hospital, Birmingham, UK; 5 Department of Haematology, St Bartholomew s Hospital, London, UK; 6 Centre for Haematology, Imperial College, London, UK; 7 Department of Haematology, University College London, London, UK; 8 Department of Haematological Medicine, King s College London Denmark Hill Campus, London, UK; 9 Department of Haematology, University Hospitals Bristol NHS Foundation Trust, Bristol, UK; 1 Department of Haematology, The Churchill Hospital, Oxford, UK; 11 Cambridge University Hospitals NHS Foundation Trust, Cambridge, UK and 12 Department of Haematology, St George s Hospital, London, UK. Correspondence: Dr FL Dignan, Manchester Royal Infirmary, Oxford Road, Manchester SM2 5PT, UK. fldignan@doctors.org.uk Received 31 October 213; revised 2 January 214; accepted 6 January 214; published online 24 February 214
2 clinical response was defined as a 5 99% improvement in one organ when compared with baseline and no evidence of cgvhd progression in other organs. In addition, a minimal response was defined as a 25 49% response in one organ compared with baseline and no evidence of cgvhd progression in other organs. A mixed response was defined as a complete or partial response in one organ but progression of disease in another, and stable disease was defined as o25% improvement or o25% deterioration in cgvhd organ score. Progressive disease was defined as X25% deterioration in cgvhd organ score. Specifically, a partial response in cutaneous GVHD was defined as a 5 99% reduction in the body surface area involved. A partial response in oral GVHD was defined as a 5 99% reduction in oral score. Oral pain score was documented but was not used to determine response. A partial response in ocular GVHD was defined as a 5 99% reduction in ocular pain score. A partial response in joint GVHD was defined as a 5 99% improvement in range of movement. Many patients had multi-organ involvement, and the ability to reduce immunosuppression after 6 months of treatment was used as a global measure of response to ECP. QoL assessment Patients were asked to complete two questionnaires to assess healthrelated QoL at the start of treatment and at 3-monthly intervals thereafter. The first questionnaire was the Lee chronic GVHD symptom scale (cgvhd SS). 1 A change of 6 7 points in cgvhd SS was considered to be a clinically significant change. 11,12 The second was the dermatology QoL index (DLQI). 13 A change of 3.2 points in the DLQI score was considered clinically significant. ( Extracorporeal photopheresis ECP treatment was administered on 2 consecutive days every 2 weeks until a partial clinical response was achieved and was then reduced to a monthly schedule as per the UK consensus statement. 14 ECP was performed using the UVAR XTS or CELLEX photopheresis systems (Therakos, Ascot, UK). The technique has been described previously. 2 Blood parameters Full blood count, urea and electrolytes and liver function tests were measured at the start of treatment and on the first day of each cycle of ECP treatment. Statistical analysis Descriptive data were summarised using median values, ranges and percentages. The comparison of QoL scores at baseline and after 6 months of treatment was undertaken using the Student s t-test. A P-value of o.5 was considered significant. RESULTS Demographics Patient characteristics are summarised in Table 1. The median time from transplant to commencing ECP was 1.7 years (3 months to 7 years and 9 months). In all, 3/38 patients had classic cgvhd, 5/38 had overlap syndrome and 3/38 had developed GVHD following DLI. Using the NIH global scoring system for cgvhd, 11/38 patients with cgvhd had severe disease and 27/38 had moderate disease. 15 Twenty-two patients (58%) had a history of previous acute GVHD. Thirty-two patients had cutaneous disease. Twelve patients had sclerodermoid disease and 15 had lichenoid disease. Five patients had features of both sclerodermoid and lichenoid disease. Seventeen patients had oral disease. Other organs involved included liver (8), eyes (14), gut (7), lung (3) and muscles/joints (6). At the start of ECP, 36/38 patients were receiving immunosuppressive drugs. The remaining two patients had a previous history of steroid intolerance or steroid-refractory disease. The median dose of prednisolone at the start of treatment was 17.5 mg ( mg). The median dose of cyclosporin was 2 mg daily (2 15 mg twice daily). The median dose of mycophenolate mofetil was 2 g per day (1 5 g). The number of immunosuppressive agents that each patient was receiving is detailed in Table 1. Table 1. Patient characteristics (n ¼ 38) Characteristic No. of patients, n (%) Male 19 (5) Female 19 (5) Median age (range) years 47.2 ( ) Diagnosis Acute leukaemia/myelodysplastic 27 (71) syndrome Lymphoma 4 (11) Chronic leukaemia 5 (13) Other a 2 (5) Donor type Unrelated donor 24 (63) Sibling/related donor 14 (37) Donor sex Male 22 (58) Female 11 (29) Unknown 5 (13) Stem cell source Peripheral blood 38 (1) Conditioning Full intensity 11 (29) Reduced intensity 27 (71) T-cell depletion 18 (47) Number of GVHD treatments None 2 (5) One 9 (24) Two 2 (53) Three 7 (18) a Plasma cell leukaemia, Waldenstrom s macroglobulinaemia. Duration of ECP treatment Eleven patients (11/38, 29%) were no longer receiving ECP at the time of analysis. Twenty-seven patients (27/38, 71%) were receiving ongoing treatment but had received at least 6 months of ECP. One patient had reduced the frequency of ECP to monthly after 3 months of ECP and the others all received fortnightly therapy. Response Clinical assessment of overall response. Twenty-seven out of 38 patients were evaluable for response following 6 months of ECP treatment. Two patients had died of infectious complications of the transplant and nine patients had completed less than 6 months of treatment because of relapse of underlying malignant disease (3), lack of efficacy of ECP (1), lost to follow-up as patient left UK (1), catheter-related infection (1), line thrombosis (1) and being too unwell to travel for treatment because of GVHD symptoms or related infections (2). This group included five patients with severe cgvhd and six with moderate cgvhd. An intention-to-treat analysis showed that 19/38 (5%) of patients had a complete or partial improvement in symptoms and signs of GVHD. Nineteen out of 27 (7%) patients who completed 6 months of ECP showed an overall complete or partial response. Two patients had a complete improvement and seventeen had a partial improvement. Three patients had progressive disease, two had a minimal response and three had a mixed response (complete response in one organ and progressive disease or new disease in another organ). Three patients developed signs of oral GVHD while on ECP treatment. Table 2 shows the response in each organ and the overall response. 75 & 214 Macmillan Publishers Limited Bone Marrow Transplantation (214) 74 78
3 76 Table 2. GVHD subtype, response in each organ and overall response to ECP in patients who completed 6 months of treatment Patient no. GVHD subtype Skin response Oral response Ocular response Other (specify) Other response Overall response 1 Classic PD New Gut CR Mixed 2 Classic SD Gut CR Partial 3 Classic PD MR Progressive 4 Classic PD PD Progressive 5 Classic CR CR Complete 6 Classic MR Minimal 7 Classic CR MS SD Partial 8 Classic PR Partial 9 Classic PR Gut CR Partial 1 Overlap SD CR Partial 11 Classic SD PR Partial 12 Classic CR SD CR Partial 13 Classic PR PR Partial 14 Classic CR MS SD Partial 15 Classic CR Gut CR Complete 16 Classic MR SD SD Minimal 17 Classic CR CR MR Partial 18 Classic CR SD MS PR Partial 19 Classic CR PR PR Partial 2 Overlap PR New CR Mixed 21 Classic SD MS þ lung PR Partial 22 Classic SD gut CR Partial 23 Classic CR gynae SD Partial 24 Classic PR New SD Mixed 25 Classic PD lung SD Progressive 26 Classic MS PR Partial 27 Overlap PR CR MR Partial Abbreviations: CR ¼ complete response; MR ¼ minimal response; MS ¼ musculoskeletal; New ¼ new onset of disease while receiving ECP; PR = partial response; SD = stable disease. % BSA involved Patients % BSA baseline % BSA 6 months Figure 1. Skin scores in patients with lichenoid GVHD at baseline and after 6 months of ECP. Clinical assessment of response in each organ. The skin scores for lichenoid and non-movable sclerodermoid disease are shown in Figures 1 and 2; the oral clinical and pain scores in Figure 3. In the 1 with lichenoid disease who completed 6 months of ECP treatment, 7 (5%) patients had a CR, 3 (22%) had a PR, 2 (14%) had stable disease and 2 (14%) had PD. In the 1 patients with non-movable sclerodermoid disease who completed 6 months of ECP treatment, 5 (5%) patients had a CR, 3 (3%) had a PR (including those where non-movable sclerosis had become movable), 1 (1%) had a minimal response and 1 (1%) had stable disease. In the 11 patients with oral disease who had completed 6 months of ECP treatment, 3 (27%) patients had a CR, 1 (9%) a PR, 1 (9%) had a minimal response, 5 (46%) had stable disease and 1 (9%) had progressive disease. Table 2 shows the response in each organ and the overall response. Change in immunosuppressive dose. Thirty-six patients were receiving immunosuppressive drugs at the start of ECP treatment. Twenty-five were reassessed at 6 months. The remaining 11 patients had either died (2) or completed less than 6 months of treatment (9). Assuming that the patients who died or did not complete 6 months of ECP did not respond to treatment, 2/36 % BSA involved % BSA baseline % BSA 6 months Figure 2. Skin scores in patients with non-movable sclerosis at baseline and after 6 months of ECP. (55%) had a reduction in immunosuppression. Twenty out of 25 (8%) patients who completed 6 months of ECP had a reduction in immunosuppressive dose. Twenty-eight patients were receiving steroids at the start of ECP treatment. Nineteen patients were evaluable for assessment at 6 months. Seventeen patients (89%) had a dose reduction (5 stopped completely, 4X75% reduction, 4X5% reduction and 4o5% reduction). Two patients doses were stable and one patient had started steroids. The median dose was 1 mg ( mg). Figure 4 is a flow chart showing change in dose in patients who were on steroids at the start of ECP treatment. Six out of 27 patients who were evaluable for assessment at 6 months were not receiving steroids at the start of ECP but were receiving an alternative immunosuppressive medication. Three patients remained on the same dose of cyclosporin, Bone Marrow Transplantation (214) & 214 Macmillan Publishers Limited
4 Oral scores Oral exam score baseline Oral exam score 6 months Oral pain score baseline Oral pain score 6 months Figure 3. Oral examination and pain scores at baseline and after 6 months of ECP. cgvhd score cgvhd score baseline cgvhd score 6 months Figure 5. cgvhd symptom scores at baseline and after 6 months treatment. 77 Dose Reduction: 17 patients Stopped: 5 patients 75% dose 5% dose Total : 38 patients Completed 6 months ECP: 27 patients Steroids at start: 19 patients Dose stable: 2 patients Dose Increase: patients out of 18 (94%) showed an improvement in scores and in 13/18 (72%) this was a clinically significant improvement. In the patients who had completed 6 months of ECP treatment and questionnaires at both time points (n ¼ 18), the mean cgvhd SS was significantly lower after 6 months of ECP (22 compared with 36, P ¼.12). Figure 5 shows cgvhd SS scores at baseline and after 6 months of ECP. Sixteen patients completed the DLQI score at baseline and after 6 months of ECP treatment. Baseline scores ranged from /3 to 15/3 with a median score of 7/3. Thirteen out of 16 (81%) patients showed an improvement in scores and in 6/16 (38%) this was a clinically significant improvement. In the patients who had completed 6 months of ECP treatment and questionnaires at both time points (n ¼ 16), the mean DLQI score was significantly lower after 6 months of ECP treatment (3.4 compared with 6.9, P ¼.9). Thirteen out of these 18 patients (72%) had a PR, one patient had a CR, two patients had a mixed response, one a minimal response and one patient had progressive disease. All the patients who had a CR or PR had an improvement in both scores except for one. The patients who had a minimal or mixed response had a clinically significant change in cgvhd scores but not in DLQI. The patient with progressive disease did not have a clinically significant change on cgvhd SS but did have on the DLQI. All the three patients with overlap syndrome achieved a clinically significant improvement on cgvhd SS but not on the DLQI. Toxicity. Low numbers of toxicities were found. Five patients developed indwelling catheter-related infections during the course of ECP treatment. One patient had a catheter-related thrombosis. One patient had an increase in red cell transfusion requirements, which was felt to be due to ECP alone. Five patients reported fatigue following treatment. < 5% dose Figure 4. A flow chart to show change in steroid dose after 6 months of ECP treatment. mycophenolate mofetil and imatinib, respectively. Two patients had a 5% dose reduction in the dose of mycophenolate mofetil and one patient had a 75% dose reduction in ciclosporin. Two patients were not receiving immunosuppression at the start of ECP. One of these patients commenced steroids and the other did not start any additional agents during ECP treatment. QoL assessment. Eighteen patients completed the cgvhd SS at baseline and after 6 months of ECP treatment. The remaining patients did not return questionnaires. Baseline scores ranged from 8/12 to 64/12 with a median score of 38/12. Seventeen DISCUSSION This paper reports a prospective evaluation of patients treated with fortnightly ECP for cgvhd. There are very few previous prospective studies of ECP in cgvhd because of the rarity of the disease, complexity of the treatment and absence of a standardised regimen. Previous reports have used a variety of schedules and have not reported the effect on QoL using validated questionnaires. 6 1 This is the first prospective study to investigate the effect of a fortnightly schedule of ECP on clinical response and QoL in cgvhd using two validated questionnaires. This report benefits from a standardised regimen of ECP, prospective data accrual, lack of inter-observer variation and stringent use of NIH criteria. The results are remarkably consistent with the retrospective study we have reported previously. 2 The earlier study showed that 77% of patients who completed 6 months of ECP treatment had a reduction in immunosuppression, and the prospective study showed that 8% of patients who completed 6 months of ECP had a reduction in immunosuppression. & 214 Macmillan Publishers Limited Bone Marrow Transplantation (214) 74 78
5 78 One limitation of this study was the number of patients who did not complete 6 months of treatment (11/38, 29% of patients). This figure reflects the high morbidity and mortality rate in patients with steroid-refractory cgvhd. 16 In addition, the ECP facility is an out-patient unit, so patients had to be well enough to attend treatment. Another limitation is that only a minority of patients who completed 6 months of treatment had visceral localisation of GVHD. This study population may represent a favourable cohort of patients who may be more likely to respond to ECP. A number of previous reports have reported an adverse impact of cgvhd on QoL following HSCT To date, very few studies have investigated the impact of ECP on QoL. In the only randomized controlled trial to date, Flowers et al. 1 used a Targeted Symptoms Assessment questionnaire, which included 12 questions to assess the effect of cutaneous, ocular and oral GVHD on various aspects of patients QoL. In this study, baseline scores were similar between the two arms, and after 12 weeks of ECP there was a significant difference between the median improvement in TSA scores in the ECP arm compared with the control arm (19% vs 2.5%, P ¼.1). Other studies have used performance status as a surrogate marker of response. 23,24 The current report used two validated questionnaires, the organ-specific DLQI 13 and the cgvhd SS, 12 to assess QoL at baseline and after 6 months of ECP treatment. This study showed a significant improvement in both cgvhd SS and DLQI scores in patients who completed 6 months of ECP, which is in keeping with previous reports of improvement in TSA and performance status. It is interesting to note that even the four patients who did not achieve a PR or CR in symptoms or signs of GVHD in this study obtained an improvement in either the cgvhd of DLQI QoL assessments. This finding may be due partly to the placebo effect of regular medical and nursing assessments and the opportunity during ECP treatment to talk to other patients with similar problems. Another limitation is possible selection bias because of the fact that the patients who chose to complete the questionnaires may have been the ones who had noticed an improvement in QoL. In conclusion, this paper reports on a prospective study of the role of fortnightly ECP in managing patients with cgvhd. The findings suggest that our previously reported data from a retrospective analysis are reproducible in a prospective cohort of patients, with 8% of patients who completed 6 months of ECP having a reduction in immunosuppression. In addition, it adds to the current literature by suggesting that ECP may help to improve QoL as assessed by two validated questionnaires. Further randomised studies are required to assess the optimal regimen of ECP and the effect of the treatment on patients QoL and should aim to include a longer follow-up period. CONFLICT OF INTEREST FLD has received research funding, honoraria and speakers fees from Therakos, a Johnson and Johnson company. BES, JFA and JJS have received honoraria and speakers fees from Therakos, a Johnson and Johnson company. FJC and KR have received honoraria from Therakos, a Johnson and Johnson company. ACKNOWLEDGEMENTS We wish to thank Stephanie Lee and Andrew Finlay for their permission to use the cgvhd SS and DLQI questionnaires. JFA is grateful for the support from the NIHR Biomedical Research Centre funding scheme. REFERENCES 1 Edelson R, Berger C, Gasparro F, Jegasothy B, Heald P, Wintroub B et al. Treatment of cutaneous T-cell lymphoma by extracorporeal photochemotherapy. N Engl J Med 1987; 316: Dignan FL, Greenblatt D, Cox M, Cavenagh J, Oakervee H, Apperley JF et al. 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