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Nail Dystrophy, Edema, and Eosinophilia: Harbingers of Severe Chronic GVHD of the Skin in Children

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Nail Dystrophy, Edema, and Eosinophilia: Harbingers of Severe Chronic GVHD of the Skin in Children Bone Marrow Transplantation (2014) 49, 1521–1527 © 2014 Macmillan Publishers Limited All rights reserved 0268-3369/14 www.nature.com/bmt ORIGINAL ARTICLE Nail dystrophy, edema, and eosinophilia: harbingers of severe chronic GVHD of the skin in children JT Huang1, CN Duncan2, D Boyer3, H Khosravi4, LE Lehmann2 and A Saavedra5 The prognostic value of adnexal findings in chronic GVHD (cGVHD) has not been investigated in children. Dermatologic examinations were performed in a severe cohort of 11 children with skin cGVHD seen over a 2-year period. Findings were compared with 25 additional patients with skin cGVHD and 97 control patients. In 36 patients with skin cGVHD, nail dystrophy was present in 45% of patients, and was significantly associated with sclerotic disease and lung cGVHD. Pterygium inversum unguis (PIU) was associated with severe lung disease, with significantly lower % predicted FVC and FEV1 in those with PIU than those without. Forty-four percent of GVHD patients had preceding peripheral edema and 56% had preceding peripheral eosinophilia. Peripheral edema and eosinophilia were significantly associated with sclerotic cGVHD and persisted until the diagnosis of cGVHD in all patients. Comparison of data with control patients showed that incidence of nail dystrophy, incidence of peripheral edema and mean peak peripheral eosinophil count of patients with skin cGVHD was significantly higher than those without cGVHD. This study suggests that nail dystrophy, persistent peripheral edema and persistent peripheral eosinophilia are harbingers of severe cGVHD of the skin in children. The presence of PIU may be a harbinger of severe lung involvement. Bone Marrow Transplantation (2014) 49, 1521–1527; doi:10.1038/bmt.2014.194; published online 22 September 2014 INTRODUCTION seen by pediatric dermatologists at Dana-Farber Cancer Institute/Boston ’ Chronic GVHD (cGVHD) is a significant cause of morbidity and Children s Hospital over a 2-year period (February 2011 through March – 2013). Retrospective chart review of pediatric HSCT recipients transplanted mortality in children, second only to relapse of disease.1 3 4 between 2006 and 2012 was also performed. IRB approval through the Mortality from pediatric cGVHD has been estimated at 41%. Office of Human Research Studies at DFCI was obtained. However, prognostic indicators for morbidity and mortality For the cross-sectional cohort study, inclusion criteria included age at secondary to cGVHD have not been clearly identified in children. HSCT ⩽ 18 years, recipient of allogeneic HSCT, and the diagnosis of skin The skin is the most commonly affected organ in cGVHD and its cGVHD. Exclusion criteria included recipient of ⩾ 2 HSCT, and HSCT involvement may be predictive of a poor prognosis.5 Chronic skin performed at an outside institution. For the diagnosis of cGVHD, patients GVHD may present in multiple different ways ranging from xerosis either met diagnostic criteria established by the 2005 NIH Consensus Development Project, or had a new onset persistent skin eruption to erythroderma to sclerotic changes. Adnexal structures may also 8 be involved in cGVHD, resulting in nail dystrophy or alopecia. consistent with a feature listed in this report. Informed consent was Clinically, we have observed that patients with adnexal obtained by the patient and/or legal guardian. During their dermatology visit, eligible patients were recruited and involvement are less likely to respond to standard therapies. The enrolled in the study, which included a one time evaluation of their skin. nail matrix and hair follicle are known to be sites of immune Participants had a complete examination of the skin, mucous membranes, privilege, with decreased HLA-A, B and C expression on hair and nails by at least one of the two dermatologists (authors JTH, AS). keratinocytes and melanocytes as well as decreased MHC class II All abnormalities were documented and photographed. Patients and their – expression of epidermal antigen presenting cells.5 7 Downregula- legal guardians completed age-appropriate PedsQL questionnaires.9 tion of antigen recognition and T-cell activation decreases the Medical records of participants were reviewed and additional data were likelihood of cGVHD at these sites. Thus adnexal involvement may gathered, including general demographic data (age, gender), primary indicate more profound immune dysregulation and predict disease/reason for HSCT, source of HSCT, conditioning regimen, HLA treatment-refractory disease. match, gender of donor, history of acute GVHD (aGVHD), past and current The primary goal of our study was to investigate whether the immunosuppressive medications. Laboratory results and relevant radio- graphic studies were reviewed. When available, lowest pulmonary function presence of adnexal involvement in skin cGVHD was associated test (PFT) data (%predicted FVC and FEV1) were recorded. with severe disease. We also examined the incidence of edema Medical records of all pediatric patients who received an unrelated HSCT and eosinophilia as potential early signs of skin cGVHD. Finally, between May 2006 and August 2012 (date range HSCT was performed in we provide a descriptive analysis of a severe cohort of pediatric study cohort) were also reviewed. We gathered data on two separate patients with skin cGVHD. populations: (1) those with a history of skin cGVHD and (2) those without any history of cGVHD (control group). Patients excluded from this analysis MATERIALS AND METHODS included those with ⩾ 2 HSCT (including autologous HSCT), double cord transplants, death due to acute complications, and relapse of primary Study design condition. In patients with skin cGVHD, any documentation of nail This study was a single-center cross-sectional cohort study of pediatric dystrophy, eosinophil counts, and peripheral edema around time of hematopoietic SCT (HSCT) recipients with a diagnosis of skin cGVHD cGVHD diagnosis was recorded. In control patients, any documentation of 1Dermatology Program, Boston Children’s Hospital, Boston, MA, USA; 2Department of Pediatric Oncology, Dana-Farber Cancer Institute, Boston, MA, USA; 3Division of Respiratory Diseases, Boston Children’s Hospital, Boston, MA, USA; 4 Harvard Medical School, Boston, MA, USA and 5Department of Dermatology, Brigham and Women’s Hospital, Boston, MA, USA. Correspondence: Dr JT Huang, Dermatology Program, Boston Children’s Hospital, Fegan 6, 300 Longwood Avenue, Boston, MA 02115, USA. E-mail: [email protected] Received 3 March 2014; revised 3 July 2014; accepted 17 July 2014; published online 22 September 2014 Harbingers of severe skin cGVHD in children JT Huang et al 1522 Table 1. Characteristics of skin cGVHD in patients transplanted between 2006–2012 Characteristics Study cohort (11) Nonstudy cohort (25) P-valuea Total (36) History of acute cutaneous GVHD 1.0 Yes 5 (45%) 10 (40%) 15 (42%) No 6 (55%) 15 (60%) 21 (58%) Time from HSCT to cGVHD 0.94 Mean in days (s.d.) 245 (92) 249 (172) 248 (151) Onset of cGVHD 0.70 Progressive 4 (36%) 6 (24%) 10 (28%) Quiescent 1 (9%) 5 (20%) 6 (17%) De novo 6 (55%) 14 (56%) 20 (56%) Onset of skin involvement 0.7 Presenting organ 7 (64%) 18 (72%) 25 (69%) Subsequent organ 4 (36%) 7 (28%) 11 (31%) Type of skin cGVHD 0.025 Sclerotic 8 (73%) 7 (28%) 15 (42%) Nonsclerotic 3 (27%) 18 (72%) 21 (58%) Steroid responsiveness 0.15 Steroid responsive 3 (27%) 15 (60%) 18 (50%) Steroid resistant 8 (73%) 10 (40%) 18 (50%) Extracutaneous involvement 0.69 None 3 (27%) 8 (32%) 11 (31%) Mucous membranes 1 (9%) 4 (16%) 5 (14%) Visceral organs 1 (9%) 5 (20%) 6 (17%) Mucous membranes and visceral organs 6 (55%) 8 (32%) 14 (39%) Lung cGVHD 0.22 Yes 5 (45%) 5 (20%) 10 (28%) No 6 (55%) 20 (80%) 26 (72%) Death at time of publicationb 1.0 Yes 4 (36%) 9 (36%) 13 (36%) No 7 (64%) 16 (64%) 23 (64%) aP-values based on Fisher’s exact test for categorical variables and two-sample t-test for continuous variables. bJune 2014. nail dystrophy, eosinophil counts and peripheral edema from 100 days RESULTS post-HSCT to May 2013 was recorded. In controls, high eosinophil counts Demographics attributed to acute GVHD were excluded. Eleven pediatric HSCT recipients with skin cGVHD were enrolled in the cross-sectional cohort study (study cohort). These patients Study aims were transplanted between May 2006 and August 2012. There The primary aim of our study was to investigate whether adnexal were an additional 25 patients with skin cGVHD who were involvement, including nail dystrophy and alopecia, in skin cGVHD was transplanted during this time period, 12 of whom had active skin predictive of more severe disease. Secondary aims of our study were to disease during the study time period of 2011 to 2013. Of these identify early signs of skin cGVHD, and to provide a descriptive analysis of 12 patients, 10 were noted to have eczematous or erythematous our cohort. skin eruptions, and were not seen by dermatologists during the study period. The remaining two had sclerotic disease; one declined study enrollment, and the other was critically ill and Study definitions fi deemed unsuitable for the study. Date of cGVHD was de ned as onset of symptoms that were ultimately Between May 2006 and August 2012, there were 209 recipients diagnostic of cGVHD. Determination of overall cGVHD severity was based of unrelated HSCT performed at our institution. Of these 209 on the scoring system proposed by 2005 NIH Consensus Development 8 patients, 18 had received ⩾ 2 HSCT (including autologous HSCT), Project. Fully matched patients had no identified mismatches at HLA-A, -B, -C and –DRB1 by high resolution typing if the graft source was BM or no 1 had a double cord transplant, 25 died of acute complications, 21 identified mismatches at HLA-A, -B, -DRB1 by intermediate resolution had subsequent relapse of their primary condition and 47 patients typing if the graft source was cord blood. De novo onset type of cGVHD had chronic GVHD (36 of whom had skin involvement).
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