Clinical, Histopathological and Immunohistochemical Study of Cases Presenting with Erythroderma
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1 Clinical, Histopathological and Immunohistochemical Study of Cases Presenting with Erythroderma A Thesis Submitted For Partial Fulfillment of Master Degree in Dermatology By Suzan Mohamed Ameen Shalaby M.B.B.Ch Supervised by Dr. Mona R.E.Abdel-halim Assistant Professor of Dermatology Faculty of medicine Cairo University Dr. Eman Ahmed El-Nabarawy Assistant Professor of Dermatology Faculty of medicine Cairo University Prof. Magda Ibraheem Assaf Professor of Pathology Faculty of Medicine Zagazig University Faculty of Medicine Cairo University 2012
2 Contents List of Contents Acknowledgment Abstract List of abbreviations List of figures List of tables I III V VII VIII Introduction 1 Review of literature Chapter 1: Erythroderma 3 Chapter 2: Clinical presentations of erythroderma 19 Chapter 3: Diagnosis of erythroderma 37 Patients and methods 71 Results 79 Case Presentations 125 Discussion 137 Recommendations 148 Summary 149 References 154 Appendix 170 Arabic summary
3 Acknowledgment Acknowledgment Thanks to ALLAH, the most generous and the most merciful for allowing me to complete this work and for blessing me with supportive family, supervisors and friends who were there for me along every step of the journey. Dr. Mona Abdel-halim, your leadership, attention to every single detail and hard work set me an example I hope to match one day. Thanks for your continuous support, for guarding my first steps in dermatopathology, for your patience in teaching me and during our lovely arguments. Dr. Eman El-Nabarawy, I m grateful for your sincere advice and kindness which guided my way through this work. Prof. Dr. Magda Assaf, to whom I m deeply indebted, for this work wouldn t have been possible without her great help and experience in the field of dermatopathology. Prof. Dr. Hoda Rasheed, thanks for your support and for your confidence in your junior residents. Prof. Dr. Mohamed El-Darouti, your extraordinary success as a clinical dermatologist and dermatopathologist set your students high standards of performance. Thanks for opening us a door to a new field of practice and for establishing the dermatopathology unit. Dr. Rania Mounir, for her valuable help and effort in the statistical analysis of this work. I
4 Acknowledgment My dear parents, thanks for your unconditioned love and support. All words of gratitude cannot express mine. Thanks for always encouraging me to do my best in this work and all through my life. Thanks to all my friends and colleagues who helped me through this work. Suzan Shalaby 2012 II
5 Abstract Abstract Background: Erythroderma is a morphologic presentation of a variety of cutaneous and systemic diseases. Diagnosing erythroderma is very challenging mainly as regards the differentiation between neoplastic and benign (inflammatory) causes. Aim of work: This work aimed at studying cases presenting with erythroderma, clinically, histopathologically and immunohistochemically in order to develop criteria that help in reaching a final diagnosis and in differentiating between benign (inflammatory) and neoplastic causes of this condition. Patients and methods: Thirty patients with erythroderma aged more than 12 years old were included. Each was subjected to complete medical history, thorough general and cutaneous examination as well as laboratory investigations. Accordingly, a provisional clinical diagnosis was reached. Two Skin biopsies were examined blindly to any clinical data and a histopathological diagnosis was defined. Cases with mismatched provisional clinical and histopathological diagnoses as well as histopathologically unsettled cases were subjected to further clinical correlation and immunohistochemical study of the expression of CD2, CD5, CD7, CD4 and CD8 to verify the diagnosis. Immunohistochemistry was also done for cases representing both inflammatory and neoplastic conditions in order to characterize their immunophenotypic profile. Results: Based on the constellation of clinical, histopathological and immunohistochemical data, the final diagnoses of studied cases included: 15 cases (50%) of erythroderma due to a pre-existing dermatosis namely: 12 cases of psoriasis (40%), 2 cases of atopic dermatitis (6.7 %), and 1 case of pemphigus foliaceus (3.3%). The remaining 15 cases were diagnosed as drug induced erythroderma in 7 cases (23.3%), 1 case (3.3%) of papuloerythroderma of Ofuji and 7 cases (23.3%) of III
6 Abstract erythrodermic CTCL which included 1 case (3.3%) of Sézary syndrome and 6 cases (20%) of erythrodermic MF. On clinical basis, a diagnosis of psoriasis was significantly associated with fiery red erythema, dry white silvery scales, absent oozing, palmoplantar scaling and erythema (P value =0.003, <0.0001, =0.031 and respectively). A diagnosis of CTCL was significantly associated with dusky red erythema, fine branny scales, infiltrated areas, alopecia and palmoplantar keratoderma (P value =0.003, <0.0001, =0.043, =0.015 and respectively). Eosinophilia was significantly seen in cases of drug induced erythroderma (P value = 0.015). On histopathological basis, psoriasiform hyperplasia, hypogranulosis and superficial perivascular infiltrate were significantly seen in cases of psoriasis (P value < , = 0.011, =0.005 respectively). Irregular hyperplasia, epidermotropism, the presence of atypical lymphocytes in the infiltrate, band like infiltrate, dense infiltrate and wiry fibrosis in the papillary dermis were significantly seen in CTCL (P value = 0.001,= 0.002, <0.0001, =0.045, and 0.001respectively). The presence of vacuolar degeneration along the dermoepidermal junction was significantly seen in cases of drug induced erythroderma (P value = 0.007). Immunohistochemical results showed variable expression of CD4 and CD8 in malignant cases with tendency towards loss of pan T cell markers and a CD8-ve profile while inflammatory conditions mainly showed a CD8+ve profile. Conclusion: Diagnosis of cases of erythroderma is a complex process that depends on a proper constellation of clinical, histopathological and immunohistochemical data. Multiple biopsies from different sites as well as repeated biopsies in chronic cases are highly recommended. Although immunohistochemistry is helpful, it has many limitations. Keywords: Erythroderma, Clinical, Histopathology, Immunohistochemistry, Psoriasis, Eczema, CTCL, MF, Drug reaction. IV
7 List of Abbreviations List of Abbreviations HIV Human immunodeficiency virus CTCL Cutaneous T cell lymphoma ICAM-1 Intercellular adhesion molecules-1 ICAM-2 Intercellular adhesion molecules-2 VCAM-1 Vascular cell adhesion molecule-1 ELAM-1 Endothelial leukocyte adhesion molecule- 1 CD Clusters of differentiation GMP-140 Granule membrane protein-140 TNF Tumor necrosis factor VPF Vascular permeability factor VEGF Vascular endothelial growth factor Th1 T helper 1 Th2 T helper 2 g/d Gram per day DRESS Drug rash with esinophilia and systemic symptoms syndrome PUVA Psoralen combined with ultraviolet A treatment mg/kg Milligram per kilogram AD Atopic dermatitis PRP Pityriasis Rubra Pilaris SCARD Severe cutaneous adverse reactions to drugs SJS Stevens-Johnson syndrome TEN Toxic epidermal necrolysis E-CTCL Erythrodermic cutaneous T cell lymphoma SS Sézary syndrome E-MF Erythrodermic mycosis fungoides MF Mycosis fungoides NOS Not otherwise specified IgE Immunoglobulin E AIDS Acquired immunodeficiency syndrome CBC Complete blood count ESR Erythrocyte sedimentation rate ECG Electrocardiogram KOH Potassium hydroxide V
8 List of Abbreviations, continued List of Abbreviations PCR Polymerase chain reaction ELISA Enzyme-linked immunosorbent assay ANA Antinuclear antibody Anti-DNA Anti double stranded DNA H&E Hematoxylin and Eosin IFN-γ Interferon gamma CLA Common leukocyte antigen IL Interleukin IV Intravenous SDF-1 stromal cell-derived factor 1 CXCR4 C-X-C chemokine receptor type 4 TCR T cell receptor Μm Micrometer ISCL International Society for Cutaneous Lymphomas FC Flow cytometry Vβ V beta DNA Deoxyribonucleic acid SD Standard deviation NAD No abnormality detected PPK Palmoplantar keratoderma TLC Total leukocytic count BSA Body surface area HSM Hepatosplenomegaly PF Pemphigus foliaceous DEJ Dermoepidermal junction BM Basement membrane VI
9 List of Figures List of Figures Figure no. Title Page Chapter 1: Erythroderma Fig. 1 Graph presentation of age and sex distribution of erythroderma 5 Chapter 2: Clinical presenta onsof erythroderma Fig. 2 Leonine facies 34 Chapter 3: Diagnosis of erythroderma Fig.3 Erythroderma (H&E) 43 Fig. 4 Acute & chronic dermatitis (H&E) 43 Fig. 5 Erythrodermic psoriasis (H&E) 45 Fig. 6 Classic psoriatic lesions (H&E) 45 Fig. 7 Erythrodermic atopic dermatitis (H & E) 47 Fig. 8 Atopic dermatitis (H&E) 47 Fig.9 Erythrodermic lichenoid drug eruption (H&E). 48 Fig. 10 A case of erythrodermic PRP (H&E) 49 Fig. 11 Drug induced erythroderma (H&E) 51 Fig.12 Histologic findings of erythrodermic cutaneous T cell lymphoma 52 Fig. 13 A collection of epidermal atypical lymphocytes forming a Pautrier s microabscess (H & E) 54 Fig. 14 Histopathology of MF 54 Fig. 15 Skin-biopsy from a patient with the Red Man Syndrome 55 Fig. 16 Skin biopsy of patient with papuloerythroderma 56 Fig. 17 Histologic findings of erythrodermic cutaneous T cell lymphoma 59 Fig. 18 Photomicrograph of a small (A) and large (B) Sézary cell. 66 Fig. 19 Electron microscopy to show the convoluted nucleus in a typical Sézary cell 67 Fig. 20 Algorithm for the evaluation and diagnosis of erythroderma due to cutaneous T-cell lymphoma (E-CTCL) versus reactive causes of erythroderma Results Fig. 21 Case Fig. 22 Case Fig. 23 Case Fig. 24 Case Fig. 25 Case Fig. 26 Case Fig. 27 Case Fig. 28 Case Fig. 29 Case Fig. 30 Case Fig. 31 Case Fig. 32 Case VII
10 List of Tables List of Tables Table No. Title Page Chapter 1: Erythroderma Table 1 Causes of erythroderma 7 Table 2 Incidence of different causes of erythroderma according to previous studies 8 Chapter 2: Clinical presenta onsof erythroderma Table 3 Drugs associated with erythroderma 30 Table 4 Subsets of erythrodermic CTCL 32 Chapter 3: Diagnosis of erythroderma Table 5 Basic investigations in erythroderma 38 Table 6 Disease specific investigations in erythroderma 39 Table 7 Results of previous studies on the diagnostic value of skin biopsies (H&E) in diagnosis of erythroderma 41 Patients and Methods Table 8 Erythroderma clinical sheet 75 Table 9 Specific clues used to establish a provisional clinical diagnosis of each case 76 Table 10 Items of assessment in routine H&E histopathological evaluation. 77 Table 11 Specific clues for routine H&E histopathological diagnosis 78 Results Table 12 Patients demographic data 79 Table 13 Results of history 81 Table 14 Results of general examination 83 Table 15 Results of cutaneous examination Table 16 Results of investigations 90 Table 17 Provisional clinical diagnoses 92 Table 18 Comparison between different provisional clinical diagnoses groups as regards clinical items assessed 94 Table 19 Histopathological diagnoses 99 Table 20 Comparison between different histopathological diagnoses as regards different items assessed. Table 21 Comparison between different subgroups of drug induced erythroderma as 105 regards different pathological findings Table 22 Matching between provisional clinical and histopathological diagnoses (routine H&E) 107 Table 23 Immunohistochemical findings in controversial cases. 109 Table 24 Immunohistochemical findings in MF cases 110 Table 25 Immunohistochemical findings in cases diagnosed histopathologically as drug induced erythroderma with matched or accepted clinical diagnoses. 111 VIII
11 List of Tables List of tables (continued): Table 26 Immunohistochemical findings in cases diagnosed histopathologically as psoriasis with matched clinical diagnoses. Table 27 Immunohistochemical findings in cases diagnosed histopathologically as subacute/chronic spongiotic dermatitis with matched or accepted clinical 112 diagnoses Table 28 Established final diagnoses Table 29 Final diagnoses 115 Table 30 Matching between provisional clinical diagnoses and final diagnoses. 116 Table 31 Comparison between different final diagnoses groups as regards different clinical findings Table 32 Matching between histopathological diagnoses and final diagnoses 119 Table 33 Table 34 Comparison between different final diagnoses groups as regards different histopathological findings Comparison between CTCL group and drug induced erythroderma group and risk estimate IX
12 INTRODUCTION & AIM OF WORK
13 Introduction and Aim of work Introduction Erythroderma refers to a generalized or nearly generalized sustained erythema of the skin, involving more than 90% of the body surface accompanied by a variable degree of scaling (Khaled et al., 2010). It is actually a clinical syndrome that represents the morphologic presentation of a variety of cutaneous and systemic diseases, thus a thorough workup is essential to reach the diagnosis and establish the management in order to avoid serious complications and metabolic burden (Okoduwa et al., 2009). According to Xiao-Ying and colleagues in 2010, erythrodermic patients are categorized into four groups: erythroderma due to preexisting dermatoses, drug induced erythroderma, malignant erythroderma and idiopathic erythroderma. Most studies of erythroderma did not correlate the presenting clinical features of erythroderma with the etiology, as they are usually not specific (Hafeez et al., 2010), however the classic inflammatory clinical picture can be modified according to individual causes giving some clues for diagnosis (Kraft and Lynde, 2008). Skin biopsy is one of the corner stones in the diagnosis of erythroderma, but interpretation of such specimens is difficult, due to the fact that the histopathological expression of the underlying disorder is more subtle in the setting of erythroderma, hence, in many cases, the microscopic changes are not diagnostic (Walsh et al., 1994 and Wolff et al., 2010) and only few series addressed the issue of its histopathological features (Wolff et al., 2010) with conflicting results regarding the diagnostic value of skin biopsies (Rym et al., 2005). 1
14 Introduction and Aim of work The main difficulty in diagnosis of erythroderma is distinguishing benign (inflammatory) from malignant cases (mainly cutaneous T cell lymphoma) with overlapping histopathological features. As a result, recent immunohistochemical studies focus on the expression of the T cell markers, where neoplastic cells have aberrant expression of various T-cell markers compared with normal cells (Nagler et al., 2011). According to Vonderheid (2006), malignant T cells show: loss of pan-t cell markers defined as loss of CD2, CD3 or CD5 expression on more than 50% of T cells of the infiltrate in skin biopsies of erythrodermic patients. Also they show a CD4:CD8 ratio greater than 10 and a CD4+CD7- ratio of at least 40 %. All these criteria are helpful rather than definitive tools in the diagnosis of erythrodermic cutaneous T cell lymphoma (Nagler et al., 2011). Another tool for diagnosis is T cell receptor rearrangement, where PCR evidence of a T-cell clone in a skin biopsy that is otherwise nonspecific (non-diagnostic histology and absence of an aberrant immunophenotype) strongly suggests the diagnosis of CTCL in an erythrodermic patient, and if an identical clone is also present in the blood, the diagnosis can be rendered with certainty (Nagler et al., 2011). Aim of work To evaluate cases of erythroderma as regards clinical presentation, histopathological features as well as immunohistochemical expression of the following T cell markers: CD4, CD8, CD2, CD5 and CD7, in order to sum-up a constellation of findings that help in differentiating inflammatory from lymphomatous causes. 2
15 REVIEW OF LITERATURE
16 Chapter 1 ERYTHRODERMA
17 Review of literature Erythroderma Chapter 1 Erythroderma Erythroderma/exfoliative dermatitis is an extreme state of skin irritation resulting in extensive erythema and/or scaling (Sehgal et al., 2004). It is a serious disorder, mainly because of its metabolic burden and complications. It may be the morphologic presentation of a variety of cutaneous and systemic diseases and a thorough workup is essential to elicit possible etiological factors. Accordingly, management of erythroderma continues to be a challenge and the prognosis is determined mainly by the underlying cause (Okoduwa et al., 2009). Definition: Erythroderma refers to a generalized or nearly generalized sustained erythema of the skin, involving more than 90% of the body surface accompanied by a variable degree of scaling (Khaled et al., 2010). Involvement of 70-90% of body surface area is known as subtotal erythroderma (Nick, 2009). Although erythroderma and exfoliative dermatitis are largely synonymous; erythroderma is the preferred term and is currently in vogue. Exfoliative dermatitis emphasizes mainly marked scaling, where in some cases the scaling or erythema might be just perceptible (Sehgal et al., 2004). Historical classifications: In 1868, Hebra proposed a classification based on clinical features: Hebra's pityriasis rubra, Brock's exfoliative dermatitis, scarlatiniform erythema and epidermal exfoliative dermatitis (Vasconcellos et al., 1995). 3
18 Review of literature Erythroderma However, the historic classification of exfoliative dermatitis into Wilson- Brocq (chronic process associated with exacerbation and remissions), Hebra or pityriasis rubra (relentlessly progressive disease) and Savill (self-limiting) types, lacks any clinical significance (Umar, 2009). In 1913, Nicolis and Helwig, after studying 135 patients with erythroderma, proposed a classification based on etiology: drug related (40%), previous dermatosis related (26.8%), mycosis fungoides and lymphoma related (17.8%), internal malignancy related (2.8%), miscellaneous etiology (0.7%) and unknown etiology (11.9%) (Vasconcellos et al., 1995). In 1933, Montgomery established another classification based on histopathologic findings: idiopathic or primary and secondary to an underlying dermatosis or reticulosis (Vasconcellos et al., 1995). The term red man syndrome is reserved for idiopathic erythroderma in which no primary cause can be found, despite serial examinations and tests. The term l'homme rouge refers to erythroderma that is secondary to cutaneous T-cell lymphoma (Umar, 2009). Incidence: It is hard to obtain a precise incidence for erythroderma as most reports are retrospective, and do not address the issue of overall incidence (Karakayli et al., 1999). This aspect was dealt with for the first time by Sehgal and Srivastava in 2004 in a large prospective study from the Indian subcontinent, where the incidence was recorded as 35 per 100,000 dermatologic outpatients. In another survey from The Netherlands (Sigurdsson et al., 2001), the annual incidence was recorded as 0.9 per 100,000 inhabitants. In a study based on an analysis of 138 consecutive 4
19 Review of literature Erythroderma erythroderma patients from South Africa, Morar in 2001 found that 75% were black, 22.5% Indian and 2.5% white. In addition, a large number of patients were HIV positive, in which a drug reaction was the most common cause of erythroderma. Males are affected 2 3 times more frequently, with an average male to female ratio of 2:1 to 4:1 (Fig.1) as reported in different studies (Sterry and Assaf, 2008). The age incidence is usually variable, and any age group may be affected; however, affected patients are usually over 45 years of age (excluding hereditary disorders/atopic dermatitis), with an average age of onset at 55 years (Fig.1) (Sehgal et al., 2004; Khaled et al.,2010). Erythroderma in children has a mean age of onset of 3.3 years, with a male to female ratio of 0.89: 1.18 (Sehgal et al., 2004). Fig.1: Graph presentation of age and sex distribution of erythroderma (Kondo et al., 2006). 5
20 Review of literature Erythroderma Most of the published series originate from Western countries. A few prospective studies have been carried out in Asia, and till 2005 there was only one report from Africa, conducted in Dakar by Ndiaye and colleagues in 1979, followed by few studies mainly in Tunisia (Rym et al., 2005 and Khaled et al., 2010). In addition to the paucity of information on erythroderma in Africa, other factors exacerbate the life-threatening nature of this condition including: the growing increase in use of herbal medicines, the HIV epidemic, hospital visits in advanced disease stages and limited investigational resources in Third World environments (Okoduwa et al., 2009). Causes : Erythroderma is not a skin disease but a clinical syndrome that can be due to many different causes. A major challenge lies in establishing its underlying cause (Rothe et al., 2005 and Nick, 2009) (Table 1). Several studies were conducted to identify the incidence of its different causes (Khaled et al., 2010) (Table 2). 6
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