Frequency of disease subsets and patterns of organ involvement among Egyptian scleroderma patients
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1 Frequency of disease subsets and patterns of organ involvement among Egyptian scleroderma patients THESIS Submitted for fulfillment of Master Degree in Rheumatology and Rehabilitation PRESENTED BY Shaimaa Ra'fat Ahmad M.B, B.Ch. Cairo University SUPERVISED BY Prof. Dr. Geilan Abd El-Moneim Mahmoud Professor of Rheumatology and Rehabilitation Faculty of Medicine Cairo University Assistant Prof. Dr. Hanan El Sayed Ali Darweesh Assistant Professor of Rheumatology and Rehabilitation Faculty of Medicine Cairo University Dr. Mervat Ismael Abd EL Azeem Lecturer of Rheumatology and Rehabilitation Faculty of Medicine Bani Swief University Faculty of Medicine Cairo University (2012)
2 Acknowledgement First of all, I thank "ALLAH" the most merciful and the most graceful. I would like to show my deepest thanks, appreciation and gratitude to Dr. Geilan Abd El-Moneim for her utmost support, complete understanding and continuous encouragement, which helped accomplishing the work in the best way possible. Working with her was a true honor and it added a lot to my scientific knowledge and way of thinking. I would also like to thank Dr. Hanan Darweesh for her outstanding efforts, accurate assessment and scientific guidance. I truly appreciate her patience in answering all my questions. I would like to thank Dr. Mervat Ismael Abd EL Azeem for her support, accurate assessment and scientific guidance. She dedicated a lot of time and effort to this thesis. I would like to express my special gratitude to my family for their love, encouragement and support. Last, but not least, I would like to thank my professors, friends and colleagues. Shaimaa Ra'fat
3 Abstract Background: Systemic Sclerosis (SSc) is an autoimmune connective tissue disease of unknown etiology characterized by abnormalities of vasculature, immune system, and extracellular matrix that lead to fibrosis of the skin and internal organs (lungs, gastrointestinal tract, heart, and kidneys). The disease has a female predilection and typically occurs in the third to fifth decades of life. The clinical expression, severity and progression are rather heterogeneous; the disease may progress very slowly with no or mild visceral injury, whereas sometimes it dramatically evolves with early severe organ damage. Aim of work: The aim of this study is to determine the disease patterns and manifestations of organ involvement among Egyptian scleroderma patients. Patients and methods: A retrospective study including 75 patients with systemic sclerosis who fulfilled the criteria for scleroderma described by the subcommittee For Scleroderma Criteria of the American College of Rheumatology (1980), they were following up in Rheumatology departments in Kasr al Ainy and Bani swief university hospital. Their ages ranged from 17 to 70 years with a mean age of years old. Results: Our study found that Systemic sclerosis is more common in females with a male : female ratio of 1 : 4.3. Limited scleroderma subtype was found to be more frequent than the diffuse subtype with a ratio of 4.3:1. The commonest first presenting manifestation was Raynaud s phenomenon in 77.3%. Regarding frequency of organ involvement it was as follows: Raynaud's reported in 97.3%, digital ischemia in74.6%, dysphagia in 68%, interstitial lung disease (ILD) in 53.3%,arthritis in 40%, esophageal reflux in 38.7%, hypopigmentation in 22.7%, myositis in 20%, pulmonary hypertension (P HTN) in 14.7%, dysmotility in 10.7%, proteinuria in 6.7% and pericardial effusion in 5.3% of the patients. Diffuse disease subset was found to be associated with significantly higher frequencies of ILD, P HTN and dysmotility. Conclusion: among Egyptians, systemic sclerosis is more common in females; limited systemic sclerosis is more common than diffuse systemic sclerosis. Significant difference in the frequency of organ involvement between limited and diffuse subtypes was found in ILD, P HTN, intestinal dysmotility and proteinuria. No significant difference in the frequency of organ involvement between males and females was found. These data should facilitate research regarding the role of geographic, ethnic, racial, and environmental factors for this disease in comparing populations. Keywords: Systemic sclerosis Limited cutaneous systemic sclerosis Diffuse cutaneous systemic sclerosis Males Females Interstitial lung disease Pulmonary hypertension.
4 List of contents Acknowledgment List of abbreviations List of figures List of tables Abstract Introduction & aim of work Review of literature.. Chapter (1): Scleroderma Chapter (2): Outcome measures, prognostic factors and mortality in patients with systemic sclerosis Patients & methods.. Results.. Discussion. Summary & conclusion... References. Arabic summary... Page
5 List of abbreviations ACAs: anti-centromere antibodies. ACE: angiotensin converting enzyme. ACE: angiotensin-converting enzyme ACR: American college of rheumatology. ARAs: anti-rna polymerase III antibodies. ASE: appearance self esteem. ATAs: anti-topoisomerase antibodies. ATP: Adenosine triphosphate BAL: Bronchoalveolar lavage. BAL: bronchioalveolar lavage. BAL: bronchoalveolar lavage. bfgf: basic fibroblast growth factor. bfgf: Basic fibroblast growth factor BMI: Body mass index. BNP: brain natriuretic peptide. BNP: brain natriuretic peptide. c-abl: Abelson kinase. CC: chemokines. CCL: chemokine ligand. cgmp: Cyclic guanosine monophosphate CHF: congestive heart failure. CTD: connective tissue disease. CTGF: connective tissue growth factor. CTGF: connective tissue growth factor. CYC: cyclophosphamide. dcssc: Diffuse cutaneous systemic sclerosis. DLCO: diffusing capacity for carbon monoxide. DNA: Deoxyribonucleic acid DP: D-penicillamin. EC: endothelial cell. ECG: electrocardiogram. ECM: extracellular matrix. ECM: extracellular matrix. EMG: Electromyography. epap: estimated pulmonary arterial pressure. ESR: erythrocyte sedimentation rate. ET: Endothelin. EULAR: European League Against Rheumatism FDA: Food and Drug Administration FS: functional score.
6 FTP: finger-to-palm. FVC: forced vital capacity. FVC: forced vital capacity. GAVE: gastric antral vascular ectasia. GENISOS: genetics versus environment in scleroderma outcome study. GFR: glomerular filtration rate. GIT: gastrointestinal tract. GIT: gastrointestinal tract. GVH: graft-versus-host. HAQ-DI: health assessment questionnaire disability index. HDAC: histone deacetylases. HIF: hypoxia-inducible factor. HLA: human leukocyte antigen HRCT: High resolution computed tomography. HRQOL: health-related quality of life. HSCT: hematopoietic stem cell transplantation. Hx: history. ICAM: intercellular adhesion molecule IFN: interferon: IFN-γ: Gamma interferon. IL: interleukin. ILD: interstitial lung disease. IPAH: idiopathic pulmonary arterial hypertension. lcssc: Limited cutaneous systemic sclerosis. LDH: lactate dehydrogenase. lssc: limited systemic sclerosis. LT: Lung transplantation. LVEF: left ventricular ejection fraction. MCP: metacarpo- phalangeal (joint). MDRD: modification of diet in renal disease. MHC: major histocompatability. MMF: Mycophenolate mofetil. MMP: matrix metalloproteinase. mpap: mean pulmonary artery pressure. MRI: magnetic resonance image. mrrs: modified Rodnan skin score. NK: Natural killer. NVC: nailfold video capillaroscopy. PAH: pulmonary arterial hypertension. PAP: pulmonary artery pressure. PDE: phosphodiesterase PDGF: platelet-derived growth factor.
7 PDGF: platelet-derived growth factor. PDGF: platelet-derived growth factor. PDGFR: Platelet Derived Growth Factor Receptor PFT: pulmonary function test. PH: pulmonary hypertension. P HTN: pulmonary hypertension. PVOD: pulmonary vascular occlusive disease. PVR: pulmonary vascular resistance RA: rheumatoid arthritis. RCT: randomized controlled trial. RF: rheumatoid factor. RNA: Ribonucleic acid RP: Raynaud s phenomenon. SF-36: Short Form 36. SMA: smooth muscle actin. SMRs: standardized mortality ratios. spap: systolic pulmonary artery pressure. SPECT: single photon emission computed tomography. SRC: scleroderma renal crisis. SSc: Systemic sclerosis. ssssc: Systemic sclerosis sine scleroderma. T reg: regulatory T (cell). TGF: transforming growth factor. Th: T helper (cell). TNF: tumor necrosis factor. US: Ultrasound. VAS: visual analogue scale. VCAM: Vascular cell Adhesion Molecule VEGF: vascular endothelial growth factor. WHO: World Health Organization. 6MWD: 6 minute walk distance.
8 List of Figures: PAGE (Fig 1): Schematic diagram of the involvement of different cell types in the pathogenesis of SS... (Fig 2): Cellular interactions in pathogenesis of SSc... (Fig 3): Calcinosis and acrolysis (Fig 4): Nailfold capillaroscopy... (Fig 5): Magnetic resonance arteriography image of the hand of a patient with systemic sclerosis (Fig 6): Plain X ray chest showing Pulmonary fibrosis.. (Fig 7): Prone axial HRCT scan from an SSc patient. (Fig 8): Endoscopic appearance of long-segment Barrett's oesophagus.. (Fig 9): Gastric antral vascular ectasias (Watermelon stomach). (Fig 10): Intestinal diverticulosis. (Fig 11): Images showing secondary criteria in the hands of different patients with systemic sclerosis. (Fig 12): The mrss for quantitative assessment of skin sclerosis (Fig 13): Histogram sowing the frequency of organ involvement in limited and diffuse systemic sclerosis subtype groups.. (Fig 14): Histogram sowing the frequency of organ involvement in male and female groups
9 List of Tables Table 1: European Scleroderma Trials and Research group (EUSTAR) Systemic Sclerosis Activity Score... Table 2: Core set items selected for 11 domains. PAGE Table 3: Medsger scleroderma severity scale Table 4: Aassociation between specific autoantibodies and clinical features in SSc patients. Table 5: Demographic data of all patients included in our study. Table 6: Comparison between lcssc and dcssc regarding to duration, age of onset and age.. Table 7: Difference in age, age at disease onset and disease duration between males and females within disease subsets... Table 8: First presenting manifestations and their frequencies.. Table 9: Comparison of the frequency of the first presenting symptom within limited and diffuse groups.. Table 10: First presenting manifestation in males and females Table 11: Frequency of the two disease subsets Table 12: Frequency of males and females within subsets Table 13: Frequency of organ involvement in limited and diffuse subtypes.. Table 14: Frequency of organ involvement in male and female groups... Table 15: Medications
10 Introduction & Aim of the work Introduction Systemic Sclerosis (SSc) is an autoimmune connective tissue disease of unknown etiology characterized by abnormalities of vasculature, immune system, and extracellular matrix that lead to fibrosis of the skin and internal organs (lungs, gastrointestinal tract, heart, and kidneys) (Rossi et al., 2010). The disease has a female predilection with female: male ratio of 3:1 and typically occurs in the third to fifth decades of life (Strollo and Goldin, 2010). Vascular injury and endothelial activation are among the earliest and potentially primary events in the pathogenesis of SSc (Abraham and Distler, 2007). SSc is an important disease with significant mortality, causing significant disability, at times quickly and dramatically, especially in patients with diffuse cutaneous SSc (Matucci-Cerinic et al., 2009). The clinical expression, severity and progression are rather heterogeneous; the disease may progress very slowly with no or mild visceral injury, whereas sometimes it dramatically evolves with early severe organ damage (Steen and Medsger, 2000). The obvious first aim of disease classification into subsets is to distinguish disease from non-disease. Such subsets could possibly reflect differences in pathogenesis (Wollheim, 2005). Predicting outcome early in the course of the disease is critical in deciding on the appropriate treatment, but is not yet sufficiently reliable in many patients (Walker et al., 2007). 1
11 Introduction & Aim of the work LeRoy et al., 1988 subdivided scleroderma into limited and diffuse cutaneous scleroderma (lcssc and dcssc respectively). This was based on a number of clinical characteristics rather than on distinct criteria. This simple system has been widely accepted. However, a number of SSc patients do not fit into the simple scheme. 2
12 Introduction & Aim of the work Aim of work The aim of our study is to determine the disease patterns and manifestations of organ involvement among scleroderma patients presented to our department. 3
13 Chapter (1): SCLERODERMA Scleroderma Definition Scleroderma (from the Greek words "skleros" meaning hardness, and "derma" meaning skin, literally means hard skin), is a chronic multi system autoimmune disease that is highly heterogeneous and has multiple overlapping and poorly defined clinical subsets. The prominent features of the disease reflect the characteristic pathophysiologic triad of vascular, immunological, and fibrotic processes, which contribute to clinical manifestations and morbidity and must be addressed in the treatment plan (Varga, 2008). It is a clinically heterogeneous disease ranging from a milder form with less extensive involvement of the internal organs to a more severe type with widespread internal organ involvement, characterized by rapid progression and resulting in disability and death within several years (Assassi et al., 2009). Epidemiology The relative rarity and clinical heterogeneity of Systemic sclerosis (SSc) have made formal epidemiological studies difficult. The estimated prevalence from population based studies is between 1 and 2 per 10,000 population, with a higher estimated prevalence in North America. Reliable estimates of incidence are also elusive, but 1 in 100,000 per year is considered reasonably accurate. There appear to be two peaks of 4
14 Chapter (1): SCLERODERMA disease onset the early 30s and mid 50s and, in common with most other autoimmune diseases, there is a female predominance (Derrett- Smith and Denton, 2010). Diagnostic criteria & Classification Criteria of the American College of Rheumatology (ACR) for classification of scleroderma: The American College of Rheumatology (former American Rheumatism Association - ARA) has defined criteria that are 97 % sensitive and 98 % specific for systemic sclerosis (SSc) as follows: Major criterion: Proximal diffuse (truncal) sclerosis (skin tightness, thickening, non-pitting induration) Minor criteria: Sclerodactyly (only fingers and/or toes) Digital pitting scars or loss of substance of the digital finger pads (pulp loss) Bilateral basilar pulmonary fibrosis The patient should fulfil the major criterion or two of the three minor criteria (ARA, 1980). On 2001 LeRoy and Medsger proposed criteria for limited forms of SSc (lssc) which are: Raynaud s phenomenon (RP), objectively documented Plus 5
15 Chapter (1): SCLERODERMA *Abnormal nailfold capillaroscopy (consisting of dilatation and/or avascular areas). Or *SSc selective autoantibodies (anticentromere, antitopoisomerase I, antifibrillarin, anti-pm-scl, anti-fibrillin or anti-rna polymerase I or III in a titer of 1:100 or higher). If RP is subjective only, both SSc capillary pattern and SSc selective autoantibodies (in titre >1:100) are required to define lssc. lssc can overlap with other disease (LeRoy and Medsger., 2001). The group of diseases called scleroderma falls into two main classes: localized scleroderma and systemic sclerosis. Both groups are furtherly divided in to subgroups. The following is a common way of classifying these diseases: (LeRoy et al., 1988) Localized Scleroderma (Localized cutaneous fibrosis) Limited or generalized morphea: Circumscribed patches of sclerosis. Linear scleroderma: Linear lesions seen in childhood. En coup de sabre: Linear lesions of the scalp or face. Systemic Sclerosis (Cutaneous and noncutaneous involvement) Limited cutaneous systemic sclerosis (lcssc), formerly called CREST syndrome (calcinosis of the digits, Raynaud's phenomenon, esophageal dysmotility, sclerodactyly, and telangiectasias) Diffuse cutaneous systemic sclerosis (dcssc): Sclerosis of proximal extremities, trunk, and face 6
16 Chapter (1): SCLERODERMA Systemic sclerosis sine scleroderma (ssssc): Organ fibrosis only; no skin thickening. Diffuse Cutaneous Systemic Sclerosis (dcssc) Onset of Raynaud's within 1 year of onset of skin changes. Truncal and acral skin involvement. Presence of tendon friction rubs. Early and significant incidence of interstitial lung disease, oliguric renal failure, diffuse gastrointestinal disease, and myocardial involvement. Absence of anticentromere antibodies. Nailfold capillary dilation and capillary destruction. Antitopoisomerase antibodies (30% of patients). Limited Cutaneous Systemic Sclerosis (LcSSc) Raynaud's phenomenon for years (occasionally decades). Skin involvement limited to hands, face, feet, and forearms (acral). A significant late incidence of pulmonary hypertension, with or without interstitial lung disease, trigeminal neuralgia, skin calcifications, telangiectasias. A high incidence of anticentromere antibodies (70%-80%). Dilated nailfold capillary loops, usually without capillary dropout. 7
17 Chapter (1): SCLERODERMA Pathogenesis Systemic sclerosis (SSc) is a complex autoimmune disease characterized by an excessive deposition of matrix molecules, leading to fibrosis of multiple organs including the skin, lungs, heart and gastrointestinal tract, and often leading to severe morbidity and premature death (Radstake et al., 2009). The precise aetiology of systemic sclerosis (SSc) remains elusive, but significant advances over the past years have improved the understanding of the underlying pathogenic processes and identified key pathways and mediators that are potential therapeutic targets but The situation is complicated by the clinical heterogeneity of SSc and the differential pathogenesis that underlies the two commonest subsets, namely diffuse and limited cutaneous disease. However, there are common mediators that could be targeted to provide clinical benefit in both types of disease (Denton, 2007). It is clear from studies of lesional skin in SSc that there is a common sequence of pathogenic events. This sequence starts with microvascular change, including endothelial cell activation, which is followed by inflammation and immune cell activation, with a perivascular infiltration of inflammatory cells initially from the innate immune system and including cells of the monocyte/macrophage lineage. Later, there is evidence of involvement of the adaptive immune system. Lymphocytic infiltrates are noted, including T cells bearing markers of activation. Recent studies have also identified B-cell genetic signature as a hallmark feature of SSc skin. As the disease progresses there is evidence of a profibrotic fibroblastic cell population becoming established within the skin. This leads to increased extracellular matrix deposition. Early studies showed that these profibrotic cells are initially located around blood 8
18 Chapter (1): SCLERODERMA vessels but that later they are more generally distributed. As the disease becomes well established lesional skin becomes relatively avascular, and after 12 to 18 months there is often little evidence of ongoing inflammation. This suggests that there are probably distinct phases, at least in the skin, when the component processes of SSc might be amenable to therapeutic modulation (Denton et al., 2006 "a"). Immunological basis of systemic sclerosis The pathogenesis of SSc is complex and, although progress in the understanding of the multiple processes underlying SSc has been made in recent years, no single unifying hypothesis explaining all aspects of this disease exists. Recent studies have suggested that the activation of the immune system is a key stimulus to vascular abnormalities and fibrosis. Once T-cells are activated, they infiltrate the skin lesions early, and produce the profibrotic cytokine IL-4. They are also required for autoantibody production. B-cells may contribute to fibrosis, as deficiency of CD19, a B-cell signal transduction molecule, results in decreased fibrosis in animal models (Zuber and Spertini, 2006). Cellular immunity in SSc: Immune activation is an early event in SSc. However, it is not known whether it is the initiating event or whether it is secondary to other disease processes. Some of the earliest evidences suggesting that chronic and persistent inflammation may play a role in the pathogenesis of SSc were provided by the demonstration of infiltrates of T-cells, macrophages, mast cells and, rarely, B-lymphocytes in affected skin from patients with disease of recent onset (Prescott et al., 1992). 9
19 Chapter (1): SCLERODERMA In fact, inflammation may appear in the skin before any histological evidence of fibrosis. Progressively, as fibrosis increases, the inflammatory infiltrates tend to decrease (Prescott et al., 1992). The mononuclear cells within the skin infiltrates are predominantly CD4 + T-cells (which outnumber CD8 + T-cells) and macrophages. Natural killer (NK) cells are present in reduced number in the skin of patients with SSc. CD4 + T-cells in cutaneous infiltrates are activated, as indicated by the increased proportion of T-cells bearing activation markers such as IL-2 receptor and class II MHC antigen. The data available on the characteristics of T-cells infiltrating organs in patients with SSc are heterogeneous. Most data support a role for pathogenic T-cells from tissues undergoing fibrosis in SSc by outlining the preferential production of IL-4, a Th2 cytokine (Sakkas and Platsoucas, 2004). IL-4 and transforming growth factor β (TGF-β) are the major fibrogenic cytokines in SSc. IL-4 increases collagen production by fibroblasts in patients with SSc and induces the production of TGF-β. TGF-β stimulates the synthesis of various collagens, proteoglycans and fibronectin, and inhibits extracellular matrix degradation by decreasing the synthesis of matrix metalloproteinases (MMP) and by increasing the synthesis of the tissue inhibitor of MMP. IL-17, a T-cell cytokine that can be produced by both Th1 and Th2 cells, is overexpressed in peripheral blood and skin of patients with SSc. It enhances the proliferation of fibroblasts, promotes macrophage production of TNF-α and IL-1 (which in turn induces fibroblast production of collagen, IL-6 and platelet-derived growth factor [PDGF]), and induces endothelial cell production of IL-1, IL-6 and adhesion molecules ICAM-1 and VCAM-1 (Kurosawa et al., 2000). Most authors consider that Th2 cells (producing IL-4) stimulates collagen synthesis and Th1 cells (producing IFN-γ) inhibits collagen synthesis, but 10
20 Chapter (1): SCLERODERMA in contrast, other authors report that Th2 cells can reduce type I collagen synthesis by dermal fibroblasts (Chizzolini et al., 2003), and that an increased percentage of IFN-γ positive cells can be observed in peripheral T-cells from SSc patients (Valentini et al., 2001). Therefore, it is possible that Th1 cytokines, in addition to Th2 cytokines, also play a role in the development of SSc. Other cytokines that are at increased levels in the sera and tissues of patients with SSc include IL-1, IL-6 and connective tissue growth factor (CTGF). All these mediators are implicated in the pathogenesis of SSc and affect fibroblasts, endothelial cells and macrophages (Fig. 1). Expansion of CD4 + T-cells within the tissue appears to be oligoclonal, as shown in studies of T-cell receptor transcripts in the skin of patients with SSc (Sakkas et al., 2002). These results suggest an antigen-driven T-cell response, although at present the putative antigen or antigens that may be involved are not known. T-cells may induce fibrosis through cytokines or through direct contact with fibroblasts. However, whether the alterations observed in T- lymphocytes and various cytokines are secondary to disease activity or reflect a more fundamental pathogenic event is unknown (Zuber and Spertini, 2006). Humoral immunity in SSc: B-cells are activated in SSc, as indicated by hypergammaglobulinaemia, the presence of autoantibodies, the overexpression of the B-cell transduction molecule CD19 in peripheral blood, expanded naive B-cells and activated, but diminished, memory B-cells (Sato et al., 2004). Furthermore, in animal models of fibrosis, deficiency of CD19 results in decreased fibrosis, suggesting that B-cells may also contribute to fibrosis. Activated B-cells are known to produce IL-6 and IL-10, and both these 11
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