Behçet s Syndrome. Yusuf Yazıcı, MD
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1 Behçet s Syndrome Yusuf Yazıcı, MD Assistant Professor of Medicine, NYU School of Medicine Director, Seligman Center for Advanced Therapeutics & Behcet s Syndrome Evaluation, Treatment and Research Center NYU Hospital for Joint Diseases
2 History Hulusi Behçet described (1937) 3 patients with aphthous mouth ulcers genital ulceration hypopyon uveitis All 3 patients studied over 17 years First to describe triple symptom complex German medical journal (Dermatologische Wochenschrift) Prof. Mischner first proposed the name Morbus Behcet at a medical congress in Geneva (1947) 2
3 INTERNATIONAL STUDY GROUP CRITERIA FOR THE DIAGNOSIS (Classification) OF BEHÇET S SYNDROME Oral ulcers (100%) + 2 of the following: a. genital ulcers (80%) b. eye lesions (50%) c. skin lesions (80%) d. pathergy (50%) 3
4 Distribution of Behçet s disease 4
5 Symptoms 5
6 Demographics Mediterranean basin, Korea, Japan Silk road? Very few cases in India Before puberty or after 6 th decade, rare Usual onset 3 rd decade Male: female equal numbers, Worse disease in males 400/100,000 (16 yrs or older) in Turkey 1 3/100,000 in Olmstead County, MN 6
7 BS, not so rare Estimate the prevalence of BS in and around Paris 26% non European descent 7.1/100,000 European 2.4 North African 17.5 Asian 34.6 Similar to rates in original countries Prevalence was similar regardless of age at immigration Possibly primarily has a hereditary basis Capture recapture, likely underestimates Interestingly, Behcet s rates were similar to combined WG, CS and MPA combined, studied by the same group Mahr A, et al. Arthritis Rheum 2008, in press
8 BS in Paris France (/ ) Disease Non European European Overall BS* frican: 35 Asian: 17.5 SuS. African: 5.1 N-Cont. French: PAN MPA WG CSS Total (1,2,3,4) A Mahr et al Arthritis Rheum 2001; A Mahr et al. Arthritis Rheum in print; H Yazici et al Arhritis Rheum in print
9 CLINICAL MANIFESTATIONS
10 Oral ulcers Virtually all patients Frequently first manifestation Minor aphthous ulcers are most common Lips, gingiva, cheeks and tongue Unlike herpes, skin covered part of lips not involved Usually heal in 15 days without scarring Some complain of premenstrual activation Major ulcers Larger, may scar, lasts longer, less common Recurrent aphthous stomatitis (RAS) 20% in population Very rare for RAS to have another clinical finding No HLA B51 association There are no differences among the two ulcers histologically 10
11 Genital ulcers Papules or pustules that ulcerate quickly Punched out appearance Aseptic ones heal in 3 weeks, very likely to get secondary infections In males usually scrotum is involved, scars, and absence of lesions on glans penis is typical All females should have a gynecologic examination, scarring in the right clinical picture is good evidence 11
12 Skin manifestations of BS Papulopustular (acne) lesions (85%) Indistinguishable from acne vulgaris Later decades of life vs. teens Atypical places, arms Acne is androgen dependent, however, androgen levels are normal Increased severity in males? 12
13 Acne and arthritis in BS 44 patients with BS and arthritis 42 patients with BS without arthritis 21 patients with RA 33 healthy controls Acne scores were very significantly higher among BS patients with arthritis E Diri et al Ann Rheum Dis
14 Target organ associations in BS An Analysis of 272 consecutive patients Factor I : oral ulcers + genital ulcers+ erythema nodosum Factor II: superficial vein thrombosis + deep vein thrombosis Factor III: Uveitis Factor IV: acne + arthritis Tunc R, et al J Rheumatol
15 Enthesopathy and BS To test if enthesopathy was increased in the acne/arthritis cluster 35 BS with acne/arthritis 38 BS without arthritis 37 AS 25 RA 25 HC 5 enthesal sites by US Sup/inf poles of patella Tibial tuberosity Hatemi G et al, Arthritis Rheum 2008
16 Hatemi G et al, Arthritis Rheum 2008 Enthesopathy
17 Nodular lesions of BS 60 % of patients 50% e.nodosum like lesions (more common in women) 50% superficial thrombophlebitis (associated with major vessel involvement) Difficult to tell one from the other. 17
18 CNS involvement in BS CNS involvement has a frequency of 4 % in prospective, cross sectional studies. The frequency goes up to 10 % in longer follow up. Peripheral neuropathy is distinctly rare. CNS involvement has two distinct forms: A. Parenchymal disease (80%, bad prognosis) B. Dural sinus thrombi (20%, favourable prognosis) A and B rarely co exist 18
19 CNS disease differential diagnosis Brainstem, diancephelon and pontobulbar regions mainly effected Peripheral neuropathy very rare CNS lesions do not follow a specific vascular pattern Isolated cerebellar disease rare Meningeal symptoms and on ocasion convulsions can be seen Multiple sclerosis, and on occasion sarcoidosis can cause problems 19
20 Behçet s Syndrome vs Multiple Sclerosis MS BS Headache ± +++ Optic neuritis +++ ± Sensory problems +++ ± PV and SC lesions +++ ± Brainstem lesions Small, no upward Large, with upward extension extension Spinal cord lesions Inflammatory CSF ± +++ OCB > 90% ~ 10%
21 Pulmonary Artery Aneurysms Unique complication of BS Diagnosed mainly at postmortem until 1980 the most frequent arterial complication today Strongly associated with venous thrombosis Large proximal branches of pulmonary arteries 21
22 Mortality in PAA Survival rate: 62% at 5 years (new cohort) 70% of the deaths occurred within 1 year following emergence of PAA Hamuryudan V, et al Am J Med
23 BS vs. Crohn s Disease Korman U, et al Abdominal Imaging
24 Pathergy reaction Non specific hyperreactivity to minor trauma Can also be seen in pyoderma gangrenosum Standard technique 20 gauge needle Papule or pustule in 48 hours Induration required More common in Middle East Interestingly PPD is not augmented in BS patients Hatemi G et al. Rheumatology
25 Eye disease in BS Most serious when considering frequency and morbidity Leading cause of non traumatic blindness after DM in Japan, Israel Non granulomatous panuveitis and retinal vasculitis Over all 50% 70% of males <25 yr Frequently present at onset or first 2 3 yrs Rare after 5 years of disease Bilateral in 90% Hypopyon is classical finding in eye disease (20%) Almost always accompanied by severe retinal vasculitis 25
26 26
27 Thrombophilia in BS 1/3 of patients have thrombophlebitis Abundant evidence for functional impairment of the vessel wall; an autoinflammatory endothelitis? Abnormalities in the coagulation cascade? 27
28 DVT DVT in BS is an inflammatory reaction to the endothelium It is a sticky and very hard clot, no trailing tail formation Very rare for it to break off and embolise? Anti coagulation in DVT with BS 28
29 Long term mortality and morbidity of BS: Two decade outcome study 428 (286M / 142F) BS patients registered at CerrahpaşaBS Multidisciplinary Outpatient Clinic between Found to have died: 42(9.8 %) 39M / 3F Could not be reached: 41(9.6 %) 24M /17F) Seyahi E, et al. Medicine (Baltimore)
30 STANDARDIZED MORTALITY RATIOS OF 286 MALE PATIENTS WITH BS STRATIFIED AS TO THE AGE OF ONSET AND EVALUATED AT 7 YEAR INTERVALS YEARS 14 YEARS YEARS
31 Main causes of death among 42 patients Vascular disease: 17 (venous 5) CNS disease: 5 Amyloidosis: 3 Malignancy: 4 Suicide: 2 Misc: 11 PAA Main reason for mortality Frequently associated with thrombi in inferior vena cava and iliac femoral system Presents with hemoptysis, may look similar to PE Anticoagulation contraindicated 31
32 Onset of eye disease in males (54%) % OD (16%) 16 (9%) 8 (4%) 10 (6%) 4 (2%) 5 (3%) 6 (3%) 4 (2%) 2 (1%) Years 32
33 Other manifestations Beginning End OU (%) 345 (100.0) 220 (63.7)* GU (%) 310 (89.9) 90 (26.1)* EN (%) 223 (64.4) 88 (25.5)* Arthritis (%) 140 (40.6) 34 (9.9)* * P=
34 Disease course in BS The disease burden of BS decreases with the passage of time During the disease course the occurrence of all manifestations seem decrease in frequency accept for CNS disease and major vascular pathology. This disease course is unlike what has been reported for RA and SLE. It s biological meaning remains to be understood. 34
35 Differential diagnosis Sacroiliitis and spinal joint involvement are not features of BS Skin lesions do not include psoriasis Urethral discharge is not a feature of BS GI involvement with ileocaecal ulceration and sometimes colonic perforation is distinct 35 from typical IBD
36 Clinical evidence for autoimmunity in BS? Uncommon/not seen in BS: Sjögren s syndrome Association with other autoimmune diseases Raynaud s phenomenon Polyserositis Hemolytic anemia Sun sensitivity No autoantibodies Unique to BS: Pathergy Genital ulcers scrotal Pulmonary artery aneurysms Clinical course 36
37 Autoinflammatory? (FMF as the prototype) Epidemiology - Mediterranean vs. Japan Rare and almost all defined from the West - Children vs. adults Clinical findings Genetic aspects - HLA B51 -Pyrin Response to treatment (colchicine story) Well defined mutations (TNF-receptor, pyrin or CARD/NOD) and transmission Usually a non - abating course 37
38 CAD in Patients with Severe Vascular Disease of BS 24 males Age: 37.5 ± 4.5 yrs. Disease duration: 13.2 ± 3.9 yrs. Smoking: 88% Steroid use: 63% 3/24 (12.5%) had angina pectoris Coronary calcification and stenosis: 3/24 (12.5%) Seyahi-Kural E et al. Rheumatology,
39 Prevalence of carotid artery plaques in male patients vs healthy controls Diseases * n (%) Adjusted** p OR (95%CI) BS (n =162) 31 (19) 1.5 ( ) 0.33 RA (n = 24) 11 (46) 3.5 ( ) AS (n =58) 9 (16) 1.3 ( ) 0.64 HC (n = 83) 10 (12) - - *: Mean age for BS: 40 ±7, RA: 46 ± 7, AS: 39 ± 7, HC: 38 ± 8 years **: Adjusted for age and presence or absence of diabetes mellitus and hypertension Kural-Seyahi et al Ann Rheum Dis,
40 Genetics of Behcet HLA B51? HLA A26 in Japanese and Turkish GWAS IL 10 IL 10 knockout mice intestinal inflammation UC, Crohn s Increasing IL 10 may restore imbalance and control hyperinflmmation Interferon? aplha? IL 23R, shared between Japanese and Turks Also found in spondyloarthritis group AS, IBD, psoriasis Genetic variants don t overlap IL 12RB2 Gul A. Clin Exp Rheumatol 2011
41 Genetic? Environmental? Japanese living in Hawaii Hirohata et al. Hawaii Med J, 1975 Turkish immigrants vs Germans in Berlin NG Papoutsiset al. Clin Exp Rheumatol 2006 Arabs/Druzes vs Jews in Israel I Krause et al. Clin Rheumatol 2007 North African immigrants vs Europeans in Paris A Mahr et al. A Mahr et al. Arthritis Rheum,
42 Treatment 42
43 Systematic literature search: 2402 articles Exclusions: Duplications Review articles Editorials Case reports Studies where the results for BD was not given separately 137 articles 20 randomized controlled trials 43
44 Colchicine in BS 44
45 Corticosteroids 45
46 Corticosteroids in BS (Skin Mucosa Manifestations) 46
47 Azathioprine in BS (I) Prevents emergence of eye disease in the unaffected (p < 0.01) Prevents eye disease becoming bilateral (p < 0.001) Prevents eye disease getting severe (thus leading to withdrawal from the study) among the affected (p < 0.001) Less frequent attacks of hypopyon (p < 0.001) Preserves vision Yazici H, et al New Engl J Med
48 Azathioprine in BS (II) Less frequent oral ulcers (p<0.005) Less frequent genital ulcers (p<0.001) Less frequent arthritis (p<0.02) Less frequent thrombophlebitis (p<0.10>0.05) Yazici H, et al New Engl J Med
49 Azathioprine in BS (III) Reassesment after 8 years Total loss of vision more in those initially allocated to placebo (p = 0.02) Beneficial effects on visual acuity mainly among those who had been allocated to azathioprine within 2 years of onset of eye disease (p = 0.05 and 0.07 for either eye) A trend for less frequent extraocular manifestations among the groups that received azathioprine Hamuryudan V, et al Arhtritis Rheum
50 Azathioprine in BS (IV) Data avaliable had been for the 2.5 mg /kg/day dose! Onset of action is slow (> 3 months) Leukopenia with azathioprine + interferon 50
51 Interferon α in BS Effective in controlling oro-genital ulceration Alpsoy E et al Arch Dermatol 2002 Most probably effective in controlling acute eye disease (eyes improved in 5/6 patients in the Alpsoy study) In the retracted paper the significant effects were seen only after the drug was stopped. IFN alpha and corticosteroids 45 pt since 1988 Mean treatment duration 30m 26/79 (of 90 eyes) had recurrance Krause L et al. J Rheum 2008 The time of onset of effect? Concurrent administration with immunosuppresives? Problems: Flu like illness, leucopenia, psoriasis, autoimmune disease, hair loss, itching and depresion 51
52 Effect of etanercept on mucocutaneous manifestations of BS 40 males with mainly mucocutaneous BS were randomised to receive either etanercept (25 mg sc. 2x/wk) or placebo for 4 weeks. Weekly assessments were made as well as a 3 month evaluation after the trial ended. Pathergy reaction and the dermal response to MSU crystals were also measured before and after the trial. Melikoğlu M et al. J Rheumatol,
53 Effect of etanercept on mucocutaneous manifestations of BS There was 40% chance of remaining oral ulcer (OU) free in the etanercept arm versus 5% in the placebo arm (p log =0.002) at the end of 4 weeks. There were also significant decreases in the number OU, nodular lesions, acne lesions and arthritis with the expected exacerbations at 3 months after the trial ended. No effect on the pathergy reactions. Melikoğlu M, et al J Rheumatol
54 Infliximab for severe and treatment resistant uveitis of BS 4 studies (open): Fast (<24 hours) onset of action Complete (attack free) remission: 31 75% Infusions need to be continued for sustained remission Ohno S et al J Rheumatol 2004 Sfikakis P et al. Ann Intern Med 2004 Lindstedt EW et al. Br J Ophthalmol 2005 Tugal Tutkun I et al. Arthritis Rheum
55 Infliximab Active uveitis despite treatment Azathioprine, steroids, cyclosporine Infliximab treatment for 13 patients All male, all bilateral uveitis Weeks 0 22=infusion period Weeks 23 54=observation period Tugal-Tutkun I e al Arthritis Rheum Aug;52(8):
56 Infliximab 56
57 Hatemi G, et al. EULAR 2013 Apremilast
58 OU % Percent % 70.9% 50.0% Placebo 30 mg BID Complete Response Partial Response
59 OU time to response Mean Number of Oral Ulcers All patients in the PBO group switched to APR from week 12 visit wk0 wk2 wk4 wk6 wk8 wk10 wk12 wk14 wk16 wk18 wk20 wk22 wk24 wk26 wk28 Placebo mg BID
60 OU Pain over time 60.0 Mean Oral Ulcer Pain VAS wk0 wk2 wk4 wk6 wk8 wk10 wk12 wk14 wk16 wk18 wk20 wk22 wk24 wk26 wk28 Placebo mg BID
61
62
63 EULAR Guidelines Ann Rheum Dis 2008 Inflammatory eye disease with posterior segment involvement should be on azathioprine+corticosteroids Severe eye disease, retinal disease Cyclosporine or infliximab added Interferon alpha No firm guidelines for major vascular disease DVT= immunosupression PAA and peripheral aneurysm= CYC+corticosteroids No data about use of anticoagulants, anti platelet agents but not recommended No evidence base for GI treatment Immunosupression, TNF In most patients, arthritis can be managed with colchicine 63
64 EULAR guidelines (2) No data on CNS disease management AZA, CYC preferred, IFN alpha, TNF inhibitors Cyclosporine should not be used in CNS, unless needed for eye inflammation Mucocutaneous lesions, systemic treatment if resistant to topical measures 64
65 Management in 2013 Consider natural course, age, sex Steroids: not for long term use Colchicine: arthritis (M+F) e. nodosum (M+F) genital lesions among the females Thalidomide: Good for all mucocutaneous lesions toxicity precludes long term use Azathioprine slow acting, usually under dosed Cyclosporine fastest acting agent for eye disease; CNS toxicity? Interferon: masked studies in eye disease needed TNF inhibitors Quick response, use in combination Plaquenil, MTX, Cellcept,... No anticoagulation for thrombophilia 65
66 What have we learned? We have agents that can rather satisfactorily control the eye, skin mucosa, arthritis and, to some extent, major vascular problems of Behçet s syndrome patients. Earlier treatment is better. Females not only have less severe disease but respond better to treatment.
67 What have we not learned? How to manage CNS disease, thrombophilia and GI disease Whether there is a subset of patients that respond to colchicine Comparative efficacy (including time of onset of action)/safety of cyclosporin, interferon and a TNF agents in controlling eye disease Role of high dose corticosteroids in disease control Role of other biologicals Prophylactic drug use (the young male) How long to continue treatment
68 NYU HJD Behçet s Syndrome Evaluation, Treatment and Research Center Started in 2005 ~700 patient seen ABDA RCT 68
69 Methods Patients were analyzed as the whole cohort and then also separated into to 2 groups: Non Ethnic= Patients with ethnic background in northern Europe and North America and /or self declared Caucasians without background around the Mediterranean and/or the Far East Ethnic= Patients with an ethnic background in the Mediterranean, Middle East, North Africa, and Far East. Israel 42, Italy 42, Arabic 23, Far East 23, Turkish 18, G k9
70 Demographics Total of 471 (female 365, 77%) 296 meet ISBD criteria (63%) 237 (80% female) Non ethnic: 163 (55%) Ethnic: 133 (45%) Caucasian: 240 (81%), Hispanic 24(8%), Asian 13 (4%), other 11 (4%), African American 10 (3%) Patients from 45 states
71 Demographics (3) Non Ethnic Ethnic Total N Mean SD N Mean SD N Mean SD p Age (Years) Female (%) % % % Married (%) % % % Duration (Years) Symptom Duration (Years) Education (Years) Function [0 10] Pain [0 10] Global [0 10] Fatigue [0 10] RAPID3 [0 30] BSAS [0 100] Adjusted Critical Value p=0.025
72 Symptoms Non Ethnic (N=163) Ethnic (N=133) Total (N=296) Symptom N % Positive N % Positive N % Positive p Oral ulcers % % %. Genital ulcers % % % Skin lesions % % % Eye disease % % % uveitis % % % retinitis 3 1.8% 5 3.8% 8 2.7% episcleritis 5 3.1% 6 4.5% % other % % % DVT 9 5.5% 7 5.3% % CNS % % % Vascular 4 2.5% 8 6.0% % Pulmonary 5 3.1% 0 0.0% 5 1.7% Arthritis % % % GI % % % ulcerations % % % blood % 9 6.8% % diarrhea % % % biopsy 5 3.1% 6 4.5% % Thrombophlebitis 3 1.8% 3 2.3% 6 2.0% Headache % % % Epididymitis 2 1.2% 2 1.5% 4 1.4% HLA B51 (Done = 114) % % % Pathergy (Done = 130) % % % Adjusted Critical Value p=0.005
73 266 US vs 93 JPN BS patients
74 Treatment Significantly more patients had been treated with azathioprine, methotrexate, and TNF inhibitors among US patients Significantly more patients in JPN received sulfasalazine, and Differences were noted for colchicine, corticosteroids, or cyclosporine use among cohorts.
75 BSAS BSAS consists of 10 questions, each scored Patient reported measures VAS for patient s level of discomfort oral ulcers, genital ulcers, skin lesions or acne, and current disease activity. The BSAS also categorizes the number of oral ulcers, genital ulcers, and acne lesions present, and records if there is GI involvement, vascular involvement, or eye involvement.
76 Table 1 Pearson correlations between the measures BSAS BDCAF QoL r p r p r p BDCAF < QoL < MD Global <
77 MDHAQ in Behcet s
78 MDHAQ in Behcet s
79 Current studies Apremilast OU, double blind, placebo controlled Xoma IL 1 NIH Abatacept OU, open label Tocilizumab OU, double blind, placebo controlled Neurology NYU HJD and NIH Functional imaging
80 Conclusions BS is not very rare. It has distinct features from connective tissue diseases Disease clusters In many patients it is a mild disease which can also go away by itself. We can successfully manage a substantial majority of the remaining patients. CNS disease and thrombophilia are still problems. We are doing considerably better now than did 20 years ago 80
81 Thank you Hasan Yazici, MD Maria Filopoulos Thalia Gooden, DO Pamela Sharaf Monalyn De Los Reyes Labitigan, MD Chelsey Forbess, MD Nicole Moses, MD Johannes Nowatzky, MD Hui Zhan Ranit Shriky
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