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Journal of Rheumatic Diseases Vol. 19, No. 4, August, 2012 http://dx.doi.org/10.4078/jrd.2012.19.4.225 Case Report Etanercept 를포함한스테로이드, Cyclosporine A 병용요법으로호전된대식세포활성증후군 1 예 심영석 1 ㆍ김현수 2 ㆍ김광남 1 한림대학교의과대학한림대학교의료원소아과학교실 1, 진단검사의학교실 2 A Case of Macropharge Activation Syndrome Successfully Treated with Combination Therapy Including Etanercept Young Seok Shim 1, Hyun Soo Kim 2, Kwang Nam Kim 1 Departments of Pediatrics 1, Laboratory Medicine 2, Hallym University Medical Center, Hallym University College of Medicine, Seoul, Korea Macrophage activation syndrome (MAS) is a severe, potentially life-threatening complication of childhood systemic inflammatory disorder, primarily systemic onset juvenile rheumatoid arthritis (SoJRA). It is characterized by pancytopenia, liver insufficiency, coagulopathy, and neurologic symptoms. The clinical manifestations are caused by the activation and uncontrolled proliferation of T lymphocytes and macrophages, leading to cytokine overproduction including tumor necrosis factor-α (TNF-α). Methylprednisolone pulse therapy and cyclosporine A have made a considerable progress in the treatment of MAS. However, the mortality rate remains high suggesting the need of another therapeutic agent. Several cases of MAS successfully treated with TNF-α inhibitor (etanercept) have been reported. We report the first Korean case of MAS successfully treated with combination therapy of corticosteroid, cyclosporine A and etanercept. Key Words. Macrophage activation syndrome (MAS), Etanercept 서론대식세포활성증후군 (Macropharge activation syndrome, MAS) 은대식세포가정상조절상태를벗어나과량으로활성되고증식되어나타나는임상증후군을일컫는다 (1). MAS는기저질환과관련해서발생하는이차성 (secondary or reactive) 혈구탐식림프조직구증 (hemophagocytic lymphohistiocytosis, HLH) 로간주된다 (2). 감염질환, 종양질환, 혈액질환, 류마티스질환에서발생하며, 전신형소아류마티스관절염 (systemic onset juvenile rhrumatoid arthritis, SoJRA) 에서가장흔하게발생한다 (3). 임상증상으로는급성병색으로고열, 간비종대, 림프절병증, 범혈구감소증, 간효소치증가, 혈액응고장애, 고중성지방혈증, 고페리틴혈증이있다. MAS는생명을위협하는치명적인경과를보일수있으므로조기에진단하여적절히치료하는것이필수적이다. 현재스테로이드, cyclosporine A가치료의근간이되고있다. 이에실패하는경우가있어다른치료가시도되고있다. TNF-α 길항제 (etanercept) 로 MAS를치료한예가있으나국내에서는아직보고된바가없었다. <Received:September 14, 2011, Revised (1st: October 10, 2011, 2nd: October 13, 2011), Accepted:October 13, 2011> Corresponding to:kwang Nam Kim, Department of Pediatrics, Hallym University Medical Center, Hallym University College of Medicine, 896, Pyeongchon-dong, Anyang 431-070, Korea. E-mail:rheumatol@korea.com pissn: 2093-940X, eissn: 2233-4718 Copyright c 2012 by The Korean College of Rheumatology This is a Free Access article, which permits unrestricted non-commerical use, distribution, and reproduction in any medium, provided the original work is properly cited. 225

226 심영석외 저자들은 MAS로진단된환자에서 etanercept를포함한스테로이드, cyclosporine A의병용요법으로치료성공한예를경험하였기에문헌고찰과함께보고하는바이다. 증례환자 : 14세남자주소 : 1개월전시작된발열과피부발진현병력 : 14세남자는 3주전갑자기발열이시작되어모대학병원에입원하여 2주간검사및치료받았으나호전되지않아본원에불명열로전원되어입원하였다. 환자는 3 주전갑자기발열이시작되어하루에 2 3회씩 40 o C에이르는발열과동반증상으로배꼽주위와오른쪽아랫배통증, 오심, 구토와양겨드랑부위 (axillary area), 양샅굴부위 (inguinal area), 양어깨의통증이있었고일주일간외래치료하였으나증상호전되지않아 2주전입원하였다. 타병원혈액검사에서백혈구 3,790/mm 3, 혈색소 13.0 g/dl, 혈소판 177,000/mm 3 이었고, 적혈구침강속도 (erythrocyte sedimentation rate, ESR) 54 mm/hr, C-반응단백 (C-reactive protein, CRP) 10.0 mg/dl ( 정상 0.06 0.76 mg/dl), aspartate aminotransferase (AST) 59 IU/L ( 정상 5 45 IU/L), alanine aminotransferase (ALT) 26 IU/L ( 정상 5 45 IU/L) 이었고소변과대변검사에서는정상이었다. 혈액, 소변, 대변그리고뇌척수액배양검사에서는균배양되지않았으며 anti-ebv VCA IgM antibody, anti-cmv IgM antiboby, 류마티스인자 (rheumatoid factor, RF), 항핵항체 (anti-nuclear antibody, ANA) 모두음성이었다. 입원후에도하루 2 3회씩 38 40 o C에이르는발열은지속되었으며, 크기 0.5 1.0 cm 크기의반구진발진이전신에발생하였다. 입원 7일째추적혈액검사에서백혈구 2,830/mm 3, 혈색소 12.1 g/dl, 혈소판 184,000/mm 3 이었고, 적혈구침강속도는 56 mm/hr, C-반응단백 14.7 mg/dl, AST 205 IU/L, ALT 141 IU/L, 프로트롬빈시간 (prothrombin time, PT) 13.9 초 ( 정상 10.2 12.0초 ), 부분트롬보플라스틴시간 (activated partial thromboplastin time, aptt) 58.0초 ( 정상 26 37초 ), 피브리노겐 (fibrinogen) 612 mg/dl ( 정상 154 448 mg/dl), 피브린분해산물 (fibrin degradation product, FDP) 음성, D-dimer 2.41 μg/ml ( 정상 0 0.5 μg/ml) 였다. 복부전산화단층촬영과골수 (bone marrow) 조직검사 (biopsy) 를시행하였으나특이소견보이지않았다. 불명열로진단후치료하였으나전혀반응보이지않아입원 14일째전원되었다. 과거력 : 출생체중 3.4 kg로재태기간 41 +3 주에자연분만하였으며출생시분만손상등의특이소견은없었다. 예방접종은연령에맞게모두시행받았다. 가족력 : 부모님이있었고형제는없었으며, 가족중에특이병력은없었다. 신체검사소견 : 입원당시활력징후는혈압 110/70 mmhg, 맥박수 78회 / 분, 호흡수 20회 / 분, 체온 39.3 o C이었고의식은명료하였다. 신장은 168 cm (75 90 th percentile), 몸무게 53.0 kg (25 50 th percentile) 이었다. 급성병색을보였고신체검사에서는전신피부에붉은색의반구진과반구진이서로융합된붉은색반양상의반 (Figure 1), 양목림프절 1 2 cm, 양겨드랑, 양샅굴림프절이 0.5 1 cm 크기로커져있었으며, 간이 1횡지로만져졌다. 검사실소견 : 입원당일혈액검사에서백혈구 1,480/mm 3, 혈색소 12.3 g/dl, 혈소판 126,000/mm 3, 적혈구침강속도는 42 mm/hr, C-반응단백 102.8 mg/l ( 정상 0.8-7.6 mg/l), AST 2,555 IU/L, ALT 1,575 IU/L, 젖산탈수소효소 (lactate dehydrogenase, LDH) 5,300 IU/L, 중성지방 (triglyceride, TG) 161 mg/dl ( 정상 40 150 mg/dl), PT 12.2 초, aptt 34.6 Figure 1. A typical skin rash of macropharge activation syndrome (MAS). Figure 2. Bone marrow aspirate smears of a macropharge activation syndrome (MAS) demonstrating hemophagocytosis (arrow) (Wright stain, 1,000).

Etanercept 를포함한병용요법으로호전된대식세포활성증후군 1 예 227 초, fibrinogen 602 mg/dl, FDP 양성, D-dimer >4.0 μg/ml, 페리틴 (ferritin 29,970 ng/ml ( 정상 7 140 ng/ml) 이었다. 방사선소견 : 흉부ㆍ복부단순촬영을포함한관절방사선검사, 목의림프선초음파, 관절초음파에서는특이소견은보이지않았다. 임상경과및치료 : 입원 2일째골수조직검사를실시하였으며골수흡인검사에서혈구탐식식세포 (hemophagocyte) 관찰되어 (Figure 2) MAS로진단하고바로스테로이드충격요법 (methylprednisolone pulse therapy, 30 mg/kg/day, max 1,000 mg/day) 을 3일간실시하였다. 3일간의스테로이드충격요법후입원 5일째부터는경구스테로이드 (prednisolone 1 mg/kg), cyclosporine A (2 mg/kg/day), etanercept (25 mg twice a week) 로치료하여더이상열없고, 피부의발진호전, 림프선크기감소등증상호전되었다. 입원 7일째추적혈액검사에서는백혈구 5,610/mm 3, 혈색소 11.3 g/dl, 혈소판 216,000/mm 3 이었고, 적혈구침강속도 18 mm/hr, CRP 5.9 mg/l, AST/ALT 53/370 IU/L, LDH 399 IU/L로검사도호전되어입원 8일째퇴원하였다. 그후추적관찰에서 4개월후부터환자는오른어깨, 팔꿈치, 무릎, 발목관절의통증, 압통과운동제한등관절증상이발생하여 SoJRA로진단, 치료하며경과관찰중이다. 고찰 Hadchouel 등은 1985년 SoJRA 환자에서급성혈액학적이상, 간부전, 신경학적이상을동반하는임상증후군을보 Table 1. Cotemporary classification of histiocytic disorder (5) Disorders of varied biological behavior Dendritic-cell related Langerhans cell histiocytosis Secondary dendritic cell processes Juvenile xantogranuloma and related disorders Solitary histiocytomas of various dendritic cell phenotypes Macrophage-related Hemophagocytic syndromes Primary hemophagocytic lymphohistiocytosis Secondary hemophagocytic syndromes Infection-associated Malignancy associated Rheumatic-disease associated Other Rosai-Dorfman disease Solitary histiocytoma with macrophage phenotype Malignant disorders Monocyte-related Leukemias Monocytic leukemia M5A and B Acute myelomonocytic leukemia M4 Chronic myelomonocytic leukemia Extramedullary monocytic tumor or sarcoma Dendritic cell-related histiocytic sarcoma Macrophage-related histiocytic sarcoma 고하였다 (1). 1993년 Stephan 등은이증후군을 MAS라는용어로제안하였다 (4). 1997년미국조직구증학회 (Histiocytosis Association of America) 에서제안한분류법에 (5) 따르면혈구탐식증후군 (hemophagocystic syndrome) 을대식세포와관련된 (macropharge-related) 조직구성질환 (histiocytic disorder) 으로, 크게원발성혹은가족성 (primary) 과속발성또는반응성 (secondary or reactive) 으로구분하였다 (Table 1). 원발성 HLH는상염색체열성유전양상을보이며, 주로영아기에발현되어수개월내에사망할수있는치명적인질환이다. 속발성 HLH는감염, 악성종양, 류마티스질환과관련하여발생한다. MAS를정의할때, 속발성 HLH 중류마티스질환과연관된 (rheumatic disease- associated) 경우로제한하자는의견도있지만 (1) 류마티스질환뿐만아니라 Kikuchi 병과 Kawasaki 병을포함한다른전신염증성질환에서도 MAS가발병한예가있기에 (6,7) MAS는속발성 HLH와같은개념으로이해될수도있겠다. 하지만이는아마도초기 MAS를진단못하고 Kikuchi 병과 Kawasaki 병으로오인했을가능성도있다. MAS는남녀간발생률차이는없고, 어느연령에서도발생가능하다. 특히류마티스분야에서 MAS는 SoJRA와연관되어나타나고, SoJRA 환자에서높은이환율, 사망률의중요한원인이다. 외국의연구에의하면 3차의료기관에서 SoJRA 환자를후향적으로연구한결과 6.7% 의환자에서 MAS가발생하였다 (8). SoJRA와연관된 MAS의경우병의어느경과중에서도발생가능하여발병당시에첫증상으로나타날수있고 (9) 심지어는 SoJRA 관해후에발생하였다는보고도있었다 (10). SoJRA 환자에서 MAS 유발요인으로는약물 (aspirin, NSAID, gold salts, methotrexate, etanercept, anakinra), 감염 (Ebstein-Barr virus, varicella, parvovirus B19, salmonella) 등이있다 (1,3). 본증례에서환자는내원시에관절증상없이 MAS로발현한 SoJRA로생각된다. MAS의병태생리는아직잘알려져있지않으나정상조절을벗어난림프구와대식세포에서과다생성된 tumor necrosis factor-α (TNF-α), interleukin (IL)-1, IL-6, and interferon-γ 등의사이토카인 (cytokine) 과관련되어있다 (11). 증가된사이토카인으로인해고열, 간비종대, 림프절병증, 출혈, 중추신경계이상등의증상과범혈구감소증, 증가된간효소값, 응고장애, 적혈구침강속도감소, 고중성지방혈증등의검사소견이나타난다. 일차성 (primary) HLH 와같이 perforin 유전자의돌연변이로 perforin 생성이감소되어 MAS가유발될수있다 (12). Perforin은활성화된림프구에서분비되는세포독성단백질로서바이러스에감염된세포를제거하는역할을하고림프구증식에도관여한다. Perforin 감소는림프구를지속된활성상태를유지해 interferon-γ와같은사이토카인이지속적으로분비되어대식세포를활성화시킨다. MAS는소아기전신염증질환이나발병초기에는패혈증과유사하여조기치료가힘들다. 특히 SoJRA 환자에서

228 심영석외 Table 2. Diagnostic guidelines for hemophagocytic lymphohistiocytosis: HLH 2004 protocol (3) The diagnosis HLH can be established if one of either 1 or 2 below is fulfilled (1) A molecular diagnosis consistent with HLH (2) Diagnostic criteria for HLH fulfilled (five or more out of the eight criteria below) (A) Initial diagnostic criteria (to be evaluated in all patients with HLH) Fever Splenomegaly Cytopenias (affecting 2 of 3 lineages in the peripheral blood) Hemoglobin<90 g/l Platelets<100 10 9 /L Neutrophils<1.0 10 9 /L Hypertriglyceridemia and/or hypofibrinogenemia: Fasting triclycerides 265 mg/dl Fibrinogen<1.5 g/l Hemophagocytosis in bone marrow, spleen, lymph nodes No evidence of malignancy (B) New diagnostic criteria Low or absent natural killer cell activity (according to local laboratory reference) Elevated ferritin ( 500 mg/l) Soluble CD25 (i.e. soluble interleukin-2 receptor) 2,400 U/mL The diagnosis of hemophagocytic lymphohistiocytosis (HLH) can be established by one or both of the criteria described in the table. 증상악화가반복된다면 MAS가발병한것인지감염, 약제부작용으로인한것인지감별이쉽지않다. 따라서조기에치료를시작하기위해서는, 감별진단중하나로써 MAS를고려하여세심하게환자의증상을관찰하고혈소판과백혈구, ferritin, 간효소, 중성지방, LDH 등의 MAS를지지하는검사를확인해야한다 (Table 2). 또한초기에는골수생검에서도혈구탐식증이발견되지않을수있기때문에 (5) 임상경과와검사소견을총괄적으로판단하는것이필요하다. MAS 치료의핵심은초기고용량스테로이드치료이다. 거의절반의환자에서고용량의스테로이드단독요법만으로 MAS가치료되었다는보고가있다 (10). 고용량정맥용면역글로블린 (intravenous immunoglobulins, IVIG), cyclophosphamide, 혈장교환술 (plasma exchachange) 과 etoposide, cyclosporine A 등이이차약제로사용될수있다. Cyclosporine A는임상증상이심하거나, 스테로이드-저항성 MAS의치료에효과가입증되었다 (13). MAS 환자에서 TNF-α가높아져있고 (11) 병태생리기전으로이사이토카인이중심적역할을담당해 etanercept가효과적일것이라는보고가지속적으로있었다. Prahalad 등은증상조절을위해고용량의스테로이드가필요했던환자에서 etanercept로치료에성공하였음을보고하였다 (9). 그후 Makay 등은고용량스테로이드와 Cyclosporine A 치료로호전을보이지않는 MAS 환자에서 etanercept 치료로성공한사례를보고하였다 (14). 국내에서는아직까지 MAS 환자에서 etanercep를사용한보고는없었다. 본증례에서는앞에서언급한외국의치료와는다르게스테로이드와 cyclosporine A와함께초기부터 etanercept를사용하였다. 그이유는저자들은과거에 MAS 환자를스테로이드와 cyclosporine A로치료하였으나재발한예가있었고, 질병발생시초기부터 TNF-α가관여함이알려져있기에초기부터 etanercept를추가하는병용요법으로치료하였다. MAS는치명적일수있으며적극적인치료에도불구하고사망률이 8% 에이른다 (10). 예후인자로는진단지연, 심한다장기손상, 심한중성구감소, 혈액응고장애와중추신경계손상이예후에나쁜영향을미치는것으로알려져있다. 이러한예후인자가있을때조기에 etanercept를병용투여하는것이고려될수있겠다. Etanercept에대한치료지침이확립되어있지않아투여기간과투여적응증이앞으로제시되어야할것으로사료된다. 요약 MAS는조기진단과치료가중요하지만의심하지않으면진단하기힘든질환이다. 치료에도잘해열되지않는열이지속되거나, 류마티스기저질환에서갑자기악화된경우에 MAS를의심해보아야한다. 저자들은 MAS로진단된환자에서코르티코스테로이드, cyclosporine A와함께초기부터 etanercept 추가하여치료한환자를경험하였다. 이는현재까지알려진 MAS의병태생리기전에부합되는치료로생각되나아직치료지침이정립되지않아이에대한연구가필요할것으로생각된다. 참고문헌 1. Hadchouel M, Prieur AM, Griscelli C. Acute hemorrhagic, hepatic, and neurologic manifestations in juvenile rheumatoid arthritis: possible relationship to drugs or infection. J Pediatr 1985;106:561-6. 2. Athreya BH. Is macrophage activation syndrome a new entity? Clin Exp Rheumatol 2002;20:121-3.

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