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1 대한내과학회지 : 제 70 권부록 2 호 2006 심장이식후발생한 NK/T Cell Lymphoma 1 예 울산대학교의과대학서울아산병원내과학교실, 흉부외과 2, 병리과 3 박혜원 변승운 김재중 송명근 2 한은미 3 허주령 3 서철원 =Abstract= A case of NK/T-cell lymphoma in a cardiac transplant recipient Hye Won Park, M.D., Seung Woon Byun, M.D., Jae Joong Kim, M.D., Meong Gun Song, M.D. 2, Eun Mee Han, M.D. 3, Joo Ryung Hugh, M.D. 3 and Cheolwon Suh, M.D. Department of Internal Medicine, Thoracic surgery 2 and Pathology 3, Asan Medical Center, University of Ulsan College of Medicine, Seoul, Korea Posttransplant lymphoproliferative disorder (PTLD) represent a potentially life-threatening complication following organ transplantation. The majority of PTLD are of B cell origin and strongly associated with Epstein-Barr Virus (EBV). PTLD of T cell origin are uncommon and have a poor prognosis. We encountered a case of NK/T-cell lymphoma involving posterior hypopharynx and appendix in a cardiac transplant recipient. The patient was a 67 year old woman who underwent cardiac transplantation in She was admitted in December 2004 after complaining of a sore throat for 2 weeks. The posterior hypopharyngeal mass was detected by laryngoscopic exam. On the 10 th hospital day, fever and abdominal pain developed. Ultrasonography revealed acute appendicitis and appendectomy was performed. Excisional biopsy of posterior hypopharyngeal mass and appendectomy specimen showed nasal type NK/T-cell lymphoma, and it was assessed as PTLD. (Korean J Med 70:S335-S340, 2006) Key Words : Lymphoproliferative disorder, Malignancy, Heart transplantation, Ebstein-Barr virus 서론장기이식후림프증식질환 (Posttransplant lymphoproliferative disorder, PTLD) 은 1969년 Penn 등 1) 이처음으로발표한이후지속적으로증가하고있으며장기이식후면역억제제를사용하는환자에서 PTLD가발생하는빈도는이식장기에따라많은차이를보이고있지만대략 1~32% 정도이다 2, 3). PTLD의발생에는 Epstein -Barr Virus (EBV) 가중 요한역할을하는것으로알려져있다 4). EBV는주로 B 세포에감염되며 EBV에감염된 B 세포는세포독성 T 세포 (cytotoxic T cell) 나자연살세포 (natural killer cell,nk) 에의한조절을받지않기때문에비정상적인증식을통하여 PTLD로진행하게된다. 따라서대부분의 PTLD는 B 세포기원인경우가많고국내에서보고된경우도대부분이 B 세포기원이다 5, 6). 저자들은심장이식후발생한 PTLD가하인두와충수돌기를침범하였으며조직검사에서 NK/T 세포기원으로 접수 : 2005년 5월 31일 통과 : 2005년 8월 3일 교신저자 : 서철원, 서울시송파구풍납동 388-1, 서울아산병원내과 ( ) csuh@amc.seoul.kr -S 335 -

2 - 대한내과학회지 : 제 70 권부록 2 호 Figure 1. The initial biopsy of hypopharygeal mass shows diffuse lymphoid infiltrate with coagulative necrosis and ulcer (H&E stain, 40). Figure 2. High power view shows angiodestructive and angioinvasive tumor composed of small to medium-sized lymphoid cells with pale cytoplasm, pleomorphic nuclei, abundance of apoptotic bodies (H&E, 400). 밝혀진 1예를경험하였기에문헌고찰과함께보고하는바이다. 증례 67세여자환자가 2주간지속되는인후통, 연하통그리고호흡곤란이있어서 2004년 12월 22일서울아산병원심장내과에입원하였다. 과거력상환자는확장성심근병증으로 1995년 7월 12일심장이식수술을받았다. 이후면역억제제 ( 시클로포스파미드, 시클로스포린, 메틸프레드니솔론 ) 복용하며정기적으로추적관찰하고있던중이었다. 2004년 11월 13일인후통으로입원한병력이있었는데, 당시신체검사소견상인두발적, 인두삼출물이동반되어있었고, C-반응단백수치 (CRP) 가 8.4 mg/dl로증가되어있었다. 급성인후염으로진단하고경구항생제투여후증상호전되면서퇴원하였다. 퇴원 1 주일뒤다시인후통이발생하였고, 열과오한이동반되고연하통, 호흡곤란이동반되었다. 급성인후염재발로판단하고 2004년 12월 22일입원하여정주항생제투여를시작하였다. 2004년 12월 23일이비인후과에서후두경검사결과, 하인두후벽에종괴가발견되었다. 2004년 12월 24일이종괴에대한절제조직검사를시행하였다. 조직검사결과를기다리던중, 2004년 12월 28일식욕부진, 오심증세가새로나타나고 12월 30일에는체온 의열이발생하였다. 신체검사상오른쪽아랫배에압통이있어급성충수돌기염을의심하고 2004년 12월 31 일복부초음파검사를시행하였다. 검사결과충수돌기 의직경이 7 mm로증가되어있어, 충수돌기염으로진단하고응급수술을시행하였다. 수술소견에서충수돌기는화농성변화를보이고있었고, 충수돌기주변액체저류양도많았다. 떼어낸충수돌기의크기는길이 48 mm, 직경 7 mm였다. 수술후환자는심장계중환자실로옮겨져집중치료를받던도중, 체온 38 의열과빈맥이나타나며저혈압, 저산소증, 소변량감소를보였다. 생화학검사에서진행하는산증, 저혈소판증의결과를보여임상적으로패혈쇼크로판단하고혈액배양검사시행후광범위항생제와혈압상승제를투여하였으나호전을보이지않았고환자는 2005년 1월 3일사망하였다. 이후보고된혈액배양검사결과는음성이었다. 2005년 1월 5일하인두후벽종괴와충수돌기에대한조직검사결과가보고되었다. PTLD, NK/T cell lymphoma, extranodal, nasal type 소견을보였다. 하인두후벽종괴에서보이는비정형림프구들은 ( 그림 1, 2) 면역조직화학염색에서 CD3에양성, Leukocyte Common Antigen 에양성, CD56 에양성 ( 그림 3A, 3C) 을보이면서 B림프구표지자인 CD 20에음성을보였다. 거의모든림프구에서 EBV에대한동소보합결합반응이양성이었다 ( 그림 3B). 충수돌기조직에서보이는비정형림프구들은 ( 그림 4, 5) 면역조직화학염색에서 CD3에양성, Leukocyte Common Antigen 에양성, CD56 에양성을보이면서 B 림프구표지자인 CD20 에음성을보였다. 또한 EBV에대한동소보합결합반응이양성이었다 ( 그림 6). 이식전, 후혈청 EBV 항체검사가시행되지않아 EBV의전신감염상태는알수없었다. -S 336 -

3 - 박혜원외 6 인 : 심장이식후발생한 NK/T Cell Lymphoma 1 예 - A B C Figure 3. (A) The results of immunostain for CD56 with positive staining along tumor cell membranes ( 400). (B) Immunostain for in situ hybridization for EBV encoded RNA (EBER) shows strong positive results in virtually every tumor cell nucleus ( 400). (C) Ki-67 labelling index of 95% ( 400) are typical of the CD56(+), extranodal NK/T-cell lymphoma of nasal type ( 400). Figure 4. The appendectomy specimen shows diffuse infiltrate of lymphoid cells throughout the entire thickness of the appendiceal wall (H&E, 1:1 scan). Figure 5. High power view shows similar tumor cells with numerous apoptotic bodies, penetrating through the smooth muscle fibers of the proper muscle layer in the appendiceal wall (H&E, 400). 고찰 -S 337 -

4 - 대한내과학회지 : 제 70 권부록 2 호 Figure 6. Immunostain for in situ hybridization for EBV encoded RNA(EBER) shows strong positive signals in nearly all tumor cell nuclei ( 400). 장기이식의중요한합병증인 PTLD는 1969년 Penn 등이 5명의신이식환자에서림프종발생을기술한이후이의발병기전과진단및치료에있어상당한발전이있어왔다 1). PTLD는주로림프절외조직을침범하고 7), 여러조직학적형태를지니며 8), EBV와의연관성 7) 및면역형또는유전형단클론성의증거가없고 9), 림프종의치료에사용되는화학요법및방사선치료에잘반응하지않는다는면에서다른림프종과구별이된다 1, 9). PTLD는일반적으로이식후 1년이내에가장많이발생하며그이후로는발생빈도가감소한다 10). 사용하는면역억제제의종류에따라 PTLD의발생시기가달라진다는보고들도있다 11, 12). 본증례는심장이식후 PTLD 를진단하기까지약 114개월이걸려서 PTLD가매우늦게발생한경우이다. 이식장기에따라면역억제의정도가다르기때문에 PTLD의발생빈도도심폐이식후 9.4%, 폐이식후 6.2%, 신장-췌장이식후 5.2%, 심장이식후 1.8~2%, 신장이식후 1~2.5%, 간이식후 1.4~2.2%, 골수이식후 0.6% 등이식장기에따라보고되는빈도가다르다 2, 3). 본원에서는 2002년 5월까지 14예의 PTLD가진단되었다. 106예의신장이식중 6예, 479예의간이식중 8예가있었다. 2002년까지심장이식은 106예였고, 이중 2002년 9월까지의종양발생은 2예의 Bowen's disease와 1예의 Kaposi's sarcoma 뿐이었고, PTLD는없었다. PTLD의발생에는면역억제제의사용과 EBV의초기감염이나재활성화에의한 B 세포의감염이주요한역 할을하는것으로알려져있다 13). Purtilo 13) 에의하면면역억제제의사용으로면역기능이저하된환자에서는 EBV에대한면역력이약화되어지속적으로 EBV의증식이일어남으로써종양화된다고하였다. PTLD 발생의연관인자로는 EBV와 CMV 감염여부 14, 15), 이식장기의종류, 면역억제제의종류와용량, 사용기간등이있다. 수여자가이식후 EBV에감염되거나잠복감염의재활성화가있을때 PTLD의발생빈도가증가한다. EBV는 PTLD의 90% 이상에서증명되며, PTLD 발생전이식편생검에서도 70~90% 의양성률을보여 PTLD가발생하지않은환자의이식편생검에서의 7% 보다월등히높다 16). 또한이식후 EBV에감염된경우가잠복감염의재활성화보다 PTLD 발생률이 24배높다 14). CMV 항체가음성인수여자가 CMV 양성인공여자의장기를받았을때 PTLD 발생률이더높다. 이식장기의종류에따른발생빈도는앞서기술하였다. 과도한면역억제가가장중요한위험인자로 PTLD와관련되어보고되는면역억제제로는시클로스포린 12, 17), 아자시오프린 12), OKT3 11), FK506 등이며특히시클로스포린과 OKT3의도입과더불어 PTLD의발생이지속적으로증가해오고있다. 본증례에서도시클로스포린은초기용량 300 mg/day에서점차로용량을감소하여 100 mg/ day로유지하여총 113개월간, 시클로포스파미드는 25 mg/day 를격일로총 56개월간복용해오고있어서장기간면역억제제가투여된경우였다. PTLD의발병부위는림프절, 림프절외여러장기들과중추신경계등인것으로알려져있다. 림프절외장기로는위장, 간, 대장등의순으로많았다. 일반인의림프종과는달리 PTLD는림프절외장기에서주로발생한다. EBV는주로 B 세포를감염시켜서변형을일으키고면역억제제에의해서기능을상실한세포독성 T 세포는 B 세포에대한조절기능을상실함으로써 B 세포의계속적인증식을가능하게하여 PTLD가발생하게된다 4). 따라서대부분의 PTLD는 B 세포형이며드물게 T 세포형이발생한다. T 세포형은 B 세포형보다예후가좋지못하며 B 세포형에비하여 EBV와의연관성이비교적적다 18). T 세포 PTLD에서도 EBV를발견하였다는보고가있으나 18), 아직까지 EBV에의한 T 세포 PTLD의발생과관련된정확한기전에대해서밝혀진것은없다. 본증례의경우 NK/T cell lymphoma, extranodal, nasal -S 338 -

5 - 박혜원외 6 인 : 심장이식후발생한 NK/T Cell Lymphoma 1 예 - type으로최종진단되었고종양조직에서의 EBV에대한동소보합결합반응이양성이었다. 세계보건기구 (WHO) 의분류체계에따라 PTLD는 1) 조기병변 (early lesion) 2) 다형성 (polymorphic)-ptlds 3) 단형성 (monomorphic)-ptlds 4) Hodgkin lymphoma and Hodgkin lymphoma-like PTLDs로분류할수있다 19). PTLD의진단은림프구로이루어진팽창성결절, B 림프구가우세한침윤, 핵의이형성, 림프구침윤내의괴사동반, 동소보합결합반응에서의 EBV 양성으로쉽게진단할수있다 5). 본증례의경우조직학적으로세포질이풍부하고, 핵은심한다형성을보이며림프구침윤내의괴사를동반하고있었으며, EBV에대한동소보합결합반응이양성이었다. WHO 분류체계에따르면본증례의경우는단형성 PTLD에속한다. PTLD에대한적절한치료가아직없고, 명확히확립된지침도없으며치료결과도만족스럽지못하다. PTLD로진단되면면역억제제를중단하거나감량하는것이가장우선되어야한다. 면역억제제를중단하거나감량함으로써 PTLD의진행을억제하고병변의소실까지도유도할수있다. 그러나간이식이나심장이식과같이이식장기의거부반응이생명의위협과직결된경우에는면역억제제의중단을신중히결정해야한다. PTLD가국한성일때는수술적제거로치료가가능하다 20). 또한종양의크기를줄이거나, 위출혈, 위천공등의합병증의대처에도수술치료가도움이된다. 방사선요법은국한성 PTLD에대해제한적으로사용되기도하지만대개는중추신경계에발생한병변에대하여항암화학요법과더불어사용된다 20). 항바이러스제재와 Interferon α, 감마글로불린등이바이러스의증식을억제하는효과가있기때문에 PTLD의치료에이용되기도한다. 최근들어 CD21, CD24 등 B 세포에대한단클론항체를이용한치료등이연구되고있다 20). 요약 PTLD는여러장기의이식이늘어나고, 보다강력한면역억제제가사용되면서점차로증가하는추세이다. PTLD는아직까지적절한치료방법이없고예후가나쁘기때문에조기에진단하는것이매우중요하지만 PTLD의발생부위가다양하고증상이비특이적이어서 조기진단이어렵다. 특히 NK/T 세포형 PTLD는매우드물고 B 세포형보다훨씬예후가나쁘며경과가빠르기때문에더많은주의를필요로한다. 저자들은심장이식후발생한 PTLD가하인두와충수돌기를침범하였으며조직검사에서 NK/T 세포기원으로밝혀진 1예를경험하였기에문헌고찰과함께보고하는바이다. 중심단어 : 림프증식질환, 심장이식 REFERENCES 1) Penn I, Hammon W, Brettschneider L, Starzl TE. Malignant lymphomas in transplantation patients. Transplant Proc 1: , ) Nalesnik MA, Jaffe R, Starzl TE, Demetris AJ, Porter K, Burnham JA, Makowka L, Ho M, Locker J. The pathology of post-transplant lymproliferative disorders occuring in the setting of cyclosporine A-prednisone immunosuppression. Am J Pathol 133: , ) Walker RC, Paya CV, Marshall WF, Strickler JG, Wiesner RH, Velosa JA, Habermann TM, Daly RC, McGregor CG. Pretransplantation seronegative Ebstein-Barr virus status is the primary risk factor for posttransplantation lymphoproliferative disorder in adult heart, lung, and other solid organ transplantation. J Heart Lung Transplant 14: , ) Hanto DW, Frizzera G, Gajl-Peczalska KJ, Simmons RL. Ebstein-Barr virus, immunodeficiency, and B- cell proliferation. Transplantation 39: , ) 장선희, 허주령, 김경모, 한덕종, 이승규, 유은실. 이식후림프증식성질환 : 4 예보고. 대한병리학회지 36:45-50, ) 최성희, 한지숙, 김유선, 박기일. 신이식후발생한 Posttransplant lymphoproliferative disorder (PTLD) 4 예. 대한이식학회지 14: , ) Hanto DW, Frizzera G, Purtilo DT, Sakamoto K, Sullivan JL, Saemundsen AK, Klein G, Simmons RL, Najarian JS. Clinical spectrum of lymphoproliferative disorderd in renal transplant recipients and evidence for the role of Epstein-Barr virus. Cancer Res 41: , ) Frizzera G, Hanto DW, Gajl-Peczalska KJ, Rosai J, McKenna RW, Sibley RK, Holahan KP, Lindquist LL. Polymorphic diffuse B-cell hyperplasia and lymphomas in renal transplant recipients. Cancer Res 41: , ) Hanto DW, Gajl-Peczalska KJ, Frizzera G, Arthur DC, Balfour HH, McClain K, Simmons RL, Najarian JS. Epstein-Barr virus induced polyclonal and -S 339 -

6 - 대한내과학회지 : 제 70 권부록 2 호 monoclonal B-cell lymphoproliferative diseases and monoclonal B-cell lymphoproliferative diseases occurring after renal transplantation. Ann Surg 198: , ) Opelz G, Henderson R. Incidence of non-hodgkin lymphoma in kidney and heart transplant recipients. Lancet 342: , ) Penn I. The changing pattern of posttransplant malignancies. Transplant Proc 23: , ) Gruber SA, Skjie KL, Sothern RB, Robison L, Tzardis P, Moss A, Gillingham K, Canafax DM, Matas AJ, Dunn DL. Cancer development in renal allograft recipients treated with conventional and cyclosporine immunosuppression. Transplant Proc 23: , ) Purtilo DT. Epstein-Barr virus- induced oncogenesis in immune deficient indivisuals. Lancet 1: , ) Williams RC, Martial WF, Strickler JG, Wiesner RH, Velosa JA, Habermann TM, McGregor CG, Paya CV. Pretransplant assessment of the risk of lymphoproliferative disorder. Clin Infect Dis 20: , ) Swinnen LJ, Costanzo-Nordin MR, Fisher SG, O'Sullivan EJ, Johnson MR, Heroux AL, Dizikes GJ, Pifarre R, Fisher RI. Increased incidence of lymphoproliferative disorder after immunosuppression with the monoclonal antibody OKT3 in cardiac transplant recipients. N Engl J Med 323: , ) Harris NL, Ferry JA, Swerdlow SH. Posttransplant lymphoproliferative disorders: summary of society for hematopathology workshop. Semin Diagn Pathol 14:8-14, ) Boubenider S, Jiesse C, Groupy C, Kriaa F, Marchand S, Charpentier B. Incidence and consequences of posttransplantation lymphoproliferative disorders. J Nephrol 10: , ) van Gorp J, Doomewaard H, Verdonck LF, Klopping C, Vos PF, van den Tweel JG. Posttransplant T-cell lymphoma: report of three cases and a review of the literature. Cancer 73: , ) Andreone P, Gramenzi A, Lorenzini S, iselli M, Cursaro C, Pileri S, Bernardi M. Posttransplantation lymphoproliferative disorders. Arch Intern Med 163: , ) 김상욱, 성수아, 조상경, 조원용, 김형규, 원남희. 신이식후발생한다발성장기의 NK/T-cell lymphoma. 대한신장학회지 23: , S 340 -

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