액와림프절의다양한질환의영상소견과병리적소견의비교 1 류근호 장윤우 김형환 2 이동화 3 권귀향 최득린 황정화 양승부 4 액와림프절종대는다양한양성과악성질환들이원인이될수있으며염증성림프절종대와전이성림프절종대가대표적이다. 전이성림프절종대는유방암환자에매우중요한예후인자이므로악성림프절종대의영상의학적특징을알고검사여부를결정하는것은매우중요하다. 최근들어초음파유도하에액와림프절종대의조직검사법이악성림프절종대를진단하는데유용하게사용되고있다. 저자들은다양한질환들로인한액와림프절종대의영상소견을병리적인소견과비교하여특징적인소견을알아보고조직검사의여부를결정하는데도움이되고자한다. 액와는액와동정맥, 상완신경총및림프절이포함된상완과흉벽사이의피라미드형태의공간으로다양한질환이발생할수있다. 액와림프절종대는유방암의전이가원인인경우가많으므로양성과악성을감별하고조직학적검사여부를결정하는것은매우중요하다. 액와림프절종대는초음파검사로진단할수있으며초음파유도세침검사나핵생검으로확진할수있다. 저자들은액와림프절종대로나타난다양한질환들을병리소견과비교하고조직검사여부를결정하는데도움이되고자한다. 액와림프절검사방법 액와림프절은소흉근을기준으로세부분으로나뉘는데 Level I은소흉근의하외측면의하방부위이며 level II는소흉근의후방부위이고 level III 는소흉근의내측면의상방이다 (1). 유방촬영술에서정상액와림프절은다양한크기의난원형의결절로중심지방을가지는지방문이보인다. 비정상액와림프절은크기가 2 cm 이상이고높이와폭이 1.5 이하로둥글거나불규칙모양을가지고지방문의소실과증가한음영을보인다. 그러나 5 cm 이상의정상림프절이나 5 mm 이하의전이성림프절도있을수있어림프절의크기나모양으로양성과악성을감별하는것은어렵다 (1-3). 또한, 유방촬영술은커진림프절이포함되지않을수있어신뢰할만한검사법은 1 순천향대학교병원영상의학과 3 순천향대학교병원병리과 2 천안순천향병원영상의학과 4 구미순천향병원영상의학과이논문은 2009년 11 월 13일접수하여 2010년 1월 17일에채택되었음. 501 아니다. 초음파검사에서정상액와림프절은얇은피질과상대적으로큰지방문을가지며지방문내에단일동정맥을가진다 (Fig. 1). 비정상액와림프절은크기가크고두껍고편심성으로팽창된피질을가지고지방문이작거나소실되어보인다. 색도플러초음파검사에서는지방문에과혈류를보이며악성세포침윤으로폐문혈관이파괴되어주변혈관들이커지는비정상적인비문혈류 (nonhilar blood flow) 를보이나이런소견은반응성림프절종대나염증에의해서도발생할수있다 (1, 4, 5) (Fig. 2). 그러므로초음파검사의림프절종대는양성과악성종대가중복되는소견을보일수있어초음파유도세침검사나핵생검이유용한방법이다 (1, 5) (Fig. 2). 액와림프절의초음파유도하에세침검사나핵생검은덜침습적인검사방법으로유방암환자에서전이성림프절을예측하는데높은민감도, 특이도와음성예측도를가진다 (5, 6). 세침검사를사용한세포의확인은덜침습적이고저렴하며편리한방법이지만시술자의경험과경험이풍부한세포병리학자가있어야하므로많은병원에서시행하기에는제한이있다. 핵생검역시안전하고빠르게시행될수있으며시술자에게덜의존적이고더많은조직을얻어면역학적염색법으로검사를시행할수있다 (5). CT는림프절종대를평가하는데가장유용한방법이지만전이를평가하는데있어믿을만한림프절종대의크기가정해져있지않으며다양한민감도와특이도를가진다. PET- CT 나유방 MRI를이용하는평가방법도시도되고있으나제한적이다.
류근호외 : 액와림프절의다양한질환의영상소견과병리적소견의비교 양성림프절종대반응성종대 (Reactive Hyperplasia of Lymph Node) 반응성림프절종대는염증, 교원혈관질환, 육아종성질환, 후천성면역결핍증이나실리콘림프절병증등의다양한원인에의해생기며전신성질환에동반되어생길경우양측성반응성종대로발생한다 (2). 결핵 (Tuberculosis) 결핵에의한림프절종대는두경부나쇄골하림프절의종대가흔하며액와부종대는드물다. 결핵에의한림프절종대는치유되었을때석회화를보일수있으며유방촬영술에서크기 가크고거친석회화를동반한고밀도의림프절종대는결핵성림프절종대를시사할수있다 (Fig. 3). 유방촬영술에서석회화를동반한림프절종대는결핵성림프절외에석회화성전이, 류마티스관절염치료에생긴금침전물혹은유방성형후삽입된실리콘의파열등을고려할수있다 (7). 초음파에서는크기가큰피질의비후와지방문의소실을보이는다수의림프절비대를보이며내부에농양을형성하기도한다 (Fig. 4). 전이성림프절종대, 림프종, 감염성림프절종대와감별할수없으나석회화가보이거나융합된농양형태의림프절종대가보이면의심할수있고초음파유도하조직검사등을통한병리검사가필수적이다. 병리소견은건락괴사와상피양세포를보인다 (8) (Fig. 4). 기꾸치병 (Kikuchi s Disease) 기꾸치병은 1972년처음기술되었으며조직학적으로괴사 Fig. 1. xillary ultrasonography finding of normal lymph node. Normal lymph node has a smooth, hypoechogenic, thin cortex (white arrow) with a centrally located, preserved relatively large sized fatty hilum. Fig. 3. Tuberculosis in a 50-year-old women. Mammography shows calcified lymph nodes (black arrows) in both axilla that are possible of sequale of old pulmonary tuberculosis correlated with past history. Fig. 2. Reactive hyperplasia of lymph node in a 38-year-old women.. Ultrasonography shows enlarged lymph node with eccentrical thickening of cortex and small sized fatty hilum.. Ultrasonography guided 20G needle aspiration was performed and pathology reveals reactive hyperplasia of lymph node (white arrow). 502
Fig. 4. Tuberculosis in a 46-year-old women.. Ultrasonography shows abnormal multiple, hypoechoic enlarged lymph nodes (white arrow) with loss of hilar echogenecity.. Photography reveals chronic granulomatous inflammation with caseous necrosis (H & E). Fig. 5. Kikuchi disease in a 40-year-old women.. Ultrasonography demonstrates a well-circumscribed, round or oval, hypoechogenic masses (white arrows) in left axilla. Sonoguided biopsy was performed using 14G needle.. Contrast enhanced CT with MPR reconstruction image shows several homogeneous enhancing lymph nodes (white arrow) in left axilla. C. Photography of the biopsied lymph node demonstrates plump histiocytes intermixed with nuclear debris and lymphocytes. There is an absence of neutrophils and plasma cells (H & E). C 503
류근호외 : 액와림프절의다양한질환의영상소견과병리적소견의비교 성림프절염으로특징지어진다. 임상적으로젊은여성에서통증이있는경부림프절종대가흔하며액와, 복부, 흉부, 골반등의림프절종대도보일수있다. 지속적인발열, 체중감소, 피부발진, 소화기증상을보이나 1-4개월내에저절로호전된다. 초음파에서는균질혹은비균질에코의종괴로지방문이유지되어있으며동심성피질비후를보이나비특이적이며전이성림프절과의감별이어려워조직학적확진이요구된다 (9) (Fig. 5). CT에서는균질한조영증강을보이며림프절주위지방의소실을보일수있다 (10) (Fig. 5). 조직학적으로기꾸치병은피질이나피질주면의괴사와림프절정상구조의완전한소실을보이나과립구 (granulocyte), 형질세포 (plasma cell) 혹은호산구 (eosinophil) 는보이지않는다 (10) (Fig. 5C). 캐슬만병 (Castleman s Disease) 캐슬만병은 1956년에처음기술된원인을알수없는드문양성림프증식성질환이다. 자주생기는부위는종격동이며액와부에발생하는경우는약 2% 로드물다. 임상적으로는국소성 (localized) 과미만성 (disseminated) 으로나누며병리적으로초자혈관형 (hyaline vascular type) 과형질세포형 (plasma cell type) 으로나뉘는데 91% 는초자혈관형으로나 타난다. 초음파소견은단일형의저에코종괴이며색도플러초음파를시행하였을때혈류의증가세를보인다 (Fig. 6). CT 에서는균일한조영증강의종괴로보인다 (Fig. 6). 병리소견은초자혈관형은잘발달한초자혈관변화를가지는종자중심 (germinal center) 이현저하며형질세포형은여포간조직 (interfollicular tissue) 내에미만성형질세포 (plasma cell) 의증식을보인다 (Fig. 6C). 영상의학적으로비특이적인소견을보이므로조직학적인확진이필요하다 (11). 톡소포자충증 (Toxoplasmosis) 톡소포자충증은세포내원충인톡소포자충 (Toxoplasmosis gondii) 의감염으로고양이가숙주로알려져있다. 태반을통과하는감염에의한선천적감염이나다른원인에의한후천적인감염에의해발생할수있으며임상적으로는안구의맥락망막염이흔하나증상이없거나전신적인감염을보일수있다 (12). 후천적감염일경우경부림프절종대가가장흔하며후두골하방, 쇄골상방, 액와, 서혜부및종격동의림프절종대를보일수있다. 증상이없다면림프절종대는림프종과유사하게보일수있으며액와절림프절종대는유방암의전이와도감별하여야한다. 초음파소견은경계가분명하고내부괴사가없으며균질한저에코를보여비특이적이다 (Fig. 7). Fig. 6. Castleman s disease in a 65-years-old women. Ultrasonography shows several well-circumscribed, ovoid, hypoechogenic lymph nodes (white arrows) in left axilla.. Contrast enhanced CT scan shows the multiple, conglomerated, enlarged lymph nodes (white arrow) with homogeneous enhancement in left axilla, level I. C. Photograph of a histopathologic specimen shows lymphoid follicles with stroma of hyperplastic capillaries, venules, and arterioles. In the germinal center, there is concentric layering of the multinucleated and pleomorphic follicular lymphocytes around the hyalinized central vessel (H & E). C 504
색도플러에서는림파절괴사가없으므로지방문의혈류가보인다 (13) (Fig. 7). 병리적으로는반응성림프소포과다형성 (reactive follicularl hyperplasia), 상피모양조직구종 (epithelioid histiocytes) 의불규칙한군집단핵구모양세포 (monocytoid cell) 에의한잔기둥글 (trabecular sinus) 과피막하국소팽창의소견을보인다 (Fig. 7C) (12, 13). Fig. 7. Toxoplasmosis in a 44-year-old women. Ultrasonography shows enlarged lymph node with cortical thickening and fatty echogenicity in lymph node (white arrow) in hilar portion of left axilla.. Color Doppler sonography shows increased hilar vascularity of lymph node. C. Photography reveals multiple small sized epithelioid granulomas (H & E). C Fig. 8. Metastatic lymphadenopathy from breast cancer in a 76-year-old women. Ultrasonography shows about 1cm sized, enlarged lymph node (white arrow) with loss of fatty hilum and cortical thickening in right axilla.. Contrast-enhanced CT scan shows enhancing LN (white arrow) in right axilla (level I). 505
류근호외 : 액와림프절의다양한질환의영상소견과병리적소견의비교 악성림프절종대유방암전이액와림프절은유방암에서가장흔하게전이되는부위로림프절전이여부는예후를결정하는가장중요한인자이다. 초음파에서보이는림프절의피질두께, 크기, 모양및비문혈류를사용하여수술전림프절전이를평가하였을때민감도는 35-95% 로다양하게보고되었다 (5, 6). 폐문의소실은 93% 의양성예측도를보이나민감도는 33% 로보고되었다 (14). 림프절피질의두께도림프절전이를평가하는중요한예측인자이며 2.3 mm에서 3 mm를기준으로하는연구들이있으며절대적인피질의두께보다는림프절단경에대한피질의상대적 인두께를측정하는것이민감도의특이도를모두만족하게한다는보고가있다 (5, 6). 초음파에서림프절의장단경의비가 1.5이하이거나편심성 (eccentric) 으로피질의두꺼워지거나지방문의소실을보이는경우전이성림프절종대로여겨진다 (4) (Fig. 8, 9). 색도플러초음파에서주변부혈류와구불거리는이상형태의신생혈관들이악성에서더보인다는보고도있다 (1, 4, 15). 하지만동심성 (contentric) 피질을가지는경우림프절전이를배제할수없으므로초음파유도하액와부림프절세침검사나핵생검이전이성림프절을평가하는데이용될수있다. 유방암수술전초음파유도하에세침검사을통해액와림프절의전이를먼저확인함으로써감시림프절을절개를따로시행할필요성이줄어들수있으며보조적항암치료의적응증이될 Fig. 9. Metastatic lymphadenopathy breast cancer in a 37-year-old women. Sonography shows enlarged lymph nodes (white arrow) in axilla with subcutaneous and skin nodules (white arrowheads).. enhanced CT scan with MPR reconstruction image shows conglomerated axillary lymph nodes (white arrows) (level I,II and III) with low-density necrotic portions, representing metastases. Fig. 10. Metastatic lymphadenopathy from breast cancer in a 54-year-old women. Sonography shows an enlarged lymph node (white arrow) between the pectoralis major and minor mulscle (Rotter s node).. multiplanar reformation (MPR) reconstruction image shows metastatic lymph nodes (white arrows) in left axilla level I, II. Identifying enlarged Rotter s node can be important because metastases can give rise to chest wall invasion. 506
Fig. 11. Metastatic lymphadenopathy from melanoma in a 45-year-old women. Ultrasonography shows a lobulated heterogeneous hypoechoic mass (white arrow) and daughter nodules in left axillar.. Contrast-enhanced CT scan with MPR reconstruction image shows multiple conglomerated, heterogeneously enhanced masses (white arrow) in left axillar. Fig. 12. xillary metastatic lymphadenopathy from primary breast malignant lymphoma in a 43-year-old women. Ultrasonography shows lobulating, heterogeneous and hypoechogenic mass (white arrow) in right axilla.. 18F FDG PET CT shows multiple FDG uptake right breast masses (white arrowhead) (SUV 22) and huge right axillary lymphadenopathies (white arrow) with FDG uptakes. C. Pathology revealed diffuse proliferation of large atypical lymphocystes compatible with diffuse large -cell lymphoma (H& E). C 507
류근호외 : 액와림프절의다양한질환의영상소견과병리적소견의비교 수있다 (16). 감시림프절생검에서전이로판명된경우액와부박리를시행하는데수술전림프절전이가확인된다면감시림프절생검을시행할필요가없어지므로수술시간을줄이는데도움이된다 (5, 6). CT에서는편심성으로불규칙한피질의모양과장단경의비가 2 이하는경우악성림프절을나타내는중요한소견으로여겨진다 (17) (Fig. 8, 9). 흉근내림프절 (Rotter s node) 은유방암환자의약 10% 에서침범된다 (18) (Fig. 10, ). 유방암외악성전이대부분의선암 (adenocarcinoma) 이액와림프절로전이될수있으며폐암, 갑상선암, 위암, 대장암과췌장암이전이된다. 악성흑색종은피부나볼점막에서발생하나약 5% 는피부외에서발생한다. 액와부위원발성흑색종은드물며액와부가침범되는경우다른부위흑색종에서전이된경우가더많다 (19). 유방암이외의악성종양의림프절전이의초음파나 CT 의영상의학적인소견은유방암의전이성림프절과감별점은없다 (Fig. 11, ). 악성림프종유방의원발성악성림프종은 0.1~0.5% 로매우드물게보고되며다른부위의림프종전이에의한이차적림프종이더많다. 유방의원발성림프종의진단은병리적확진, 유방조직과림프절침윤이가까이존재하며전신성림프종이나이전의유방외림프종이배제되어야한다. 유방촬영에서는경계가잘그려지는단일혹은다발성결절을보이며액와부에일측성혹은양측성으로군집된액와부림프절종대와지방문의소실을보인다. 초음파에서는경계가잘그려지는둥글거나계란모양의균질한저음영의종괴로보이며낭성괴사로인해저음영의가낭성형태로나타날수있다 (8) (Fig. 12). FDG PET- CT 영상은림프종의병기와추적검사에도움이된다 (20) (Fig. 12). 유방의악성림프종은비호치킨림프종이대부분이며 T세포림프종보다 세포림프종이더흔하다 (21) (Fig. 12C). 결 액와부림프절종대는양성및악성의다양한질환들에의해생기며영상소견은유사하게보이므로감별이어렵다. 액와림프절이둥글고지방문의소실을보이며피질이편심성으로두꺼워진종대를보이더라도영상소견은양성질환과악성전이를감별하는데비특적이므로초음파유도하의세침검사나생검등을통한조직학적확진이요구된다. 론 참고문헌 1. be H, Schmidt R, Sennett C, Shimauchi, Newstead GM. USguided core needle biopsy of axillary lymph nodes in patients with breast cancer: why and How to do it. Radiographics 2007;27:S91- S99 2. Lee JY, Kim EK, Kim MJ, Youk JH, Oh KK. Imaging findings of palpable benign masses in axilla. J Korean Soc Med Ultrasound 2006;25:21-29 3. Shetty MK, Carpenter WS. Sonographic evaulation of isolated abnormal axillary lymph nodes identified on mammography. J Ultrasound Med 2004;23:63-71 4. Yang WT, Chang J, Metreweli C. Patients wit breast cancer: differences in color Doppler flow and gray-scale US features of benign and malignant axillary lymph nodes. Radiology 2000;215:568-573 5. be H, Schmidt R, kulkarni K, Sennet C, Mueller JS, Newstead GM. xillary lymph nodes suspicious for breast cancer metastasis: sampling with US-guided 14-gauge core-needle biopsy-clinical experience in 100 patients. Radiology 2009;250:41-49 6. Deurloo EE, Tanis PJ, Gilhije KG, Muller SH, Kröger R, Peterse JL, et al. Reduction in the number of sentinel lymph node procedures by preoperative ultrasonography of the axilla in breast cancer. Eur J Cancer 2003;39:1068-1073 7. Muttarak M, Pojchamarnwiputh S, Chaiwun. Mammographic features of tuberculous axillary lymphadenitis. ustralas Radiol 2002;46:260-263 8. Kim HJ, Kim KW, Park YS, Chung DJ, Cho YJ, Hwang CM, et al. Spectrum of axillary disorders (Excluding metastasis from breast cancer): radiolgical and pathological correlation: a pictorial essay. J Korean Radiol Soc 2007;57:583-594 9. Youk JH, Kim EK, Ko KH, Kim MJ. Sonographic features of axillary lymphadenopathy caused by kikuchi disease. J Ultrasound Med 2008;27:847-853 10. Kwon SY, Kim TK, Kim YS, Lee KY, Lee NJ, Seol HY. CT findings in kikuchi disease: analysis of 96 cases. JNR m J Neuroradiol 2004;25:1099-1102 11. ui-mansfield LT, Chew FS, Myers CP. ngiofollicular lymphoid hyperplasia (Castleman s disease) of the axilla. JR m J Roentgenol 2000;174:1060 12. Eapen M, Mathew CF, ravindan KP. Evidence based criteria for the histopathological diagnosis of toxoplasmic lymphadenopathy. J Clin Pathol 2005;58:1143-1146 13. Ridder GJ, oedeker CC, Lee TK, Sander. -mode sonographic criteria for differential diagnosis of cervicofacial lymphadenopathy in cat-scratch disease and toxoplasmosis. Head Neck 2003;25:306-312 14. Shin JH, Choi HY, Moon I, Sung SH. In vitro sonographic evaluation of sentinel lymph nodes for detecting metastasis in breast cancer: comparison with histopathologic results. J Ultrasound Med 2004;23:923-928 15. edi DG, Krishnamurthy R, Krishnamurthy S, Edeiken S, Le Petross H, Fornage D, et al. Cortical Morphologic features of axillary lymph nodes as a predictor of metastasis in breast cancer: in vitro sonographic study. JR m J Roentgenol 2008;191:646-652 16. Sapino, Cassoni P, Zanon E, Fraire F, Croce S, Coluccia C, et al. Ultrasonographically-guided fine-needle aspiration of axillary lymph nodes: role in breast cancer management. r J Cancer 2003;88:702-706 17. Uematsu T, Sano M, Homma K. In vitro high resolution helical CT of small axillary lymph nodes in patients with breast cancer: correlation of CT and histology. JR m J Roentgenol 2001;176:1069-1074 18. Oran I, Memis, Ustun EE. Ultrasonographic detection of interpectoral (Rotter s) node involvement in breast cancer. J Clin Ultrasound 1996;24:519-522 19. Easson M, Rotstein LE, Mccready DR. Lymph node assessment in melanoma. J Surg Oncol 2009;99:176-185 508
20. Schaefer NG, Hany TF, Taverna C, Seifert, Stumpe KD, von Schulthess GK, et al. Non-Hodgkin lymphoma and Hodgkin disease:coregistered FDG PET and CT at staging and restaging-do we need contrast-enhanced CT? Radiology 2004;232:823-829 21. Uesato M, Miyazawa Y, Gunji Y, Ochiai T. Primary non-hodgkin s lymphoma of the breast: report of a case with special reference to 380 cases in the japaneses literature. reast Cancer 2005;12:154-158 J Korean Soc Radiol 2010;62:501-509 Radiologic Findings of Various Diseases of the xillary Lymph Node with Pathologic Correlations 1 Guen Ho Ryu, M.D., Yun-Woo Chang, M.D., Hyung Hwan Kim, M.D. 2, Dong Wha Lee, M.D. 3, Kui Hyang Kwon, M.D., Deuk Lin Choi, M.D., Jung Hwa Hwang, M.D., Seung oo Yang, M.D. 4 Departments of 1 Radiology, 3 Pathology, Soonchunhyang University Hospital Departments of Radiology, 2 Soonchunhyang Cheonan Hospital, 4 Soonchunhyang Gumi Hospital xillary lymphadenopathy has multiple variable pathologic conditions such as a malignant or benign condition. It is important that we determine the radiologic findings of malignant lymphadenopathy and in turn determine the further course of evaluation for the lesion, because metastatic axillary lymphadenopathy represents an important prognostic factor. Recently, an ultrasonographic-guided axillary lymph node biopsy has been widely used as a diagnostic tool. We discuss the radiologic and pathologic findings of variable axilla diseases and outline the specific findings for determining the results of a lymph node biopsy. Index words : xilla Lymphatic system Radiography ddress reprint requests to : Yun-Woo Chang, M.D., Department of Radiology, Soonchunhyang University Hospital 22 Daesakwan-gil, Yongsan-gu, Seoul 140-743, Korea. Tel. 82-2-709-9396 Fax. 82-2-709-3928 E-mail: ywchang@hosp.sch.ac.kr 509