Intest Res 2013;11(1):14-22 나, 과거에는비교적드문질환이고병에대한정확한이해가부족하여명확하게분류되지못했다 년세계보건기구 (World Health Organizati

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1 REVIEW ISSN Intest Res 2013;11(1):14-22 Variable Clinical Classifications and Diagnostic Coding Systems of Colorectal Neuroendocrine Tumor Byung Chang Kim, Cheol Hee Park 1, Tae Il Kim 2, Suck-Ho Lee 3, Jin-Oh Kim 4, Hyun Soo Kim 5, Dong-Hoon Yang 6, Bora Keum 7, Sung Pil Hong 2, Seong-Eun Kim 8, Hyun Gun Kim 4, Jeong Eun Shin 9, Jae Myung Cha 10, Young Eun Joo 11, Dong Il Park 12, Hwang Choi 13, Kyu Chan Huh 14, Seung-Jae Myung 6, Dong Kyung Chang 12, Seun Ja Park 15 National Cancer Center, Goyang, Department of Internal Medicine, Hallym University College of Medicine 1, Anyang, Yonsei University College of Medicine 2, Seoul, Soonchunhyang University College of Medicine 3, Cheonan, Soonchunhyang University College of Medicine 4, Seoul, Yonsei University, Wonju College of Medicine 5, Wonju, University of Ulsan College of Medicine 6, Korea University College of Medicine 7, Ewha Womans University School of Medicine 8, Dankook University College of Medicine 9, Kyung Hee University School of Medicine 10, Seoul, Chonnam National University Medical School 11, Gwangju, Sungkyunkwan University School of Medicine 12, The Catholic University of Korea College of Medicine 13, Konyang University College of Medicine 14, Daejeon, Kosin University College of Medicine 15, Busan, Korea The incidence of colorectal carcinoid tumor is recently increasing as screening colonoscopy increased. Traditional carcinoid tumor had been known as low grade, malignant neuroendocrine cell orign tumor. In 2000, World Health Organization (WHO) suggested that carcinoid was called well-differentiated neuroendocrine tumor (NET). It recently updated in 2010 by WHO; according to the differentiation and malignant potential, NET classified with NET Grade 1, Grade 2, and neuroendocrine carcinoma. They suggested that NET had malignant potential in accordance with histopathologic characteristics. Therefore, WHO recommended the behavior code of NET as malignant. However, European Neuroendocrine Tumor Society (ENETS) proposed the behavior of NET to four grades based on the histopathologic features; benign, benign or low grade malignant, low grade malignant, and high grade malignant. Also, American Joint Committee on Cancer (AJCC) suggested that topography codes of NET were defined as malignant. Korean Standard Classification of Diseases (KCD) described the different codings of carcinoid (NET). The discrepancies of behavior code or coding system exist among WHO, ENETS, AJCC and KCD. Also, there were differences in the perception for topographic coding system between clinicians and pathologists. NETs of colorectum were reported with the variable clinical characteristics (especially, metastasis) and long term prognosis from many studies. Especially, risk of metastasis and long term prognosis of small sized NET (<1 cm) had some discrepancies and should be investigated prospectively. Therefore, the consensus about topographic codes of NET should be needed with multidisplinary approach among gastroenterologists, pathologists and surgeons. (Intest Res 2013;11:14-22) Key Words: Carcinoid tumor; Neuroendocrine tumor; Neuroendocrine carcinoma 서론 카르시노이드종양은 1907 년에독일의병리학자 Oberndorfer 에의 Received March 26, Revised September 20, Accepted September 21, Correspondence to Cheol Hee Park, Department of Internal Medicine, Hallym University Sacred Heart Hospital, 22 Gwanpyeong-ro 170beon-gil, Dongangu, Anyang , Korea. Tel: , Fax: , 해서일반적인샘암종에비해서비교적저등급의악성임상경과를보이는종양이라는의미로 karzinoid (carcinoma-like) 라고처음소개되었다. 그후 1914 년에 Gosset 과 Masson 등이내분비관련종양임을확인하였으며, 1963 년에 Williams 와 Sandler 는발생기원에따라서앞창자 ( 폐, 위, 상부공장, 췌장 ), 중간창자 ( 하부공장, 회장, 충수, 맹장 ), 뒤창자 ( 대장, 직장 ) 카르시노이드종양으로분류하였다. 1,2 카르시노이드종양은장크롬친화성세포 (enterochromaffin cell, EC 세포 ), 가스트린세포등여러세포에서발생할수있어다양한호르몬을분비하게되고, 이와관련한다양한임상양상을보일수있으 Copyright Korean Association for the Study of Intestinal Diseases. All rights reserved. This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.

2 Intest Res 2013;11(1):14-22 나, 과거에는비교적드문질환이고병에대한정확한이해가부족하여명확하게분류되지못했다 년세계보건기구 (World Health Organization, WHO) 는췌장과갑상샘의내분비종양, 부신경절종 (paraganglioma), 폐의소세포암, 피부의 Merkel 세포종양을제외한대부분의내분비종양을카르시노이드종양으로분류하였다. 그러나, 다양한임상양상을보이는이종양에적용하기에제한이있어, 호르몬과임상양상에관계없이분화가좋은신경내분비종양 (neuroendocrine tumor, NET) 에대해서 카르시노이드종양 이라는용어가사용되었고, 종양의발생빈도, 발생부위별분포, 악성도에따라서분류및진단기준측면이변화하였다 년 WHO 분류에서는소화기계와내분비계분야에서서로다른분류를제시하였다. 즉내분비종양분류에서는 카르시노이드종양 보다는신경내분비종양이라는용어사용을권고하였고, 분화도와악성도에따라서 3가지 (well-differentiated endocrine tumor, well-differentiated endocrine carcinoma, poorly-differentiated endocrine carcinoma/small cell carcinoma) 로분류할것을제시하였다 년 WHO 분류에서는신경내분비종양으로용어를통일하였고세포증식정도 (Ki- 지수또는유사분열수 ) 에따라서악성정도를 Grade 1 (G1), Grade 2 (G2), Grade 3 (G3) 로분류하였다. 2,6 이와같이카르시노이드종양에대해서는여러가지분류법이제시되어혼돈을불러일으키고있는데, 본고에서는결장및직장의신경내분비종양의여러가지분류에따른시각차이를알아보고자한다. 대장신경내분비종양의분류 1. WHO 분류 2, 년내분비계종양에대한 WHO 분류에서는조직학적소견및임상양상 ( 크기, 위치, 호르몬생성, 분화도, 증식비율 ) 에따라서고분화신경내분비종양 (well-differentiated NET; carcinoid, 유암종 ), 고분화신경내분비암종 (well-differentiated neuroendocrine carcinoma, 저등급악성 ), 미분화신경내분비암종 (poorly-differentiated neuroendocrine carcinoma, 고등급악성 ) 의 3 군으로구분하였다 년과 2007 년유럽내분비종양학회 (European Neuroendocrine Tumor Society, ENETS) 에서제시한등급 (grading) 분류와발생장 기에따른병기체계를근거로 2010 년 WHO 분류에서는 1) 발생부 위에따라서종양의차이가있는이질성, 2) 종양세포의분화도에따 른차이, 3) 오랜경과관찰에서신경내분비종양이결국악성종양이 라는개념을도입하였고, 분화도에따라서고분화신경내분비종양을 신경내분비종양 G1 (NET G1) 으로, 고분화신경내분비암종을 신 경내분비종양 G2 (NET G2) 로, 미분화신경내분비암종은 신경내 분비암종 (neuroendocrine carcinoma, NEC) 으로다시분류하였다 (Table 1). 2,6 등급은형태학적인기준과유럽내분비종양학회에서제안한증식 정도를기반으로분류하였다 (Table 2). 7 그러나, 이등급체계가위, 십이지장, 췌장의신경내분비종양에는유용하지만, 장 ( 특히, 직장 ) 에서발생하는신경내분비종양에도유효한지에대해서는아직근거 가부족하다. 6 결장에서발생하는신경내분비종양은매우드물게발생하지만, Table 2. Grade of Neuroendocrine Tumor from Rindi et al. 7 Grade Mitotic count (10 HPF)* Ki-67 index (%) G1 (low) <2 2 G2 (intermediate) G3 (high) >20 >20 *10 HPF; high power field=2 mm 2, at least 40 fields (at 40 magnification) evaluated in areas of highest mitotic density. MIB1 antibody; percent of 2,000 tumor cells in areas of highest nuclear labeling. Table 1. Transition Scheme for the New Classification (WHO 2010) Including Previous Definitions for Neuroendocrine Neoplasms of the Digestive System (WHO 1980 and 2000) 6 WHO 1980 WHO 2000 WHO Carcinoid 1. Well-differentiated endocrine tumor (WDET)* 1. NET G1 (carcinoid) 2. Well-differentiated endocrine carcinoma (WDEC) 2. NET G2 3. Poorly-differentiated endocrine/small cell carcinoma (PDEC) 3. NEC (large cell or small cell type), 2. Mucocarcinoid 4. Mixed exocrine-endocrine carcinoma (MEEC) 4. Mixed adenoneuroendocrine carcinoma (MANEC) 3. Mixed forms carcinoid-adenocarcinoma 4. Pseudotumor lesions 5. Tumor-like lesions (TLL) 5. Hyperplastic and preneoplastic lesions WHO, World Health Organization; G, grade (for definition, see text); NET, neuroendocrine tumor; NEC, neuroendocrine carcinoma. *The difference between WDET and WDEC was defined according to staging features in the WHO 2000 classification. G2 NET does not necessarily translate into WDEC of the WHO 2000 classification. Definition in parentheses for the international Classification of Diseases for Oncology (ICD-O) coding. NET G3 has been used for this category but is not advised, since NETs are by definition well-differentiated. 15

3 Byung Chang Kim, et al. Classification and Diagnosis of Colorectal NET 대부분조직병리학적으로미분화신경내분비암종이며이미진단당시전이된경우가많아나쁜예후를보인다. 8 면역조직화학염색에서는시냅토피신양성과소마토스타틴양성소견을보인다. 2 직장신경내분비종양은결장에서발생하는종양과비교하여더흔하게발생하고대부분내시경도중에우연히발견되며분화도가좋고, 크기는 1 cm 미만이며점막하층에국한되어있어전이위험성이낮아결장신경내분비종양과비교하여양호한예후를보인다. 그러나, 고유근층을침범하거나크기가 2 cm 이상인경우는전이위험성이증가한다 년보완된 WHO 분류에서는이러한조직병리학적인인자들을바탕으로소화관신경내분비종양의생물학적인습성을네가지분류로나누어예후를평가하였으며, 결장과직장의신경내분비종양의분류는다음과같다. 2 cm 이하, 비기능성이고, 점막하층에국한된혈관침범이없는경우를 양성고분화신경내분비종양 (benign well-differentiated NET) 으로, 양성고분화신경내분비종양의요소에혈관침범이추가된경우를 양성또는저등급악성고분화신경내분비종양 (uncertain malignant potential NET) 으로, 고 유근층을침범하거나전이가있는경우를 저등급악성고분화신경내분비종양 (low-grade malignant NET) 으로, 미분화신경내분비종양은 고등급악성신경내분비종양 (high-grade malignant NET) 으로분류하였다 (Tables 3, 4). 2,9 대장신경내분비종양은발생학적인세포형태에따라서 EC 세포와엔테로글루카곤세포 (enteroglucagon cell; L 세포 ) 종양으로분류될수있다. 직장신경내분비종양은약 80% 정도에서글루카곤유사펩타이드 (glucagon-like peptide) 및 pancreatic polypeptide/ polypeptide YY- (PP/PYY-) 를생성하는 L 세포형태를보이며, 결장신경내분비종양은주로 EC 세포형태를보인다. EC 세포신경내분비종양은 L 세포신경내분비종양과달리크로모그라닌 A, 시냅토피신, 세로토닌등 EC 세포에서생성하는단백질에양성소견을보이고, 속이들어찬둥지모양으로종양세포들이배열 (solid nests, with peripheral palisades) 되어있으며어떤경우에는샘형태 (glandular aspects) 배열을보이기도한다. 6,10 종양학에대한국제질병분류 (International Statistical Classification Table 3. Criteria for Assessing the Prognosis of Neuroendocrine Tumors of the Gastrointestinal Tract 9 Biological behavior Metastases Invasion of muscularis propria Histological differentiation Tumor size (cm) Angioinvasion Ki-67 index (%)* Hormonal syndrome Benign Negative Negative Well-differentiated 1 Negative <2 Negative Benign or low-grade Negative Negative Well-differentiated 2 Negative/positive <2 Negative malignant Low-grade malignant Positive Positive Well-differentiated >2 Positive >2 Positive High-grade malignant Positive Positive Poorly-differentiated Any Positive >20 Negative *MIB1 antibody; percent of 2,000 tumor cells in areas of highest nuclear labeling. Benign or low grade malignant means uncertain malignant potential. Table 4. Stratified Prognosis Based on ENTES and 2004 WHO Revised Classification of Neuroendocrine Tumors of Cecum, Colon and Rectum 2 A. Well-differentiated neuroendocrine tumor (carcinoid) a-1. Benign: nonfunctioning, confined to mucosa-submucosa, nonangioinvasive, 2 cm (colon-rectum) 2 (<1 cm; The Gastrointestinal Pathology Study Group of Korean Society of Pathologists) 11 Serotonin-producing tumor Enteroglucagon-producing tumor a-2. Benign or low grade malignant (uncertain malignant potential): nonfunctioning, confined to mucosa-submucosa, angioinvasive, or <2 cm (colon-rectum) 2 (1-2 cm; The Gastrointestinal Pathology Study Group of Korean Society of Pathologists) 11 Serotonin-producing tumor Enteroglucagon-producing tumor B. Well-differentiated neuroendocrine carcinoma (malignant carcinoid) b. Low grade malignant: invasion of the muscularis propria or beyond, or metastases Nonfunctioning or functioning serotonin-producing carcinoma (with carcinoid syndrome) Nonfunctioning enteroglucagon-producing carcinoma C. Poorly-differentiated neuroendocrine carcinoma High grade malignant ENETS, European Neuroendocrine Tumor Society; WHO, World Health Organization. 16

4 Intest Res 2013;11(1):14-22 Diseases and Related Health Problems-Oncology, ICD-O) 코드도변화되어왔다 년 WHO 분류는대장에서발생하는신경내분비종양, 신경내분비암종및 mixed adenoneuroendocrine carcinoma (MANEC) 를행태코드 (biological behavior code) /3으로구분하였다. EC 세포신경내분비종양과세로토닌생성신경내분비종양은 /3 로분류하나, L 세포신경내분비종양은 /1 ( 경계형 ) 으로분류하고있다. EC 세포신경내분비종양은 2000 년분류에서도 /3으로구분되었으나, L 세포신경내분비종양의행태코드는 2010 년부터새롭게제시되었다. 6 이러한분류는 L 세포신경내분비종양이 EC 세포신경내분비종양과달리세로토닌생성보다는글루카곤유사펩타이드및 PP/PYY- 를생성하고, 핵의형태가비교적균일하고, 유사분열수가 10 고배율당대부분 2개미만이기때문이다. L 세포신경내분비종양은크로모그라닌 A가거의대부분음성이지만전립선산프로테아제 (prostatic acid protease) 양성이 80% 이상에서관찰된다. 6 그러나, 아직 EC 세포신경내분비종양과 L 세포신경내분비종양을정확하게구분할수있는객관적인진단기준및합의가없는상태이다. 2. 국제종양학분류 (ICD-O) 12 ICD-O 는신생물의형태분류에대한내용으로 2000 년도에개정 3판 (ICD-O-3) 이발행되었는데개정이전의분류와연계해서사용의편의를돕기위해새로이제정한신생물형태의부호화된명명법 을고시하였다. 부호를포함하여살펴보면형태분류번호는 5자리로구성되어있는데처음 4자리수는신생물의조직학적형태 (morphology code) 를표시하고사선뒤의 5째자리수는행동양식을표시하는행태코드이다. 행태코드에서양성종양은 /0으로, 원발부위의악성은 /3, 양성또는악성여부가불확실한종양또는경계형악성또는낮은악성잠재성또는불확실한악성잠재성은 /1, 상피내신생물 (intraepithelial neoplasia grade III) 과비침윤성암의경우 /2를부여하였다. 카르시노이드종양 ( 충수제외 ), EC 세포카르시노이드, 악성 EC 유사세포종양, 그리고신경내분비암종은행태코드를 /3을부여하나, 불확실한악성잠재성의카르시노이드종양, EC 유사세포카르시노이드, 관상카르시노이드등은 /1를부여하고있다 (Table 5). 12 ICD-O-3 코드는조직학적으로같은종양이라도발생장기및부위에따라행태코드를포함하여코드가달라질수있다는점을감안해야한다. 3. 유럽내분비종양학회 (ENETS) 7 유럽내분비종양학회에서도 카르시노이드종양 을분화도와발생위치에따라구분하였다. 13 고분화카르시노이드종양 (WHO 분류에의하면 NET, G1), 고분화카르시노이드암종또는악성카르시노이드 (WHO 분류에의하면 NET, G2) 및미분화된소세포내분비암종 Table 5. Biologic Behavior Codes of ICD-O-3 in Colon and Rectum 12 Code Disease ICD-10 Classification /0 Benign D12 ICD-O-3 /1 Uncertain behavior whether benign or malignant D Carcinoid tumor of uncertain malignant potential (M8240/1) Borderline malignancy Low malignant potential Uncertain /2 Carcinoma in situ D01.0-D01.2 Intraepithelial Noninfiltrating Noninvasive EC like cell carcinoid (M8242/1) Tubular carcinoid (M8245/1) Carcinoid tumor at appendix (M8240/1) /3 Malignant, primary site C18, C19, C20 Carcinoid tumor (except appendix) (M8240/3) /6 Malignant, metastatic site /9 Malignant, secondary site Malignant, uncertain whether primary or metastatic site EC cell carcinoid (M8241/3) NEC (M8246/3) EC cell like carcinoid, malignant (M8242/3) ICD-O, International Statistical Classification Diseases and Related Health Problems-Oncology; EC, enterochromaffin; NEC, neuroendocrine carcinoma. 17

5 Byung Chang Kim, et al. Classification and Diagnosis of Colorectal NET (WHO 분류에의하면 NEC) 으로나누었다. 13 조직병리소견을보면, 고분화된카르시노이드종양은균일한형태세포, 유사분열세포가거의없고, 점액생산이없고, 점막하층에주로분포하고, 림프관, 혈관, 신경, 근육층침범이거의없다. 고분화카르시노이드암종또는악성카르시노이드는고분화된카르시노이드종양보다유사분열수가많고, 근육층과림프관및혈관침범소견이관찰된다. 미분화된소세포내분비암종은중심부에괴사가관찰되고, 많은유사분열수를갖는심한이형성, 근육층을넘어서는침범이흔하고혈관및림프관침범이더많이관찰된다. 13,14 직장내에서발생하는신경내분비종양은현미경소견에서기둥모양 (trabecular pattern) 형태가특징이고, 결장내종양은소장에서주로관찰되는섬모양또는둥지모양형태또는혼합형태를보인다. 6,10 신경내분비종양의예후예측에는종양세포의분화도와증식도가도움이될수있다. 분화도는고분화또는미분화로분류되고, 증식도는유사분열수혹은증식지수 (high proliferative index) 를사용하며, 증식지수는 Ki-67/MIB1 염색을통해서결정된다. 조직병리학적으로전이위험요소에는림프관또는혈관침범, 크기, 고유근층침범등이있다. 그러나, 이러한위험요소들이없어도경과관찰하는도중에재발하는경우가있어유럽내분비종양학회에서는유사분열수와증식지수를기준으로 G1부터 G3까지 3단계로고분화신경내분비종양을구분하였다 (Table 2). 7 T 병기는 7판 American Joint Committee on Cancer (AJCC) 병기와동일하게 T1 병기를 1 cm 미만은 T1a, 1-2 cm는 T1b로구분하 였다. T2는 2 cm 초과하거나, 고유근층까지침범하는경우로정의하였다 (Table 6). 7,15 유럽내분비종양학회에서는 T1a, T1b을기준으로 Stage IA 와 IB 로구분하지만 WHO 와 7판 AJCC 에서는구분하지않고 Stage I으로정의하였다. 4. 대장신경내분비종양의 7판 AJCC 분류 (Table 5) 15 신경내분비종양의병기체계는 7판 AJCC 분류에서새로이추가되었으며, 발생장기에따라서다른병기체계를사용하였다. 7판 AJCC 분류는카르시노이드종양, 고분화신경내분비종양, 비정형카르시노이드암종, 고분화신경내분비암종등에는신경내분비종양병기가적용되는반면, 고등급신경내분비암종또는혼합형샘신경내분비세포암종 (mixed glandular/well-differentiated NEC) 에대해서는샘종성암종의병기가적용되었다. 15 예후인자는발생장기에따라차이가있으며, 다른연구들에서와같이혈장크로모그라닌 A, 소변내 5-hydroxyindolacetic acid (5- HIAA) 의양및유사분열수등이연관이있다. 조직학적등급을분류할때세포의다형태성 (pleomorphism) 이유용하지않고, 높은증식지수가나쁜생물학적인행태를보였다. 특히, 중간창자의신경내분비종양은높은유사분열수를보이는경우가더침습적이므로전신항암치료를권유하기도한다. 15 분류코드는 ICD-O-3 를따르며, 위치에따라서직장은 C20.9, 소장은 C17.0-C17.9, 대장은 C18.0-C19.9 로코드를부여한다. 조 Table 6. Proposal for TNM Classification, and Stages for Endocrine Tumors of Colon and Rectum by ENETS 7,15 TNM Stages (ENETS) T N M T-primary tumor IA T1a N0 M0 TX Primary tumor cannot be assessed IB T1b N0 M0 T0 No evidence of primary tumor IIA T2 N0 M0 T1 Tumor invades mucosa or submucosa IIB T3 N0 M0 T1a Size <1 cm IIIA T4 N0 M0 T1b Size 1-2 cm IIIB Any T N1 M0 T2 Tumor invades muscularis propria or size >2 cm IV Any T Any N M1 T3 Tumor invades subserosa/pericolic/perirectal fat T4 Tumor directly invades other organs/structures and/or perforates visceral peritoneum WHO AJCC 7th T N M For any T add (m) for multiple tumors I T1 N0 M0 N-regional lymph nodes IIA T2 N0 M0 N X Regional lymph node status cannot be assessed IIB T3 N0 M0 N0 No regional lymph node metastasis IIIA T4 N0 M0 N1 Regional lymph node metastasis IIIB Any T N1 M0 M-distant metastases (subspecification as in small bowel) IV Any T Any N M1 M X Distant metastasis cannot be assessed M0 No distant metastases M1 Distant metastasis ENETS, European Neuroendocrine Tumor Society. 18

6 Intest Res 2013;11(1):14-22 직학적행태에따라서는 M8240 ( 카르시노이드종양 )-M8242 ( 장크롬친화성유사세포종양 ), M8246 ( 신경내분비암종 ) 및 M8249 ( 비정형적카르시노이드종양 ) 등을부여하였다 한국표준질병사인분류 (Korean Standard Classification of Disease, KCD) 16 KCD 분류는통계청에서통계기준설정의일환으로 WHO 의권고에따라 1952 년 ICD 를번역하여공표한이래 2010 년까지모두 6차례의개정을시행하였는데, 6차개정까지모두 WHO 에서권고하고있는 ICD 의기준과체계를따르고있다. 특히, 우리나라에서많이발생하는 300 대질병에대해서세분화하였고, WHO 의 ICD-10 의업데이트내용을반영하였다. KCD 의항목분류는 ICD 와마찬가지로위치에따라 3단위로분류하고세부항목은 4단위로분류하였다. 결장과직장의악성신생물은 C18 ( 결장 ), C19 ( 직장구불결장이행부 ), C20 ( 직장 ) 코드로분류되며세부위치에따라 4단위로나뉜다. 상피내신생물 ( 제자리신생물 ) 은 D00-D09 의 3단위코드로구분되는데 4단위코드의경우결장은 D01.0, 직장구불결장이행부는 D01.1, 직장은 D01.2 로분류되었다. 그러나, 점막하층에서발생하는신경내분비종양은 D01 분류에해당사항이없다. D12 코드는결장의양성종양을 D12.6 으로, 직장의양성종양은 D12.7 로세분화할수있다 년도에개정된 KCD-6 에서는악성신생물인경우진행정도를표기하기위해서 5 단위를추가하면서국내고유코드를도입하였다. 5단위에서 0은초기, 1은진행성, 9는상세불명으로사용한다 (Table 7). 16 KCD 코드는악성신생물의조직형태에상관없이 ( 암종, 육종, 중피종등 ) 포괄적 Table 7. The KCD Classification of Neoplasm and Subclassification of Colorectum 16 Malignant neoplasm (C18, C19, C20, C21) C18; Colon C19; Rectosigmoid junction C20; Rectum C21; Anus and anal canal KCD-6 (Korean unique code) e.g.) ; early ; advanced ; unspecified In situ neoplasm (D01.0-D01.3) D01; CIS of other and unspecified digestive organs KCD, Korean Standard Classification of Diseases;, Korean unique code; CIS, carcinoma in situ. Benign neoplasm (D12.0-D12.9) D12; Benign neoplasm of colon, rectum, anus and anal canal Table 8. Results of Questionnaire for ICD-O-3 Code of Gastrointestinal Carcinoid Tumor (The Gastrointestinal Pathology Study Group of Korean Society of Pathologists) 11 Organ or subject Carcinoid tumor Appendix Rectum Diagnosis ICD-O-3 code (n=240) NA All except appendix and rectum Carcinoid tumor (=well differentiated neuroendocrine tumor: Size <1 cm, no invasion) Carcinoid tumor (=well differentiated neuroendocrine carcinoma: Any size, mesoappendix invasion, metastasis, angioinvasion) Carcinoid tumor (=well differentiated neuroendocrine tumor: size <1 cm, no invasion) Carcinoid tumor (=well differentiated neuroendocrine carcinoma: Any size, muscle invasion, angioinvasion, node or distant metastasis) The proposition on the 1st Education Program for Gastrointestinal Pathology sponsored by the Korean Society of Pathologists in 2011 All gastrointestinal carcinoid tumor except appendix and rectum /3 Rectum NET G1, L cell type (size <1cm, no angioinvasion) /1 NET G1, EC cell, or L cell (with risk factors) /3 NET G2 /3 NEC /3 NA, not available; G, grade; L cell, Enteroglucagon cell; EC cell, Enterochromaffin cell; NET, neuroendocrine tumor; NEC, neuroendocrine carcinoma. Risk factors; any size, muscle invasion, angioinvasion, node or distant metastasis. 19

7 Byung Chang Kim, et al. Classification and Diagnosis of Colorectal NET 으로적용하는코드이며이러한조직학적인행태를보완하기위해서 ICD-O 행태코드를추가해서사용하도록권고하고있다. 따라서신경내분비종양은 KCD 항목에서 D 코드 (D12), C 코드 (C18-21) 에대한정확한언급은없고 ICD-O 행태코드에대한언급만있다. 6. 병리의사를위한소화기계암등록에대한제안 년대한병리학회소화기병리연구회에서는 2000 년에 WHO 에서제시한것과같이카르시노이드종양보다는 고분화신경내분비성종양 으로기술하기로하고, 증상없이우연히발견된크기가작은종양이라도악성종양의가능성을가지고있으므로적어도 ICD-O-3 의 /1 이상의행태코드를부여하였다. 일반적으로카르시노이드종양은분화, 크기, 혈관침윤, 증식도, 전이, 주변장기로의침윤, 호르몬분비등에따라예후가결정되고, 발생하는위치에따라서크기가같은경우일지라도생물학적인특성과예후가다르다. ICD-O-3 행태코드와유사하게충수의관상카르시노이드종양을제외한카르시노이드종양에대해서행태코드 /3을부여하였다. 충수에우연히발견되는 1 cm 미만의혈관침범이없는작은신경내분비종양은 2004 년보완된 WHO 분류에근거하여행태코드 /1을부여하는것이타당하다고하였다. 또한직장의 1 cm 미만의 고분화신경내분비종양 은악성종양의가능성은있지만, 점막하층에국한되고혈관침범이없는경우국소절제만으로적절하게치료된다는점에서행태코드 /1을부여하는것이타당하다고하였다. 그러나, 근층또는혈관침범소견을보이는경우는크기에관계없이행태코드 /3을권고하였다 (Table 4, 8). 2, 년 WHO 분류가개정된후 2011 년개최된소화기병리연구회연수교육에서직장신경내분비종양행태코드부여는크기가 1 cm 미만이고, 혈관계침범이없으며, L 세포형태인신경내분비종양 G1 을 /1로하고나머지직장신경내분비종양은 /3로할것을제안하였다 (Table 8) 대장신경내분비종양전이위험인자종양악성화의대표적인요소는림프절및다른장기로의원격전이이다. 직장신경내분비종양의전이와연관된병리요소들은종양의크기, 림프관및혈관침윤, 침윤깊이, 및유사분열수등이있다. 신경내분비종양이붉은색을띄는경우와함몰및궤양의소견을가지는경우에전이위험이증가한다. 직장신경내분비종양의크기에따른전이위험은다양하게보고되고있다. 대부분의연구에서는 2 cm 이상직장신경내분비종양인경우림프절및원격전이위험성이 45-74% 로매우높다. 1-2 cm 크기의직장신경내분비종양인경우전이확률은 % 이며, 점막하층에국한된경우 18.6% 까지보고되고있다. 1 cm 이하의직장신경내분비종양의경우에도전이위험성은 0-9.7% 까지매우다양하게보고되었다 cm 이하의직장신경내분비종양에서림프절전이는림프관또는혈관침윤, 높은유사분열수, 고유근층침윤등이있는경우발 생하나, 이들위험요소가없는경우에도림프절전이가가능하다. 18 국내에서는이와관련된두가지다기관연구가보고되었다. 25,26 Park 등 26 은 2 cm 미만의 402 예의직장신경내분비종양을대상으로분석하였다. 전이와연관된인자는크기, 유사분열비율, 림프관및혈관침윤이었고, 1 cm 이하에서는전이소견이없었으며, 크기는 14 mm 미만이고다른전이위험인자가없다면전이위험성이거의없었다. 크기에관계없이직장신경내분비종양을진단받은 514 예를대상으로한연구에서는 25 1 cm 이하인경우림프절전이율은 1.99% 가관찰되었고, 추가적인위험인자에따른전이위험성은분석하지않았다. 8. 직장신경내분비종양분류의문제점앞서언급한여러가지기준을보면, 2 cm가넘는직장의신경내분비종양은악성으로진단하는것에는이견이없는것으로보인다. 그러나, 경계영역인 1-2 cm 사이는양성또는악성 ( 저등급악성 ; 불명확한악성도 ) 으로유럽내분비종양학회에서는분류하였지만전이위험성이 10-15% 로있으며, 특히 Soga 23 는 27.6% 까지전이가있다고보고하고있어, 1-2 cm 사이의직장신경내분비종양은악성으로분리하자는의견도있다. 7 특히 1 cm 미만의직장신경내분비종양에대해서는 D코드로진단을할지아니면 C코드로진단해야하는지에대해논란이많다. 1) D코드입장직장신경내분비종양은결장신경내분비종양에비해서좋은경과를가지며, 특히혈관침윤이없고 2 cm 이하인경우 2004 년개정 WHO 및유럽신경내분비종양학회분류에서는양성으로분류하였으나, 년 대한병리학회소화기병리연구회 에서는 1 cm 이하이면서점막하층에국한되어있고, 혈관침범이나원격전이소견이없는분화가좋은신경내분비종양에서도 3% 에서전이가있을수있으므로 ICD-O-3 /1 code 인 불명확한악성도 로분류할것을제안하였다. 11 Konishi 등 20 도 1 cm 이하이며혈관및림프관침범이없는경우, 국소적인치료가가능하고림프절이나원격전이가능성은낮다고하였다. 1 cm 미만의직장신경내분비종양은국제종합암네트워크 (National Comprehensive Cancer Network) 가이드라인에서는고유근층침범이없고림프절전이소견이없는경우국소절제후추적관찰이필요없는것으로권고하고있다. 27 2) C코드입장 2007 년 대한병리학회소화기병리연구회 에서는크기에관계없이근육층또는혈관침윤이있는경우와림프절또는원격전이가있는경우는악성으로분류할것을제안하였다. 11 이러한위험인자들이없는 1 cm 이하에서도진단당시림프절전이소견 ( %) 이관찰되거나국소치료후추적관찰도중에재발하는경우가보고되기도한다. 9,14,18,23,25,28,29 특히 Soga 23 는 5 mm 이하인카르시노이드종양에서도림프절또는원격전이를 3.7% 로보고하였고, cm 크기에서는 13.2% 로보고하였다. 그러므로크기가 1 cm 미만이더라도국 20

8 Intest Res 2013;11(1):14-22 소및원격전이의위험이있는악성도가존재한다. 그러나, 최근 2010 년 WHO 개정판에서신경내분비종양의세포형 태에따른분류를추가하여행태코드도각각악성과불명확한악성 도로구분하였으나병리학적인명확한진단기준이정립되어있지않 아임상적으로적용하기위해서는더많은연구가필요하다. 결론 지금까지대장신경내분비종양에대해서 WHO 분류, 유럽신경내 분비종양학회분류, 그리고 AJCC 분류기준과질병등록코드및한 국에서사용하고있는코드를살펴보았다. 대장신경내분비종양의 특성과예후는아직명확하게밝혀지지않았다. 현재대장신경내분 비종양의예후와전이위험인자에대한연구들이많이보고되고있 는데, 향후 1 cm 미만의직장신경내분비종양에대한전이위험인자 및장기예후에대한연구가필요하며, 직장신경내분비종양의질병 코드에대해서는소화기내과, 병리과등을포함한다학제적의견교 환에의한정립이필요하다고생각한다. REFERENCES 1. Van Eeden S, Quaedvlieg PF, Taal BG, Offerhaus GJ, Lamers CB, Van Velthuysen ML. Classification of low-grade neuroendocrine tumors of midgut and unknown origin. Hum Pathol 2002;33: Klöppel G, Perren A, Heitz PU. The gastroenteropancreatic neuroendocrine cell system and its tumors: the WHO classification. Ann N Y Acad Sci 2004;1014: Chetty R. An overview of practical issues in the diagnosis of gastroenteropancreatic neuroendocrine pathology. Arch Pathol Lab Med 2008;132: Klimstra DS, Modlin IR, Adsay NV, et al. Pathology reporting of neuroendocrine tumors: application of the Delphic consensus process to the development of a minimum pathology data set. Am J Surg Pathol 2010;34: Washington MK, Tang LH, Berlin J, et al; Members of the Cancer Committee, College of American Pathologists. Protocol for the examination of specimens from patients with neuroendocrine tumors (carcinoid tumors) of the colon and rectum. Arch Pathol Lab Med 2010;134: Bosman F, Carneiro F, Hruban R, Theise N. WHO classification of tumours of the digestive system. 4th ed. Lyon: IARC, Rindi G, Klöppel G, Couvelard A, et al. TNM staging of midgut and hindgut (neuro) endocrine tumors: a consensus proposal including a grading system. Virchows Arch 2007;451: Grabowski P, Schönfelder J, Ahnert-Hilger G, et al. Expression of neuroendocrine markers: a signature of human undifferentiated carcinoma of the colon and rectum. Virchows Arch 2002;441: Klöppel G, Rindi G, Anlauf M, Perren A, Komminoth P. Sitespecific biology and pathology of gastroenteropancreatic neuroendocrine tumors. Virchows Arch 2007;451(Suppl 1):S9-S Hamilton SR, Aaltonen LA. Pathology and genetics of tumours of the digestive system. 1st ed. Lyon: IARC, Cho MY, Kang YK, Kim KM, et al. Porposal for creating a guideline for cancer registration of the gastrointestinal tumors (I). Korean J Pathol 2008;42: Fritz A, Jack A, Parkin DM, et al. International classification of diseases for oncology (ICD-O). 3rd ed. Geneva: World Health Organization, Plöckinger U, Rindi G, Arnold R, et al; European Neuroendocrine Tumour Society. Guidelines for the diagnosis and treatment of neuroendocrine gastrointestinal tumours. A consensus statement on behalf of the European Neuroendocrine Tumour Society (ENETS). Neuroendocrinology 2004;80: Ramage JK, Goretzki PE, Manfredi R, et al; Frascati Consensus Conference participants. Consensus guidelines for the management of patients with digestive neuroendocrine tumours: welldifferentiated colon and rectum tumour/carcinoma. Neuroendocrinology 2008;87: Edge SB. AJCC cancer staging manual. 7th ed. New York; London: Springer, Statistics Korea. Korean standard classification of dieases and causes of death Daejeon: Statistics Korea, Shields CJ, Tiret E, Winter DC; International Rectal Carcinoid Study Group. Carcinoid tumors of the rectum: a multi-institutional international collaboration. Ann Surg 2010;252: Fujimoto Y, Oya M, Kuroyanagi H, et al. Lymph-node metastases in rectal carcinoids. Langenbecks Arch Surg 2010;395: Tsukamoto S, Fujita S, Yamaguchi T, et al. Clinicopathological characteristics and prognosis of rectal well-differentiated neuroendocrine tumors. Int J Colorectal Dis 2008;23: Konishi T, Watanabe T, Kishimoto J, et al; Japanese Society for Cancer of the Colon and Rectum. Prognosis and risk factors of metastasis in colorectal carcinoids: results of a nationwide registry over 15 years. Gut 2007;56: Läuffer JM, Zhang T, Modlin IM. Review article: current status of gastrointestinal carcinoids. Aliment Pharmacol Ther 1999;13: Naunheim KS, Zeitels J, Kaplan EL, et al. Rectal carcinoid tumors--treatment and prognosis. Surgery 1983;94: Soga J. Early-stage carcinoids of the gastrointestinal tract: an analysis of 1914 reported cases. Cancer 2005;103: Kobayashi K, Katsumata T, Yoshizawa S, et al. Indications of endoscopic polypectomy for rectal carcinoid tumors and clinical usefulness of endoscopic ultrasonography. Dis Colon Rectum 2005;48: Colonoscopy Study Group of Korean Society of Coloproctology. Clinical characteristics of colorectal carcinoid tumors. J Korean Soc Coloproctol 2011;27: Park CH, Cheon JH, Kim JO, et al. Criteria for decision making after endoscopic resection of well-differentiated rectal carcinoids with regard to potential lymphatic spread. Endoscopy 2011;43: Clark OH, Benson AB 3rd, Berlin JD, et al; NCCN neuroendocrine tumors panel members. NCCN clinical practice guidelines 21

9 Byung Chang Kim, et al. Classification and Diagnosis of Colorectal NET in oncology: neuroendocrine tumors. J Natl Compr Canc Netw 2009;7: Fahy BN, Tang LH, Klimstra D, et al. Carcinoid of the rectum risk stratification (CaRRs): a strategy for preoperative outcome assessment. Ann Surg Oncol 2007;14: Li AF, Hsu CY, Li A, et al. A 35-year retrospective study of carcinoid tumors in Taiwan: differences in distribution with a high probability of associated second primary malignancies. Cancer 2008;112:

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