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1 1425 COMMENTARY Classification Schemes for Tumors Diagnosed in Adolescents and Young Adults Ronald D. Barr, M.B., Ch.B., M.D. 1 3 Eric J. Holowaty, M.D., M.Sc. 4 Jillian M. Birch, B.Sc., M.Sc., Ph.D. 5 1 Department of Pediatrics, McMaster University, Hamilton, Ontario, Canada. 2 Department of Pathology, McMaster University, Hamilton, Ontario, Canada. 3 Department of Medicine, McMaster University, Hamilton, Ontario, Canada. 4 Research and Development, Informatics Unit, Cancer Care Ontario, Toronto, Ontario, Canada. 5 Cancer Research UK, University of Manchester, Manchester, United Kingdom. Address for reprints: Ronald D. Barr, M.B., Ch.B., M.D., Departments of Pediatrics, Pathology, and Medicine, McMaster University, 1200 Main Street West, Hamilton, Ontario, L8S 4J9, Canada; Fax: (905) ; rbarr@mcmaster.ca Received June 7, 2005; revision received October 3, 2005; accepted October 6, The International Classification of Diseases for Oncology (ICD-O) is a collaborative undertaking of the International Agency for Research on Cancer (IARC) and the National Cancer Institute (NCI) in the U.S., under the aegis of the World Health Organization (WHO). The first edition of the ICD-O (published in 1976) is an extension of the second chapter ( Neoplasms ) of the ninth revision of the International Classification of Diseases (ICD-9) and, in addition to the ICD-9 codes (which describe anatomic sites of tumors), also allows the coding of histology. The second edition of the ICD-O (published in 1990) 1 similarly extends the second chapter of the 10th revision of the International Statistical Classification of Diseases and Related Health Problems (ICD-10). The ICD-O codes tumors based on topography (anatomic location), morphology (histology), and behavior (malignant, benign, in situ, of uncertain behavior, or metastatic) but not staging. The topography codes are listed as C00.0 to C80.9. The morphology codes (M) in the second edition were modified in particular for non-hodgkin lymphoma to accommodate the Working Formulation for this group of diseases. The morphology codes range from 8000/0 to 9989/1, in which the first 4 digits of the code indicate the specific histology and the 5th digit (after the slash) is the behavior code. A separate 1-digit code identifies histologic grading (differentiation) and also is used for T cell and B cell categorization in leukemias and lymphomas. Accordingly, the full description of a neoplasm in the ICD-O is a 10-item alpha numeric: 4 for topography, 4 for morphology, 1 for behavior, and 1 for histologic grade. As an example, acute lymphoblastic leukemia of B precursor type is coded as C /3 6. Although the ICD-O system generally is applicable to cancers diagnosed in childhood, it is recognized that morphology takes precedence over topography in classifying neoplasms occurring in children. For example, rhabdomyosarcoma occurs nearly everywhere in 2006 American Cancer Society DOI /cncr Published online 17 February 2006 in Wiley InterScience (
2 1426 CANCER April 1, 2006 / Volume 106 / Number 7 TABLE 1 International Classification of Childhood Cancer. Province of Ontario, Canada, (Incident Cases among Adolescents and Young Adults, Both Genders Combined) ICCC category Age range yrs yrs yrs No. % No. % No. % I Leukemia II Lymphoma III CNS tumors IV SNS tumors V Retinoblastoma VI Renal tumors VII Hepatic tumors VIII Bone tumors IX Soft tissue sarcomas X Germ cell tumors XI Carcinomas XII Other/unspecified tumors Not classified Invalid values Total ICCC: International Classification of Childhood Cancer; CNS: central nervous system; SNS: sympathetic nervous system. Adapted from the Ontario Cancer Registry Incidence File, Cancer Care Ontario ( ) (OCRIS 03/2005). Software used was Surveillance Research Program of the U.S. National Cancer Institute (SEER*Stat software, version 5.2.2; National Cancer Institute, Bethesda, MD). TABLE 2 Classification of Cancer by Morphology, ICCC Categories XI, XII, and Not Classified. Province of Ontario, Canada, (Incident Cases among Adolescents and Young Adults, Both Genders Combined) Morphology group Age range yrs yrs yrs No. % No. % No. % Neoplasm, NOS Carcinoma, NOS Squamous cell Basal cell Transitional cell Adenocarcinoma Cystic/mucinous/serous Ductal/lobular Other epithelial Melanomas Sarcomas Leukemias Others Total ICCC: International Classification of Childhood Cancer; NOS: not otherwise specified. Adapted from the Ontario Cancer Registry Incidence File, Cancer Care Ontario ( ) (OCRIS 03/2005). Software used was Surveillance Research Program of the U.S. National Cancer Institute (SEER*Stat software, version 5.2.2; National Cancer Institute, Bethesda, MD). TABLE 3 Classification of Cancer by Primary Site, ICCC Categories XI, XII, and Not Classified. Province of Ontario, Canada, (Incident Cases among Adolescents and Young Adults, Both Genders Combined) Primary site a Age range yrs yrs yrs No. % No. % No. % Oral cavity/pharynx Esophagus Stomach Colon and rectum Pancreas Lung/bronchus Skin melanoma Breast Cervix Uterine corpus Ovary Prostate Testis Urinary bladder Kidney/renal pelvis Brain/other CNS Thyroid Total a ICCC: International Classification of Childhood Cancer; CNS: central nervous system. a Most prevalent sites only. Adapted from the Ontario Cancer Registry Incidence File, Cancer Care Ontario ( ) (OCRIS 03/2005). Software used was Surveillance Research Program of the U.S. National Cancer Institute (SEER*Stat software, version 5.2.2; National Cancer Institute, Bethesda, MD). the body. Furthermore, for the purposes of international comparison and the facilitation of analysis, an aggregation of diagnostic codes is valuable. To this end, a classification scheme was developed for widespread use 2 based on the system used at the Manchester (U.K.) Children s Tumour Registry. Included in the considerations at that time were the desirability of having a standard framework while allowing for the flexibility of subdivisions within a small number of main groups, and the allocation of the maximum number of codes to specific categories so that the number of malignancies grouped as other is minimized. That classification scheme was updated in 1996 while maintaining the framework of 12 main diagnostic groups. 3 The major modifications were the exclusion of Langerhans cell histiocytoses, a subgroup of germ cell tumors for those occurring in the central nervous system (CNS), a subgroup for Kaposi sarcoma within soft tissue sarcomas, a subgroup for skin carcinoma within epithelial neoplasms, and the assign-
3 Classification in Pediatric Cancer/Barr et al TABLE 4 Classification of Cancers in Adolescents and Young Adults a ICD-02 Diagnostic group Morphology code Topography code restrictions 1. LEUKEMIAS 1.1 Acute lymphoid leukemia 9821, 9825, 9826, Acute myeloid leukemia 9840, 9861, 9866, 9891, 9910, Chronic myeloid leukemia Other and unspecified leukemias Other lymphoid leukemia and lymphoid leukaemia, NOS 9820,9822,9823, Other myeloid leukemia and myeloid leukaemia, NOS 9860,9862,9864, Other specified leukemias 9810, 9830, 9841, 9842, 9850, 9867, 9868, 9870, 9880, 9890, 9892, 9893, 9894, 9900, 9920, 9930, 9931, 9932, 9940, Unspecified leukemias LYMPHOMAS NHL, specified subtype , , Unspecified NHL 9590, 9591, Hodgkin disease: Hodgkin disease, specified subtype Hodgkin disease, NOS CNS AND OTHER INTRACRANIAL AND INTRASPINAL NEOPLASMS (tumors with any behavior code were included) 3.1 Astrocytoma Specified low-grade astrocytic tumors 9380 C None Glioblastoma and anaplastic astrocytoma 9401, , 9481 None Astrocytoma, NOS 9400 None 3.2 Other glioma 9380 Except C , 9430, None 3.3 Ependymoma None 3.4 Medulloblastoma and other PNET Medulloblastoma C Supratentorial PNET Except C Other specified intracranial and intraspinal neoplasms 8140, , 8300, 9161, 9350, , Except C70.0 C72.9 C75.1, C , 9480, 9505, , Unspecified intracranial and intraspinal neoplasms Unspecified malignant intracranial and intraspinal neoplasms (behavior , 9990 C70.0 C72.9, C75.1, C75.3 code of 3 or more) Unspecified benign and borderline intracranial and intraspinal neoplasms (behavior code of less than 3) , 9990 C70.0 C72.9, C75.1, C OSSEOUS AND CHONDROMATOUS NEOPLASMS, EWING TUMOR, AND OTHER NEOPLASMS OF BONE 4.1 Osteosarcoma None 4.2 Chondrosarcoma None 4.3 Ewing tumor 9260, 9364 b None c 4.4 Other specified and unspecified bone tumors Other specified bone tumors 8812, 9250, 9261, 9370 None Unspecified bone tumors , 8800, 8801, 8803 C40.0 C SOFT TISSUE SARCOMAS 5.1 Fibromatous neoplasms 8810, 8811, None 5.2 Rhabdomyosarcoma , 8991 None 5.3 Other specified soft tissue sarcoma: Specified 8804, , 8990, , , None d 9170, 9251, 9561,9581, ,9560 Except C70.0 C72.9, C75.1, C Unspecified Except C40.0 C GERM CELL AND TROPHOBLASTIC NEOPLASMS 6.1 Germ cell and trophoblastic neoplasms of gonads C56.9, C62.0 C Germ cell and trophoblastic neoplasms of nongonadal sites Intracranial (tumors with any behavior code are included) C70.0 C72.9, C75.1, C75.3 (continued)
4 1428 CANCER April 1, 2006 / Volume 106 / Number 7 TABLE 4 (continued) ICD-02 Diagnostic group Morphology code Topography code restrictions Other nongonadal sites Any site except C56.9, C62.0 C62.9, C70.0 C72.9, C75.1, C MELANOMA AND SKIN CARCINOMAS 7.1 Melanoma None 7.2 Skin carcinomas C44.0 C CARCINOMAS 8.1 Thyroid carcinoma C Other carcinoma of head and neck Nasopharyngeal carcinoma C11.0 C Other sites in lip, oral cavity and pharynx C00.0 C10.9, C12.0 C Nasal cavity, middle ear, sinuses, larynx, and other and ill-defined head C30.0 C32.9, C76.0 and neck 8.3 Carcinoma of trachea, bronchus, and lung C33.0 C Carcinoma of breast C50.0 C Carcinoma of genitourinary tract: Carcinoma of kidney C Carcinoma of bladder C67.0 C Carcinoma of gonads C56.0, C62.0 C Carcinoma of cervix and uterus C53.0 C Carcinoma of other and ill-defined sites in genitourinary tract C51.0 C52.9, C57.0 C57.9, C60.0 C61.9, C63.0 C63.9, C65.9, C66.9, C68.0 C Carcinoma of gastrointestinal tract Carcinoma of colon and rectum C18.0 C Carcinoma of stomach C16.0 C Carcinoma of liver and intrahepatic bile ducts C22.0, C Carcinoma of pancreas C25.0 C Carcinoma of other and ill-defined sites in gastrointestinal tract C15.0 C15.9, C17.0 C17.9, C23.0 C24.9, C26.0 C Carcinoma of other and ill-defined sites, NEC Adrenocortical carcinoma C74.0 C Carcinoma of other and ill-defined sites, NEC Any other C codes including C58.9 except C70.0 C72.9, C75.1, C MISCELLANEOUS SPECIFIED NEOPLASMS, NEC 9.1 Other pediatric and embryonal tumors, NEC: Wilms tumor Neuroblastoma 9490, Other pediatric and embryonal tumors, NEC 8963, 8964, , 8981, Other specified neoplasms, NEC Paraganglioma and glomus tumors Other specified gonadal tumors , Myeloma, mast cell tumors, and miscellaneous lymphoreticular neoplasms, NEC Other specified neoplasms, NEC , 8980, 9020, , 9110, UNSPECIFIED MALIGNANT NEOPLASMS, NEC 10. Unspecified malignant neoplasms, NEC ,9990 Any site except: C40.0 C41.9, C70.0 C72.9, C75.1, C75.3 ICD-O2: International Classification of Diseases for Oncology, 2nd edition; NOS: not otherwise specified; NHL: non-hodgkin lymphoma; CNS: central nervous system; PNET: primitive neuroectodermal tumor; NEC: not elsewhere classified. a Unless otherwise specified, only tumors with behavior codes of 3 or more were included. b Included peripheral neuroectodermal tumors. c Includes Ewing tumor and peripheral neuroectodermal tumors coded to extraskeletal sites. d Includes malignant fibrous histiocytoma of the bone.
5 Classification in Pediatric Cancer/Barr et al ment of the majority of other specified and unspecified neoplasms to subgroups within the main diagnostic groups. As useful as the International Classification of Childhood Cancer (ICCC) has proven to be, even when applied to the malignant diseases afflicting adolescents, 4 it is well appreciated that the distribution of neoplasms affecting the adolescent and young adult (AYA) age group (commonly defined as those ages yrs) is very different from that found in early childhood. The embryonal tumors so characteristic of the latter group of patients are seldom encountered among the former group, whereas carcinomas assume much greater importance in the AYA group. An example of the limitations of the ICCC as applied to cancers diagnosed in AYA patients is illustrated in Tables 1 3 using population-based data from the Province of Ontario, Canada. The proportion of cases in categories XI, XII, and Not classified increases progressively in the successive age quintiles of years, years, and years from 20% to nearly 50% (Table 1). The comparable proportion in patients ages birth 14 years is approximately 5%. In the AYA population, these ICCC categories are comprised mainly of squamous cell carcinoma, adenocarcinoma, and melanoma (Table 2). Although the thyroid is the most common site overall (accounting for greater than 33% of tumors diagnosed in males and 50% of tumors diagnosed in females in the yrs age group), there is a notable progressive increase in tumors of the breast and uterine cervix across the quintiles (Table 3). Consequently, a classification scheme has been proposed that is tailored to the particular circumstances of AYA patients with cancer (Table 4). 5 Again, this scheme is based on the ICD-O. Ten main diagnostic groups are defined, all but 1 of which (No. 10, unspecified ) have subgroups of which nearly half are subdivided further. The classic embryonal tumors that typically occur in young children are largely grouped together. In the proposed classification, malignant germ cell tumors, which are more prevalent among AYA patients than children, form a separate group. Likewise, carcinomas are addressed in more detail. Additional innovations include the grouping of all Ewing sarcomas and related tumors together, and a more detailed classification of malignant CNS tumors. In situ tumors and neoplasms of uncertain behavior occurring outside the CNS are excluded. Algorithms for selecting tumor groups according to this scheme are provided at URL: biomed2.man.ac.uk/crcpfcrg/crukpfcrg/pfcrg.htm [accessed February 2, 2006]. The scheme was formulated on the basis of tabulations of the frequencies of ICD-O histology codes among a national dataset of 25,000 cases of cancer diagnosed among young people in England who were ages years. It provides a much more balanced vehicle for the presentation of data regarding cancers occurring in the AYA age group compared with the ICCC. ICCC Groups IV, V, VI, and VII, which mainly comprise the non-cns embryonal tumors of childhood, are irrelevant in patients within the AYA age range. Conversely, carcinomas of the head and neck, breast, genitourinary system, colon, and rectum, and other aerodigestive tract carcinomas that are significant in young adults, are not dealt with adequately in the ICCC but form specified subgroups and are discussed in detail in the AYA scheme. A standardized system for the analysis and presentation of data regarding malignancies diagnosed in the AYA age group that addresses the major disease types occurring in this age group will facilitate international comparisons of incidence and subsequently the generation of hypotheses concerning the etiology of such tumors. Versions of this classification are available in both the first and second editions of the ICD-O. 5 A third edition of the ICD-O (ICD-O3) has been published. 6 This new edition is not yet widely in use but is in the process of being adopted by cancer registries internationally. The ICD-O3 includes many new codes of relevance to tumors occurring in the AYA population. The most extensive revisions are with regard to leukemias and lymphomas. The codes incorporate the WHO classification, 7,8 which superceded the Revised European American Lymphoma (REAL) classification for lymphomas 9 and the French American British (FAB) classification for leukemias. 10 The ICCC recently was adapted for use with the ICD A revised version of the AYA classification scheme based on the ICD-O3 will be made available during REFERENCES 1. Percy C, Van Holten V, Muir C, editors. International classification of diseases for oncology, 2nd ed. Geneva: World Health Organization, Birch JM, Marsden HB. A classification scheme for childhood cancer. Int J Cancer. 1987;40: Kramarova E, Stiller CA. The international classification of childhood cancer. Int J Cancer. 1996;68: Fritschi L, Coates M, McCredie M. Incidence of cancer among New South Wales adolescents: which classification scheme describes adolescent cancers better? Int J Cancer. 1995;60: Birch JM, Alston RD, Kelsey AM, Quinn JM, Babb P, McNally RJQ. Classification and incidence of cancers in adolescents and young adults in England Br J Cancer. 2002; 87: Fritz A, Percy C, Jack A, et al., editors. International classification of diseases for oncology, 3rd ed. Geneva: World Health Organization, 2000.
6 1430 CANCER April 1, 2006 / Volume 106 / Number 7 7. Harris NL, Jaffe ES, Diebold J, et al. World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues: report of the Clinical Advisory Committee meeting Airlie House, Virginia, November J Clin Oncol. 1999;17: Harris NL, Jaffe ES, Diebold J, et al. The World Health Organization classification of neoplastic diseases of the hematopoietic and lymphoid tissues. Report of the Clinical Advisory Committee meeting, Airlie House, Virginia, November, Ann Oncol. 1999;10: Harris NL, Jaffe ES, Stein H, et al. A revised European American classification of lymphoid neoplasms: a proposal from the International Lymphoma Study Group. Blood. 1994;84: Bennett JM, Catovsky D, Daniel MT, et al. Proposals for the classification of acute leukaemias. Br J Haematol. 1976;33: Steliarova-Foucher E, Stiller C, Lacour B, Kaatsch P. International classification of childhood cancer. Cancer. 2005; 103:
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