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Proposed classification of lymphoid neoplasms for epidemiologic research from the Pathology Working Group of the International Lymphoma Epidemiology Consortium (InterLymph)
Open accessAbstract
Recent evidence suggests that there is etiologic heterogeneity among the various subtypes of lymphoid neoplasms. However, epidemiologic analyses by disease subtype have proven challenging due to the numerous clinical and pathologic schemes used to classify lymphomas and lymphoid leukemias over the last several decades. On behalf of the International Lymphoma Epidemiology Consortium (InterLymph) Pathology Working Group, we present a proposed nested classification of lymphoid neoplasms to facilitate the analysis of lymphoid neoplasm subtypes in epidemiologic research. The proposed classification is based on the World Health Organization classification of lymphoid neoplasms and the International Classification of Diseases–Oncology, Third Edition (ICD-O-3). We also provide a translation into the proposed classification from previous classifications, including the Working Formulation, Revised European-American Lymphoma (REAL) classification, and ICD-O-2. We recommend that epidemiologic studies include analyses by lymphoma subtype to the most detailed extent allowable by sample size. The standardization of groupings for epidemiologic research of lymphoma subtypes is essential for comparing subtype-specific reports in the literature, harmonizing cases within a single study diagnosed using different systems, as well as combining data from multiple studies for the purpose of pooled analysis or meta-analysis, and will probably prove to be critical for elucidating etiologies of the various lymphoid neoplasms.
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Population‐based study of autoimmune conditions and the risk of specific lymphoid malignancies
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“D, 2,4–Dichlorophenoxyacetic acid; DDT, dichlorodiphenyltrichloroethane; MCPA, 2–methyl–4–chlorophenoxyacetic acid; NHL, OC, Organochlorine; OP; Organophosphorus.”
InfluentialEpidemiological patterns of leukaemia in 184 countries: a population-based study
Miranda-Filho, A., Piñeros, M., Ferlay, J., Soerjomataram, I., Monnereau, A., & Bray, F. (2018) · The Lancet Haematology · doi:10.1016/s2352-3026(17)30232-6 · Cited by 293
Linet, M. S., Vajdic, C. M., Morton, L. M., de Roos, A. J., Skibola, C. F., Boffetta, P., Cerhan, J. R., Flowers, C. R., de Sanjose, S., Monnereau, A., et al. (2014) · JNCI Monographs · doi:10.1093/jncimonographs/lgu006 · Cited by 241
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MethodGenome-wide association study identifies multiple risk loci for chronic lymphocytic leukemia
Berndt, S. I., Skibola, C. F., Vijai, J., Camp, N. J., Nieters, A., Wang, Z., Cozen, W., Monnereau, A., Wang, S., Kelly, R. S., et al. (2013) · Nature Genetics · doi:10.1038/ng.2652 · Cited by 211
Self-citationMorton, L. M., Curtis, R. E., Linet, M. S., Bluhm, E. C., Tucker, M. A., Caporaso, N. E., Ries, L. A. G., & Fraumeni, J. F. (2010) · Journal of Clinical Oncology · doi:10.1200/jco.2010.29.1112 · Cited by 205
“Eligible patients were identified by using International Classification of Diseases for Oncology, third edition (ICD-O-3)(33) morphology codes (CLL/SLL: 9670, 9823; DLBCL: 9678 to 9680, 9684 [B-cell immunophenotype only]; FL: 9690 to 9691, 9695 to 9698).(1,34) Together, these major subtypes include two thirds of all p…”
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“Diffuse large B-cell lymphoma (DLBCL) is the most common non-Hodgkin lymphoma subtype accounting for approximately 30% of all the cases [1].”
BackgroundLeon, M. E., Schinasi, L. H., Lebailly, P., Freeman, L. E. B., Nordby, K.-C., Ferro, G., Monnereau, A., Brouwer, M., Tual, S., Baldi, I., et al. (2019) · International Journal of Epidemiology · doi:10.1093/ije/dyz017 · Cited by 179
“Each entity was grouped according to the International Lymphoma Epidemiology Consortium.(27) Here we report findings for non-Hodgkin lymphoid malignancies overall and for the most common subtypes of mature B-cell NHL, including chronic lymphocytic leukaemia/small lymphocytic lymphoma (CLL/SLL), diffuse large B-cell ly…”
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Self-citationEtiologic heterogeneity among non-Hodgkin lymphoma subtypes
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An Update of Cancer Incidence in the Agricultural Health Study
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“This corresponds with the InterLymph clustering of the World Health Organization (WHO) classification of lymphoid malignancies into categories designed for lymphoma epidemiological research.(18) Before 2001, ICD-O-3 codes for PEL and mediastinal large B-cell lymphoma were not available, and these groups were coded as…”
MethodYoon, S. O., Suh, C., Lee, D. H., Chi, H., Park, C. J., Jang, S., Shin, H., Park, B., & Huh, J. (2010) · American Journal of Hematology · doi:10.1002/ajh.21824 · Cited by 149
“When applicable, the algorithm proposed by the Pathology Working Group of the International Lymphoma Epidemiology Consortium A (InterLymph) was used [44].”
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“Cancers were classified according to ICD10, with the exception of Kaposi sarcoma and lymphoid and hematopoietic neoplasms, which were classified according to ICDO3 morphology codes.(23) Standardized Incidence Ratios The ratio of the observed to the expected numbers of cancers, the standardised”
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“Cases were classified according to the World Health Organization classification (23,24) using guidelines from the InterLymph Pathology Working Group (25,26).”
Self-citationThe Occurrence of Rare Cancers in U.S. Adults, 1995–2004
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Epidemiology of marginal zone lymphoma
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“Because the numbers of specific NHLs were sometimes small, we also grouped them into larger categories including all B-cell, all T-cell, indolent, and aggressive similar to strategies in other population-based analyses.(18) We were also able to obtain more complete assessment of LPL/WM in relatives by linking them to…”
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“Similar methods were used to calculate the incidence of other morphologically and clinically distinct B-cell malignancies reported to the SEER program during the same time period, including multiple myeloma (MM; ICD-O-3 9732), chronic lymphocytic leukemia (CLL; ICD-O-3 9823), mantle cell lymphoma (MCL; ICD-O-3 9673),…”
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Self-citationShiels, M. S., Engels, E. A., Linet, M. S., Clarke, C. A., Li, J., Hall, H. I., Hartge, P., & Morton, L. M. (2013) · Cancer Epidemiology, Biomarkers & Prevention · doi:10.1158/1055-9965.epi-13-0040 · Cited by 112
“The following subtypes were defined using SEER’s lymphoma subtype recode, based on the International Lymphoma Epidemiology Consortium (InterLymph) classification (21): DLBCL, follicular, marginal zone, peripheral T-cell, andmantle cell lymphomas, mycosis fungoides/S ezary syndrome, other, speci-”
Self-citationBerndt, S. I., Camp, N. J., Skibola, C. F., Vijai, J., Wang, Z., Gu, J. H., Nieters, A., Kelly, R. S., Smedby, K. E. E., Monnereau, A., et al. (2016) · Nature Communications · doi:10.1038/ncomms10933 · Cited by 118
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Self-citationHematopoietic Malignancies Associated with Viral and Alcoholic Hepatitis
Anderson, L. A., Pfeiffer, R. M., Warren, J. L., Landgren, O., Gadalla, S. M., Berndt, S. I., Ricker, W., Parsons, R., Wheeler, W., & Engels, E. A. (2008) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-08-0408 · Cited by 109
“Codes for lymphoproliferative malignancies were grouped into diagnostic entities according to a recently proposed hierarchical system (28) based on the WHO classification (29).”
MethodPersonal Use of Hair Dye and the Risk of Certain Subtypes of Non-Hodgkin Lymphoma
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“For this pooled analysis, NHL cases were classified according to the World Health Organization classification system and as proposed by the InterLymph Pathology Working Group (21).”
Self-citationLi, T., Foran, J. M., Clarke, C. A., Gomez, S. L., & Keegan, T. H. M. (2014) · Blood · doi:10.1182/blood-2013-07-517110 · Cited by 107
Self-citationNew insights into the epidemiology of non-Hodgkin lymphoma and implications for therapy
Chihara, D., Nastoupil, L. J., Williams, J. N., Lee, P. Y. K., Koff, J. L., & Flowers, C. R. (2015) · Expert Review of Anticancer Therapy · doi:10.1586/14737140.2015.1023712 · Cited by 105
Lymphoma survival patterns by WHO subtype in the United States, 1973–2003
Han, X., Kilfoy, B. A., Zheng, T., Holford, T. R., Zhu, C., Zhu, Y. L., & Zhang, Y. (2008) · Cancer Causes & Control · doi:10.1007/s10552-008-9147-4 · Cited by 103
“schemes [9] in that it represents a worldwide consensus [10]; and is based upon the morphology, immunophenotype, genetics, and clinical features [11, 12].”
BackgroundSelf-citationThomas, R. J., Seiser, E., Motsinger‐Reif, A. A., Borst, L. B., Valli, V. E., Kelley, K. L., Suter, S. E., Argyle, D. J., Burgess, K. E., Bell, J. S., et al. (2011) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428194.2011.559802 · Cited by 102
“Anaplastic large cell lymphoma (ALCL) is among the more common hTCL subtypes (*15% of all hTCL cases [44]) and has received moderate cytogenetic characterization, but is uncommon in the dog (52% of cTCL [18]).”
Highly increased familial risks for specific lymphoma subtypes
Goldin, L. R., Björkholm, M., Kristinsson, S. Y., Turesson, I., & Landgren, O. (2009) · British Journal of Haematology · doi:10.1111/j.1365-2141.2009.07721.x · Cited by 101
“These subtypes are associated with different incidence rate patterns and aetiological risk factors (Morton et al, 2007).”
BackgroundB-cell non-Hodgkin lymphoma linked to Coxiella burnetii
Melenotte, C., Million, M., Audoly, G., Gorse, A., Dutronc, H., Roland, G., Dekel, M., Moreno, A., Cammilleri, S., Carrieri, P., et al. (2015) · Blood · doi:10.1182/blood-2015-04-639617 · Cited by 98
Sanfilippo, K. M., Wang, T., Gage, B. F., Liu, W., & Carson, K. R. (2015) · Thrombosis Research · doi:10.1016/j.thromres.2015.01.012 · Cited by 97
“Study Population Patients diagnosed with diffuse large B-cell lymphoma between October 1, 1998 and December 31, 2008 or follicular lymphoma between October 1, 1998 and December 31, 2010 were identified in the VHA Central Cancer Registry by using ICD–O-3 codes consistent with the InterLymph classification system[8].”
MethodWang, S., Purdue, M. P., Cerhan, J. R., Zheng, T., Menashe, I., Armstrong, B. K., Lan, Q., Hartge, P. A., Kricker, A., Zhang, Y., et al. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005360 · Cited by 97
“using the International Lymphoma Epidemiology Consortium (InterLymph) guidelines”
MethodSelf-citationLymphoid malignancies in US Asians: incidence rate differences by birthplace and acculturation
Clarke, C., Glaser, S., Gomez, S., Wang, S. S., Keegan, T., Yang, J., & Chang, E. (2011) · Cancer Epidemiology, Biomarkers and Prevention · doi:10.1158/1055-9965.epi-11-0038 · Cited by 91
“By using InterLymph Consortium guidelines (9, 10), we further classified lymphoid malignancies by histologic subtype into diffuse large B-cell lymphoma (DLBCL; ICD-O-3 morphology codes 9680 and 9684, excluding those with code 9684 and a T-cell, NK-cell, or null-cell immunophenotype);”
Self-citationCarson, K. R., Bartlett, N. L., McDonald, J. R., Luo, S., Zeringue, A., Liu, J., Fu, Q. J., Chang, S., & Colditz, G. A. (2012) · Journal of Clinical Oncology · doi:10.1200/jco.2011.39.2100 · Cited by 94
“Records of 3,227 patients with DLBCL (International Classification of Diseases [ICD] –O3 code 9680) or immunoblastic lymphoma (ICD-O3 code 9684) were identified, consistent with the InterLymph classification system.(25) Data were obtained from all 21 regional VHA districts throughout the United States.”
MethodAtopic Disease and Risk of Non–Hodgkin Lymphoma: An InterLymph Pooled Analysis
Vajdic, C. M., Falster, M. O., de Sanjosé, S., Martı́nez-Maza, O., Becker, N., Bracci, P. M., Melbye, M., Smedby, K. E. E., Engels, E. A., Turner, J., et al. (2009) · Cancer Research · doi:10.1158/0008-5472.can-08-4372 · Cited by 90
Self-citationFwu, C., Chien, Y.-C., You, S., Nelson, K. E., Kirk, G. D., Kuo, H., Feinleib, M., & Chen, C. (2011) · Hepatology · doi:10.1002/hep.24150 · Cited by 89
“We defined NHL subtypes using ICD-O-FT codes specified by the World Health Organization-based classification of lymphoid neoplasms recommended by the Pathology Working Group of the International Lymphoma Epidemiology Consortium.22 The major NHL subtypes included diffuse large B-cell lymphoma (9680-9682, 9684), follicu…”
MethodHairy cell leukemia: 2020 update on diagnosis, risk stratification, and treatment
Maître, E., Cornet, É., & Troussard, X. (2019) · American Journal of Hematology · doi:10.1002/ajh.25653 · Cited by 85
Bracci, P. M., Benavente, Y., Turner, J., Paltiel, O., Slager, S. L., Vajdic, C. M., Norman, A. D., Cerhan, J. R., Chiu, B. C. ‐., Becker, N., et al. (2014) · JNCI Monographs · doi:10.1093/jncimonographs/lgu011 · Cited by 85
“Our use of the InterLymph NHL classification (14,15), combined with site information, helped to diminish additional mis-”
Self-citationCollaborators, F. T. M. W. S., Kroll, M. E., Murphy, F., Pirie, K. L., REEVES, G. K., Green, J., & Beral, V. (2012) · British Journal of Cancer · doi:10.1038/bjc.2012.333 · Cited by 84
“A hierarchical classification based on ICDO-3 has been used in recent international collaborative studies (Morton et al, 2007; Sant et al, 2010; Turner et al, 2010).”
MethodSmoking, alcohol use, obesity, and overall survival from non‐Hodgkin lymphoma
Geyer, S. M., Morton, L. M., Habermann, T. M., Allmer, C., Davis, S., Cozen, W., Severson, R. K., Lynch, C. F., WANG, S. S., Maurer, M. J., et al. (2010) · Cancer · doi:10.1002/cncr.25114 · Cited by 84
“We grouped cases into NHL subtypes according to the InterLymph guidelines.(23)”
MethodSelf-citationA pooled investigation of Toll-like receptor gene variants and risk of non-Hodgkin lymphoma
Purdue, M. P., Qing Lan, B., WANG, S. S., Kricker, A., Menashe, I., Zheng, T., Hartge, P. A., Grulich, A. E., Zhang, Y., Morton, L. M., et al. (2008) · Carcinogenesis · doi:10.1093/carcin/bgn262 · Cited by 83
Self-citationThompson, C. A., Habermann, T. M., Wang, A. H., Vierkant, R. A., Folsom, A. R., Ross, J. A., & Cerhan, J. R. (2009) · International Journal of Cancer · doi:10.1002/ijc.24830 · Cited by 81
Self-citationHead and neck non-Hodgkin's lymphoma: a 20-year demographic study of 381 cases
Etemad‐Moghadam, S., Tirgary, F., Keshavarz, S., & Alaeddini, M. (2010) · International Journal of Oral and Maxillofacial Surgery · doi:10.1016/j.ijom.2010.03.029 · Cited by 81
Troy, J. D., Hartge, P. A., Weissfeld, J. L., Oken, M. M., Colditz, G. A., Mechanic, L. E., & Morton, L. M. (2010) · American Journal of Epidemiology · doi:10.1093/aje/kwq085 · Cited by 82
“We defined NHL subtypes using International Classification of Diseases for Oncology codes specified by the World Health Organization-based classification of lymphoid neoplasms recommended by the Pathology Working Group of the International Lymphoma Epidemiology Consortium (34, 35).”
Self-citationEpidemiology of Follicular Lymphoma
Cerhan, J. R. (2020) · Hematology/Oncology Clinics of North America · doi:10.1016/j.hoc.2020.02.001 · Cited by 80
Self-citationLymphoid neoplasm incidence by WHO subtype in Australia 1982–2006
van Leeuwen, M. T., Turner, J., Joske, D. J. L., Falster, M. O., Srasuebkul, P., Meagher, N. S., Grulich, A. E., Giles, G. G., & Vajdic, C. M. (2014) · International Journal of Cancer · doi:10.1002/ijc.28849 · Cited by 80
“The WHO Classification represents consensus classification for clinical, pathologic and scientific use and wholly incorporates the International Classification of Diseases for Oncology, Third Edition (ICD-O-3, 2001).(6,11) Herein we use population-based cancer registry data to systematically describe subtype-specific…”
MethodSelf-citationSurvival of European patients diagnosed with myeloid malignancies: a HAEMACARE study
Maynadié, M., Angelis, R. D., Marcos‐Gragera, R., Visser, O. J., Allemani, C., Ţereanu, C., Capocaccia, R., Giacomin, A., Lutz, J.-M., Martos, C., et al. (2012) · Haematologica · doi:10.3324/haematol.2012.064014 · Cited by 82
“11,12 The aim of the present study was to estimate survival of patients with myeloid malignancies alive at some point in 2000-2002, using data from European population-based cancer registries, with malignancies grouped according to the HAEMACARE system.”
Self-citationCancer incidence in the Agricultural Health Study after 20 years of follow-up
Lerro, C. C., Koutros, S., Andreotti, G., Sandler, D. P., Lynch, C. F., Louis, L. M., Blair, A. E., Parks, C. G., Shrestha, S., Lubin, J. H., et al. (2019) · Cancer Causes & Control · doi:10.1007/s10552-019-01140-y · Cited by 76
Winquist, A., Hodge, J. M., Diver, W. R., Rodriguez, J. L., Troeschel, A. N., Daniel, J., & Teras, L. R. (2023) · Environmental Health Perspectives · doi:10.1289/ehp13174 · Cited by 75
“78 For hematologic malignancies, we used the proposed hierarchical clas-si fi cation for epidemiological research from the Pathology Working Group of the International Lymphoma Epidemiology Consortium 79 to de fi ne several subgroups (see Figure S2).”
MethodPark, H. J., Park, E., Jung, K., Kong, H., Won, Y., Lee, J. Y., Yoon, J. H., Park, B.-K., Lee, H., Eom, H., et al. (2012) · The Korean Journal of Hematology · doi:10.5045/kjh.2012.47.1.28 · Cited by 74
“tion (WHO) classification and with agreements of experts, they classified statistics on hematologic malignancies that fit the objectives of epidemiology and public health care, and published the statistical reports [3-5].”
BackgroundMarcos‐Gragera, R., Allemani, C., Ţereanu, C., Angelis, R. D., Capocaccia, R., Maynadié, M., Luminari, S., Ferretti, S., Johannesen, T. B., Sankila, R. J., et al. (2011) · Haematologica · doi:10.3324/haematol.2010.034264 · Cited by 74
Self-citationOccupational exposures in rare cancers: A critical review of the literature
Charbotel, B., Fervers, B., & Droz, J. (2013) · Critical Reviews in Oncology/Hematology · doi:10.1016/j.critrevonc.2013.12.004 · Cited by 72
Prevalence of HIV Infection among U.S. Hodgkin Lymphoma Cases
Shiels, M. S., Koritzinsky, E. H., Clarke, C. A., Suneja, G., Morton, L. M., & Engels, E. A. (2013) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-13-0865 · Cited by 73
Self-citationWu, X., Andrews, P. A., Chen, V. W., & Groves, F. D. (2009) · Cancer Epidemiology · doi:10.1016/j.canep.2009.09.006 · Cited by 71
A prospective investigation of serum 25‐hydroxyvitamin D and risk of lymphoid cancers
Lim, U., Freedman, D. M., Hollis, B. W., Horst, R. L., Purdue, M. P., Chatterjee, N., Weinstein, S. J., Morton, L. M., Schatzkin, A. G., Virtamo, J. R. K., et al. (2008) · International Journal of Cancer · doi:10.1002/ijc.23984 · Cited by 70
Self-citationHabermann, T. M., WANG, S. S., Maurer, M. J., Morton, L. M., Lynch, C. F., Ansell, S. M., Hartge, P. A., Severson, R. K., Rothman, N., Davis, S., et al. (2008) · Blood · doi:10.1182/blood-2007-09-111658 · Cited by 70
Self-citationMonnereau, A., Troussard, X., Belot, A., Guizard, A., Woronoff, A., Bara, S., Lapôtre‐Ledoux, B., Iwaz, J., Trétarre, B., Maynadié, M., et al. (2012) · International Journal of Cancer · doi:10.1002/ijc.27889 · Cited by 70
“These groups and subtypes were classified according to the International Classification of Diseases-Oncology 3 (ICD-O-3)(15) using the groupings published by Morton et al.(16) in 2007 for the Lymphoid neoplasms (Table 1).”
MethodSelf-citationBassig, B. A., Qing Lan, B., Rothman, N., Zhang, Y., & Zheng, T. (2012) · Journal of Cancer Epidemiology · doi:10.1155/2012/978930 · Cited by 69
Self-citationCheckoway, H., Boffetta, P., Mundt, D. J., & Mundt, K. A. (2012) · Cancer Causes & Control · doi:10.1007/s10552-012-0055-2 · Cited by 69
“The InterLymph Consortium of lymphoma epidemiology has made an effort to adapt the last two versions of the WHO classification to epidemiologic studies, following a hierarchical approach [33, 34].”
MethodMorton, L. M., Purdue, M. P., Zheng, T., Wang, S., Armstrong, B. K., Zhang, Y., Menashe, I., Chatterjee, N., Davis, S., Lan, Q., et al. (2009) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-08-1037 · Cited by 71
Self-citationWANG, S. S., Vajdic, C. M., Linet, M. S., Slager, S. L., Voutsinas, J. M., Nieters, A., de Sanjosé, S., Cozen, W., Alarcón, G. S., Martı́nez-Maza, O., et al. (2015) · American Journal of Epidemiology · doi:10.1093/aje/kwu290 · Cited by 67
Self-citationA prospective study of 67 serum immune and inflammation markers and risk of non-Hodgkin lymphoma
Purdue, M. P., Hofmann, J. N., Kemp, T. J., Chaturvedi, A. K., Qing Lan, B., Park, J.-H., Pfeiffer, R. M., Hildesheim, A., Pinto, L. A., & Rothman, N. (2013) · Blood · doi:10.1182/blood-2013-01-481077 · Cited by 66
“Cases were classified according to the International Classification of Diseases for Oncology, Second Edition, and categorized into histologic subtypes on the basis of the Interlymph proposed hierarchical classification of lymphoid neoplasms for epidemiologic research.(10) Of the 301 cases, 125 had been included in our…”
A genome-wide association study of marginal zone lymphoma shows association to the HLA region
Vijai, J., Wang, Z., Berndt, S. I., Skibola, C. F., Slager, S. L., de Sanjosé, S., Melbye, M., Glimelius, B., Bracci, P. M., Conde, L., et al. (2015) · Nature Communications · doi:10.1038/ncomms6751 · Cited by 65
“To determine the NHL subtype, phenotype data for all NHL cases were reviewed centrally at the International Lymphoma Epidemiology Consortium (InterLymph) Data Coordinating Center and harmonized using the hierarchical classification proposed by the InterLymph Pathology Working Group 24,25 based on the World Health Organ…”
Self-citationWANG, S. S., Flowers, C. R., Kadin, M. E., Chang, E. T., Hughes, A. M., Ansell, S. M., Feldman, A. L., Lightfoot, T., Boffetta, P., Melbye, M., et al. (2014) · JNCI Monographs · doi:10.1093/jncimonographs/lgu012 · Cited by 65
“Cases were classified according to the World Health Organization classification (3,19) using guidelines from the InterLymph Pathology Working Group (20,21).”
BackgroundMethodSelf-citationA Case–Control Study of Occupational Exposure to Trichloroethylene and Non-Hodgkin Lymphoma
Purdue, M. P., Bakke, B., Stewart, P. A., Roos, A. J. D., Schenk, M., Lynch, C. F., Bernstein, L., Morton, L. M., Cerhan, J. R., Severson, R. K., et al. (2010) · Environmental Health Perspectives · doi:10.1289/ehp.1002106 · Cited by 64
“Environmental Health Perspectives • volume 119 | number 2 | February 2011 235 We conducted analyses of specific histologically defined NHL subtypes (diffuse large B-cell lymphoma, follicular lymphoma, and small lymphocytic lymphoma and chronic lymphocytic leukemia) (Morton et al. 2007) using polytomous regression to e…”
BackgroundMethodSelf-citationGBV‐C/hepatitis G virus infection and non‐Hodgkin lymphoma: a case control study
Krajden, M., Yu, A., Braybrook, H., Lai, A. S., Mak, A., Chow, R., Cook, D. A., Tellier, R., Petric, M., Gascoyne, R. D., et al. (2009) · International Journal of Cancer · doi:10.1002/ijc.25035 · Cited by 62
Self-citationMorton, L. M., Sampson, J. N., Cerhan, J. R., Turner, J., Vajdic, C. M., WANG, S. S., Smedby, K. E. E., de Sanjosé, S., Monnereau, A., Benavente, Y., et al. (2014) · JNCI Monographs · doi:10.1093/jncimonographs/lgu005 · Cited by 62
“The higher proportion of NOS cases from the Working Formulation studies is due to low correspondence between certain Working Formulation and WHO subtypes (64).”
BackgroundMethodResultInfluentialSelf-citationMachiela, M. J., Lan, Q., Slager, S. L., Vermeulen, R. C. H., Teras, L. R., Camp, N. J., Cerhan, J. R., Spinelli, J. J., Wang, S. S., Nieters, A., et al. (2016) · Human Molecular Genetics · doi:10.1093/hmg/ddw027 · Cited by 58
“NHL diagnoseswere verified bymedical and pathology reports to meet InterLymph and World Health Organization (WHO) criteria (32,33).”
MethodSelf-citationCarson, K. R., Riedell, P. A., Lynch, R. C., Nabhan, C., Wildes, T. M., Liu, W., Ganti, A., Roop, R. P., Sanfilippo, K. M., O’Brian, K., et al. (2015) · Journal of Geriatric Oncology · doi:10.1016/j.jgo.2015.01.003 · Cited by 61
“Patients age 80 and older with newly diagnosed DLBCL between October 1, 1998 and December 31, 2008 were identified in the Veteran's Health Administration cancer registry based on the InterLymph classification system (International Classification of Diseases-O3 codes 9680 or 9684), which allows conversion of tumor regi…”
Circulating cytokines and risk of B-cell non-Hodgkin lymphoma: a prospective study
Gu, Y., Shore, R. E., Arslan, A. A., Koenig, K. L., Liu, M., Ibrahim, S., Lokshin, A. E., & Zeleniuch‐Jacquotte, A. (2010) · Cancer Causes & Control · doi:10.1007/s10552-010-9560-3 · Cited by 60
“a n = Number of subjects b p-Values from mixed-effects regression models for continuous variables and conditional logistic regression models for categorical variables c Numbers of subjects with missing values for the covariates are as followings: race [18], height [1], weight [3], body mass index [4], education [35],…”
Kontny, U., Oschlies, I., Woessmann, W., Burkhardt, B., Lisfeld, J., Salzburg, J., Janda, A., Attarbaschi, A., Niggli, F. K., Zimmermann, M., et al. (2014) · British Journal of Haematology · doi:10.1111/bjh.13216 · Cited by 59
Attarbaschi, A., Abla, O., Padilla, L. A., Beishuizen, A., Burke, G. A. A., Brugières, L., Bruneau, J., Burkhardt, B., dʼAmore, E. S. G., Klapper, W., et al. (2020) · Pediatric Blood & Cancer · doi:10.1002/pbc.28416 · Cited by 58
Delioukina, M. L., Zain, J. M., Palmer, J. M., Tsai, N., Thomas, S. H., & Forman, S. J. (2011) · Bone Marrow Transplantation · doi:10.1038/bmt.2011.16 · Cited by 58
Metadata
- Authors
- Morton, L. M., Turner, J. J., Cerhan, J. R., Linet, M. S., Treseler, P. A., Clarke, C. A., Jack, A., Cozen, W., Maynadié, M., Spinelli, J. J., Costantini, A. S., Rüdiger, T., Scarpa, A., Zheng, T., & Weisenburger, D. D.
- Affiliations
- National Institutes of Health (US)
- St Vincent's Hospital Sydney (AU)
- Mayo Clinic (US)
- University of California, San Francisco (US)
- Cancer Prevention Institute of California (US)
- National Health Service (GB)
- University of Southern California (US)
- CHU Dijon Bourgogne (FR)
- BC Cancer Agency (CA)
- Occupational and Environmental Epidemiology Unit, Center for Study and Prevention of Cancer, Scientific Institute of Tuscany, Florence, Italy;
- University of Würzburg (DE)
- University of Verona (IT)
- Yale University (US)
- University of Nebraska Medical Center (US)
- ORCID
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2007-07-15
- Volume
- 110
- Issue
- 2
- Pages
- 695-708
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- PMC
- PMC1924473
- OpenAlex
- W2061918976
- Cited by
- 387
- References
- 58
- Citations by year
- 2026: 4 · 2025: 6 · 2024: 8 · 2023: 17 · 2022: 14 · 2021: 16 · 2020: 14 · 2019: 14 · 2018: 14 · 2017: 15 · 2016: 23 · 2015: 30 · 2014: 45 · 2013: 28 · 2012: 34
- FWCI
- 20.35
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Blood (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health
- National Cancer Institute (P50CA97274, R01CA092153, R01CA062006, N01-CN-35136, CA 62006-05, R01CA92153, P50CA097274)
- Topics
- Health Sciences › Medicine › Pathology and Forensic Medicine › Lymphoma Diagnosis and Treatment
- Health Sciences › Medicine › Oncology › Viral-associated cancers and disorders
- Health Sciences › Medicine › Hematology › Chronic Lymphocytic Leukemia Research
- Keywords
- lymphoid malignancies, lymphoma subtypes, classification standardization, lymphoid leukemia, ICD-O-3, WHO classification of lymphoid neoplasms, REAL classification, Working Formulation, lymphoma etiology
- MeSH terms
- Europe, Hodgkin Disease, Humans, Lymphoma, Lymphoma, Non-Hodgkin, North America, Reproducibility of Results
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