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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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“With respect to lymphoma subtype and sex, the results of our study were consistent with previous reports.(5,8,9) Specifically, we observed a male predominance for the majority of lympho ma subtypes, especially BPDC neoplasm and T lymphoblastic lymphoma, and a female predominance for SPTCL.”
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Epidemiology of Hematologic Malignancies
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“The incidence of follicular lymphoma and marginal zone lymphoma was high, whereas that of chronic lymphocytic leukemia/small lymphocytic lymphoma and Hodgkin's lymphoma was extremely low in our cohort compared with western countries (1, 17).”
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Self-citationDietary vitamin D and risk of non-Hodgkin lymphoma: the multiethnic cohort
Erber, E., Maskarinec, G., Lim, U., & Kolonel, L. N. (2009) · British Journal Of Nutrition · doi:10.1017/s0007114509992029 · Cited by 20
“NHL was classified into the most common subtypes according to the adaptation of the WHO classification for epidemiologic studies((8,9)).”
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Expression of KLF4 is a predictive marker for survival in pediatric Burkitt lymphoma
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Expected long-term survival of older patients diagnosed with non-Hodgkin lymphoma in 2008–2012
Pulte, D. D., Gondos, Á., & Brenner, H. (2011) · Cancer Epidemiology · doi:10.1016/j.canep.2011.08.006 · Cited by 20
“Follicular lymphomas (apart from pediatric and cutaneous) are categorized as a single group in the Interlymph system that corresponds to the ICD-O-3 histology codes used in SEER for follicular lymphoma [12].”
BackgroundMethodBirmann, B. M., Barnard, M. E., Bertrand, K. A., Bao, Y., Crous‐Bou, M., Wolpin, B. M., Vivo, I. D., & Tworoger, S. S. (2016) · American Journal of Public Health · doi:10.2105/ajph.2016.303337 · Cited by 22
Bulka, C. M., Nastoupil, L. J., Koff, J. L., Bernal‐Mizrachi, L., Ward, K. C., Williams, J. N., Bayakly, A. R., Switchenko, J. M., Waller, L. A., & Flowers, C. R. (2016) · Southern Medical Journal · doi:10.14423/smj.0000000000000545 · Cited by 20
“05 (National Cancer Institute, Bethesda, MD) was used to access the SEER 13 Registries Database and standardize the DLBCL incidence rates from Georgia to national DLBCL incidence rates.(16) Age-, sex-, and race-specific crude DLBCL incidence rates were obtained for the 1999–2008 period to standardize Georgia census tr…”
MethodHeinen, M. M., Verhage, B. A. J., Schouten, L. J., Goldbohm, R. A., Schouten, H. C., & van den Brandt, P. A. (2013) · International Journal of Cancer · doi:10.1002/ijc.28175 · Cited by 19
“Using the histology codes provided by the cancer registries, we subdivided the lymphoid neoplasms into categories based on the hierarchical groupings of the International Lymphoma Epidemiology Consortium (InterLymph) nested classification (Table 1).(29) This classification is based on the World Health Organization (WH…”
MethodDandoit, M., Mounier, M., Guy, J., Petrella, T., Girard, S., Casasnovas, O., Martin, L., Bonnetain, F., & Maynadié, M. (2014) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428194.2014.956315 · Cited by 19
Self-citationSkibola, C. F., Slager, S. L., Berndt, S. I., Lightfoot, T., Sampson, J. N., Morton, L. M., & Weisenburger, D. D. (2014) · JNCI Monographs · doi:10.1093/jncimonographs/lgu009 · Cited by 19
“Cases were classified according to the World Health Organization classification (15,16) using guidelines from the InterLymph Pathology Working Group (17,18).”
MethodSelf-citationChiu, Y., Bertrand, K. A., Zhang, S., Laden, F., Epstein, M. M., ROSNER, B. A., Chiuve, S. E., Campos, H., Giovannucci, E. L., Chavarro, J. E., et al. (2018) · International Journal of Cancer · doi:10.1002/ijc.31602 · Cited by 18
“Baseline BMI(1), kg/m(2) 24 (23, 28) 25 (23, 30) 25 (23, 27) 24 (22, 25) 25 (23, 27) 25 (23, 28)”
Environmental pesticide exposure and non-Hodgkin lymphoma survival: a population-based study
Poh, C., McPherson, J. D., Tuscano, J. M., Li, Q., Parikh‐Patel, A., Vogel, C. F. A., Cockburn, M., & Keegan, T. H. M. (2022) · BMC Medicine · doi:10.1186/s12916-022-02348-7 · Cited by 18
Koutros, S., Graubard, B. I., Bassig, B. A., Vermeulen, R. C. H., Appel, N., Hyer, M., Stewart, P. A., & Silverman, D. T. (2023) · Environmental Health Perspectives · doi:10.1289/ehp12840 · Cited by 18
Prognostic value of some inflammatory markers in patients with lymphoma
Anber, N. H., El-Sebaie, A. H., Darwish, N. H. E., Mousa, S. A., & Shamaa, S. S. A. (2019) · Bioscience Reports · doi:10.1042/bsr20182174 · Cited by 18
Lim, U., Kocarnik, J., Bush, W. S., Matise, T. C., Caberto, C., Park, S. L., Carlson, C. S., Deelman, E., Duggan, D. J., Fesinmeyer, M. D., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0089791 · Cited by 17
“Also, heterogeneity in the SNP-cancer associations across common NHL subtypes (DLBCL, FL, CLL/SLL) was examined in the MEC, where all subtypes were ascertained, by performing polytomous logistic regression using common controls.”
MethodInfluentialRisk assessment of second primary cancer according to histological subtype of non-Hodgkin lymphoma
Rossi, C., Jegu, J., Mounier, M., Dandoit, M., Colonna, M., Daubisse‐Marliac, L., Trétarre, B., Ganry, O., Guizard, A., Bara, S., et al. (2015) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428194.2015.1007505 · Cited by 17
Self-citationRoos, A. J. D., Martı́nez-Maza, O., Jerome, K. R., Mirick, D. K., Kopecky, K. J., Madeleine, M. M., Magpantay, L. I., Edlefsen, K. L., & LaCroix, A. Z. (2013) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-13-0240 · Cited by 17
“B-cell NHL cases were further grouped on the basis of the World Health Organization and the International Lymphoma Epidemiology Consortium (InterLymph) guidelines (26, 27), including 142 chronic lymphocytic leukemia/small lymphocytic lymphoma/prolymphocytic leukemia (CLL/SLL/PLL; 28.”
MethodLymphoma and multiple myeloma in cohorts of persons exposed to ionising radiation at a young age
Little, M. P., Wakeford, R., Zablotska, L. B., Borrego, D., Griffin, K., Allodji, R. S., de Vathaire, F., Lee, C., Brenner, A. V., Miller, J. S., et al. (2021) · Leukemia · doi:10.1038/s41375-021-01284-4 · Cited by 17
Self-citationEpstein, M. M., ROSNER, B. A., Breen, E. C., Batista, J. L., Giovannucci, E. L., Magpantay, L. I., Aster, J. C., Rodig, S. J., Bertrand, K. A., Laden, F., et al. (2018) · Haematologica · doi:10.3324/haematol.2017.183236 · Cited by 17
“Study pathologists (JCA, SJR) classified NHL histological subtype(19) according to World Health Organization(20,21) and International Lymphoma Epidemiology (InterLymph) Consortium guidelines.(22,23) We analyzed common B-cell (B-)NHL subtypes individually [diffuse large”
MethodKato, I., Chlebowski, R. T., Hou, L., Wactawski‐Wende, J., Ray, R. M., Abrams, J., Bock, C. H., Desai, P. M., & Simon, M. S. (2015) · International Journal of Cancer · doi:10.1002/ijc.29819 · Cited by 16
Wade, R. L., Bernardo, M. C. D., Richards, S. M., Rossi, D., Crowther-Swanepoel, D., Gaïdano, G., Oscier, D., Catovsky, D., & Houlston, R. S. (2011) · Haematologica · doi:10.3324/haematol.2011.043471 · Cited by 18
“Chronic lymphocytic leukemia (CLL) is the commonest lymphoid malignancy in Western populations.(1,2) While staging systems (Binet, Rai) are clinically useful for predicting prognosis and treatment requirements in CLL(3) there is variability in the outcome of patients who apparently have the same stage of disease.”
BackgroundChang, C. M., WANG, S. S., Davé, B. J., Jain, S., Vasef, M. A., Weisenburger, D. D., Cozen, W., Davis, S., Severson, R. K., Lynch, C. F., et al. (2010) · International Journal of Cancer · doi:10.1002/ijc.25717 · Cited by 15
Self-citationTo Each Its Own: Linking the Biology and Epidemiology of NHL Subtypes
Koff, J. L., Chihara, D., Phan, A., Nastoupil, L. J., Williams, J. N., & Flowers, C. R. (2015) · Current Hematologic Malignancy Reports · doi:10.1007/s11899-015-0267-0 · Cited by 15
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“However, we excluded the latter from our analyses, because the nodular lymphocyte-predominant subtype is considered biologically and clinically separate from classical subtypes [25].”
Self-citationRichiardi, L., Marco, L. D., Gillio‐Tos, A., Merletti, F., Fiano, V., Palli, D., Masala, G., Agnoli, C., Tagliabue, G., Panico, S., et al. (2010) · Cancer Epidemiology · doi:10.1016/j.canep.2010.07.014 · Cited by 15
The Challenges of Epidemiologic Research in Non-Hodgkin Lymphoma
Evens, A. M. (2008) · JAMA · doi:10.1001/jama.2008.589 · Cited by 15
Trends in excess mortality in follicular lymphoma at a population level
Mounier, M., Bossard, N., Belot, A., Remontet, L., Iwaz, J., Dandoit, M., Girard‐Boulanger, S., Herry, A., Woronoff, A., Casasnovas, O., et al. (2014) · European Journal Of Haematology · doi:10.1111/ejh.12403 · Cited by 14
“For lymphoma, the new classification was largely based on the Revised European American Lymphoma Classification published in 1994 (32), and the incidence of FL was only slightly affected by changes in cancer classification.”
MethodSelf-citationKasperzyk, J. L., Chang, E. T., Birmann, B. M., Kraft, P., Zheng, T., & Mueller, N. E. (2011) · American Journal of Epidemiology · doi:10.1093/aje/kwr190 · Cited by 14
“We excluded the latter from our analyses, because the nodular lymphocyte-predominant subtype is considered biologically and clinically separate from classical subtypes (24).”
ResultSelf-citationDesai, M., Newberry, K. J., Romaguera, J. E., Zhang, L., Ou, Z., & Wang, M. L. (2013) · Journal of Hematology & Oncology · doi:10.1186/1756-8722-6-55 · Cited by 14
“FL is the most common indolent NHL [25,26].”
BackgroundMalaria and risk of lymphoid neoplasms and other cancer: a nationwide population-based cohort study
Wyss, K., Granath, F. N., Wångdahl, A., Djärv, T., Fored, M., Nauclér, P., & Färnert, A. (2020) · BMC Medicine · doi:10.1186/s12916-020-01759-8 · Cited by 14
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MethodInfluentialPrimary Lymphoma of Nasal Cavity and Paranasal Sinuses
Azarpira, N., Ashraf, M. J., Monabati, A., Makarempour, A., Khademi, B., Hakimzadeh, A., Abedi, E., & Valibeigi, B. (2012) · Laboratory Medicine · doi:10.1309/lmkh083qcxfuuigs · Cited by 14
Switchenko, J. M., Bulka, C. M., Ward, K. C., Koff, J. L., Bayakly, A. R., Ryan, P. B., Waller, L. A., & Flowers, C. R. (2016) · Cancer Epidemiology · doi:10.1016/j.canep.2016.01.008 · Cited by 14
Ebied, A., Huan, V. T., Makram, O. M., Sang, T. K., Ghorab, M. M. E., Ngo, H. T., Iraqi, A., Kamel, M. G., Đăng, T. N., Vuong, N. L., et al. (2018) · Cancer Medicine · doi:10.1002/cam4.1280 · Cited by 14
Lee, D. Y., Kang, K. S., Jung, H., Park, Y. M., Cho, J., Baek, S., Kwon, S. Y., Jung, K., & Woo, J. (2018) · Auris Nasus Larynx · doi:10.1016/j.anl.2018.05.006 · Cited by 14
Herr, M. M., Schonfeld, S. J., Dores, G. M., Engels, E. A., Tucker, M. A., Curtis, R. E., & Morton, L. M. (2019) · Blood Advances · doi:10.1182/bloodadvances.2019030924 · Cited by 14
“We included the following specific NHL subtypes, defined by International Classification of Diseases for Oncology, third edition (ICD-O-3), morphology codes and grouped according toWorld Health Organization classification: DLBCL (ICD-O-3 codes M9678-9680, 9684 [B-cell immunophenotype only], 9688, 9712, 9737-9738), FL…”
MethodSelf-citationLeo, Q. J. N., Ollberding, N. J., Wilkens, L. R., Kolonel, L. N., Henderson, B. E., Marchand, L. L., & Maskarinec, G. (2015) · European Journal of Clinical Nutrition · doi:10.1038/ejcn.2015.139 · Cited by 14
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“Relationship between ambient ultraviolet radiation and Hodgkin lymphoma subtypes in the United States”
Self-citationWANG, S. S., & Nieters, A. (2010) · Expert Review of Anticancer Therapy · doi:10.1586/era.09.194 · Cited by 13
Neoplasms of the lungs, airways, and pleura
Hansell, D. M., Lynch, D. A., McAdams, H. P., & Bankier, A. A. (2010) · Elsevier eBooks · doi:10.1016/b978-0-7234-3496-2.00018-x · Cited by 13
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“NLPHL was identified by the International Classification of Diseases for Oncology, 3rd Edition histology code 9659/3, according to the International Lymphoma Epidemiology Consortium (InterLymph) hierarchical classification of lymphoid neoplasms for epidemiologic research.(18) Stage was categorized as early (stage IA/B…”
MethodWang, C., Li, W., Liu, C., He, H., & Bai, O. (2015) · Blood Cells Molecules and Diseases · doi:10.1016/j.bcmd.2015.12.004 · Cited by 12
Liu, J., Yu, X., Liu, Y., Jin, H., Ma, D., Qu, T., Wang, T., & Sun, Q. (2014) · Chinese Medical Journal · doi:10.3760/cma.j.issn.0366-6999.20132424 · Cited by 12
Zhong, C., Gragert, L. A., Maiers, M. J., Hill, B. T., Garcia-Gomez, J. F., Gendzekhadze, K., Senitzer, D., Song, J. Y., Weisenburger, D. D., Goldstein, L., et al. (2019) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428194.2019.1617858 · Cited by 12
“A total of 1977 patients with histologically confirmed NHL per Interlymph/WHO classification [29,30] and 15,020 donors were identified between January 1995 and October 2015.”
BackgroundSelf-citationPrimary Diffuse Large B-Cell Lymphoma of the Urinary Tract: A Population-Based Analysis
Liu, Z., Yang, L., Song, P., Fang, K., Zhou, J. W., Peng, Z., & Dong, Q. G. (2021) · Frontiers in Oncology · doi:10.3389/fonc.2021.609882 · Cited by 12
“The most commonly diagnosed non-Hodgkin’s lymphoma (NHL) subtype is diffuse large B-cell lymphoma (DLBCL), which accounts for approximately 30% of NHL cases (1).”
BackgroundEpidemiology and management of lymphoma in low‐income countries
Zucca, E., Rohatiner, A., MAGRATH, I. T., & Cavalli, F. (2010) · Hematological Oncology · doi:10.1002/hon.945 · Cited by 12
“These observations led the International Lymphoma Epidemiology Consortium (InterLymph) to propose a nested classification of lymphoid neoplasms (based on the WHO classification) to facilitate the analysis of lymphoma subtypes in epidemiologic research [3].”
MethodAssociation of Obesity and Type 2 Diabetes with Non-Hodgkin Lymphoma: The Multiethnic Cohort
Maskarinec, G., Brown, S., Lee, J., Bogumil, D. D., Walsh, C. P., Haiman, C. A., Setiawan, V. W., Shvetsov, Y. B., & Marchand, L. L. (2023) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-23-0565 · Cited by 11
Michi, Y., Harada, H., Oikawa, Y., Okuyama, K., Kugimoto, T., Kuroshima, T., Hirai, H., Mochizuki, Y., Shimamoto, H., Tomioka, H., et al. (2022) · BMC Oral Health · doi:10.1186/s12903-022-02056-x · Cited by 11
“Abbreviations DLBCL: Diffuse large B‑cell lymphoma; ML: Malignant lymphoma; ECOG: Eastern Cooperative Oncology Group; CT: Computed tomography; ADC: Apparent diffusion coefficient; MRI: Magnetic resonance imaging; FDG: Fluorodeoxyglucose; PET/CT: Positron emission tomography–computed tomography; SUVmax: Maximum standar…”
BackgroundGao, X., Xue, Z., Xing, J., Lee, D., Gottschalk, S. M., Heslop, H. E., Bollard, C. M., & Wong, S. T. C. (2010) · Academic Radiology · doi:10.1016/j.acra.2009.10.026 · Cited by 11
“This diverse group of diseases is broadly classified as Hodgkin disease or non-Hodgkin’s lymphoma with several subclassification schemes to describe various cellular, genetic, and clinical subtypes (2).”
BackgroundKane, E. V., Skibola, C. F., Bracci, P. M., Cerhan, J. R., Costas, L., Smedby, K. E. E., Holly, E. A., Maynadié, M., Novak, A. J., Lightfoot, T. J., et al. (2015) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-14-1355 · Cited by 11
Self-citationXiao, D. Y., Luo, S., O’Brian, K., Liu, W., & Carson, K. R. (2016) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.1080/10428194.2016.1217526 · Cited by 11
“A retrospective cohort of patients with a new diagnosis of FL between October 1, 1998 and September 30, 2010 with follow up until October 17, 2014 was assembled from the Veteran’s Health Administration Central Cancer Registry (VACCR) based on the InterLymph classification system (International Classification of Diseas…”
MethodInfluentialCallahan, C. L., Stewart, P. A., Friesen, M. C., Locke, S. J., Roos, A. J. D., Cerhan, J. R., Severson, R. K., Rothman, N., & Purdue, M. P. (2018) · Occupational and Environmental Medicine · doi:10.1136/oemed-2017-104890 · Cited by 11
Self-citationDai, Z.-M., He, A., Zhang, W., Liu, J., Cao, X.-M., Chen, Y., Ma, X., Zhao, W., & Dai, Z.-J. (2014) · PubMed Central · Cited by 11
Cardiovascular mortality trends in non-Hodgkin’s lymphoma: a population-based cohort study
Kamel, M. G., El‐Qushayri, A. E., Thach, T. Q., & Huy, N. T. (2017) · Expert Review of Anticancer Therapy · doi:10.1080/14737140.2018.1409626 · Cited by 11
“miological research based on the 2008 WHO classification [35] and the third edition of the International Classification of Diseases for Oncology coding system [36].”
MethodAshraf, M. J., Beigomi, L., Azarpira, N., Geramizadeh, B., Khademi, B., Hakimzadeh, A., & Abedi, E. (2013) · Iranian Red Crescent Medical Journal · doi:10.5812/ircmj.4735 · Cited by 11
“The second most common malignancy of the sinonasal tract following SCC is malignant lymphoma (13, 14).”
BackgroundInfluentialGarcin, L., Gelot, A., Gomez, R., Gusto, G., Boutron‐Ruault, M., Kvaskoff, M., Severi, G., & Besson, C. (2020) · Cancer Medicine · doi:10.1002/cam4.3586 · Cited by 10
Vagal Nerve Activity Predicts Prognosis in Diffused Large B-Cell Lymphoma and Multiple Myeloma
Atar, O., Ram, R., Avivi, I. M., Amit, O., Vitkon, R., Luttwak, E., On, Y. B., & Gidron, Y. (2023) · Journal of Clinical Medicine · doi:10.3390/jcm12030908 · Cited by 10
“Introduction Diffused large B-cell lymphoma (DLBCL) is considered the most common type of non-Hodgkin’s lymphoma worldwide [1].”
BackgroundPrediagnostic Circulating Polyomavirus Antibody Levels and Risk of Non-Hodgkin Lymphoma
Teras, L. R., Rollison, D. E. M., Pawlita, M., Michel, A., Blase, J. L., Willhauck‐Fleckenstein, M., & Gapstur, S. M. (2014) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-14-1125 · Cited by 10
“NHL subtypes were categorized using INTERLYMPH guidelines (6).”
MethodBrandenburg, N. A., Phillips, S., Wells, K. E., Woodcroft, K. J., Amend, K. L., Enger, C. L., & Oliveria, S. A. (2019) · Pharmacoepidemiology and Drug Safety · doi:10.1002/pds.4711 · Cited by 10
T‐cell lymphoblastic lymphoma in children, adolescents and young adults
Vrugt, M. T., Newman, H. M., Teachey, D. T., & Burkhardt, B. (2025) · British Journal of Haematology · doi:10.1111/bjh.70053 · Cited by 9
Lemaître, M., Frénoy, P., Fiolet, T., Besson, C., & Mancini, F. R. (2021) · Environmental Research · doi:10.1016/j.envres.2021.111005 · Cited by 9
Press, D. J., McKinley, M. A., Deapen, D., Clarke, C. A., & Gomez, S. L. (2016) · Cancer Causes & Control · doi:10.1007/s10552-016-0734-5 · Cited by 9
Self-citationKim, J., Leon, M. E., Schinasi, L. H., Baldi, I., Lebailly, P., Freeman, L. E. B., Nordby, K.-C., Ferro, G., Monnereau, A., Brouwer, M., et al. (2023) · Cancer Causes & Control · doi:10.1007/s10552-023-01748-1 · Cited by 9
Hofmann, J. N., Hoppin, J. A., Lynch, C. F., Poole, J. A., Purdue, M. P., Blair, A. E., Alavanja, M. C. R., & Freeman, L. E. B. (2015) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-14-1246 · Cited by 9
“NHL and the following B-cell subtypes were defined according to the classifications proposed by the Pathology Working Group of the International Lymphoma Epidemiology Consortium (20): diffuse large B-cell lymphoma (DLBCL), follicular lymphoma (FL), chronic lymphocytic leukemia/small lymphocytic lymphoma (CLL/SLL), and…”
MethodMorgensztern, D., Walker, G. R., Koniaris, L. G., & Lossos, I. S. (2011) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428194.2010.542596 · Cited by 9
“This classification has been recently recommended by the World Health Organization for group standardization during epidemiological research of lymphoma subtypes [11].”
MethodWalking, Writing and Performance: Autobiographical Texts
Heddon, D. E., Lavery, C., & Smith, P. J. (2009) · Cited by 9
Adzersen, K. H., Friedrich, S., & Becker, N. (2015) · Journal of Cancer Research and Clinical Oncology · doi:10.1007/s00432-015-2017-z · Cited by 9
Little, M. P., Mai, J. Z., Fang, M., Chernyavskiy, P., Kennerley, V., Cahoon, E., Cockburn, M., Kendall, G., & Kimlin, M. G. (2024) · British Journal of Cancer · doi:10.1038/s41416-024-02629-3 · Cited by 7
“NHL was de fi ned using ‘ 2(a)2 Mature Non-Hodgkin lymphoma, B-cell ’ , ‘ 2(a)3 Non-Hodgkin lymphoma, B-cell, NOS ‘ , and ‘ 2(b)2 Mature Non-Hodgkin lymphoma, T-cell ’ , or with a ICD-O-3 histology code of ‘ 9832 ’ [24].”
Physical activity and the risk of non‐Hodgkin lymphoma subtypes: A pooled analysis
Boyle, T., Kleinstern, G., Bracci, P. M., Cerhan, J. R., Benavente, Y., Casabonne, D., Chiu, B. C. ‐., Habermann, T. M., Holly, E. A., Liebow, M., et al. (2022) · International Journal of Cancer · doi:10.1002/ijc.34266 · Cited by 8
“NHL subtype was classified according to Morton et al.21 Only studies with at least 20 cases of a subtype were included in that subtypespecific analyses, and only subtypes with at least 200 cases were analysed as separate subtypes.”
MethodSelf-citationQiu, Y., Wang, X., Yao, Y., Si, Y., Wang, X., Jia, M.-N., Zhou, D., Yu, J., Cao, X., & Li, J. (2023) · Experimental Hematology and Oncology · doi:10.1186/s40164-023-00382-6 · Cited by 8
“Waldenström’s macroglobulinemia (WM) is an uncommon lymphoproliferative disorder characterized by monoclonal immunoglobulin M protein production and bone marrow infiltration by lymphoplasmacstetytoid cells [1].”
BackgroundGaspard, E., Frénoy, P., Praud, D., Coudon, T., Grassot, L., Assi, A. A., Fervers, B., Gelot, A., Mancini, F. R., Severi, G., et al. (2023) · The Science of The Total Environment · doi:10.1016/j.scitotenv.2023.167330 · Cited by 8
Arcaini, L., Pascutto, C., Passamonti, F., Bruno, R., Merli, M., Rizzi, S., Orlandi, E. M., Astori, C., Rattotti, S., Paulli, M., et al. (2008) · International Journal of Cancer · doi:10.1002/ijc.24162 · Cited by 8
Gao, Y., Li, Q., Bassig, B. A., Chang, E. T., Dai, M., Qin, Q., Zhang, Y., & Zheng, T. (2013) · Cancer Causes & Control · doi:10.1007/s10552-012-0136-2 · Cited by 8
“We excluded the latter from our analyses, because the nodular lymphocyte-predominant subtype was considered biologically and clinically separate from classical subtypes [20].”
ResultSelf-citationA prospective analysis of blood donation history and risk of non-Hodgkin lymphoma
Ishii, K., Birmann, B. M., Zhang, X., Giovannucci, E. L., & Bertrand, K. A. (2015) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428194.2015.1091928 · Cited by 9
“Major histologic subtypes of NHL were determined according to the World Health Organization (WHO) classification of lymphomas [15] based on morphology and immunophenotype information available in medical records and the pathology report and consistent with recent International Lymphoma Epidemiology (InterLymph) Consor…”
MethodWadé, N. B., Chang, C. M., Conti, D. V., Millstein, J., Skibola, C. F., Nieters, A., WANG, S. S., de Sanjosé, S., Kane, E. V., Spinelli, J. J., et al. (2020) · Cancer Causes & Control · doi:10.1007/s10552-020-01266-4 · Cited by 8
Self-citationSerum concentrations of per- and polyfluorinated substances and risk of B-cell non-Hodgkin lymphoma
Rhee, J., Koponen, J. M., Sampson, J. N., Keil, A. P., Ward, M. H., Hofmann, J. N., Huang, W., Silverman, D. T., Rantakokko, P., & Purdue, M. P. (2024) · Environment International · doi:10.1016/j.envint.2024.109058 · Cited by 7
Carbaryl use and incident cancer in the Agricultural Health Study: an updated analysis
Erickson, P. A., Andreotti, G., Remigio, R. V., Ward, M. H., Parks, C. G., Sandler, D. P., Albert, P. S., Barry, K. H., Hofmann, J. N., & Freeman, L. E. B. (2025) · International Journal of Hygiene and Environmental Health · doi:10.1016/j.ijheh.2025.114615 · Cited by 8
Survival Outcomes of Limited-Stage Diffuse Large B-Cell Lymphoma Treated With Radiation Therapy
Ermann, D. A., Vardell, V. A., Shah, H., Fitzgerald, L. A., Tao, R., Gaffney, D. K., Stephens, D. M., & Hu, B. (2023) · Clinical Lymphoma Myeloma & Leukemia · doi:10.1016/j.clml.2023.09.006 · Cited by 7
On behalf of the Working Group for the Epidemiology of Hematolymphopoietic Malignancies in Italy, Parodi, S., Merlo, D. F., & Stagnaro, E. (2017) · Cancer Causes & Control · doi:10.1007/s10552-017-0909-8 · Cited by 7
Yin, X., Xu, A., Huang, Z., Fan, F., Wang, Y., Chen, L., Cui, G., Hu, Y., & Sun, C. (2021) · Translational Oncology · doi:10.1016/j.tranon.2021.101106 · Cited by 7
“The reasons might be that:(1) ecause of improved therapies, patients now survived longer.”
BackgroundInfluentialB-Cell NHL Subtype Risk Associated with Autoimmune Conditions and PRS
WANG, S. S., Vajdic, C. M., Linet, M. S., Slager, S. L., Voutsinas, J. M., Nieters, A., Casabonne, D., Cerhan, J. R., Cozen, W., Alarcón, G. S., et al. (2022) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-21-0875 · Cited by 7
Self-citationO’Brian, K., Luo, S., Ganti, A., Riedell, P. A., Lynch, R. C., Roop, R. P., Sanfilippo, K. M., Liu, W., Colditz, G. A., & Carson, K. R. (2015) · Leukemia & lymphoma/Leukemia and lymphoma · doi:10.3109/10428194.2015.1056183 · Cited by 7
Epperla, N., Shah, N., Hamadani, M., Richardson, K. J., Kapke, J. T., Patel, A., Teegavarapu, S. P., Carrum, G., Hari, P., Pingali, S. R., et al. (2016) · Clinical Lymphoma Myeloma & Leukemia · doi:10.1016/j.clml.2016.08.018 · Cited by 7
El‐Zaemey, S., Schinasi, L. H., Ferro, G., Tual, S., Lebailly, P., Baldi, I., Nordby, K.-C., Kjærheim, K., Schüz, J., Monnereau, A., et al. (2019) · Occupational and Environmental Medicine · doi:10.1136/oemed-2018-105655 · Cited by 7
Rotating Nightshift Work and Hematopoietic Cancer Risk in US Female Nurses
Zhang, Y., Birmann, B. M., Papantoniou, K., Zhou, E. S., Erber, A. C., & Schernhammer, E. S. (2020) · JNCI Cancer Spectrum · doi:10.1093/jncics/pkz106 · Cited by 7
Korat, A. V. A., Chiu, Y., Bertrand, K. A., Zhang, S., Epstein, M. M., ROSNER, B. A., Chiuve, S. E., Campos, H., Giovannucci, E. L., Chavarro, J. E., et al. (2020) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqaa251 · Cited by 7
“Histologic subtypes were determined according to the WHO classification of lymphomas and categorized as recommended by the International Lymphoma Epidemiology (InterLymph) Consortium Pathology Working Group (22, 23), as described previously (24).”
MethodThe Epidemiology of Obesity and Hematologic Malignancies
Teras, L. R., & Patel, A. V. (2012) · Springer eBooks · doi:10.1007/978-1-4614-2403-1_1 · Cited by 7
Galicia, N., Dégano, R. M., Díez, P., González‐González, M., Góngora, R., Ibarrola, N., & Fuentes, M. (2017) · Expert Review of Proteomics · doi:10.1080/14789450.2017.1307106 · Cited by 7
Chelius, M. R., Chau, K., Yang, J. C., Hajj, C., Imber, B. S., & Yahalom, J. (2021) · Hematological Oncology · doi:10.1002/hon.2865 · Cited by 6
“Across all lymphomas, approximately 30% are indolent non‐Hodgkin lymphomas (iNHLs).(3) Current National Comprehensive Cancer Network (NCCN) guidelines recommend radiation therapy (RT) in the treatment of indolent lymphomas at doses of 24–30 Gy to the involved site.”
BackgroundKim, D. Y., Nam, J., Chung, J.-S., Jeon, B. E., Lee, J. H., Jo, J., Kim, S.-W., & Shin, H. (2021) · Cancer Research and Treatment · doi:10.4143/crt.2021.944 · Cited by 6
“Multiple studies have shown that advanced disease status is a significant predictor of FN in various cancers, including NHL and breast, ovarian, lung, colorectal, and prostate cancers [23,24].”
BackgroundSayed, L. H. E., Ghoneim, H. M., Rahman, M. A. A., Mohamed, B., Rawash, S. N. A., & Elkerm, Y. (2013) · Alexandria Journal of Medicine · doi:10.1016/j.ajme.2013.07.003 · Cited by 6
“The most common B-cell lymphoma subtypes include follicular lymphoma, diffuse large B-cell lymphoma, marginal zone lymphoma and mantle cell lymphoma.(26) The clinical course of this disease is variable and the molecular and cellular mechanisms responsible for the clinical heterogeneity of B cell NHL are largely unknow…”
BackgroundComplete remission of primary hepatic lymphoma in a patient with human immunodeficiency virus
Widjaja, D. (2015) · World Journal of Clinical Cases · doi:10.12998/wjcc.v3.i2.186 · Cited by 7
Scientific Achievements May Not Reach Everyone: Understanding Disparities in Acute Leukemia
Patel, M. I. (2016) · Current Hematologic Malignancy Reports · doi:10.1007/s11899-016-0329-y · Cited by 6
Parodi, S., Costantini, A. S., Crosignani, P., Fontana, A., Miligi, L., Nanni, O., Piro, S., Ramazzotti, V., Rodella, S., Tumino, R., et al. (2019) · International Journal of Cancer · doi:10.1002/ijc.32393 · Cited by 6
“All diagnoses of NHL were revised by a single pathologist and classified according to the working formulation (WF)15 and immunophenotype.16 For the purpose of our study and of a previous investigation on dietary habits,17 each case was reclassified by a trained epidemiologist of the Liguria Cancer Registry using the m…”
MethodSelf-citation
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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