Distinct germline genetic susceptibility profiles identified for common non-Hodgkin lymphoma subtypes

Sonja I Berndt^#¹, Joseph Vijai^#², Yolanda Benavente^#^{3

4}, Nicola J Camp^#⁵, Alexandra Nieters^#⁶, Zhaoming Wang^#^{7

8}, Karin E Smedby^{9

10}, Geffen Kleinstern¹¹, Henrik Hjalgrim^{12

13

14

15}, Caroline Besson^{16

17}, Christine F Skibola¹⁸, Lindsay M Morton¹⁹, Angela R Brooks-Wilson^{20

21}, Lauren R Teras²², Charles Breeze¹⁹, Joshua Arias¹⁹, Hans-Olov Adami^{23

24

25}, Demetrius Albanes¹⁹, Kenneth C Anderson²⁶, Stephen M Ansell²⁷, Bryan Bassig¹⁹, Nikolaus Becker²⁸, Parveen Bhatti²⁹, Brenda M Birmann³⁰, Paolo Boffetta^{31

32}, Paige M Bracci³³, Paul Brennan³⁴, Elizabeth E Brown³⁵, Laurie Burdett³⁶, Lisa A Cannon-Albright^{5

37}, Ellen T Chang^{33

38}, Brian C H Chiu³⁹, Charles C Chung¹⁹, Jacqueline Clavel^{40

41}, Pierluigi Cocco⁴², Graham Colditz⁴³, Lucia Conde⁴⁴, David V Conti⁴⁵, David G Cox⁴⁶, Karen Curtin⁵, Delphine Casabonne^{3

4}, Immaculata De Vivo^{24

30}, Arjan Diepstra⁴⁷, W Ryan Diver²², Ahmet Dogan⁴⁸, Christopher K Edlund⁴⁵, Lenka Foretova⁴⁹, Joseph F Fraumeni Jr¹⁹, Attilio Gabbas⁵⁰, Hervé Ghesquières^{51

52}, Graham G Giles^{53

54

55}, Sally Glaser^{56

57}, Martha Glenn⁵, Bengt Glimelius⁵⁸, Jian Gu⁵⁹, Thomas M Habermann²⁷, Christopher A Haiman⁴⁵, Corinne Haioun⁶⁰, Jonathan N Hofmann¹⁹, Theodore R Holford⁶¹, Elizabeth A Holly³³, Amy Hutchinson³⁶, Aalin Izhar², Rebecca D Jackson⁶², Ruth F Jarrett⁶³, Rudolph Kaaks²⁸, Eleanor Kane⁶⁴, Laurence N Kolonel⁶⁵, Yinfei Kong⁶⁶, Peter Kraft^{24

67}, Anne Kricker⁶⁸, Annette Lake⁶³, Qing Lan¹⁹, Charles Lawrence⁶⁹, Dalin Li⁷⁰, Mark Liebow²⁷, Brian K Link⁷¹, Corrado Magnani⁷², Marc Maynadie⁷³, James McKay³⁴, Mads Melbye^{13

74

75

76}, Lucia Miligi⁷⁷, Roger L Milne^{53

54

55}, Thierry J Molina⁷⁸, Alain Monnereau^{40

79}, Rebecca Montalvan⁶⁹, Kari E North^{80

81}, Anne J Novak²⁷, Kenan Onel⁸², Mark P Purdue¹⁹, Kristin A Rand⁴⁵, Elio Riboli⁸³, Jacques Riby^{84

85}, Eve Roman⁶⁴, Gilles Salles², Douglas W Sborov⁵, Richard K Severson⁸⁶, Tait D Shanafelt⁸⁷, Martyn T Smith⁸⁵, Alexandra Smith⁶⁴, Kevin W Song^{88

89}, Lei Song⁹⁰, Melissa C Southey^{53

55

91}, John J Spinelli^{92

93}, Anthony Staines⁹⁴, Deborah Stephens⁵, Heather J Sutherland^{88

89}, Kaitlyn Tkachuk², Carrie A Thompson²⁷, Hervé Tilly⁹⁵, Lesley F Tinker²⁹, Ruth C Travis⁹⁶, Jenny Turner^{97

98}, Celine M Vachon⁹⁹, Claire M Vajdic¹⁰⁰, Anke Van Den Berg⁴⁷, David J Van Den Berg⁴⁵, Roel C H Vermeulen^{101

102}, Paolo Vineis^{103

104}, Sophia S Wang¹⁰⁵, Elisabete Weiderpass³⁴, George J Weiner⁷¹, Stephanie Weinstein¹⁹, Nicole Wong Doo¹⁰⁶, Yuanqing Ye⁵⁹, Meredith Yeager^{19

36}, Kai Yu¹⁹, Anne Zeleniuch-Jacquotte^{107

108

109}, Yawei Zhang¹¹⁰, Tongzhang Zheng¹¹¹, Elad Ziv¹¹², Joshua Sampson¹⁹, Nilanjan Chatterjee^{19

113

114}, Kenneth Offit², Wendy Cozen¹¹⁵, Xifeng Wu⁵⁹, James R Cerhan¹¹⁶, Stephen J Chanock¹⁹, Susan L Slager¹¹⁶, Nathaniel Rothman¹⁹

Affiliations

¹ Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Md, USA. berndts@mail.nih.gov.
² Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
³ Cancer Epidemiology Research Programme, Catalan Institute of Oncology-IDIBELL, L'Hospitalet de Llobregat, Barcelona, Spain.
⁴ CIBER de Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain.
⁵ Department of Internal Medicine and Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, UT, USA.
⁶ Institute for Immunodeficiency, University Medical Center Freiburg, Freiburg, Germany.
⁷ Department of Epidemiology and Cancer Control, St. Jude Children's Research Hospital, Memphis, TN, USA.
⁸ Laboratory of Translational Genomics, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA.
⁹ Department of Medicine, Solna, Karolinska Institutet, Stockholm, Sweden.
¹⁰ Hematology Center, Karolinska University Hospital, Stockholm, Sweden.
¹¹ School of Public Health, University of Haifa, Haifa, Israel.
¹² Department of Epidemiology Research, Division of Health Surveillance and Research, Statens Serum Institut, Copenhagen, Denmark.
¹³ Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
¹⁴ Department of Haematology, Rigshospitalet, Copenhagen, Denmark.
¹⁵ Danish Cancer Society Research Center, Danish Cancer Society, Copenhagen, Denmark.
¹⁶ Centre Hospitalier de Versailles, Le Chesnay, France.
¹⁷ Université Paris-Saclay, UVSQ, Inserm, Équipe "Exposome et Hérédité", CESP, Villejuif, France.
¹⁸ Department of Hematology and Medical Oncology, Emory University School of Medicine, Atlanta, GA, USA.
¹⁹ Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Md, USA.
²⁰ Genome Sciences Centre, BC Cancer Agency, Vancouver, BC, Canada.
²¹ Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC, Canada.
²² Department of Population Science, American Cancer Society, Atlanta, GA, USA.
²³ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
²⁴ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
²⁵ Institute of Health and Society, Clinical Effectiveness Research Group, University of Oslo, Oslo, Norway.
²⁶ Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, USA.
²⁷ Department of Internal Medicine, Mayo Clinic, Rochester, MN, USA.
²⁸ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Baden-Württemberg, Germany.
²⁹ Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
³⁰ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
³¹ Stony Brook Cancer Center, Stony Brook University, Stony Brook, New York, 11794, NY, USA.
³² Department of Medical and Surgical Sciences, University of Bologna, Bologna, 41026, Italy.
³³ Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, CA, USA.
³⁴ International Agency for Research on Cancer (IARC), Lyon, France.
³⁵ Department of Pathology, University of Alabama at Birmingham, Birmingham, AL, USA.
³⁶ Cancer Genomics Research Laboratory, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Gaithersburg, MA, USA.
³⁷ George E. Wahlen Department of Veterans Affairs Medical Center, Salt Lake City, UT, USA.
³⁸ Center for Health Sciences, Exponent, Inc., Menlo Park, CA, USA.
³⁹ Department of Public Health Sciences University of Chicago, Chicago, IL, USA.
⁴⁰ CRESS, UMR1153, INSERM, Villejuif, France.
⁴¹ Université de Paris-Cité, Villejuif, France.
⁴² Centre for Occupational and Environmental Health, Division of Population Science, Health Services Research & Primary Care, University of Manchester, Manchester, United Kingdom.
⁴³ Division of Public Health Sciences, Department of Surgery, Washington University School of Medicine, St. Louis, MO, USA.
⁴⁴ Bill Lyons Informatics Centre, UCL Cancer Institute, University College London, London, United Kingdom.
⁴⁵ Department of Population and Public Health Sciences, USC Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁴⁶ INSERM U1052, Cancer Research Center of Lyon, Centre Léon Bérard, Lyon, France.
⁴⁷ Department of Pathology and Medical Biology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.
⁴⁸ Departments of Laboratory Medicine and Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
⁴⁹ Department of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute, Brno, Czech Republic.
⁵⁰ Department of Public Health, Clinical and Molecular Medicine, University of Cagliari, Monserrato, Cagliari, Italy.
⁵¹ Department of Hematology, Hospices Civils de Lyon, Lyon Sud Hospital, Pierre Benite, France.
⁵² CIRI, Centre International de Recherche en Infectiologie, Team Lymphoma Immuno-Biology, Univ Lyon, Inserm, U1111, Université Claude Bernard Lyon 1, CNRS, UMR5308, ENS de Lyon, Lyon, France.
⁵³ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, VC, Australia.
⁵⁴ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, VC, Australia.
⁵⁵ Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, VC, Australia.
⁵⁶ Cancer Prevention Institute of California, Fremont, CA, USA.
⁵⁷ Stanford Cancer Institute, Stanford, CA, USA.
⁵⁸ Department of Immunology, Genetics and Pathology, Uppsala University, Uppsala, Sweden.
⁵⁹ Department of Epidemiology, MD Anderson Cancer Center, Houston, TX, USA.
⁶⁰ Lymphoid Malignancies Unit, Henri Mondor Hospital and University Paris Est, Créteil, France.
⁶¹ Department of Biostatistics, Yale School of Public Health, New Haven, CT, USA.
⁶² Division of Endocrinology, Diabetes and Metabolism, The Ohio State University, Columbus, OH, USA.
⁶³ MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.
⁶⁴ Department of Health Sciences, University of York, York, United Kingdom.
⁶⁵ Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, USA.
⁶⁶ Information Systems and Decision Sciences, California State University, Fullerton, Fullerton, CA, USA.
⁶⁷ Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
⁶⁸ Sydney School of Public Health, The University of Sydney, Sydney, NSW, Australia.
⁶⁹ Westat, Rockville, MA, USA.
⁷⁰ F. Widjaja Family Foundation Inflammatory Bowel and Immunobiology Research Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
⁷¹ Department of Internal Medicine, Carver College of Medicine, The University of Iowa, Iowa City, IA, USA.
⁷² CPO-Piemonte and Unit of Medical Statistics and Epidemiology, Department Translational Medicine, University of Piemonte Orientale, Novara, Italy.
⁷³ INSERM U1231, EA 4184, Registre des Hémopathies Malignes de Côte d'Or, University of Burgundy and Dijon University Hospital, Dijon, France.
⁷⁴ Jebsen Center for Genetic epidemiology, NTNU, Trondheim, Norway.
⁷⁵ Danish Cancer Society Research Center, Copenhagen, Denmark.
⁷⁶ Department of Genetics, Stanford University Medical School, Stanford, CA, USA.
⁷⁷ Environmental and Occupational Epidemiology Unit, Cancer Prevention and Research Institute (ISPO), Florence, Italy.
⁷⁸ Department of Pathology, APHP, Necker and Robert Debré, Université Paris Cité, Institut Imagine, INSERM U1163, Paris, France.
⁷⁹ Registre des hémopathies malignes de la Gironde, Institut Bergonié, Bordeaux, Cedex, France.
⁸⁰ Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
⁸¹ Carolina Center for Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
⁸² Donald and Barbara Zucker School of Medicine, Hofstra/Northwell, Hempstead, New York, NY, USA.
⁸³ School of Public Health, Imperial College London, London, United Kingdom.
⁸⁴ Department of Epidemiology, School of Public Health and Comprehensive Cancer Center, University of Alabama at Birmingham, Birmingham, AL, USA.
⁸⁵ Division of Environmental Health Sciences, University of California Berkeley School of Public Health, Berkeley, CA, USA.
⁸⁶ Department of Family Medicine and Public Health Sciences, Wayne State University, Detroit, MI, USA.
⁸⁷ Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA.
⁸⁸ Leukemia/Bone Marrow Transplantation Program, BC Cancer Agency, Vancouver, BC, Canada.
⁸⁹ Department of Medicine, University of British Columbia, Vancouver, BC, Canada.
⁹⁰ Center for Cancer Research, National Cancer Institute, Frederick, MA, USA.
⁹¹ Department of Clinical Pathology, Melbourne Medical School, The University of Melbourne, VC, 3010, Australia.
⁹² Cancer Control Research, BC Cancer Agency, Vancouver, BC, Canada.
⁹³ School of Population and Public Health, University of British Columbia, Vancouver, BC, Canada.
⁹⁴ School of Nursing, Psychotherapy and Community Health, Dublin City University, Dublin, Ireland.
⁹⁵ Centre Henri Becquerel, Université de Rouen, Rouen, France.
⁹⁶ Cancer Epidemiology Unit, University of Oxford, Oxford, United Kingdom.
⁹⁷ Faculty of Medicine and Health Sciences, Macquarie University, Sydney, NSW, Australia.
⁹⁸ Department of Histopathology, Douglass Hanly Moir Pathology, Sydney, NSW, Australia.
⁹⁹ Department of Quantitative Health Sciences, Mayo Clinic, Rochester, MN, USA.
¹⁰⁰ The Kirby Institute, University of New South Wales, Sydney, NSW, Australia.
¹⁰¹ Institute for Risk Assessment Sciences, Utrecht University, Utrecht, The Netherlands.
¹⁰² Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands.
¹⁰³ MRC-PHE Centre for Environment and Health, School of Public Health, Imperial College London, London, United Kingdom.
¹⁰⁴ Human Genetics Foundation, Turin, Italy.
¹⁰⁵ Division of Health Analytics, City of Hope Beckman Research Institute, Duarte, CA, USA.
¹⁰⁶ Concord Clinical School, University of Sydney, Concord, NSW, Australia.
¹⁰⁷ Department of Population Health, New York University School of Medicine, New York, NY, USA.
¹⁰⁸ Department of Environmental Medicine, New York University School of Medicine, New York, NY, USA.
¹⁰⁹ Perlmutter Cancer Center, NYU Langone Medical Center, New York, NY, USA.
¹¹⁰ Department of Environmental Health Sciences, Yale School of Public Health, New Haven, CT, USA.
¹¹¹ Department of Epidemiology, Brown University, Providence, RI, USA.
¹¹² Division of General Internal Medicine, Department of Medicine, Institute of Human Genetics, Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, CA, USA.
¹¹³ Department of Biostatistics, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MA, USA.
¹¹⁴ Department of Oncology, School of Medicine, Johns Hopkins University, Baltimore, MA, USA.
¹¹⁵ Chao Family Comprehensive Cancer Center, University of California, Irvine, Irvine, CA, USA.
¹¹⁶ Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.

^# Contributed equally.

PMID: 36273105
PMCID: PMC10337695
DOI: 10.1038/s41375-022-01711-0

Distinct germline genetic susceptibility profiles identified for common non-Hodgkin lymphoma subtypes

Sonja I Berndt et al. Leukemia. 2022 Dec.

. 2022 Dec;36(12):2835-2844.

doi: 10.1038/s41375-022-01711-0. Epub 2022 Oct 22.

Authors

Affiliations

¹ Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Md, USA. berndts@mail.nih.gov.
² Department of Medicine, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
³ Cancer Epidemiology Research Programme, Catalan Institute of Oncology-IDIBELL, L'Hospitalet de Llobregat, Barcelona, Spain.
⁴ CIBER de Epidemiología y Salud Pública (CIBERESP), Barcelona, Spain.
⁵ Department of Internal Medicine and Huntsman Cancer Institute, University of Utah School of Medicine, Salt Lake City, UT, USA.
⁶ Institute for Immunodeficiency, University Medical Center Freiburg, Freiburg, Germany.
⁷ Department of Epidemiology and Cancer Control, St. Jude Children's Research Hospital, Memphis, TN, USA.
⁸ Laboratory of Translational Genomics, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, MD, USA.
⁹ Department of Medicine, Solna, Karolinska Institutet, Stockholm, Sweden.
¹⁰ Hematology Center, Karolinska University Hospital, Stockholm, Sweden.
¹¹ School of Public Health, University of Haifa, Haifa, Israel.
¹² Department of Epidemiology Research, Division of Health Surveillance and Research, Statens Serum Institut, Copenhagen, Denmark.
¹³ Department of Clinical Medicine, University of Copenhagen, Copenhagen, Denmark.
¹⁴ Department of Haematology, Rigshospitalet, Copenhagen, Denmark.
¹⁵ Danish Cancer Society Research Center, Danish Cancer Society, Copenhagen, Denmark.
¹⁶ Centre Hospitalier de Versailles, Le Chesnay, France.
¹⁷ Université Paris-Saclay, UVSQ, Inserm, Équipe "Exposome et Hérédité", CESP, Villejuif, France.
¹⁸ Department of Hematology and Medical Oncology, Emory University School of Medicine, Atlanta, GA, USA.
¹⁹ Division of Cancer Epidemiology and Genetics, National Cancer Institute, Bethesda, Md, USA.
²⁰ Genome Sciences Centre, BC Cancer Agency, Vancouver, BC, Canada.
²¹ Department of Biomedical Physiology and Kinesiology, Simon Fraser University, Burnaby, BC, Canada.
²² Department of Population Science, American Cancer Society, Atlanta, GA, USA.
²³ Department of Medical Epidemiology and Biostatistics, Karolinska Institutet, Stockholm, Sweden.
²⁴ Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
²⁵ Institute of Health and Society, Clinical Effectiveness Research Group, University of Oslo, Oslo, Norway.
²⁶ Department of Medical Oncology, Dana-Farber Cancer Institute, Harvard Medical School, Boston, MA, USA.
²⁷ Department of Internal Medicine, Mayo Clinic, Rochester, MN, USA.
²⁸ Division of Cancer Epidemiology, German Cancer Research Center (DKFZ), Heidelberg, Baden-Württemberg, Germany.
²⁹ Division of Public Health Sciences, Fred Hutchinson Cancer Research Center, Seattle, WA, USA.
³⁰ Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, MA, USA.
³¹ Stony Brook Cancer Center, Stony Brook University, Stony Brook, New York, 11794, NY, USA.
³² Department of Medical and Surgical Sciences, University of Bologna, Bologna, 41026, Italy.
³³ Department of Epidemiology and Biostatistics, University of California San Francisco, San Francisco, CA, USA.
³⁴ International Agency for Research on Cancer (IARC), Lyon, France.
³⁵ Department of Pathology, University of Alabama at Birmingham, Birmingham, AL, USA.
³⁶ Cancer Genomics Research Laboratory, Division of Cancer Epidemiology and Genetics, National Cancer Institute, Gaithersburg, MA, USA.
³⁷ George E. Wahlen Department of Veterans Affairs Medical Center, Salt Lake City, UT, USA.
³⁸ Center for Health Sciences, Exponent, Inc., Menlo Park, CA, USA.
³⁹ Department of Public Health Sciences University of Chicago, Chicago, IL, USA.
⁴⁰ CRESS, UMR1153, INSERM, Villejuif, France.
⁴¹ Université de Paris-Cité, Villejuif, France.
⁴² Centre for Occupational and Environmental Health, Division of Population Science, Health Services Research & Primary Care, University of Manchester, Manchester, United Kingdom.
⁴³ Division of Public Health Sciences, Department of Surgery, Washington University School of Medicine, St. Louis, MO, USA.
⁴⁴ Bill Lyons Informatics Centre, UCL Cancer Institute, University College London, London, United Kingdom.
⁴⁵ Department of Population and Public Health Sciences, USC Keck School of Medicine, University of Southern California, Los Angeles, CA, USA.
⁴⁶ INSERM U1052, Cancer Research Center of Lyon, Centre Léon Bérard, Lyon, France.
⁴⁷ Department of Pathology and Medical Biology, University of Groningen, University Medical Center Groningen, Groningen, The Netherlands.
⁴⁸ Departments of Laboratory Medicine and Pathology, Memorial Sloan Kettering Cancer Center, New York, NY, USA.
⁴⁹ Department of Cancer Epidemiology and Genetics, Masaryk Memorial Cancer Institute, Brno, Czech Republic.
⁵⁰ Department of Public Health, Clinical and Molecular Medicine, University of Cagliari, Monserrato, Cagliari, Italy.
⁵¹ Department of Hematology, Hospices Civils de Lyon, Lyon Sud Hospital, Pierre Benite, France.
⁵² CIRI, Centre International de Recherche en Infectiologie, Team Lymphoma Immuno-Biology, Univ Lyon, Inserm, U1111, Université Claude Bernard Lyon 1, CNRS, UMR5308, ENS de Lyon, Lyon, France.
⁵³ Cancer Epidemiology Division, Cancer Council Victoria, Melbourne, VC, Australia.
⁵⁴ Centre for Epidemiology and Biostatistics, Melbourne School of Population and Global Health, University of Melbourne, Melbourne, VC, Australia.
⁵⁵ Precision Medicine, School of Clinical Sciences at Monash Health, Monash University, Clayton, VC, Australia.
⁵⁶ Cancer Prevention Institute of California, Fremont, CA, USA.
⁵⁷ Stanford Cancer Institute, Stanford, CA, USA.
⁵⁸ Department of Immunology, Genetics and Pathology, Uppsala University, Uppsala, Sweden.
⁵⁹ Department of Epidemiology, MD Anderson Cancer Center, Houston, TX, USA.
⁶⁰ Lymphoid Malignancies Unit, Henri Mondor Hospital and University Paris Est, Créteil, France.
⁶¹ Department of Biostatistics, Yale School of Public Health, New Haven, CT, USA.
⁶² Division of Endocrinology, Diabetes and Metabolism, The Ohio State University, Columbus, OH, USA.
⁶³ MRC-University of Glasgow Centre for Virus Research, Glasgow, United Kingdom.
⁶⁴ Department of Health Sciences, University of York, York, United Kingdom.
⁶⁵ Cancer Epidemiology Program, University of Hawaii Cancer Center, Honolulu, HI, USA.
⁶⁶ Information Systems and Decision Sciences, California State University, Fullerton, Fullerton, CA, USA.
⁶⁷ Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, MA, USA.
⁶⁸ Sydney School of Public Health, The University of Sydney, Sydney, NSW, Australia.
⁶⁹ Westat, Rockville, MA, USA.
⁷⁰ F. Widjaja Family Foundation Inflammatory Bowel and Immunobiology Research Institute, Cedars-Sinai Medical Center, Los Angeles, CA, USA.
⁷¹ Department of Internal Medicine, Carver College of Medicine, The University of Iowa, Iowa City, IA, USA.
⁷² CPO-Piemonte and Unit of Medical Statistics and Epidemiology, Department Translational Medicine, University of Piemonte Orientale, Novara, Italy.
⁷³ INSERM U1231, EA 4184, Registre des Hémopathies Malignes de Côte d'Or, University of Burgundy and Dijon University Hospital, Dijon, France.
⁷⁴ Jebsen Center for Genetic epidemiology, NTNU, Trondheim, Norway.
⁷⁵ Danish Cancer Society Research Center, Copenhagen, Denmark.
⁷⁶ Department of Genetics, Stanford University Medical School, Stanford, CA, USA.
⁷⁷ Environmental and Occupational Epidemiology Unit, Cancer Prevention and Research Institute (ISPO), Florence, Italy.
⁷⁸ Department of Pathology, APHP, Necker and Robert Debré, Université Paris Cité, Institut Imagine, INSERM U1163, Paris, France.
⁷⁹ Registre des hémopathies malignes de la Gironde, Institut Bergonié, Bordeaux, Cedex, France.
⁸⁰ Department of Epidemiology, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
⁸¹ Carolina Center for Genome Sciences, University of North Carolina at Chapel Hill, Chapel Hill, NC, USA.
⁸² Donald and Barbara Zucker School of Medicine, Hofstra/Northwell, Hempstead, New York, NY, USA.
⁸³ School of Public Health, Imperial College London, London, United Kingdom.
⁸⁴ Department of Epidemiology, School of Public Health and Comprehensive Cancer Center, University of Alabama at Birmingham, Birmingham, AL, USA.
⁸⁵ Division of Environmental Health Sciences, University of California Berkeley School of Public Health, Berkeley, CA, USA.
⁸⁶ Department of Family Medicine and Public Health Sciences, Wayne State University, Detroit, MI, USA.
⁸⁷ Department of Medicine, Stanford University School of Medicine, Stanford, CA, USA.
⁸⁸ Leukemia/Bone Marrow Transplantation Program, BC Cancer Agency, Vancouver, BC, Canada.
⁸⁹ Department of Medicine, University of British Columbia, Vancouver, BC, Canada.
⁹⁰ Center for Cancer Research, National Cancer Institute, Frederick, MA, USA.
⁹¹ Department of Clinical Pathology, Melbourne Medical School, The University of Melbourne, VC, 3010, Australia.
⁹² Cancer Control Research, BC Cancer Agency, Vancouver, BC, Canada.
⁹³ School of Population and Public Health, University of British Columbia, Vancouver, BC, Canada.
⁹⁴ School of Nursing, Psychotherapy and Community Health, Dublin City University, Dublin, Ireland.
⁹⁵ Centre Henri Becquerel, Université de Rouen, Rouen, France.
⁹⁶ Cancer Epidemiology Unit, University of Oxford, Oxford, United Kingdom.
⁹⁷ Faculty of Medicine and Health Sciences, Macquarie University, Sydney, NSW, Australia.
⁹⁸ Department of Histopathology, Douglass Hanly Moir Pathology, Sydney, NSW, Australia.
⁹⁹ Department of Quantitative Health Sciences, Mayo Clinic, Rochester, MN, USA.
¹⁰⁰ The Kirby Institute, University of New South Wales, Sydney, NSW, Australia.
¹⁰¹ Institute for Risk Assessment Sciences, Utrecht University, Utrecht, The Netherlands.
¹⁰² Julius Center for Health Sciences and Primary Care, University Medical Center Utrecht, Utrecht, The Netherlands.
¹⁰³ MRC-PHE Centre for Environment and Health, School of Public Health, Imperial College London, London, United Kingdom.
¹⁰⁴ Human Genetics Foundation, Turin, Italy.
¹⁰⁵ Division of Health Analytics, City of Hope Beckman Research Institute, Duarte, CA, USA.
¹⁰⁶ Concord Clinical School, University of Sydney, Concord, NSW, Australia.
¹⁰⁷ Department of Population Health, New York University School of Medicine, New York, NY, USA.
¹⁰⁸ Department of Environmental Medicine, New York University School of Medicine, New York, NY, USA.
¹⁰⁹ Perlmutter Cancer Center, NYU Langone Medical Center, New York, NY, USA.
¹¹⁰ Department of Environmental Health Sciences, Yale School of Public Health, New Haven, CT, USA.
¹¹¹ Department of Epidemiology, Brown University, Providence, RI, USA.
¹¹² Division of General Internal Medicine, Department of Medicine, Institute of Human Genetics, Helen Diller Family Comprehensive Cancer Center, University of California, San Francisco, San Francisco, CA, USA.
¹¹³ Department of Biostatistics, Bloomberg School of Public Health, Johns Hopkins University, Baltimore, MA, USA.
¹¹⁴ Department of Oncology, School of Medicine, Johns Hopkins University, Baltimore, MA, USA.
¹¹⁵ Chao Family Comprehensive Cancer Center, University of California, Irvine, Irvine, CA, USA.
¹¹⁶ Department of Health Sciences Research, Mayo Clinic, Rochester, MN, USA.

^# Contributed equally.

PMID: 36273105
PMCID: PMC10337695
DOI: 10.1038/s41375-022-01711-0

Erratum in

Correction: Distinct germline genetic susceptibility profiles identified for common non-Hodgkin lymphoma subtypes.
Berndt SI, Vijai J, Benavente Y, Camp NJ, Nieters A, Wang Z, Smedby KE, Kleinstern G, Hjalgrim H, Besson C, Skibola CF, Morton LM, Brooks-Wilson AR, Teras LR, Breeze C, Arias J, Adami HO, Albanes D, Anderson KC, Ansell SM, Bassig B, Becker N, Bhatti P, Birmann BM, Boffetta P, Bracci PM, Brennan P, Brown EE, Burdett L, Cannon-Albright LA, Chang ET, Chiu BCH, Chung CC, Clavel J, Cocco P, Colditz G, Conde L, Conti DV, Cox DG, Curtin K, Casabonne D, De Vivo I, Diepstra A, Diver WR, Dogan A, Edlund CK, Foretova L, Fraumeni JF Jr, Gabbas A, Ghesquières H, Giles GG, Glaser S, Glenn M, Glimelius B, Gu J, Habermann TM, Haiman CA, Haioun C, Hofmann JN, Holford TR, Holly EA, Hutchinson A, Izhar A, Jackson RD, Jarrett RF, Kaaks R, Kane E, Kolonel LN, Kong Y, Kraft P, Kricker A, Lake A, Lan Q, Lawrence C, Li D, Liebow M, Link BK, Magnani C, Maynadie M, McKay J, Melbye M, Miligi L, Milne RL, Molina TJ, Monnereau A, Montalvan R, North KE, Novak AJ, Onel K, Purdue MP, Rand KA, Riboli E, Riby J, Roman E, Salles G, Sborov DW, Severson RK, Shanafelt TD, Smith MT, Smith A, Song KW, Song L, Southey MC, Spinelli JJ, Staines A, Stephens D, Sutherland HJ, Tkachuk K, Thompson CA, Tilly H, Tinker LF, Travi… See abstract for full author list ➔ Berndt SI, et al. Leukemia. 2023 Oct;37(10):2142. doi: 10.1038/s41375-023-01978-x. Leukemia. 2023. PMID: 37666943 No abstract available.

Abstract

Lymphoma risk is elevated for relatives with common non-Hodgkin lymphoma (NHL) subtypes, suggesting shared genetic susceptibility across subtypes. To evaluate the extent of mutual heritability among NHL subtypes and discover novel loci shared among subtypes, we analyzed data from eight genome-wide association studies within the InterLymph Consortium, including 10,629 cases and 9505 controls. We utilized Association analysis based on SubSETs (ASSET) to discover loci for subsets of NHL subtypes and evaluated shared heritability across the genome using Genome-wide Complex Trait Analysis (GCTA) and polygenic risk scores. We discovered 17 genome-wide significant loci (P < 5 × 10^-8) for subsets of NHL subtypes, including a novel locus at 10q23.33 (HHEX) (P = 3.27 × 10^-9). Most subset associations were driven primarily by only one subtype. Genome-wide genetic correlations between pairs of subtypes varied broadly from 0.20 to 0.86, suggesting substantial heterogeneity in the extent of shared heritability among subtypes. Polygenic risk score analyses of established loci for different lymphoid malignancies identified strong associations with some NHL subtypes (P < 5 × 10^-8), but weak or null associations with others. Although our analyses suggest partially shared heritability and biological pathways, they reveal substantial heterogeneity among NHL subtypes with each having its own distinct germline genetic architecture.

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Conflict of interest statement

Competing Interests:

Tait Shanafelt received research support to his institution from Genetech, Pharacyclics, AbbVie, Cephalon, Hospira, GlaxoSmithKline, Polyphenon E International, Merck, and Celgene and holds a patent (US14/292,075) on green tea extract epigallocatechin gallate in combination with chemotherapy for chronic lymphocytic leukemia. Karin Smedby received research funding from Janssen Pharmaceuticals AB for research unrelated to this project. Corinne Haioun received honoraria from Novartis, Amgen, Servier/Pfizer, and Gilead Sciences, acted as a consultant or advisor to Roche, Celgene, Janssen-Cilag, Gilead Sciences, Takeda, Miltenyi Biotec, Abbvie, and ADC Therapeutics, and received travel, accommodations and/or expenses from Roche, Celgene, and Amgen. Kenan Onel is currently a full-time employee at Sema4. The other authors declare no competing interests.

Figures

**Figure 1.. Regional association plot of novel locus at chromosome 10q23.33 (rs11187157) for the NHL subset of CLL, FL, and MZL.**
Shown are the -log₁₀ association P values from the discovery log-additive genetic model for all SNPs in the region (dots) and rs11187157 (diamond). The lead SNP is shown with results from both the discovery (dark purple diamond) and combined discovery and replication (light purple diamond) analyses. Estimated recombination rates from the 1000 Genome Project are plotted in blue. Locations of recombination hotspots are depicted by peaks corresponding to the rate of recombination. The SNPs surrounding the most significant SNP are color-coded to reflect their r² correlation with the lead SNP. Pairwise r² values are from European ancestry subjects in the 1000 Genomes Project. Genes, position of exons and direction of exons and direction of transcription from UCSC genome browser are denoted. Plot was generated using LocusZoom.

**Figure 2.. Shared genetic correlations and pleiotropy among four NHL subtypes (CLL, DLBCL, FL, and MZL).**
a) Shared genetic correlations based on GCTA analysis. b) Heat plot of directional Z-scores of associations with sentinel SNPs at established genetic loci for individual lymphoid malignancies [e.g., chronic lymphocytic leukemia (CLL), diffuse large B-cell lymphoma (DLBCL), follicular lymphoma (FL), marginal zone lymphoma (MZL), multiple myeloma (MM), acute lymphocytic leukemia (ALL), Hodgkin lymphoma (HL)]. Red color indicates positive association/correlation, and blue indicates inverse or negative association/correlation.

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References

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Distinct germline genetic susceptibility profiles identified for common non-Hodgkin lymphoma subtypes

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Distinct germline genetic susceptibility profiles identified for common non-Hodgkin lymphoma subtypes

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