Genetically predicted longer telomere length is associated with increased risk of B-cell lymphoma subtypes
Open accessAbstract
Evidence from a small number of studies suggests that longer telomere length measured in peripheral leukocytes is associated with an increased risk of non-Hodgkin lymphoma (NHL). However, these studies may be biased by reverse causation, confounded by unmeasured environmental exposures and might miss time points for which prospective telomere measurement would best reveal a relationship between telomere length and NHL risk. We performed an analysis of genetically inferred telomere length and NHL risk in a study of 10 102 NHL cases of the four most common B-cell histologic types and 9562 controls using a genetic risk score (GRS) comprising nine telomere length-associated single-nucleotide polymorphisms. This approach uses existing genotype data and estimates telomere length by weighing the number of telomere length-associated variant alleles an individual carries with the published change in kb of telomere length. The analysis of the telomere length GRS resulted in an association between longer telomere length and increased NHL risk [four B-cell histologic types combined; odds ratio (OR) = 1.49, 95% CI 1.22-1.82,P-value = 8.5 × 10(-5)]. Subtype-specific analyses indicated that chronic lymphocytic leukemia or small lymphocytic lymphoma (CLL/SLL) was the principal NHL subtype contributing to this association (OR = 2.60, 95% CI 1.93-3.51,P-value = 4.0 × 10(-10)). Significant interactions were observed across strata of sex for CLL/SLL and marginal zone lymphoma subtypes as well as age for the follicular lymphoma subtype. Our results indicate that a genetic background that favors longer telomere length may increase NHL risk, particularly risk of CLL/SLL, and are consistent with earlier studies relating longer telomere length with increased NHL risk.
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Longer telomere length is associated with increased risk of B cell lymphoma and chronic lymphocytic leukaemia.
“Another observation in support of the telomere tumour suppressor pathway is that longer telomere length has been associated with an increased risk of B cell lymphoma and chronic lymphocytic leukaemia (CLL)65–67.”
From Telomeres in cancer: tumour suppression and genome instability (2017) · cites this paper as [66]
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Gramatges, M. M., Morton, L. M., Yasui, Y., Arnold, M., Neglia, J. P., Leisenring, W. M., Machiela, M. J., Dagnall, C. L., Chanock, S. J., Armstrong, G. T., et al. (2018) · Cancer Epidemiology Biomarkers & Prevention · doi:10.1158/1055-9965.epi-18-0972 · Cited by 11 · see citing works
“Genetically estimated LTL was determined using methods described by Machiela and colleagues (3).”
BackgroundMethodSelf-citationGroarke, E. M., Calado, R. T., & Liu, J. M. (2022) · Seminars in Hematology · doi:10.1053/j.seminhematol.2022.01.003 · Cited by 10 · see citing works
Telomere length and hTERT genetic variants as potential prognostic markers in multiple myeloma
Dratwa, M., Łacina, P., Butrym, A. K., Porzuczek, D., Mazur, G. J., & Bogunia‐Kubik, K. (2023) · Scientific Reports · doi:10.1038/s41598-023-43141-7 · Cited by 8 · see citing works
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Predicted leukocyte telomere length and risk of myeloid neoplasms
Sullivan, S. M., Cole, B., Lane, J., Meredith, J. J., Langer, E. K., Hooten, A. J., Roesler, M. A., McGraw, K. L., Pankratz, N., & Poynter, J. N. (2023) · Human Molecular Genetics · doi:10.1093/hmg/ddad126 · Cited by 7 · see citing works
Optimizing antiviral agents for hepatitis B management in malignant lymphomas
Ozoya, O. O., Chávez, J. C., Sokol, L., & Dalia, S. M. (2017) · Annals of Translational Medicine · doi:10.21037/atm.2016.12.25 · Cited by 7 · see citing works
Genome-wide association study of mitochondrial copy number
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Parental Age and Risk of Lymphoid Neoplasms
Larfors, G., Glimelius, I. C., Eloranta, S., & Smedby, K. E. E. (2017) · American Journal of Epidemiology · doi:10.1093/aje/kwx185 · Cited by 6 · see citing works
Self-citationErickson, P. A., Chang, V. C., He, S., Dagnall, C. L., Teshome, K., Machiela, M. J., Barry, K. H., Pereira, E. F. R., Gadalla, S. M., Parks, C. G., et al. (2025) · Environmental Research · doi:10.1016/j.envres.2025.121174 · Cited by 3 · see citing works
Self-citationWang, Y., Liu, Q., Liang, S., Yao, M., Zheng, H., Hu, D., & Wang, Y. (2024) · Aging · doi:10.18632/aging.205583 · Cited by 3 · see citing works
Germline Predisposition in Hematologic Malignancies
Kansal, R. (2024) · Elsevier eBooks · doi:10.1016/b978-0-443-15717-2.00126-8 · Cited by 3 · see citing works
Shelterins, a genetic crossroad in CLL
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Wong, J. Y. Y., Blechter, B., Liu, Z., Shi, J., & Roger, V. L. (2024) · Human Molecular Genetics · doi:10.1093/hmg/ddae063 · Cited by 3 · see citing works
Rap1 prevents fusions between long telomeres in fission yeast
Pan, L., Tormey, D., Bobon, N., & Baumann, P. (2022) · The EMBO Journal · doi:10.15252/embj.2021110458 · Cited by 1 · see citing works
“Interestingly, several studies have reported an association between long telomeres and an increased risk for various types of cancer (Lan et al , 2009; Lynch et al , 2013; Pellatt et al , 2013; Julin et al , 2015; Machiela et al , 2015, 2016, 2017; Ojha et al , 2016; Rode et al , 2016).”
Song, T., Liu, J., Zhao, K., Li, S., Qiu, M., Zhang, M., & Wang, H. (2024) · Medicine · doi:10.1097/md.0000000000039584 · Cited by 1 · see citing works
“[14] Recent studies have suggested that longer TL may increase the risk of lymphoma, especially NHL. [15,16] In previous case-control studies, TL measurements were often performed after the onset of disease, and malignant tumors may have affected TL changes, resulting in reverse causal bias.”
BackgroundResultJiang, G., Cao, L., Wang, Y., Li, L., Wang, Z., Zhao, H., Qiu, Y., & Feng, B. (2024) · Cancer Research Communications · doi:10.1158/2767-9764.crc-24-0402 · Cited by 1 · see citing works
Self-citationWang, Q., Sun, X., Han, X., Zhang, X., Wang, W., Wang, H., Ren, H., & Gu, L. (2026) · MedComm – Oncology · doi:10.1002/mog2.70054 · Cited by 1 · see citing works
How telomere attrition protects against cancer
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Wong, J., Blechter, B., Liu, Z., Shi, J.-X., & Roger, V. (2023) · medRxiv · doi:10.1101/2023.08.03.23293621
A multivariable approach for risk markers from pooled molecular data with only partial overlap
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- Authors
- Machiela, 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., Vijai, J., Yeager, M., Wang, Z., Ghesquières, H., McKay, J., Conde, L., de Bakker, P. I. W., Cox, D. G., Burdett, L., Monnereau, A., Flowers, C. R., De Roos, A. J., Brooks-Wilson, A. R., Giles, G. G., Melbye, M., Gu, J., Jackson, R. D., Kane, E., Purdue, M. P., Vajdic, C. M., Albanes, D., Kelly, R. S., Zucca, M., Bertrand, K. A., Zeleniuch-Jacquotte, A., Lawrence, C., Hutchinson, A., Zhi, D., Habermann, T. M., Link, B. K., Novak, A. J., Dogan, A., Asmann, Y. W., Liebow, M., Thompson, C. A., Ansell, S. M., Witzig, T. E., Tilly, H., Haioun, C., Molina, T. J., Hjalgrim, H., Glimelius, B., Adami, H.-O., Roos, G., Bracci, P. M., Riby, J., Smith, M. T., Holly, E. A., Cozen, W., Hartge, P., Morton, L. M., Severson, R. K., Tinker, L. F., North, K. E., Becker, N., Benavente, Y., Boffetta, P., Brennan, P., Foretova, L., Maynadie, M., Staines, A., Lightfoot, T., Crouch, S., Smith, A., Roman, E., Diver, W. R., Offit, K., Zelenetz, A., Klein, R. J., Villano, D. J., Zheng, T., Zhang, Y., Holford, T. R., Turner, J., Southey, M. C., Clavel, J., Virtamo, J., Weinstein, S., Riboli, E., Vineis, P., Kaaks, R., Boeing, H., Tjønneland, A., Angelucci, E., Di Lollo, S., Rais, M., De Vivo, I., Giovannucci, E., Kraft, P., Huang, J., Ma, B., Ye, Y., Chiu, B. C. H., Liang, L., Park, J.-H., Chung, C. C., Weisenburger, D. D., Fraumeni, J. F., Salles, G., Glenn, M., Cannon-Albright, L., Curtin, K., Wu, X., Smedby, K. E., de Sanjose, S., Skibola, C. F., Berndt, S. I., Birmann, B. M., Chanock, S. J., & Rothman, N.
- Affiliations
- National Cancer Institute (US)
- Utrecht University (NL)
- American Cancer Society (US)
- University of Utah (US)
- University of British Columbia (CA)
- City Of Hope National Medical Center (US)
- University Medical Center Freiburg (DE)
- Division of Cancer Epidemiology and Genetics (US)
- Centre National de la Recherche Scientifique (FR)
- Centre international de recherche sur le cancer (FR)
- Inserm (FR)
- Emory University (US)
- BC Cancer Agency (CA)
- The University of Melbourne (AU)
- Statens Serum Institut (DK)
- The University of Texas MD Anderson Cancer Center (US)
- The Ohio State University (US)
- University of York (GB)
- UNSW Sydney (AU)
- MRC Centre for Environment and Health (GB)
- Brigham and Women's Hospital (US)
- Westat (United States) (US)
- University of Alabama at Birmingham (US)
- University of Iowa (US)
- Mayo Clinic (US)
- Centre Henri Becquerel (FR)
- Hôpital Necker-Enfants Malades (FR)
- Uppsala University (SE)
- Karolinska Institutet (SE)
- Umeå University (SE)
- University of California, San Francisco (US)
- University of California, Berkeley (US)
- University of Southern California (US)
- Wayne State University (US)
- Fred Hutch Cancer Center (US)
- University of North Carolina at Chapel Hill (US)
- German Cancer Research Center (DE)
- Institut d'Investigació Biomédica de Bellvitge (ES)
- Tisch Cancer Institute (US)
- Dublin City University (IE)
- Icahn School of Medicine at Mount Sinai (US)
- Yale University (US)
- Finnish Institute for Health and Welfare (FI)
- Italian institute for Genomic Medicine (IT)
- German Institute of Human Nutrition (DE)
- Danish Cancer Society (DK)
- University of Cagliari (IT)
- Harvard University (US)
- Dalian Maritime University (CN)
- University of Chicago (US)
- Dongguk University (KR)
- Lyon 1 Université (FR)
- Karolinska University Hospital (SE)
- Corresponding author
- Machiela, Mitchell J.
- ORCID
- Machiela, Mitchell J.
- Slager, Susan L.
- Vermeulen, Roel C.H.
- Teras, Lauren R.
- Camp, Nicola J.
- Cerhan, James R.
- Wang, Sophia S.
- Vijai, Joseph
- Yeager, Meredith
- Wang, Zhaoming
- Ghesquières, Hervé
- McKay, James
- Cox, David G.
- Monnereau, Alain
- Flowers, Christopher R.
- Brooks-Wilson, Angela R.
- Giles, Graham G.
- Melbye, Mads
- Gu, Jian
- Jackson, Rebecca D.
- Kane, Eleanor
- Purdue, Mark P.
- Vajdic, Claire M.
- Albanes, Demetrius
- Kelly, Rachel S.
- Bertrand, Kimberly A.
- Hutchinson, Amy
- Zhi, Degui
- Habermann, Thomas M.
- Link, Brian K.
- Novak, Anne J.
- Asmann, Yan W.
- Liebow, Mark
- Thompson, Carrie A.
- Ansell, Stephen M.
- Witzig, Thomas E.
- Tilly, Hervé
- Molina, Thierry J.
- Hjalgrim, Henrik
- Glimelius, Bengt
- Adami, Hans-Olov
- Roos, Göran
- Bracci, Paige M.
- Smith, Martyn T.
- Holly, Elizabeth A.
- Cozen, Wendy
- Morton, Lindsay M.
- Tinker, Lesley F.
- North, Kari E.
- Becker, Nikolaus
- Benavente, Yolanda
- Boffetta, Paolo
- Brennan, Paul
- Staines, Anthony
- Crouch, Simon
- Roman, Eve
- Diver, W. Ryan
- Offit, Kenneth
- Zelenetz, Andrew
- Klein, Robert J.
- Villano, Danylo J.
- Holford, Theodore R.
- Southey, Melissa C.
- Clavel, Jacqueline
- Weinstein, Stephanie
- Vineis, Paolo
- Tjønneland, Anne
- Angelucci, Emanuele
- Giovannucci, Edward
- Kraft, Peter
- Ma, Baoshan
- Ye, Yuanqing
- Chiu, Brian C.H.
- Liang, Liming
- Park, Ju-Hyun
- Weisenburger, Dennis D.
- Salles, Gilles
- Curtin, Karen
- Wu, Xifeng
- Smedby, Karin E.
- Berndt, Sonja I.
- Birmann, Brenda M.
- Chanock, Stephen J.
- Rothman, Nathaniel
- Venue
- Human Molecular Genetics
- Publisher
- Oxford University Press (OUP)
- Published
- 2016-02-09
- Volume
- 25
- Issue
- 8
- Pages
- 1663-1676
- ISSN
- 0964-6906 (ISSN-L)
- 1460-2083
- PMC
- PMC4854019
- OpenAlex
- W2290324741
- Cited by
- 58
- References
- 41
- Citations by year
- 2026: 2 · 2025: 1 · 2024: 6 · 2023: 6 · 2022: 4 · 2021: 3 · 2020: 8 · 2019: 7 · 2018: 8 · 2017: 9 · 2016: 4
- FWCI
- 7.52
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Human Molecular Genetics (publishedVersion)
- PubMed Central (publishedVersion, public-domain)
- PubMed (publishedVersion)
- White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (submittedVersion, cc-by)
- HAL (submittedVersion)
- Archivio istituzionale della ricerca (Alma Mater Studiorum Università di Bologna) (submittedVersion)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion, public-domain)
- Utrecht University Repository (Utrecht University) (submittedVersion, other-oa)
- eScholarship (California Digital Library) (submittedVersion)
- HighWire Press Open Archive (submittedVersion)
- STM:n Hallinnonalan avoin julkaisuarkisto (Julkari) (submittedVersion)
- Utrecht University Repository (Utrecht University) (submittedVersion, public-domain)
- Funders
- U.S. Department of Health and Human Services (HHSN268201100002C, HHSN2682011 00003C, HHSN 268201100001C, HHSN268201100046C, HHSN268201100004C, HHSN-271-2011-00004C)
- American Cancer Society (CA49449, CA87969)
- U.S. Department of Veterans Affairs
- World Health Organization
- Brigham and Women's Hospital
- Yale University
- University of Southern California (HHSN261201000035C, HHSN261201000034C, 103885, HHSN261201000140C, 209057, RD06/0020)
- Utah Department of Health (HHSN261201000026C)
- Utah State University
- Ohio State University
- Memorial Sloan-Kettering Cancer Center
- Wake Forest University
- Compagnia di San Paolo
- University of Utah (HHSN 261201000026C)
- University of Pittsburgh
- National Cancer Research Institute
- Leukemia and Lymphoma Research
- Health Research Board
- Huntsman Cancer Institute (P30CA42014, HHSN261201000026C)
- MedStar Health Research Institute
- Michael Smith Health Research BC
- Cancer Research UK (RD06/0020, 209057)
- European Commission (SP23-CT-2005-006438, RD06/0020, 051210, 209057, StSch4261 and StSch4420)
- University of Sydney
- Bundesministerium für Bildung und Forschung (RD06/0020, 209057)
- Cancerfonden (02 6661)
- Generalitat de Catalunya
- Karolinska Institutet (RD06/0020, 209057)
- Stockholms Läns Landsting (20110209)
- Fondation de France (209057, RD06/0020)
- Associazione Italiana per la Ricerca sul Cancro (209057, 11855, RD06/0020)
- José Carreras Leukämie-Stiftung (DJCLS-R12/23)
- Institut National Du Cancer (CA97274, 209057, RD06/0020, P30 CA086862, P30 CA42014)
- Bundesamt für Strahlenschutz (StSch4420, StSch4261)
- Agence Nationale de Sécurité Sanitaire de l’Alimentation, de l’Environnement et du Travail (209057, RD06/0020)
- Regione Autonoma della Sardegna
- National Institutes of Health (n01pc067010-004, HHSN261201000026C, n01pc067009-004, n01co12400-79-0-22, n01pc065064-017, N01-RC- 45035, NO1-CO12400, n01pc067008-014, 5r01ca049449-18, N01RC37004, n01rc37004-9-0-0, UL1TR000135, HHSN261201000140C, HHSN261201000006C, n01cn045165-030, HHSN268201100004C, UL1TR001070, HHSN268201100046C, HHSN261201000034C, HHSN271201100004C, HHSN268201100001C, 5r01ca154643-05, RD06/0020, HHSN268201100002C, HHSN261201000035C, N01 RC037004, 209057, 5R01 CA69669-02, HHSN268201100003C, CA016087, N01-PC67010, CA098566, CA-167552, CA97274, CA186107, CA086862, ES000260, CA118444, CA 87969, CA015083, CA154643, R01 CA92153, N01-CN-45165, TR000135, UL1TR001863)
- Centers for Disease Control and Prevention (HHSN261201000034C, 1u58dp000807-01, HHSN261201000140C, HHSN261201000035C)
- University of Texas MD Anderson Cancer Center
- University of California, San Francisco (209057, RD06/0020)
- University at Buffalo
- Canadian Institutes of Health Research (209057, RD06/0020, 67008)
- Medical Research Council (RD06/0020, 209057)
- National Health and Medical Research Council (251553, 2010–2012, 209057, 251553 and 504711, 209057, 504711)
- Cancer Council Victoria (209057, RD06/0020)
- Cancer Council NSW
- National Institute on Aging (HHSN-271-2011-00004C,)
- National Heart, Lung, and Blood Institute (HHSN2682011-00001I, HHSN2682011-00002I, HHSN268201100004C, HHSN271201100004C, CA186107, HHSN2682011‐00004I, HHSN26820-1100002C, HHSN268201100046C, CA167552, HHSN268201100001C, HHSN2682011-00003I, HHSN268201100003C, CA086862)
- National Human Genome Research Institute (U01HG007033)
- National Cancer Institute (CA165923, N02-PC-71 105, P30-CA 42014, N01-PC-67010, N01CO12400, CA-167552, CA62006, CA-49449, CA148690, ES 000260, R01CA098122, N01 PC-67009, N01-CO-012400, R01-CA-154643, CA 016087, CA154643, P50CA97274, CA97274, HHSN261201000034 C, CA098122, CA134674, CA-87969, CA 92153, HHSN261201000035C, R01CA092153, CA 118444, P01CA087969, R01CA098661, N01 PC 67008, 5R01 CA69669-02, R01CA134674, CA-186107, R01CA149445, R01‐CA049449, HHSN261201000140C, N01 PC065064, NO1‐CO‐12400, RD06/0020, N01‐PC‐65064, CA42014, K07CA115687, N01 PC067008, HHSN261201000006C, 209057, U01CA118444, HHSN261201000035I, N01PC067009, R01CA062006, HHSN 261201000026C, N01 CN045165, K08CA134919, N01 CN 45165, CA1046282, CA-086862, CA149445, R25CA098566, CA 015083, UM1CA186107, R21CA165923, U01CA049449, UM1CA167552, R01CA148690, N01 PC067010, R01CA92153, P50CA097274, P30CA008748, P30CA015083, P30CA086862, P30CA042014, P30CA016087, P30CA016359, U01CA167552, R35CA197449, CA098566)
- National Institute of Environmental Health Sciences (ES-000260, P30ES000260)
- National Center for Chronic Disease Prevention and Health Promotion (U58 DP000807, #1U58DP000807-01)
- National Center for Advancing Translational Sciences
- Research Ireland
- Topics
- Health Sciences › Medicine › Physiology › Telomeres, Telomerase, and Senescence
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic Associations and Epidemiology
- Health Sciences › Medicine › Pathology and Forensic Medicine › Lymphoma Diagnosis and Treatment
- Keywords
- telomere length, non-Hodgkin lymphoma, B-cell lymphoma, chronic lymphocytic leukemia, small lymphocytic lymphoma, marginal zone lymphoma, follicular lymphoma, polygenic risk score, lymphoma risk
- MeSH terms
- Adolescent, Adult, Age Factors, Aged, Aged, 80 and over, Female, Humans, Male, Middle Aged, Prospective Studies, Lymphoma, B-Cell, Telomere, Genetic Predisposition to Disease, Genetic Association Studies
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