Skip to main content

Advertisement

SpringerLink
Log in

Infectious mononucleosis, immune genotypes, and non-Hodgkin lymphoma (NHL): an InterLymph Consortium study

  • Original Paper
  • Published:
Cancer Causes & Control Aims and scope Submit manuscript

A Correction to this article was published on 29 March 2020

This article has been updated

Abstract

Purpose

We explored the interaction between non-Hodgkin lymphoma (NHL), infectious mononucleosis (IM) history, and immune-related genotypes in a pooled case–control analysis.

Methods

A total of 7,926 NHL patients and 10,018 controls from 12 case–control studies were included. Studies were conducted during various time periods between 1988 and 2008, and participants were 17–96 years of age at the time of ascertainment/recruitment. Self-reported IM history and immune response genotypes were provided by the InterLymph Data Coordinating Center at Mayo Clinic. Odds ratios (OR) were estimated using multivariate logistic regression, and interactions were estimated using the empirical Bayes method. PACT was used to account for multiple comparisons.

Results

There was evidence of an interaction effect between IM history and two variants on T-cell lymphoma (TCL) risk: rs1143627 in interleukin-1B (IL1B) (pinteraction = 0.04, ORinteraction = 0.09, 95% confidence interval [CI] 0.01, 0.87) and rs1800797 in interleukin-6 (IL6) (pinteraction = 0.03, ORinteraction = 0.08, 95% CI 0.01, 0.80). Neither interaction effect withstood adjustment for multiple comparisons. There were no statistically significant interactions between immune response genotypes and IM on other NHL subtypes.

Conclusions

Genetic risk variants in IL1B and IL6 may affect the association between IM and TCL, possibly by influencing T-cell activation, growth, and differentiation in the presence of IM, thereby decreasing risk of immune cell proliferation.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Change history

  • 29 March 2020

    Unfortunately, the word ���Group��� is missed in the article title of the original publication. It has been corrected by this erratum.

References

  1. Morton LM, Sampson JN, Cerhan JR, Turner JJ, Vajdic CM, Wang SS, Smedby KE, De Sanjosé S, Monnereau A, Benavente Y, Bracci PM, Chiu BCH, Skibola CF, Zhang Y, Mbulaiteye SM, Spriggs M, Robinson D, Norman AD, Kane EV, Spinelli JJ, Kelly JL, La Vecchia C, Maso LD, Maynadié M, Kadin ME, Cocco P, Costantini AS, Clarke CA, Roman E, Miligi L, Colt JS, Berndt SI, Mannetje A, de Roos AJ, Kricker A, Nieters A, Franceschi S, Melbye M, Boffetta P, Clavel J, Linet MS, Weisenburger DD, Slager SL (2014) Rationale and design of the international lymphoma epidemiology consortium (interlymph) non-Hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014:1–14. https://doi.org/10.1093/jncimonographs/lgu005

    Article  PubMed  PubMed Central  Google Scholar 

  2. Grulich AE, Vajdic CM, Cozen W (2007) Altered immunity as a risk factor for non-Hodgkin lymphoma. Cancer Epidemiol Biomarkers Prev 16:405–409

    Article  CAS  PubMed  Google Scholar 

  3. Morton LM, Wang SS, Cozen W, Linet MS, Chatterjee N, Davis S, Severson RK, Colt JS, Vasef MA, Rothman N, Blair A, Bernstein L, Cross AJ, De Roos AJ, Engels E a., Hein DW, Hill D a., Kelemen LE, Lim U, Lynch CF, Schenk M, Wacholder S, Ward MH, Zahm SH, Chanock SJ, Cerhan JR, Hartge P (2008) Etiologic heterogeneity among non-Hodgkin lymphoma subtypes. Blood 112:5150–5160. https://doi.org/10.1182/blood-2008-01-133587

  4. Smedby KE, Vajdic CM, Falster M, Engels EA, Martinez-Maza O, Turner J, Hjalgrim H, Vineis P, Costantini AS, Bracci PM, Holly EA, Willett E, Spinelli JJ, La VC, Zheng T, Becker N, De Sanjosé S, Chiu BCH, Maso LD, Cocco P, Maynadie M, Foretova L, Staines A, Brennan P, Davis S, Severson R, Cerhan JR, Breen EC, Birmann B, Grulich AE, Cozen W (2008) Autoimmune disorders and risk of non-Hodgkin lymphoma subtypes: a pooled analysis within the InterLymph Consortium. Blood 111:4029–4038. https://doi.org/10.1182/blood-2007-10-119974

    Article  CAS  Google Scholar 

  5. Cozen W, Cerhan JR, Martinez-Maza O, Ward MH, Linet M, Colt JS, Davis S, Severson RK, Hartge P, Bernstein L (2007) The effect of atopy, childhood crowding, and other immune-related factors on non-Hodgkin lymphoma risk. Cancer Causes Control 18:821–831. https://doi.org/10.1007/s10552-007-9025-5

    Article  CAS  PubMed  Google Scholar 

  6. Goldin LR, Björkholm M, Kristinsson SY, Turesson I, Landgren O (2009) Highly increased familial risks for specific lymphoma subtypes. Br J Haematol 146:91–94. https://doi.org/10.1111/j.1365-2141.2009.07721.x

    Article  PubMed  PubMed Central  Google Scholar 

  7. Wang SS, Flowers CR, Kadin ME, Chang ET, Hughes AM, Ansell SM, Feldman AL, Lightfoot T, Boffetta P, Melbye M, Lan Q, Sampson JN, Morton LM, Zhang Y, Weisenburger DD (2014) Medical history, lifestyle, family history, and occupational risk factors for peripheral T-cell lymphomas: The interlymph non-hodgkin lymphoma subtypes project. J Natl Cancer Inst Monogr 2014:66–75. https://doi.org/10.1093/jncimonographs/lgu012

    Article  PubMed  PubMed Central  Google Scholar 

  8. Hosgood HD, Purdue MP, Wang SS, Zheng T, Morton LM, Lan Q, Menashe I, Zhang Y, Cerhan JR, Grulich A, Cozen W, Yeager M, Holford TR, Vajdic CM, Davis S, Leaderer B, Kricker A, Schenk M, Zahm SH, Chatterjee N, Chanock SJ, Rothman N, Hartge P, Armstrong B (2011) A pooled analysis of three studies evaluating genetic variation in innate immunity genes and non-Hodgkin lymphoma risk. Br J Haematol 152:721–726. https://doi.org/10.1111/j.1365-2141.2010.08518.x

    Article  PubMed  PubMed Central  Google Scholar 

  9. Skibola CF, Akers NK, Conde L, Ladner M, Hawbecker SK, Cohen F, Ribas F, Erlich HA, Goodridge D, Trachtenberg EA, Smith MT, Bracci PM (2012) Multi-locus HLA class I and II allele and haplotype associations with follicular lymphoma. Tissue Antigens 79:279–286. https://doi.org/10.1111/j.1399-0039.2012.01845.x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Wang SS, Abdou AM, Morton LM, Thomas R, Cerhan JR, Gao X, Cozen W, Rothman N, Davis S, Severson RK, Bernstein L, Hartge P, Carrington M (2010) Human leukocyte antigen class I and II alleles in non-Hodgkin lymphoma etiology. Blood 115:4820–4823. https://doi.org/10.1182/blood-2010-01-266775

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Thorley-Lawson DA, Gross A (2004) Persistence of the Epstein–Barr virus and the origins of associated lymphomas. N Engl J Med 350:1328–1337. https://doi.org/10.1056/NEJMra032015

    Article  CAS  PubMed  Google Scholar 

  12. Ferri C, Caracciolo F, Zignego AL, La CL, Monti M, Longombardo G, Lombardini F, Greco F, Capochiani E, Mazzoni A, Mazzaro C, Pasero G (1994) Hepatitis C virus infection in patients with non-Hodgkin’s lymphoma. Br J Haematol 88:392–394. https://doi.org/10.1111/j.1365-2141.1994.tb05036.x

    Article  CAS  PubMed  Google Scholar 

  13. Parsonnet J, Hansen S, Rodriguez L, Gelb AB, Warnke RA, Jellum E, Orentreich N, Vogelman JH, Friedman GD (1994) Helicobacter pylori infection and gastric lymphoma. N Engl J Med 330:1267–1271. https://doi.org/10.1056/NEJM199405053301803

    Article  CAS  PubMed  Google Scholar 

  14. Engels EA (2007) Infectious agents as causes of non-Hodgkin lymphoma. Cancer Epidemiol Biomarkers Prev 16:401–404. https://doi.org/10.1158/1055-9965.EPI-06-1056

    Article  CAS  PubMed  Google Scholar 

  15. Longnecker RM, Kieff E, Cohen JI (2013) Epstein-Barr virus. In: Knipe DM, Howley PM (eds) Fields virology, 6th edn. Lippincott Williams & Wilkins, Philadelphia, pp 1898–1959

    Google Scholar 

  16. Fleisher G, Henle W, Henle G, Lennette ET, Biggar RJ (1979) Primary infection with Epstein-Barr virus in infants in the United States: clinical and serologic observations. J Infect Dis 139:553–558. https://doi.org/10.2307/30111515

    Article  CAS  PubMed  Google Scholar 

  17. Luzuriaga K, Sullivan JL (2010) Infectious mononucleosis. N Engl J Med 362:1993–2000. https://doi.org/10.1056/NEJMcp1001116

    Article  CAS  PubMed  Google Scholar 

  18. Macsween KF, Johannessen I (2014) Epstein-Barr Virus (EBV): Infectious Mononucleosis and other non-malignant EBV-associated diseases. In: Kaslow RA, Stanberry LR, Duc JW (eds) Viral infections of humans: epidemiology and control. Springer, Boston, pp 867–896

    Chapter  Google Scholar 

  19. Balfour HH, Dunmire SK, Hogquist KA (2015) Infectious mononucleosis. Clin Transl Immunol 4(e33):1–7. https://doi.org/10.1038/cti.2015.1

    Article  CAS  Google Scholar 

  20. Callan MFC, Steven N, Krausa P, Wilson JDK, Moss PAH, Gillespie GM, Bell JI, Rickinson AB, Mcmichael AJ (1996) Large clonal expansions of CD8+ T cells in acute infectious mononucleosis. Nat Med 2:906–911

    Article  CAS  PubMed  Google Scholar 

  21. Long HM, Meckiff BJ, Taylor GS (2019) The T-cell response to Epstein-Barr virus—new tricks from an old dog. Front Immunol 10(2193):1–11. https://doi.org/10.3389/fimmu.2019.02193

    Article  Google Scholar 

  22. Jayasooriya S, de Silva TI, Njie-jobe J, Sanyang C, Leese AM, Bell AI, McAulay KA, Yanchun P, Long HM, Dong T, Whittle HC, Rickinson AB, Rowland-Jones SL, Hislop AD, Flanagan KL (2015) Early virological and immunological events in asymptomatic Epstein-Barr virus infection in African children. PLOS Pathog 11:e1004746. https://doi.org/10.1371/journal.ppat.1004746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Tian C, Hromatka BS, Kiefer AK, Eriksson N, Noble SM, Tung JY, Hinds DA (2017) Genome-wide association and HLA region fine-mapping studies identify susceptibility loci for multiple common infections. Nat Commun 8(599):1–13. https://doi.org/10.1038/s41467-017-00257-5

    Article  CAS  Google Scholar 

  24. McAulay KA, Higgins CD, Macsween KF, Lake A, Jarrett RF, Robertson FL, Williams H, Crawford DH (2007) HLA class I polymorphisms are associated with development of infectious mononucleosis upon primary EBV infection. J Clin Invest 117:3042–3048. https://doi.org/10.1172/JCI32377.3042

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Becker N, Falster MO, Vajdic CM, De Sanjose S, Martínez-Maza O, Bracci PM, Melbye M, Smedby KE, Engels EA, Turner J, Vineis P, Costantini AS, Holly EA, Spinelli JJ, La Vecchia C, Zheng T, Chiu BCH, Montella M, Cocco P, Maynadié M, Foretova L, Staines A, Brennan P, Davis S, Severson R, Cerhan JR, Breen EC, Birmann B, Cozen W, Grulich AE, Newton R (2012) Self-reported history of infections and the risk of non-Hodgkin lymphoma: an InterLymph pooled analysis. Int J Cancer 131:2342–2348. https://doi.org/10.1002/ijc.27438

  26. Hwang AE, Hamilton AS, Cockburn MG, Ambinder R, Zadnick J, Brown EE, Mack TM, Cozen W (2012) Evidence of genetic susceptibility to infectious mononucleosis: a twin study. Epidemiol Infect 140:2089–2095. https://doi.org/10.1017/S0950268811002457

    Article  CAS  PubMed  Google Scholar 

  27. Rostgaard K, Wohlfahrt J, Hjalgrim H (2014) A genetic basis for infectious mononucleosis: evidence from a family study of hospitalized cases in Denmark. Clin Infect Dis 58:1684–1689. https://doi.org/10.1093/cid/ciu204

    Article  PubMed  Google Scholar 

  28. Kane E, Skibola CF, Bracci PM, Cerhan JR, Costas L, Smedby KE, Holly EA, Maynadié M, Novak AJ, Lightfoot TJ, Ansell SM, Smith AG, Liebow M, Melbye M, Morton L, de Sanjosé S, Slager SL, Wang SS, Zhang Y, Zheng T, Roman E (2015) Non-Hodgkin lymphoma, body mass index, and cytokine polymorphisms: a pooled analysis from the InterLymph Consortium. Cancer Epidemiol Biomarkers Prev 24:1061–1070. https://doi.org/10.1158/1055-9965.EPI-14-1355

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Skibola CF, Bracci PM, Nieters A, Brooks-Wilson A, de Sanjosé S, Hughes AM, Cerhan JR, Skibola DR, Purdue M, Kane E, Lan Q, Foretova L, Schenk M, Spinelli JJ, Slager SL, De Roos AJ, Smith MT, Roman E, Cozen W, Boffetta P, Kricker A, Zheng T, Lightfoot T, Cocco P, Benavente Y, Zhang Y, Hartge P, Linet MS, Becker N, Brennan P, Zhang L, Armstrong B, Smith A, Shiao R, Novak AJ, Maynadie M, Chanock SJ, Staines A, Holford TR, Holly EA, Rothman N, Wang SS (2010) Tumor necrosis factor (TNF) and lymphotoxin-alpha (LTA) polymorphisms and risk of non-Hodgkin lymphoma in the InterLymph Consortium. Am J Epidemiol 171:267–276. https://doi.org/10.1093/aje/kwp383

    Article  PubMed  PubMed Central  Google Scholar 

  30. Rothman N, Skibola CF, Wang SS, Morgan G, Lan Q, Smith MT, Spinelli JJ, Willett E, De Sanjose S, Cocco P, Berndt SI, Brennan P, Brooks-Wilson A, Wacholder S, Becker N, Hartge P, Zheng T, Roman E, Holly EA, Boffetta P, Armstrong B, Cozen W, Linet M, Bosch FX, Ennas MG, Holford TR, Gallagher RP, Rollinson S, Bracci PM, Cerhan JR, Whitby D, Moore PS, Leaderer B, Lai A, Spink C, Davis S, Bosch R, Scarpa A, Zhang Y, Severson RK, Yeager M, Chanock S, Nieters A (2006) Genetic variation in TNF and IL10 and risk of non-Hodgkin lymphoma: a report from the InterLymph Consortium. Lancet Oncol 7:27–38. https://doi.org/10.1016/S1470-2045(05)70434-4

    Article  CAS  PubMed  Google Scholar 

  31. Cerhan JR, Ansell SM, Fredericksen ZS, Kay NE, Liebow M, Call TG, Dogan A, Cunningham JM, Wang AH, Liu-Mares W, Macon WR, Jelinek D, Witzig TE, Habermann TM, Slager SL (2007) Genetic variation in 1253 immune and inflammation genes and risk of non-Hodgkin lymphoma. Blood 110:4455–4463. https://doi.org/10.1182/blood-2007-05-088682

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Cerhan JR, Fredericksen ZS, Novak AJ, Ansell SM, Kay NE, Liebow M, Dogan A, Cunningham JM, Wang AH, Witzig TE, Habermann TM, Asmann YW, Slager SL (2012) A two-stage evaluation of genetic variation in immune and inflammation genes with risk of non-Hodgkin lymphoma identifies new susceptibility locus in 6p21.3 region. Cancer Epidemiol Biomarkers Prev 21:1799–1806. https://doi.org/10.1158/1055-9965.EPI-12-0696

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Conde L, Halperin E, Akers NK, Brown KM, Smedby KE, Rothman N, Nieters A, Slager SL, Brooks-Wilson A, Agana L, Riby J, Liu J, Adami H-O, Darabi H, Hjalgrim H, Low H-Q, Humphreys K, Melbye M, Chang ET, Glimelius B, Cozen W, Davis S, Hartge P, Morton LM, Schenk M, Wang SS, Armstrong B, Kricker A, Milliken S, Purdue MP, Vajdic CM, Boyle P, Lan Q, Zahm SH, Zhang Y, Zheng T, Becker N, Benavente Y, Boffetta P, Brennan P, Butterbach K, Cocco P, Foretova L, Maynadié M, de Sanjosé S, Staines A, Spinelli JJ, Achenbach SJ, Call TG, Camp NJ, Glenn M, Caporaso NE, Cerhan JR, Cunningham JM, Goldin LR, Hanson CA, Kay NE, Lanasa MC, Leis JF, Marti GE, Rabe KG, Rassenti LZ, Spector LG, Strom SS, Vachon CM, Weinberg JB, Holly EA, Chanock S, Smith MT, Bracci PM, Skibola CF (2010) Genome-wide association study of follicular lymphoma identifies a risk locus at 6p21.32. Nat Genet 42:661–664. https://doi.org/10.1038/ng.626

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Spinelli JJ, Ng CH, Weber J-P, Connors JM, Gascoyne RD, Lai AS, Brooks-Wilson AR, Le ND, Berry BR, Gallagher RP (2007) Organochlorines and risk of non-Hodgkin lymphoma. Int J Cancer 121:2767–2775. https://doi.org/10.1002/ijc.23005

    Article  CAS  PubMed  Google Scholar 

  35. Besson H, Brennan P, Becker N, Nieters A, De Sanjosé S, Font R, Maynadié M, Foretova L, Cocco PL, Staines A, Vornanen M, Boffetta P (2006) Tobacco smoking, alcohol drinking and non-Hodgkin’s lymphoma: A European multicenter case-control study (Epilymph). Int J Cancer 119:901–908. https://doi.org/10.1002/ijc.21913

    Article  CAS  PubMed  Google Scholar 

  36. Becker N, Fortuny J, Alvaro T, Nieters A, Maynadié M, Foretova L, Staines A, Brennan P, Boffetta P, Cocco PL, De Sanjose S (2009) Medical history and risk of lymphoma: Results of a European case-control study (EPILYMPH). J Cancer Res Clin Oncol 135:1099–1107. https://doi.org/10.1007/s00432-009-0551-2

    Article  PubMed  Google Scholar 

  37. Cerhan JR, Fredericksen ZS, Wang AH, Habermann TM, Kay NE, Macon WR, Cunningham JM, Shanafelt TD, Ansell SM, Call TG, Witzig TE, Slager SL, Liebow M (2011) Design and validity of a clinic-based case-control study on the molecular epidemiology of lymphoma. Int J Mol Epidemiol Genet 2:95–113

    PubMed  PubMed Central  Google Scholar 

  38. Chatterjee N, Hartge P, Cerhan JR, Cozen W, Davis S, Ishibe N, Colt J, Goldin L, Severson RK (2004) Risk of non-Hodgkin’s lymphoma and family history of lymphatic, hematologic, and other cancers. Cancer Epidemiol Biomarkers Prev 13:1415–1421

    PubMed  Google Scholar 

  39. Hughes AM, Armstrong BK, Vajdic CM, Turner J, Grulich AE, Fritschi L, Milliken S, Kaldor J, Benke G, Kricker A (2004) Sun exposure may protect against non-Hodgkin lymphoma: a case-control study. Int J Cancer 112:865–871. https://doi.org/10.1002/ijc.20470

    Article  CAS  PubMed  Google Scholar 

  40. Smedby KE, Hjalgrim H, Melbye M, Torrång A, Rostgaard K, Munksgaard L, Adami J, Hansen M, Porwit-MacDonald A, Jensen BA, Roos G, Pedersen BB, Sundström C, Glimelius B, Adami H-O (2005) Ultraviolet radiation exposure and risk of malignant lymphomas. J Natl Cancer Inst 97:199–209. https://doi.org/10.1093/jnci/dji022

    Article  PubMed  Google Scholar 

  41. Holly EA, Lele C, Bracci PM, McGrath MS (1999) Case-control study of non-Hodgkin’s lymphoma among women and heterosexual men in the San Francisco Bay Area, California. Am J Epidemiol 150:375–389

    Article  CAS  PubMed  Google Scholar 

  42. Holly EA, Bracci PM (2003) Population-based study of non-Hodgkin lymphoma, histology, and medical history among human immunodeficiency virus-negative participants in San Francisco. Am J Epidemiol 158:316–327

    Article  PubMed  Google Scholar 

  43. Morton LM, Holford TR, Leaderer B, Zhang Y, Zahm SH, Boyle P, Flynn S, Tallini G, Owens PH, Zhang B, Zheng T (2003) Alcohol use and risk of non-Hodgkin’s lymphoma among Connecticut women (United States). Cancer Causes Control 14:687–694. https://doi.org/10.1023/A:1025626208861

    Article  PubMed  Google Scholar 

  44. Smedby KE, Foo JN, Skibola CF, Darabi H, Conde L, Hjalgrim H, Kumar V, Chang ET, Rothman N, Cerhan JR, Brooks-Wilson AR, Rehnberg E, Irwan ID, Ryder LP, Brown PN, Bracci PM, Agana L, Riby J, Cozen W, Davis S, Hartge P, Morton LM, Severson RK, Wang SS, Slager SL, Fredericksen ZS, Novak AJ, Kay NE, Habermann TM, Armstrong B, Kricker A, Milliken S, Purdue MP, Vajdic CM, Boyle P, Lan Q, Zahm SH, Zhang Y, Zheng T, Leach S, Spinelli JJ, Smith MT, Chanock SJ, Padyukov L, Alfredsson L, Klareskog L, Glimelius B, Melbye M, Liu ET, Adami HO, Humphreys K, Liu J (2011) GWAS of follicular lymphoma reveals allelic heterogeneity at 6p21.32 and suggests shared genetic susceptibility with diffuse large B-cell lymphoma. PLoS Genet 7:e1001378. https://doi.org/10.1371/journal.pgen.1001378

  45. Morton LM, Turner JJ, Cerhan JR, Linet MS, Treseler PA, Clarke CA, Jack A, Cozen W, Maynadié M, Spinelli JJ, Costantini AS, Rüdiger T, Scarpa A, Zheng T, Weisenburger DD (2007) Proposed classification of lymphoid neoplasms for epidemiologic research from the Pathology Working Group of the International Lymphoma Epidemiology Consortium (InterLymph). Blood 110:695–708. https://doi.org/10.1182/blood-2006-11-051672

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Turner JJ, Morton LM, Linet MS, Clarke CA, Kadin ME, Vajdic CM, Monnereau A, Maynadiè M, Chiu BCH, Marcos-Gragera R, Costantini AS, Cerhan JR, Weisenburger DD (2010) InterLymph hierarchical classification of lymphoid neoplasms for epidemiologic research based on the WHO classification (2008): Update and future directions. Blood 116:e90–398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Swerdlow SH, Campo E, Harris NL, Jaffe ES, Pileri SA, Stein H, Thiele J, Vardiman J (2008) WHO Classification of tumours of haematopoietic and lymphoid tissues, 4th edn. International Agency for Research on Cancer, Lyon

    Google Scholar 

  48. Johnson AD, Handsaker RE, Pulit SL, Nizzari MM, O’Donnell CJ, De Bakker PIW (2008) SNAP: A web-based tool for identification and annotation of proxy SNPs using HapMap. Bioinformatics 24:2938–2939. https://doi.org/10.1093/bioinformatics/btn564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Mukherjee B, Ahn J, Gruber SB, Rennert G, Moreno V, Chatterjee N (2008) Tests for gene–environment interaction from case-control data: a novel study of type I error, power and designs. Genet Epidemiol 32:615–626. https://doi.org/10.1002/gepi.20337

    Article  PubMed  Google Scholar 

  50. Conneely KN, Boehnke M (2007) So many correlated tests, so little time! rapid adjustment of p values for multiple correlated tests. Am J Hum Genet 81:1158–1168. https://doi.org/10.1086/522036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Pike BL, Nossal GJ (1985) Interleukin 1 can act as a B-cell growth and differentiation factor. Proc Natl Acad Sci U S A 82:8153–8157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Lichtman AH, Chin J, Schmidt JA, Abbas AK (1988) Role of interleukin 1 in the activation of T lymphocytes. Proc Natl Acad Sci U S A 85:9699–9703

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Schett G, Dayer J-M, Manger B (2016) Interleukin-1 function and role in rheumatic disease. Nat Rev Rheumatol 12:14–24. https://doi.org/10.1038/nrrheum.2016.166

    Article  CAS  PubMed  Google Scholar 

  54. Nambu A, Nakae S, Iwakura Y (2006) IL-1β, but not IL-1α, is required for antigen-specific T cell activation and the induction of local inflammation in the delayed-type hypersensitivity responses. Int Immunol 18:701–712. https://doi.org/10.1093/intimm/dxl007

    Article  CAS  PubMed  Google Scholar 

  55. Hackett RJ, Davis LS, Lipsky PE (1988) Comparative effects of tumor necrosis factor-alpha and IL-1 beta on mitogen-induced T cell activation. J Immunol 140:2639–2644

    CAS  PubMed  Google Scholar 

  56. Hirbod-Mobarakeh A, Amirzargar AA, Nikbin B, Nicknam MH, Kutikhin A, Rezaei N (2015) Immunogenetics of cancer. In: Cancer immunology. Springer, Berlin, pp 295–341

  57. Kasztelewicz B, Jankowska I, Pawłowska J, Teisseyre J, Dzierzanowska-Fangrat K (2012) The impact of cytokine gene polymorphisms on Epstein–Barr virus infection outcome in pediatric liver transplant recipients. J Clin Virol 55:226–232. https://doi.org/10.1016/j.jcv.2012.07.005

    Article  CAS  PubMed  Google Scholar 

  58. Terry CF, Loukaci V, Green FR (2000) Cooperative influence of genetic polymorphisms on interleukin 6 transcriptional regulation. J Biol Chem 275:18138–18144. https://doi.org/10.1074/jbc.M000379200

    Article  CAS  PubMed  Google Scholar 

  59. Burger R (2013) Impact of Interleukin-6 in hematological malignancies. Transfus Med Hemother 40:336–343

    Article  PubMed  PubMed Central  Google Scholar 

  60. Abramson JS, Feldman T, Kroll-Desrosiers AR, Muffly LS, Winer E, Flowers CR, Lansigan F, Nabhan C, Nastoupil LJ, Nath R, Goy A, Castillo JJ, Jagadeesh D, Woda B, Rosen ST, Smith SM, Evens AM (2014) Peripheral T-cell lymphomas in a large US multicenter cohort: prognostication in the modern era including impact of frontline therapy. Ann Oncol 25:2211–2217. https://doi.org/10.1093/annonc/mdu443

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Coiffier B, Brousse N, Peuchmaur M, Berger F, Gisselbrecht C, Bryon PA, Diebold J (1990) Original article: peripheral T-cell lymphomas have a worse prognosis than B-cell lymphomas: a prospective study of 361 immunophenotyped patients treated with the LNH-84 regimen. Ann Oncol 1:45–50. https://doi.org/10.1093/oxfordjournals.annonc.a057673

    Article  CAS  PubMed  Google Scholar 

  62. Weisenburger DD, Savage KJ, Harris NL, Gascoyne RD, Jaffe ES, MacLennan KA, Rüdiger T, Pileri S, Nakamura S, Nathwani B, Campo E, Berger F, Coiffier B, Kim WS, Holte H, Federico M, Au WY, Tobinai K, Armitage JO, Vose JM (2011) Peripheral T-cell lymphoma, not otherwise specified: a report of 340 cases from the International Peripheral T-cell Lymphoma Project. Blood 117:3402–3408. https://doi.org/10.1182/blood-2010-09-310342

    Article  CAS  PubMed  Google Scholar 

  63. Talpur R, Singh L, Daulat S, Liu P, Seyfer S, Trynosky T, Wei W, Duvic M (2012) Long-term outcomes of 1,263 patients with mycosis fungoides and sézary syndrome from 1982 to 2009. Clin Cancer Res 18:5051–5060. https://doi.org/10.1158/1078-0432.CCR-12-0604

    Article  CAS  PubMed  Google Scholar 

  64. Houldcroft CJ, Kellam P (2015) Host genetics of Epstein-Barr virus infection, latency and disease. Rev Med Virol 25:71–84

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The authors would like to thank Annalie Landgren and Aaron Norman for supporting the InterLymph Consortium. In addition, the authors would like to acknowledge the support of the InterLymph Data Coordinating Center at Mayo Clinic as well as the Ulla and Mogens Folmer Andersen’s Foundation.

Funding

This work was supported by awards from National Cancer Institute/National Institutes of Health (N01-CN-75014-20, P30CA014089, R01 CA186646, P30 CA13148, R21 CA155951, U54 CA118948, CA45614, CA87014, CA104682, and CA154643); Agència de Gestió d’Ajuts Universitaris i de Recerca (AGAUR), CERCA Programme/Generalitat de Catalunya for institutional support (2017SGR1085); Spanish Ministry of Economy and Competitiveness—Carlos III Institute of Health cofunded by FEDER funds/European Regional Development Fund (ERDF)—a way to build Europe (PI14/01219); Centro de Investigación Biomédica en Red: Epidemiología y Salud Pública (CIBERESP, Spain); the Canadian Institutes for Health Research (CIHR); Canadian Cancer Society; and Michael Smith Foundation for Health Research [British Columbia]). The collection of cancer incidence data used in the UCSF study was supported by the California Department of Public Health pursuant to California Health and Safety Code Section 103885; Centers for Disease Control and Prevention’s (CDC) National Program of Cancer Registries, under cooperative agreement 5NU58DP003862-04/DP003862; and the National Cancer Institute’s Surveillance, Epidemiology, and End Results Program under contract HHSN261201000140C awarded to the Cancer Prevention Institute of California, contract HHSN261201000035C awarded to the University of Southern California (NHL MultiCenter Case–Control Study site), and contract HHSN261201000034C awarded to the Public Health Institute.

Author information

Authors and Affiliations

  1. Department of Preventive Medicine, Center for Genetic Epidemiology, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA

    Niquelle Brown Wadé, David Conti, Joshua Millstein, Jun Wang & Wendy Cozen

  2. Cigna Health and Life Insurance Company (Cigna), Bloomfield, CT, USA

    Niquelle Brown Wadé

  3. Division of Population Health Sciences, Center for Tobacco Products, Food and Drug Administration, Bethesda, MD, USA

    Cindy M. Chang

  4. USC Norris Comprehensive Cancer Center, Keck School of Medicine, University of Southern California, Los Angeles, CA, USA

    David Conti, Joshua Millstein, Jun Wang & Wendy Cozen

  5. Department of Hematology and Medical Oncology, Emory University School of Medicine, Atlanta, GA, USA

    Christine Skibola

  6. Center for Chronic Immunodeficiency (CCI), University Medical Center Freiburg, University of Freiburg, Freiburg, Germany

    Alexandra Nieters

  7. Department of Computational and Quantitative Medicine, City of Hope Comprehensive Cancer Center, Duarte, CA, USA

    Sophia S. Wang

  8. Sexual and Reproductive Health, PATH, Seattle, WA, USA

    Silvia De Sanjose

  9. Centro de Investigación Biomédica en Red: Epidemiología y Salud Pública (CIBERESP), Madrid, Spain

    Silvia De Sanjose

  10. Department of Health Sciences, University of York, York, YO10 5DD, UK

    Eleanor Kane

  11. Population Oncology, BC Cancer Agency, Vancouver, Canada

    John J. Spinelli

  12. School of Population and Public Health, University of British Columbia, Vancouver, BC, Canada

    John J. Spinelli

  13. Department of Epidemiology and Biostatistics, University of California at San Francisco, San Francisco, CA, USA

    Paige Bracci

  14. Department of Surgery, Yale School of Medicine and Yale School of Public Health, New Haven, CT, USA

    Yawei Zhang

  15. Department of Epidemiology, Mayo Clinic, Rochester, MN, USA

    Susan Slager

  16. Department of Epidemiology Research, Statens Serum Institut, Copenhagen, Denmark

    Henrik Hjalgrim

  17. Department of Haematology, Rigshospitalet, Copenhagen, Denmark

    Henrik Hjalgrim

  18. Karolinska Institutet, Sweden University Hospital, Karolinska University, Stockholm, Sweden

    Karin Ekstrom Smedby

  19. Department of Pathology, O’Neal Comprehensive Cancer Center, University of Alabama at Birmingham, Birmingham, AL, USA

    Elizabeth E. Brown

  20. MRC-University of Glasgow Centre for Virus Research, Glasgow, Scotland

    Ruth F. Jarrett

  21. Department of Pathology, Keck School of Medicine, University of Southern California, Los Angeles, CA, 90033, USA

    Wendy Cozen

Authors
  1. Niquelle Brown Wadé
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cindy M. Chang
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. David Conti
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Joshua Millstein
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Christine Skibola
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alexandra Nieters
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Sophia S. Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Silvia De Sanjose
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Eleanor Kane
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. John J. Spinelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Paige Bracci
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yawei Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Susan Slager
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Jun Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Henrik Hjalgrim
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Karin Ekstrom Smedby
    View author publications

    You can also search for this author in PubMed Google Scholar

  17. Elizabeth E. Brown
    View author publications

    You can also search for this author in PubMed Google Scholar

  18. Ruth F. Jarrett
    View author publications

    You can also search for this author in PubMed Google Scholar

  19. Wendy Cozen
    View author publications

    You can also search for this author in PubMed Google Scholar

Consortia

for the InterLymph Consortium Immunology and Infection Working

Corresponding author

Correspondence to Wendy Cozen.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Disclaimers The ideas and opinions expressed herein are those of the author(s) and do not necessarily reflect the opinions of the State of California, Department of Public Health, the National Cancer Institute, National Institutes of Health, or the Centers for Disease Control and Prevention or their Contractors and Subcontractors. The information in this article is not a formal dissemination of information by the FDA and does not represent agency position or policy. The contents are the responsibility of the authors alone. This article was prepared while Dr. Cindy Chang was employed at the National Cancer Institute.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 54 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wadé, N.B., Chang, C.M., Conti, D. et al. Infectious mononucleosis, immune genotypes, and non-Hodgkin lymphoma (NHL): an InterLymph Consortium study. Cancer Causes Control 31, 451–462 (2020). https://doi.org/10.1007/s10552-020-01266-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10552-020-01266-4

Keywords

Search

Navigation