Skip to main content
SpringerLink
Log in

Adjuvants and lymphoma risk as part of the ASIA spectrum

Immunologic Research volume 61, pages 79–89 (2015)Cite this article

Abstract

The emerging epidemic of Hodgkin and non-Hodgkin lymphomas worldwide continues to defy our understanding and forces the search for the causative factors. Adjuvants are known to act as triggers of immune and inflammatory responses. Animal experiments have demonstrated that long-term inflammation is related to aggravation of the immune network resulting in cellular and humoral responses leading to autoimmunity and lymphoma development. Chronic stimulation of the immune system is thought to be the key mechanism through which infectious diseases as well as autoimmune diseases can lead to lymphomagenesis. Many adjuvants can act similarly perturbing immune system’s function, inducing a state of prolonged immune activation related to chronic lymphatic drainage. Several mechanisms were proposed by which adjuvants induce inflammation, and they are discussed herein. Some of them are triggering inflammasome; others bind DNA, lipid moieties in cells, induce uric acid production or act as lipophilic and/or hydrophobic substances. The sustained inflammation increases the risk of genetic aberrations, where the initial polyclonal activation ends in monoclonality. The latter is the hallmark of malignant lymphoma. Thus, chronic adjuvant stimulation may lead to lymphoma.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

USD 39.95

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

References

  1. National Institutes of Health USA.gov. Understanding autoimmune diseases. October-2012. http://www.niams.nih.gov/HEALTH_INFO/Autoimmune/understanding_autoimmune.pdf.

  2. Kapatai G, Murray P. Contribution of the Epstein–Barr virus to the molecular pathogenesis of Hodgkin lymphoma. J Clin Pathol. 2007;60(12):1342–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Shehab TM, Hsi ED, Poterucha JJ, Gunaratnam NT, Fontana RJ. Helicobacter pylori-associated gastric MALT lymphoma in liver transplant recipients. Transplantation. 2001;71:1172–5.

    Article  CAS  PubMed  Google Scholar 

  4. Sagaert X, Van Cutsem E, De Hertogh G, Geboes K, Tousseyn T. Gastric MALT lymphoma: a model of chronic inflammation-induced tumor development. Nat Rev Gastroenterol Hepatol. 2010;7(6):336–46.

    CAS  PubMed  Google Scholar 

  5. Mariette X. Lymphomas complicating Sjögren’s syndrome and hepatitis C virus infection may share a common pathogenesis: chronic stimulation of rheumatoid factor B cells. Ann Rheum Dis. 2001;60:1007–10.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Bernatsky S, Ramsey-Goldman R, Labrecque J, et al. Cancer risk in systemic lupus: an updated international multi-centre cohort study. J Autoimmun. 2013;42:130–5.

    Article  PubMed Central  PubMed  Google Scholar 

  7. Shoenfeld Y, Agmon-Levin N. ‘ASIA’—autoimmune/inflammatory syndrome induced by adjuvants. J Autoimmun. 2011;36(1):4–8.

    Article  CAS  PubMed  Google Scholar 

  8. Schaefer CJ, Lawrence WD, Wooley PH. Influence of long term silicone implantation on type II collagen induced arthritis in mice. Ann Rheum Dis. 1999;58:503–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Koppang EO, Bjerkås I, Haugarvoll E. Vaccination-induced systemic autoimmunity in farmed Atlantic salmon. J Immunol. 2008;181(7):4807–14.

    Article  CAS  PubMed  Google Scholar 

  10. Schaefer CJ, Wooley PH. The influence of silicone implantation on murine lupus in MRL lpr/lpr mice. J Rheumatol. 1999;26(10):2215–21.

    CAS  PubMed  Google Scholar 

  11. Dimitrijević L, Živković I, Stojanović M, et al. Vaccine model of antiphospholipid syndrome induced by tetanus vaccine. Lupus. 2012;21:195–202.

    Article  PubMed  Google Scholar 

  12. Agmon-Levin N, Hughes GR, Shoenfeld Y. The spectrum of ASIA: ‘Autoimmune (auto-inflammatory) syndrome induced by adjuvants’. Lupus. 2012;21(2):118–20.

    Article  CAS  PubMed  Google Scholar 

  13. Perricone C, Colafrancesco S, Mazor RD, Soriano A, Agmon-Levin N, Shoenfeld Y. Autoimmune/inflammatory syndrome induced by adjuvants (ASIA) 2013: unveiling the pathogenic, clinical and diagnostic aspects. J Autoimmun. 2013;47:1–16.

    Article  CAS  PubMed  Google Scholar 

  14. Malik AF, Hoque R, Ouyang X. Inflammasome components Asc and caspase-1 mediate biomaterial-induced inflammation and foreign body response. Proc Natl Acad Sci USA. 2011;108(50):20095–100.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  15. Miranda RN, Aladily TN, Prince HM, et al. Breast implant-associated anaplastic large-cell lymphoma: long-term follow-up of 60 patients. J Clin Oncol. 2014;32:114–20.

    Article  PubMed Central  PubMed  Google Scholar 

  16. Bichel L. Postvaccinial lymphadenitis developing into Hodgkin’s disease. Acta Med Scand. 1976;199(6):523–5.

    CAS  PubMed  Google Scholar 

  17. Maubec E, Pinquier L, Viguier M, et al. Vaccination-induced cutaneous pseudolymphoma. J Am Acad Dermatol. 2005;52(4):623–9.

    Article  PubMed  Google Scholar 

  18. Hernández I, Sanmartín O, Cardá C, Góme S, Alfaro A. B-cell pseudolymphoma caused by aluminium hydroxide following hyposensitization therapy. Actas Dermosifiliogr. 2008;99(3):213–6.

    Article  PubMed  Google Scholar 

  19. Codrich D, Monai M, Pelizzo G, et al. Primary pulmonary Hodgkin’s disease and tuberculosis in an 11-year-old boy: case report and review of the literature. Pediatr Pulmonol. 2006;41(7):694–8.

    Article  PubMed  Google Scholar 

  20. Sanchez-Gonzalez B, Garcia M, Montserrat F, et al. Diffuse large B-cell lymphoma associated with chronic inflammation in metallic implant. J Clin Oncol. 2013;31(10):e148–51.

    Article  PubMed  Google Scholar 

  21. Chaudhry MS, Mather H, Marks A, Naresh K. Diffuse large B cell lymphoma complicating total knee arthroplasty: case report and literature review of the association of diffuse large B cell lymphoma with joint replacement. Acta Haematol. 2011;126(3):141–6.

    Article  PubMed  Google Scholar 

  22. Cheuk W, Chan AC, Chan JK, Lau GT, Chan VN, Yiu HH. Metallic implant-associated lymphoma: a distinct subgroup of large B-cell lymphoma related to pyothorax-associated lymphoma? Am J Surg Pathol. 2005;29(6):832–6.

    Article  PubMed  Google Scholar 

  23. Lidgren L. Chronic inflammation, joint replacement and malignant lymphoma. J Bone Joint Surg Br. 2008;90(1):7–10.

    Article  CAS  PubMed  Google Scholar 

  24. Madewell BR, Gieger TL, Pesavento PA, Kent MS. Vaccine site-associated sarcoma and malignant lymphoma in cats: a report of six cases (1997–2002). J Am Anim Hosp Assoc. 2004;40:47–50.

    Article  PubMed  Google Scholar 

  25. Anderson PN, Potter M. Induction of plasma cell tumours in BALB-c mice with 2,6,10,14-tetramethylpentadecane (pristane). Nature. 1969;222(5197):994–5.

    Article  CAS  PubMed  Google Scholar 

  26. Potter M. A resumé of the current status of the development of plasma-cell tumors in mice. Cancer Res. 1968;28:1891–6.

    CAS  PubMed  Google Scholar 

  27. Wooley PH, Whalen JD. Pristane-induced arthritis in mice. III. Lymphocyte phenotypic and functional abnormalities precede the development of pristane-induced arthritis. Cell Immunol. 1991;138(1):251–9.

    Article  CAS  PubMed  Google Scholar 

  28. Kuroda Y, Nacionales DC, Akaogi J, Reeves WH, Satoh M. Autoimmunity induced by adjuvant hydrocarbon oil components of vaccine. Biomed Pharmacother. 2004;58:325–37.

    Article  CAS  PubMed  Google Scholar 

  29. Kojima M, Itoh H, Shimizu K, et al. Malignant lymphoma in patients with systemic rheumatic disease (rheumatoid arthritis, systemic lupus erythematosus, systemic sclerosis, and dermatomyositis): a clinicopathologic study of 24 Japanese cases. Int J Surg Pathol. 2006;14(1):43–8.

    Article  CAS  PubMed  Google Scholar 

  30. Baecklund E, Smedby KE, Sutton LA, Askling J, Rosenquist R. Lymphoma development in patients with autoimmune and inflammatory disorders—What are the driving forces? Semin Cancer Biol. 2014;24:61–70.

    Article  CAS  PubMed  Google Scholar 

  31. Bichile T, Petri M. Incidence of lymphoma associated with underlying lupus: lessons learned from observational studies. Curr Opin Rheumatol. 2014;26(2):111–7.

    Article  CAS  PubMed  Google Scholar 

  32. Tarella C, Gueli A, Ruella M, Cignetti A. Lymphocyte transformation and autoimmune disorders. Autoimmun Rev. 2013;12(8):802–13.

    Article  CAS  PubMed  Google Scholar 

  33. Theander E, Henriksson G, Ljungberg O, Mandl T, Manthorpe R, Jacobsson LT. Lymphoma and other malignancies in primary Sjögren’s syndrome: a cohort study on cancer incidence and lymphoma predictors. Ann Rheum Dis. 2006;65(6):796–803.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  34. Smedby KE, Baecklund E, Askling J. Malignant lymphomas in autoimmunity and inflammation: a review of risks, risk factors, and lymphoma characteristics. Cancer Epidemiol Biomark Prev. 2006;15(11):2069–77.

    Article  CAS  Google Scholar 

  35. Voulgarelis M, Skopouli FN. Clinical, immunologic, and molecular factors predicting lymphoma development in Sjogren’s syndrome patients. Clin Rev Allergy Immunol. 2007;32(3):265–74.

    Article  CAS  PubMed  Google Scholar 

  36. Routsias JG, Goules JD, Charalampakis G, Tzima S, Papageorgiou A, Voulgarelis M. Malignant lymphoma in primary Sjögren’s syndrome: an update on the pathogenesis and treatment. Semin Arthritis Rheum. 2013;43(2):178–86.

    Article  CAS  PubMed  Google Scholar 

  37. Kristinsson SY, Landgren O, Sjöberg J, Turesson I, Björkholm M, Goldin LR. Autoimmunity and risk for Hodgkin’s lymphoma by subtype. Haematologica. 2009;94(10):1468–9.

    Article  PubMed Central  PubMed  Google Scholar 

  38. Van Baarsen LG, de Hair MJ, Ramwadhdoebe TH, et al. The cellular composition of lymph nodes in the earliest phase of inflammatory arthritis. Ann Rheum Dis. 2013;72(8):1420–4.

    Article  PubMed Central  PubMed  Google Scholar 

  39. Volkmann ER, Agrawal H, Maranian P, Furst DE. Rituximab for rheumatoid arthritis: a meta-analysis and systematic review. Clin Med Insights Ther. 2010;2:749–60.

    CAS  Google Scholar 

  40. Sluzevich JC, Hall MR, Roy V. Subcutaneous panniculitis-like T-cell lymphoma after rituximab. J Am Acad Dermatol. 2012;67(5):e223–5.

    Article  PubMed  Google Scholar 

  41. Blank M, Gershwin ME. Autoimmunity: from the mosaic to the kaleidoscope. J Autoimmun. 2008;30(1–2):1–4.

    Article  PubMed  Google Scholar 

  42. Anaya JM, Corena R, Castiblanco J, Rojas-Villarraga A, Shoenfeld Y. The kaleidoscope of autoimmunity: multiple autoimmune syndromes and familial autoimmunity. Expert Rev Clin Immunol. 2007;3(4):623–35.

    Article  CAS  PubMed  Google Scholar 

  43. Gherardi RK. Lessons from macrophagic myofasciitis: towards definition of a vaccine adjuvant-related syndrome. Rev Neurol (Paris). 2003;159(2):162–4.

    CAS  Google Scholar 

  44. Han S, Asoyan A, Rabenstein H, Nakano N, Obst R. Role of antigen persistence and dose for CD4+ T-cell exhaustion and recovery. Proc Natl Acad Sci USA. 2010;107(47):20453–8.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  45. Wherry EJ, Ha SJ, Kaech SM, et al. Molecular signature of CD8+ T cell exhaustion during chronic viral infection. Immunity. 2007;27(4):670–84.

    Article  CAS  PubMed  Google Scholar 

  46. Wherry EJ. T cell exhaustion. Nat Immunol. 2011;12(6):492–9.

    Article  CAS  PubMed  Google Scholar 

  47. Moir S, Ho J, Malaspina A, et al. Evidence for HIV-associated B cell exhaustion in a dysfunctional memory B cell compartment in HIV-infected viremic individuals. J Exp Med. 2008;205(8):1797–805.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  48. Kappel R, Cohen Tervaert J, Pruijn G. Autoimmune/inflammatory syndrome induced by adjuvants (ASIA) due to silicone implant incompatibility syndrome in three sisters. Clin Exp Rheumatol. 2014;32(2):256–8.

  49. Kim PS, Ahmed R. Features of responding T cells in cancer and chronic infection. Curr Opin Immunol. 2010;22(2):223–30.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  50. Chen YJ, Wu CY, Shen JL, Chen TT, Chang YT. Cancer risk in patients with chronic urticaria: a population-based cohort study. 35. Arch Dermatol. 2012;148(1):103–8.

    Article  PubMed  Google Scholar 

  51. Jafroodi M, Zargari O, Hoda S. Concomitant Hodgkin’s lymphoma and atopic dermatitis in a child with Celiac disease. Arch Iran Med. 2009;12(3):317–9.

    PubMed  Google Scholar 

  52. Vu J, Ho J, English JC 3rd. Dermal hypersensitivity reaction as a prodrome to Hodgkin lymphoma. J Am Acad Dermatol. 2010;63(1):e13–4.

    Article  PubMed  Google Scholar 

  53. Arellano FM, Arana A, Wentworth CE, Fernández-Vidaurre C, Schlienger RG, Conde E. Lymphoma among patients with atopic dermatitis and/or treated with topical immunosuppressants in the United Kingdom. J Allergy Clin Immunol. 2009;123(5):1111-6, 116.e1-13.

  54. Vajdic CM, Falster MO, de Sanjose S, et al. Atopic disease and risk of non-Hodgkin lymphoma: an InterLymph pooled analysis. Cancer Res. 2009;69(16):6482–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Porto DA, Comfere NI, Myers LM, Abbott JJ. Pseudolymphomatous reaction to varicella zoster virus vaccination: role of viral in situ hybridization. J Cutan Pathol. 2010;37(10):1098–102.

    Article  PubMed  Google Scholar 

  56. Cerroni L, Borroni RG, Massone C, Chott A, Kerl H. Cutaneous B-cell pseudolymphoma at the site of vaccination. Am J Dermatopathol. 2007;29(6):538–42.

    Article  PubMed  Google Scholar 

  57. Eisenbarth SC, Colegio OR, O’Connor W, Sutterwala FS, Flavell RA. Crucial role for the Nalp3 inflammasome in the immunostimulatory properties of aluminium adjuvants. Nature. 2008;453:1122–6.

    Article  CAS  PubMed  Google Scholar 

  58. Coleman DL, King RN, Andrade JD. The foreign body reaction: a chronic inflammatory response. J Biomed Mater Res. 1974;8(5):199–211.

    Article  CAS  PubMed  Google Scholar 

  59. Pan SY, Lavigne E, Holowaty EJ, et al. Canadian breast implant cohort: extended follow-up of cancer incidence. Int J Cancer. 2012;131:E1148–57.

    Article  CAS  PubMed  Google Scholar 

  60. Friis S, Hölmich LR, McLaughlin JK, et al. Cancer risk among Danish women with cosmetic breast implants. Int J Cancer. 2006;118:998–1003.

    Article  CAS  PubMed  Google Scholar 

  61. Brisson J, Holowaty EJ, Villeneuve PJ, et al. Cancer incidence in a cohort of Ontario and Quebec women having bilateral breast augmentation. Int J Cancer. 2006;118:2854–62.

    Article  CAS  PubMed  Google Scholar 

  62. US Food and Drug Administration: Anaplastic large cell lymphoma (ALCL) in women with breast implants: Preliminary FDA findings and analyses. 2013. www.fda.gov/MedicalDevices/ProductsandMedicalProcedures/ImplantsandProsthetics/BreastImplants/ucm239995.htm.

  63. Supersaxo A, Hein WR, Steffen H. Mixed micelles as a proliposomal, lymphotropic drug carrier. Pharm Res. 1991;8(10):1286–91.

    Article  CAS  PubMed  Google Scholar 

  64. Charman WN. Lipids, lipophilic drugs, and oral drug delivery-some emerging concepts. J Pharm Sci. 2000;89(8):967–78.

    Article  CAS  PubMed  Google Scholar 

  65. Kadir F. Intramuscular and subcutaneous drug delivery: encapsulation in liposomes and other methods to manipulate drug availability. Pharm World Sci. 1993;15(4):173–5.

    Article  CAS  Google Scholar 

  66. Israeli E, Agmon-Levin N, Blank M, Shoenfeld Y. Adjuvants and autoimmunity. Lupus. 2009;18(13):1217–25.

  67. Flach TL, Ng G, Hari A. Alum interaction with dendritic cell membrane lipids is essential for its adjuvanticity. Nat Med. 2011;17(4):479–87.

    Article  CAS  PubMed  Google Scholar 

  68. Mbow ML, de Gregorio E, Ulmer JB. Alum’s adjuvant action: grease is the word. Nat Med. 2011;17:415–6.

    Article  CAS  PubMed  Google Scholar 

  69. Petrovsky N. Novel human polysaccharide adjuvants with dual Th1 and Th2 potentiating activity. Vaccine. 2006;24(Suppl 2):S2-26–9.

    Google Scholar 

  70. Tomljenovic L, Shaw CA. Aluminum vaccine adjuvants: Are they safe? Curr Med Chem. 2011;18(17):2630–7.

    Article  CAS  PubMed  Google Scholar 

  71. Chen L, Zhang B, Toborek M. Autophagy is involved in nanoalumina-induced cerebrovascular toxicity. Nanomedicine. 2013;9(2):212–21.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  72. Chen L, Yokel RA, Hennig B, Toborek M. Manufactured aluminum oxide nanoparticles decrease expression of tight junction proteins in brain vasculature. J Neuroimmune Pharmacol. 2008;3(4):286–95.

    Article  PubMed Central  PubMed  Google Scholar 

  73. Marichal T, Ohata K, Bedoret D, et al. DNA released from dying host cells mediates aluminum adjuvant activity. Nat Med. 2011;17(8):996–1002.

    Article  CAS  PubMed  Google Scholar 

  74. Marrack P, McKee AS, Munks MW. Towards an understanding of the adjuvant action of aluminium. Nat Rev Immunol. 2009;9(4):287–93.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  75. Martínez-Estévez M, Racagni-Di Palma G, Muñoz-Sánchez JA, Brito-Argáez L, Loyola-Vargas VM, Hernández-Sotomayor SM. Aluminium differentially modifies lipid metabolism from the phosphoinositide pathway in Coffea arabica cells. J Plant Physiol. 2003;160(11):1297–303.

    Article  PubMed  Google Scholar 

  76. Robinson WH, Sokolove J. Citrullination of fibrinogen: generation of neoepitopes and enhancement of immunostimulatory properties. Arthritis Res Ther. 2012;14(Suppl 1):O30.

    Article  PubMed Central  Google Scholar 

  77. Fredman P, Lekman A. Glycosphingolipids as potential diagnostic markers and/or antigens in neurological disorders. Neurochem Res. 1997;22(8):1071–83.

    Article  CAS  PubMed  Google Scholar 

  78. Israeli E, Agmon-Levin N, Blank M, Chapman J, Shoenfeld Y. Guillain–Barré syndrome—a classical autoimmune disease triggered by infection or vaccination. Clin Rev Allergy Immunol. 2012;42(2):121–30.

    Article  CAS  PubMed  Google Scholar 

  79. Takayama K, Wang C, Besra GS. Pathway to synthesis and processing of mycolic acids in Mycobacterium tuberculosis. Clin Microbiol Rev. 2005;18(1):81–101.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  80. Petrovsky N, Aguilar JC. Vaccine adjuvants: current state and future trends. Immunol Cell Biol. 2004;82:488–96.

    Article  CAS  PubMed  Google Scholar 

  81. Billiau A, Matthys P. Modes of action of Freund’s adjuvants in experimental models of autoimmune diseases. J Leukoc Biol. 2001;70(6):849–60.

    CAS  PubMed  Google Scholar 

  82. Mosca F, Tritto E, Muzzi A, et al. Molecular and cellular signatures of human vaccine adjuvants. Proc Natl Acad Sci USA. 2008;105(30):10501–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  83. Butler NR, Voyce MA, Burland WL, Hilton ML. Advantages of aluminium hydroxide adsorbed combined diphtheria, tetanus, and pertussis vaccines for the immunization of infants. Br Med J. 1969;1(5645):663–6.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  84. O’Lenick T, O’Lenick T. Altering organic oils with silicones. H&PC Today. 2011;6(1):72–5.

  85. Vera-Lastra O, Medina G, del Pilar Cruz-Dominguez M, et al. Human adjuvant disease induced by foreign substances: a new model of ASIA (Shoenfeld’s syndrome). Lupus. 2012;21:128e35.

    Article  Google Scholar 

  86. Ulrichs T, Kaufmann SH. New insights into the function of granulomas in human tuberculosis. J Pathol. 2006;208:261–9.

    Article  CAS  PubMed  Google Scholar 

  87. Blum A, Abboud W, Shajrawi I, Tatour I. Prolonged fever due to silicone granulomatosis. Isr Med Assoc J. 2007;9(2):121–2.

    PubMed  Google Scholar 

  88. Gherardi RK, Coquet M, Cherin P, et al. Macrophagic myofasciitis lesions assess long-term persistence of vaccine-derived aluminium hydroxide in muscle. Brain. 2001;124(Pt 9):1821–31.

    Article  CAS  PubMed  Google Scholar 

  89. Krewski D, Yokel RA, Nieboer E, et al. Human health risk assessment for aluminium, aluminium oxide, and aluminium hydroxide. J Toxicol Environ Health B Crit Rev. 2007;10(Suppl 1):1–269.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  90. Tomljenovic L. Aluminum and Alzheimer’s disease: after a century of controversy, is there a plausible link? J Alzheimers Dis. 2011;23(4):567–98.

    CAS  PubMed  Google Scholar 

  91. www.trianglecc.com/labels/Tricard%20Silicone20100%20Label.pdf.

  92. Nagase H, Ose Y, Sato T. Possible methylation of inorganic mercury by silicones in the environment. Environ Sci Total Environ. 1988;73(1–2):29–38.

    Article  CAS  Google Scholar 

  93. Andrews JM. Cellular behavior to injected silicone fluid: a preliminary report. Plast Reconstr Surg. 1966;38(6):581–3.

    Article  CAS  PubMed  Google Scholar 

  94. Hu D, Wan L, Chen M, Caudle Y, LeSage G, Li Q, Yin D. Essential role of IL-10/STAT3 in chronic stress-induced immune suppression. Brain Behav Immun. 2014;36:118–27.

    Article  CAS  PubMed  Google Scholar 

  95. Kleinewietfeld M, Hafler DA. Regulatory T cells in autoimmune neuroinflammation. Immunol Rev. 2014;259(1):231–44.

    Article  CAS  PubMed  Google Scholar 

  96. Elefsiniotis IS, Papatsimpas G, Liatsos GD, Tasidou A, Moulakakis A. Atypical autoimmune polyglandular syndrome type 3 overlapped by chronic HCV infection resulting in carcinogenesis and fatal infection. South Med J. 2008;101(7):756–8.

    Article  PubMed  Google Scholar 

  97. Saadoun D, Terrier B, Bannock J, et al. Expansion of autoreactive unresponsive CD21−/low B cells in Sjögren’s syndrome—associated lymphoproliferation. Arthritis Rheum. 2013;65:1085–96.

    Article  CAS  PubMed  Google Scholar 

  98. Kauppi M, Pukkala E, Isomäki H. Elevated incidence of hematologic malignancies in patients with Sjögren’s syndrome compared with patients with rheumatoid arthritis (Finland). Cancer Causes Control. 1997;8(2):201–4.

    Article  CAS  PubMed  Google Scholar 

  99. Dreyer L, Faurschou M, Mogensen M, Jacobsen S. High incidence of potentially virus-induced malignancies in systemic lupus erythematosus: a long-term followup study in a Danish cohort. Arthritis Rheum. 2011;63:3032–7.

    Article  PubMed  Google Scholar 

  100. Smitten AL, Simon TA, Hochberg MC, Suissa S. A meta-analysis of the incidence of malignancy in adult patients with rheumatoid arthritis. Arthritis Res Ther. 2008;10(2):R45.

    Article  PubMed Central  PubMed  Google Scholar 

  101. Mercer LK, Davies R, Galloway J, et al. Risk of cancer in patients receiving non-biologic disease-modifying therapy for rheumatoid arthritis compared with the UK general population. Rheumatology (Oxford). 2013;52:91–8.

    Article  Google Scholar 

  102. Grainge MJ, West J, Solaymani-Dodaran M, Card TR, Logan RF. The long-term risk of malignancy following a diagnosis of coeliac disease or dermatitis herpetiformis: a cohort study. Aliment Pharmacol Ther. 2012;35(6):730–9.

    Article  CAS  PubMed  Google Scholar 

  103. Smedby KE, Åkerman M, Hildebrand H, Glimelius B, Ekbom A, Askling J. Malignant lymphomas in coeliac disease: evidence of increased risks for lymphoma types other than enteropathy-type T cell lymphoma. Gut. 2005;54(1):54–9.

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  104. Zhang JQ, Wan YN, Peng WJ, et al. The risk of cancer development in systemic sclerosis: a meta-analysis. Cancer Epidemiol. 2013;37(5):523–7.

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. The Zabludowicz Center for Autoimmune diseases, Sheba Medical Center, Tel Hashomer, Israel

    Dana Butnaru & Yehuda Shoenfeld

  2. División of Clinical Immunology, Hospital General Universitario Gregorio Marañón, Madrid, Spain

    Dana Butnaru

  3. Sackler Faculty of Medicine, Incumbent of the Laura Schwarz-Kipp Chair for Research of Autoimmune Diseases, Tel-Aviv University, Tel Aviv, Israel

    Yehuda Shoenfeld

Authors
  1. Dana Butnaru
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yehuda Shoenfeld
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dana Butnaru.

Rights and permissions

Reprints and Permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Butnaru, D., Shoenfeld, Y. Adjuvants and lymphoma risk as part of the ASIA spectrum. Immunol Res 61, 79–89 (2015). https://doi.org/10.1007/s12026-014-8622-0

Download citation

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12026-014-8622-0

Keywords

search

Navigation