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Review Article

Rheumatic diseases associated with immune checkpoint inhibitors in cancer immunotherapy

, , &
Pages 721-732 | Received 19 Jul 2018, Accepted 01 Oct 2018, Published online: 20 Dec 2018

References

  • Ribas A, Wolchok JD. Cancer immunotherapy using checkpoint blockade. Science. 2018;359(6382):1350–5.
  • Hodi FS, O’Day SJ, McDermott DF, Weber RW, Sosman JA, Haanen JB, et al. Improved survival with ipilimumab in patients with metastatic melanoma. N Engl J Med. 2010;363(8):711–23.
  • Postow MA, Sidlow R, Hellmann MD. Immune-related adverse events associated with immune checkpoint blockade. N Engl J Med. 2018;378(2):158–68.
  • Suarez-Almazor ME, Kim ST, Abdel-Wahab N, Diab A. Immune-related adverse events with use of checkpoint inhibitors for immunotherapy of cancer. Arthritis Rheumatol. 2017;69(4):687–99.
  • Brahmer JR, Lacchetti C, Schneider BJ, Atkins MB, Brassil KJ, Caterino JM, et al. Management of immune-related adverse events in patients treated with immune checkpoint inhibitor therapy: American Society of Clinical Oncology Clinical Practice Guideline. J Clin Oncol. 2018;36(17):1714–68.
  • Michot JM, Bigenwald C, Champiat S, Collins M, Carbonnel F, Postel-Vinay S, et al. Immune-related adverse events with immune checkpoint blockade: a comprehensive review. Eur J Cancer. 2016; 54:139–48.
  • Iwasaki A, Medzhitov R. Control of adaptive immunity by the innate immune system. Nat Immunol. 2015;16(4):343–53.
  • Chen L, Flies DB. Molecular mechanisms of T cell co-stimulation and co-inhibition. Nat Rev Immunol. 2013;13(4):227–42.
  • Rudd CE, Taylor A, Schneider H. CD28 and CTLA-4 coreceptor expression and signal transduction. Immunol Rev. 2009;229(1):12–26.
  • Martinez-Lostao L, Anel A, Pardo J. How do cytotoxic lymphocytes kill cancer cells? Clin Cancer Res. 2015;21(22):5047–56.
  • Luo X, Miller SD, Shea LD. Immune tolerance for autoimmune disease and cell transplantation. Annu Rev Biomed Eng. 2016;18:181–205.
  • Walunas TL, Lenschow DJ, Bakker CY, Linsley PS, Freeman GJ, Green JM, et al. CTLA-4 can function as a negative regulator of T-cell activation. Immunity 1994;1(5):405–13.
  • Leach DR, Krummel MF, Allison JP. Enhancement of antitumor immunity by CTLA-4 blockade. Science. 1996;271(5256):1734–6.
  • Linsley PS, Greene JL, Brady W, Bajorath J, Ledbetter JA, Peach R. Human B7-1 (CD80) and B7-2 (CD86) bind with similar avidities but distinct kinetics to CD28 and CTLA-4 receptors. Immunity. 1994;1(9):793–801.
  • Zou W, Chen L. Inhibitory B7-family molecules in the tumour microenvironment. Nat Rev Immunol. 2008;8(6):467–77.
  • Qureshi OS, Zheng Y, Nakamura K, Attridge K, Manzotti C, Schmidt EM, et al. Trans-endocytosis of CD80 and CD86: a molecular basis for the cell-extrinsic function of CTLA-4. Science. 2011;332(6029):600–3.
  • Wing K, Onishi Y, Prieto-Martin P, Yamaguchi T, Miyara M, Fehervari Z, et al. CTLA-4 control over Foxp3+ regulatory T cell function. Science. 2008;322(5899):271–5.
  • Tivol EA, Borriello F, Schweitzer AN, Lynch WP, Bluestone JA, Sharpe AH. Loss of CTLA-4 leads to massive lymphoproliferation and fatal multiorgan tissue destruction, revealing a critical negative regulatory role of CTLA-4. Immunity. 1995;3(5):541–7.
  • Waterhouse P, Penninger JM, Timms E, Wakeham A, Shahinian A, Lee KP, et al. Lymphoproliferative disorders with early lethality in mice deficient in Ctla-4. Science. 1995;270(5238):985–8.
  • Dong H, Strome SE, Salomao DR, Tamura H, Hirano F, Flies DB, et al. Tumor-associated B7-H1 promotes T-cell apoptosis: a potential mechanism of immune evasion. Nat Med. 2002;8(8):793–800.
  • Boussiotis VA. Molecular and biochemical aspects of the PD-1 checkpoint pathway. N Engl J Med. 2016;375(18):1767–78.
  • Keir ME, Butte MJ, Freeman GJ, Sharpe AH. PD-1 and its ligands in tolerance and immunity. Annu Rev Immunol. 2008; 26:677–704.
  • Nishimura H, Nose M, Hiai H, Minato N, Honjo T. Development of lupus-like autoimmune diseases by disruption of the PD-1 gene encoding an ITIM motif-carrying immunoreceptor. Immunity. 1999;11(2):141–51.
  • Nishimura H, Okazaki T, Tanaka Y, Nakatani K, Hara M, Matsumori A, et al. Autoimmune dilated cardiomyopathy in PD-1 receptor-deficient mice. Science. 2001;291(5502):319–22.
  • Baumeister SH, Freeman GJ, Dranoff G, Sharpe AH. Coinhibitory pathways in immunotherapy for cancer. Annu Rev Immunol. 2016;34:539–73.
  • Ribas A. Adaptive immune resistance: how cancer protects from immune attack. Cancer Discov. 2015;5(9):915.
  • Hodi FS, Mihm MC, Soiffer RJ, Haluska FG, Butler M, Seiden MV, et al. Biologic activity of cytotoxic T lymphocyte-associated antigen 4 antibody blockade in previously vaccinated metastatic melanoma and ovarian carcinoma patients. Proc Natl Acad Sci U S A. 2003;100(8):4712–7.
  • Phan GQ, Yang JC, Sherry RM, Hwu P, Topalian SL, Schwartzentruber DJ, et al. Cancer regression and autoimmunity induced by cytotoxic T lymphocyte-associated antigen 4 blockade in patients with metastatic melanoma. Proc Natl Acad Sci USA. 2003;100(14):8372–7.
  • Ribas A. Clinical development of the anti-CTLA-4 antibody tremelimumab. Semin Oncol. 2010;37(5):450–4.
  • Peggs KS, Quezada SA, Chambers CA, Korman AJ, Allison JP. Blockade of CTLA-4 on both effector and regulatory T cell compartments contributes to the antitumor activity of anti-CTLA-4 antibodies. J Exp Med. 2009;206(8):1717–25.
  • Kremer JM, Westhovens R, Leon M, Di Giorgio E, Alten R, Steinfeld S, et al. Treatment of rheumatoid arthritis by selective inhibition of T-cell activation with fusion protein CTLA4Ig. N Engl J Med. 2003;349(20):1907–15.
  • Harigai M, Ishiguro N, Inokuma S, Mimori T, Ryu J, Takei S, et al. Postmarketing surveillance of the safety and effectiveness of abatacept in Japanese patients with rheumatoid arthritis. Mod Rheumatol. 2016;26(4):491–8.
  • Golstein P, Griffiths GM. An early history of T cell-mediated cytotoxicity. Nat Rev Immunol. 2018;18(8):527–35.
  • Ahmadzadeh M, Johnson LA, Heemskerk B, Wunderlich JR, Dudley ME, White DE, et al. Tumor antigen-specific CD8 T cells infiltrating the tumor express high levels of PD-1 and are functionally impaired. Blood. 2009;114(8):1537–44.
  • Zou W. Regulatory T cells, tumour immunity and immunotherapy. Nat Rev Immunol. 2006;6(4):295–307.
  • Shah NJ, Kelly WJ, Liu SV, Choquette K, Spira A. Product review on the Anti-PD-L1 antibody atezolizumab. Hum Vaccin Immunother. 2018;14(2):269–76.
  • Sun C, Mezzadra R, Schumacher TN. Regulation and function of the PD-L1 checkpoint. Immunity. 2018;48(3):434–52.
  • Postow MA, Callahan MK, Wolchok JD. Immune checkpoint blockade in cancer therapy. J Clin Oncol. 2015;33(17):1974–82.
  • Wolchok JD, Kluger H, Callahan MK, Postow MA, Rizvi NA, Lesokhin AM, et al. Nivolumab plus ipilimumab in advanced melanoma. N Engl J Med. 2013;369(2):122–33.
  • Larkin J, Chiarion-Sileni V, Gonzalez R, Grob JJ, Cowey CL, Lao CD, et al. Combined nivolumab and ipilimumab or monotherapy in untreated melanoma. N Engl J Med. 2015;373(1):23–34.
  • Friedman CF, Proverbs-Singh TA, Postow MA. Treatment of the immune-related adverse effects of immune checkpoint inhibitors: a review. JAMA Oncol. 2016;2(10):1346–53.
  • Wu Y, Shi H, Jiang M, Qiu M, Jia K, Cao T, et al. The clinical value of combination of immune checkpoint inhibitors in cancer patients: a meta-analysis of efficacy and safety. Int J Cancer. 2017;141(12):2562–70.
  • Zhang B, Wu Q, Zhou YL, Guo X, Ge J, Fu J. Immune-related adverse events from combination immunotherapy in cancer patients: a comprehensive meta-analysis of randomized controlled trials. Int Immunopharmacol. 2018; 63:292–8.
  • Ohnuma K, Dang NH, Morimoto C. Revisiting an old acquaintance: CD26 and its molecular mechanisms in T cell function. Trends Immunol. 2008;29(6):295–301.
  • Cappelli LC, Brahmer JR, Forde PM, Le DT, Lipson EJ, Naidoo J, et al. Clinical presentation of immune checkpoint inhibitor-induced inflammatory arthritis differs by immunotherapy regimen. Semin Arthritis Rheum. 2018. [Epub ahead of print] DOI: 10.1016/j.semarthrit.2018.02.011.
  • Cappelli LC, Gutierrez AK, Bingham CO, 3rd, Shah AA. Rheumatic and musculoskeletal immune-related adverse events due to immune checkpoint inhibitors: a systematic review of the literature. Arthritis Care Res. 2017;69(11):1751–63.
  • Naidoo J, Cappelli LC, Forde PM, Marrone KA, Lipson EJ, Hammers HJ, et al. Inflammatory arthritis: a newly recognized adverse event of immune checkpoint blockade. Oncologist. 2017;22(6):627–30.
  • Kostine M, Rouxel L, Barnetche T, Veillon R, Martin F, Dutriaux C, et al. Rheumatic disorders associated with immune checkpoint inhibitors in patients with cancer-clinical aspects and relationship with tumour response: a single-centre prospective cohort study. Ann Rheum Dis. 2018;77(3):393–8.
  • Lidar M, Giat E, Garelick D, Horowitz Y, Amital H, Steinberg-Silman Y, et al. Rheumatic manifestations among cancer patients treated with immune checkpoint inhibitors. Autoimmun Rev. 2018;17(3):284–9.
  • Cappelli LC, Naidoo J, Bingham CO, 3rd, Shah AA. Inflammatory arthritis due to immune checkpoint inhibitors: challenges in diagnosis and treatment. Immunotherapy. 2017;9(1):5–8.
  • Abdel-Rahman O, ElHalawani H, Fouad M. Risk of endocrine complications in cancer patients treated with immune check point inhibitors: a meta-analysis. Future Oncol. 2016;12(3):413–25.
  • Chan MM, Kefford RF, Carlino M, Clements A, Manolios N. Arthritis and tenosynovitis associated with the anti-PD1 antibody pembrolizumab in metastatic melanoma. J Immunother. 2015;38(1):37–9.
  • Albayda J, Bingham CO, 3rd, Shah AA, Kelly RJ, Cappelli L. Metastatic joint involvement or inflammatory arthritis? A conundrum with immune checkpoint inhibitor-related adverse events. Rheumatology (Oxford). 2018;57(4):760–2.
  • Cappelli LC, Gutierrez AK, Baer AN, Albayda J, Manno RL, Haque U, et al. Inflammatory arthritis and sicca syndrome induced by nivolumab and ipilimumab. Ann Rheum Dis. 2017;76(1):43–50.
  • Liewluck T, Kao JC, Mauermann ML. PD-1 inhibitor-associated myopathies: emerging immune-mediated myopathies. J Immunother. 2018;41(4):208–11.
  • Sheik Ali S, Goddard AL, Luke JJ, Donahue H, Todd DJ, Werchniak A, et al. Drug-associated dermatomyositis following ipilimumab therapy: a novel immune-mediated adverse event associated with cytotoxic T-lymphocyte antigen 4 blockade. JAMA Dermatol. 2015;151(2):195.
  • Gallay L, Bourgeois-Vionnet J, Joubert B, Streichenberger N, Hot A. Muscular disorder related to immune checkpoint inhibitors: forewarned is forearmed. Neuro Oncol. 2018;20(6):861–2.
  • Daoussis D, Kraniotis P, Liossis SN, Solomou A. Immune checkpoint inhibitor-induced myo-fasciitis. Rheumatology (Oxford). 2017;56(12):2161.
  • Narváez J, Juarez-Lopez P, Lluch J, Narváez JA, Palmero R, Garcia Del Muro X, et al. Rheumatic immune-related adverse events in patients on anti-PD-1 inhibitors: fasciitis with myositis syndrome as a new complication of immunotherapy. Autoimmun Rev. 2018;17(10):1040–5.
  • Le Burel S, Champiat S, Mateus C, Marabelle A, Michot JM, Robert C, et al. Prevalence of immune-related systemic adverse events in patients treated with anti-Programmed cell Death 1/anti-Programmed cell Death-Ligand 1 agents: A single-centre pharmacovigilance database analysis. Eur J Cancer. 2017; 82:34–44.
  • Ipilimumab FDA, label. 2015. https://www.accessdata.fda.gov/drugsatfda_docs/label/2015/125377s073lbl.pdf.
  • Watanabe R, Zhang H, Berry G, Goronzy JJ, Weyand CM. Immune checkpoint dysfunction in large and medium vessel vasculitis. Am J Physiol Heart Circ Physiol. 2017;312(5):H1052–H9.
  • Goldstein BL, Gedmintas L, Todd DJ. Drug-associated polymyalgia rheumatica/giant cell arteritis occurring in two patients after treatment with ipilimumab, an antagonist of CTLA-4. Arthritis Rheumatol. 2014;66(3):768–9.
  • Minor DR, Bunker SR, Doyle J. Lymphocytic vasculitis of the uterus in a patient with melanoma receiving ipilimumab. J Clin Oncol. 2013;31(20):e356
  • Padda A, Schiopu E, Sovich J, Ma V, Alva A, Fecher L. Ipilimumab induced digital vasculitis. J Immunother Cancer. 2018;6(1):12
  • Fadel F, El Karoui K, Knebelmann B. Anti-CTLA4 antibody-induced lupus nephritis. N Engl J Med. 2009;361(2):211
  • Gaughan EM. Sarcoidosis, malignancy and immune checkpoint blockade. Immunotherapy. 2017;9(13):1051–3.
  • Cornejo CM, Haun P, English J, 3rd, Rosenbach M. Immune checkpoint inhibitors and the development of granulomatous reactions. J Am Acad Dermatol. 2018. [Epub ahead of print] DOI: 10.1016/j.jaad.2018.07.051.
  • Sibaud V. Dermatologic reactions to immune checkpoint inhibitors: skin toxicities and immunotherapy. Am J Clin Dermatol. 2018;19(3):345–61.
  • Minkis K, Garden BC, Wu S, Pulitzer MP, Lacouture ME. The risk of rash associated with ipilimumab in patients with cancer: a systematic review of the literature and meta-analysis. J Am Acad Dermatol. 2013;69(3):e121–8.
  • Robert C, Long GV, Brady B, Dutriaux C, Maio M, Mortier L, et al. Nivolumab in previously untreated melanoma without BRAF mutation. N Engl J Med. 2015;372(4):320–30.
  • Robert C, Schachter J, Long GV, Arance A, Grob JJ, Mortier L, et al. Pembrolizumab versus ipilimumab in advanced melanoma. N Engl J Med. 2015;372(26):2521–32.
  • Naidoo J, Page DB, Li BT, Connell LC, Schindler K, Lacouture ME, et al. Toxicities of the anti-PD-1 and anti-PD-L1 immune checkpoint antibodies. Ann Oncol. 2016;27(7):1362.
  • Belum VR, Benhuri B, Postow MA, Hellmann MD, Lesokhin AM, Segal NH, et al. Characterisation and management of dermatologic adverse events to agents targeting the PD-1 receptor. Eur J Cancer. 2016; 60:12–25.
  • Wang DY, Ye F, Zhao S, Johnson DB. Incidence of immune checkpoint inhibitor-related colitis in solid tumor patients: A systematic review and meta-analysis. Oncoimmunology. 2017;6(10):e1344805.
  • Palmieri DJ, Carlino MS. Immune checkpoint inhibitor toxicity. Curr Oncol Rep. 2018;20(9):72
  • Bertrand A, Kostine M, Barnetche T, Truchetet ME, Schaeverbeke T. Immune related adverse events associated with anti-CTLA-4 antibodies: systematic review and meta-analysis. BMC Med. 2015;13:211.
  • Tandon P, Bourassa-Blanchette S, Bishay K, Parlow S, Laurie SA, McCurdy JD. The risk of diarrhea and colitis in patients with advanced melanoma undergoing immune checkpoint inhibitor therapy: a systematic review and meta-analysis. J Immunother. 2018;41(3):101–8.
  • Adler BL, Pezhouh MK, Kim A, Luan L, Zhu Q, Gani F, et al. Histopathological and immunophenotypic features of ipilimumab-associated colitis compared to ulcerative colitis. J Intern Med. 2018;283(6):568–77.
  • Konda B, Nabhan F, Shah MH. Endocrine dysfunction following immune checkpoint inhibitor therapy. Curr Opin Endocrinol Diabetes Obes. 2017;24(5):337–47.
  • Barroso-Sousa R, Ott PA, Hodi FS, Kaiser UB, Tolaney SM, Min L. Endocrine dysfunction induced by immune checkpoint inhibitors: practical recommendations for diagnosis and clinical management. Cancer. 2018;124(6):1111–21.
  • Morganstein DL, Lai Z, Spain L, Diem S, Levine D, Mace C, et al. Thyroid abnormalities following the use of cytotoxic T-lymphocyte antigen-4 and programmed death receptor protein-1 inhibitors in the treatment of melanoma. Clin Endocrinol (Oxf). 2017;86(4):614–20.
  • Joshi MN, Whitelaw BC, Palomar MT, Wu Y, Carroll PV. Immune checkpoint inhibitor-related hypophysitis and endocrine dysfunction: clinical review. Clin Endocrinol (Oxf). 2016;85(3):331–9.
  • Eggermont AM, Chiarion-Sileni V, Grob JJ, Dummer R, Wolchok JD, Schmidt H, et al. Prolonged survival in stage III melanoma with ipilimumab adjuvant therapy. N Engl J Med. 2016;375(19):1845–55.
  • Fellner A, Makranz C, Lotem M, Bokstein F, Taliansky A, Rosenberg S, et al. Neurologic complications of immune checkpoint inhibitors. J Neurooncol. 2018;137(3):601–9.
  • Tabchi S, Messier C, Blais N. Immune-mediated respiratory adverse events of checkpoint inhibitors. Curr Opin Oncol. 2016;28(4):269–77.
  • Naidoo J, Wang X, Woo KM, Iyriboz T, Halpenny D, Cunningham J, et al. Pneumonitis in patients treated with anti-programmed death-1/programmed death ligand 1 therapy. J Clin Oncol. 2017;35(7):709–17.
  • Sanjeevaiah A, Kerr T, Beg MS. Approach and management of checkpoint inhibitor-related immune hepatitis. J Gastrointest Oncol. 2018;9(1):220–4.
  • Karamchandani DM, Chetty R. Immune checkpoint inhibitor-induced gastrointestinal and hepatic injury: pathologists’ perspective. J Clin Pathol. 2018;71(8):665–71.
  • Ganatra S, Neilan TG. Immune checkpoint inhibitor‐associated myocarditis. The Oncologist. 2018;23(8):879–86.
  • Moslehi JJ, Salem JE, Sosman JA, Lebrun-Vignes B, Johnson DB. Increased reporting of fatal immune checkpoint inhibitor-associated myocarditis. Lancet. 2018;391(10124):933.
  • Johnson DB, Balko JM, Compton ML, Chalkias S, Gorham J, Xu Y, et al. Fulminant myocarditis with combination immune checkpoint blockade. N Engl J Med. 2016;375(18):1749–55.
  • Puzanov I, Diab A, Abdallah K, Bingham CO, 3rd, Brogdon C, Dadu R, et al. Managing toxicities associated with immune checkpoint inhibitors: consensus recommendations from the Society for Immunotherapy of Cancer (SITC) Toxicity Management Working Group. J Immunother Cancer. 2017;5:95.
  • Wanchoo R, Karam S, Uppal NN, Barta VS, Deray G, Devoe C, et al. Adverse renal effects of immune checkpoint inhibitors: a narrative review. Am J Nephrol. 2017;45(2):160–9.
  • Antoun J, Titah C, Cochereau I. Ocular and orbital side-effects of checkpoint inhibitors: a review article. Curr Opin Oncol. 2016;28(4):288–94.
  • Cortazar FB, Marrone KA, Troxell ML, Ralto KM, Hoenig MP, Brahmer JR, et al. Clinicopathological features of acute kidney injury associated with immune checkpoint inhibitors. Kidney Int. 2016;90(3):638–47.
  • Johnson DB, Sullivan RJ, Ott PA, Carlino MS, Khushalani NI, Ye F, et al. Ipilimumab therapy in patients with advanced melanoma and preexisting autoimmune disorders. JAMA Oncol. 2016;2(2):234–40.
  • Gutzmer R, Koop A, Meier F, Hassel JC, Terheyden P, Zimmer L, et al. Programmed cell death protein-1 (PD-1) inhibitor therapy in patients with advanced melanoma and preexisting autoimmunity or ipilimumab-triggered autoimmunity. Eur J Cancer. 2017;75:24–32.
  • Menzies AM, Johnson DB, Ramanujam S, Atkinson VG, Wong ANM, Park JJ, et al. Anti-PD-1 therapy in patients with advanced melanoma and preexisting autoimmune disorders or major toxicity with ipilimumab. Ann Oncol. 2017;28(2):368–76.
  • Richter MD, Pinkston O, Kottschade LA, Finnes HD, Markovic SN, Thanarajasingam U. Brief report: cancer immunotherapy in patients with preexisting rheumatic disease: the Mayo Clinic experience. Arthritis Rheumatol. 2018;70(3):356–60.
  • Haanen J, Carbonnel F, Robert C, Kerr KM, Peters S, Larkin J, et al. Management of toxicities from immunotherapy: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2017;28(suppl_4):iv119–iv42.
  • U.S. Departments of Health and Human Services. National Institutes of Health. National Cancer Institutes. Common Terminology Criteria for Adverse Events (CTCAE), 4.03. Bethesda, MD: National Institutes of Health; 2010. [Available from: https://evs.nci.nih.gov/ftp1/CTCAE/CTCAE_4.03].
  • Mercer LK, Askling J, Raaschou P, Dixon WG, Dreyer L, Hetland ML, et al. Risk of invasive melanoma in patients with rheumatoid arthritis treated with biologics: results from a collaborative project of 11 European biologic registers. Ann Rheum Dis. 2017;76(2):386–91.
  • Mercer LK, Galloway JB, Lunt M, Davies R, Low AL, Dixon WG, et al. Risk of lymphoma in patients exposed to antitumour necrosis factor therapy: results from the British Society for Rheumatology Biologics Register for Rheumatoid Arthritis. Ann Rheum Dis. 2017;76(3):497–503.
  • Cappelli LC, Shah AA, Bingham CO, 3rd. Immune-related adverse effects of cancer immunotherapy- implications for rheumatology. Rheum. Dis Clin North Am. 2017;43(1):65–78.
  • Pollack MH, Betof A, Dearden H, Rapazzo K, Valentine I, Brohl AS, et al. Safety of resuming anti-PD-1 in patients with immune-related adverse events (irAEs) during combined anti-CTLA-4 and anti-PD1 in metastatic melanoma. Ann Oncol. 2018;29(1):250–5.
  • Woodworth T, Furst DE, Alten R, Bingham CO, 3rd, Yocum D, Sloan V, et al. Standardizing assessment and reporting of adverse effects in rheumatology clinical trials II: the Rheumatology Common Toxicity Criteria v.2.0. J Rheumatol. 2007;34:1401–14.

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