Skip to main content
Top
Published in: Journal of Clinical Immunology 2/2013

01-02-2013 | Original Research

Rituximab-Treated Patients Have a Poor Response to Influenza Vaccination

Authors: Robert A. Eisenberg, Abbas F. Jawad, Jean Boyer, Kelly Maurer, Kenyetta McDonald, Eline T. Luning Prak, Kathleen E Sullivan

Published in: Journal of Clinical Immunology | Issue 2/2013

Login to get access

Abstract

The efficacy of influenza vaccination in patients treated with rituximab is a clinically important question. Rheumatology clinics are populated with patients receiving rituximab for a broad array of disorders. Although several studies have explored the efficacy of other vaccines in rituximab-treated populations, results have been conflicting. We wished to define influenza vaccine efficacy in a rituximab-treated cohort. We examined 17 evaluable subjects treated with rituximab for rheumatologic conditions. T cell subsets, B cells subsets, T cell function, and B cell function were evaluated at specific time points along with hemagglutinination inhibition titers after receiving the standard inactivated influenza vaccine. T cell subset counts were significantly different than controls but did not change with rituximab. B cells depleted in all patients but were in various stages of recovery at the time of vaccination. Influenza vaccine responsiveness was poor overall, with only 16 % of subjects having a four-fold increase in titer. Pre-existing titers were retained throughout the study, however. The ability to respond to the influenza vaccine appeared to be related to the degree of B cell recovery at the time of vaccination. This study emphasizes that antibody responses to vaccine are impaired in subjects treated with rituximab and supports the concept that B cell recovery influences influenza vaccine responsiveness.
Literature
1.
go back to reference Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, Fukuda K. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA. 2003;289(2):179–86.PubMedCrossRef Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, Fukuda K. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA. 2003;289(2):179–86.PubMedCrossRef
2.
go back to reference Thompson WW, Shay DK, Weintraub E, Brammer L, Bridges CB, Cox NJ, Fukuda K. Influenza-associated hospitalizations in the United States. JAMA. 2004;292(11):1333–40.PubMedCrossRef Thompson WW, Shay DK, Weintraub E, Brammer L, Bridges CB, Cox NJ, Fukuda K. Influenza-associated hospitalizations in the United States. JAMA. 2004;292(11):1333–40.PubMedCrossRef
4.
go back to reference Neuzil KM, Mellen BG, Wright PF, Mitchel Jr EF, Griffin MR. The effect of influenza on hospitalizations, outpatient visits, and courses of antibiotics in children. N Engl J Med. 2000;342(4):225–31.PubMedCrossRef Neuzil KM, Mellen BG, Wright PF, Mitchel Jr EF, Griffin MR. The effect of influenza on hospitalizations, outpatient visits, and courses of antibiotics in children. N Engl J Med. 2000;342(4):225–31.PubMedCrossRef
5.
go back to reference Neuzil KM, Reed GW, Mitchel Jr EF, Griffin MR. Influenza-associated morbidity and mortality in young and middle-aged women. JAMA. 1999;281(10):901–7.PubMedCrossRef Neuzil KM, Reed GW, Mitchel Jr EF, Griffin MR. Influenza-associated morbidity and mortality in young and middle-aged women. JAMA. 1999;281(10):901–7.PubMedCrossRef
6.
go back to reference Neuzil KM, Coffey CS, Mitchel Jr EF, Griffin MR. Cardiopulmonary hospitalizations during influenza season in adults and adolescents with advanced HIV infection. J Acquir Immune Defic Syndr. 2003;34(3):304–7.PubMedCrossRef Neuzil KM, Coffey CS, Mitchel Jr EF, Griffin MR. Cardiopulmonary hospitalizations during influenza season in adults and adolescents with advanced HIV infection. J Acquir Immune Defic Syndr. 2003;34(3):304–7.PubMedCrossRef
7.
go back to reference Dushoff J, Plotkin JB, Viboud C, Earn DJ, Simonsen L. Mortality due to influenza in the United States–an annualized regression approach using multiple-cause mortality data. Am J Epidemiol. 2006;163(2):181–7. doi:10.1093/aje/kwj024.PubMedCrossRef Dushoff J, Plotkin JB, Viboud C, Earn DJ, Simonsen L. Mortality due to influenza in the United States–an annualized regression approach using multiple-cause mortality data. Am J Epidemiol. 2006;163(2):181–7. doi:10.​1093/​aje/​kwj024.PubMedCrossRef
9.
go back to reference Jain S, Kamimoto L, Bramley AM, Schmitz AM, Benoit SR, Louie J, Sugerman DE, Druckenmiller JK, Ritger KA, Chugh R, Jasuja S, Deutscher M, Chen S, Walker JD, Duchin JS, Lett S, Soliva S, Wells EV, Swerdlow D, Uyeki TM, Fiore AE, Olsen SJ, Fry AM, Bridges CB, Finelli L. Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N Engl J Med. 2009;361(20):1935–44. doi:10.1056/NEJMoa0906695.PubMedCrossRef Jain S, Kamimoto L, Bramley AM, Schmitz AM, Benoit SR, Louie J, Sugerman DE, Druckenmiller JK, Ritger KA, Chugh R, Jasuja S, Deutscher M, Chen S, Walker JD, Duchin JS, Lett S, Soliva S, Wells EV, Swerdlow D, Uyeki TM, Fiore AE, Olsen SJ, Fry AM, Bridges CB, Finelli L. Hospitalized patients with 2009 H1N1 influenza in the United States, April-June 2009. N Engl J Med. 2009;361(20):1935–44. doi:10.​1056/​NEJMoa0906695.PubMedCrossRef
10.
go back to reference Kim YJ, Boeckh M, Englund JA. Community respiratory virus infections in immunocompromised patients: hematopoietic stem cell and solid organ transplant recipients, and individuals with human immunodeficiency virus infection. Semin Respir Crit Care Med. 2007;28(2):222–42. doi:10.1055/s-2007-976494.PubMedCrossRef Kim YJ, Boeckh M, Englund JA. Community respiratory virus infections in immunocompromised patients: hematopoietic stem cell and solid organ transplant recipients, and individuals with human immunodeficiency virus infection. Semin Respir Crit Care Med. 2007;28(2):222–42. doi:10.​1055/​s-2007-976494.PubMedCrossRef
12.
go back to reference Malhotra A, Krilov LR. Influenza and respiratory syncytial virus. Update on infection, management, and prevention. Pediatric Clinics of North America. 2000;47(2):353–72.PubMedCrossRef Malhotra A, Krilov LR. Influenza and respiratory syncytial virus. Update on infection, management, and prevention. Pediatric Clinics of North America. 2000;47(2):353–72.PubMedCrossRef
13.
go back to reference Fiore AE, Uyeki TM, Broder K, Finelli L, Euler GL, Singleton JA, Iskander JK, Wortley PM, Shay DK, Bresee JS, Cox NJ. Prevention and control of influenza with vaccines: Recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010. MMWR Recomm Rep. 2010;59(RR-8):1–62.PubMed Fiore AE, Uyeki TM, Broder K, Finelli L, Euler GL, Singleton JA, Iskander JK, Wortley PM, Shay DK, Bresee JS, Cox NJ. Prevention and control of influenza with vaccines: Recommendations of the Advisory Committee on Immunization Practices (ACIP), 2010. MMWR Recomm Rep. 2010;59(RR-8):1–62.PubMed
14.
go back to reference Keitel WA, Couch RB, Cate TR, Hess KR, Baxter B, Quarles JM, Atmar RL, Six HR. High doses of purified influenza A virus hemagglutinin significantly augment serum and nasal secretion antibody responses in healthy young adults. J Clin Microbiol. 1994;32(10):2468–73.PubMed Keitel WA, Couch RB, Cate TR, Hess KR, Baxter B, Quarles JM, Atmar RL, Six HR. High doses of purified influenza A virus hemagglutinin significantly augment serum and nasal secretion antibody responses in healthy young adults. J Clin Microbiol. 1994;32(10):2468–73.PubMed
15.
go back to reference de Jong JC, Palache AM, Beyer WE, Rimmelzwaan GF, Boon AC, Osterhaus AD. Haemagglutination-inhibiting antibody to influenza virus. Dev Biol (Basel). 2003;115:63–73. de Jong JC, Palache AM, Beyer WE, Rimmelzwaan GF, Boon AC, Osterhaus AD. Haemagglutination-inhibiting antibody to influenza virus. Dev Biol (Basel). 2003;115:63–73.
16.
go back to reference Bachi T, Gerhard W, Yewdell JW. Monoclonal antibodies detect different forms of influenza virus hemagglutinin during viral penetration and biosynthesis. Journal of Virology. 1985;55(2):307–13.PubMed Bachi T, Gerhard W, Yewdell JW. Monoclonal antibodies detect different forms of influenza virus hemagglutinin during viral penetration and biosynthesis. Journal of Virology. 1985;55(2):307–13.PubMed
17.
go back to reference Beyer WE, Palache AM, Luchters G, Nauta J, Osterhaus AD. Seroprotection rate, mean fold increase, seroconversion rate: which parameter adequately expresses seroresponse to influenza vaccination? Virus Research. 2004;103(1–2):125–32.PubMedCrossRef Beyer WE, Palache AM, Luchters G, Nauta J, Osterhaus AD. Seroprotection rate, mean fold increase, seroconversion rate: which parameter adequately expresses seroresponse to influenza vaccination? Virus Research. 2004;103(1–2):125–32.PubMedCrossRef
18.
19.
20.
go back to reference Gross PA, Hermogenes AW, Sacks HS, Lau J, Levandowski RA. The efficacy of influenza vaccine in elderly persons. A meta-analysis and review of the literature. Ann Intern Med. 1995;123(7):518–27.PubMed Gross PA, Hermogenes AW, Sacks HS, Lau J, Levandowski RA. The efficacy of influenza vaccine in elderly persons. A meta-analysis and review of the literature. Ann Intern Med. 1995;123(7):518–27.PubMed
21.
go back to reference Govaert TM, Thijs CT, Masurel N, Sprenger MJ, Dinant GJ, Knottnerus JA. The efficacy of influenza vaccination in elderly individuals. A randomized double-blind placebo-controlled trial. JAMA. 1994;272(21):1661–5.PubMedCrossRef Govaert TM, Thijs CT, Masurel N, Sprenger MJ, Dinant GJ, Knottnerus JA. The efficacy of influenza vaccination in elderly individuals. A randomized double-blind placebo-controlled trial. JAMA. 1994;272(21):1661–5.PubMedCrossRef
22.
go back to reference Nichol KL. The efficacy, effectiveness and cost-effectiveness of inactivated influenza virus vaccines. Vaccine. 2003;21(16):1769–75.PubMedCrossRef Nichol KL. The efficacy, effectiveness and cost-effectiveness of inactivated influenza virus vaccines. Vaccine. 2003;21(16):1769–75.PubMedCrossRef
24.
go back to reference Zangwill KM, Belshe RB. Safety and efficacy of trivalent inactivated influenza vaccine in young children: A summary for the new era of routine vaccination. Pediatr Infect Dis J. 2004;23(3):189–97.PubMedCrossRef Zangwill KM, Belshe RB. Safety and efficacy of trivalent inactivated influenza vaccine in young children: A summary for the new era of routine vaccination. Pediatr Infect Dis J. 2004;23(3):189–97.PubMedCrossRef
26.
go back to reference Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, Aydintug AO, Jedryka-Goral A, de Ramon E, Fernandez-Nebro A, Galeazzi M, Haga HJ, Mathieu A, Houssiau F, Ruiz-Irastorza G, Ingelmo M, Hughes GR. Morbidity and mortality in systemic lupus erythematosus during a 5-year period. A multicenter prospective study of 1,000 patients. European Working Party on Systemic Lupus Erythematosus. Medicine (Baltimore). 1999;78(3):167–75.CrossRef Cervera R, Khamashta MA, Font J, Sebastiani GD, Gil A, Lavilla P, Aydintug AO, Jedryka-Goral A, de Ramon E, Fernandez-Nebro A, Galeazzi M, Haga HJ, Mathieu A, Houssiau F, Ruiz-Irastorza G, Ingelmo M, Hughes GR. Morbidity and mortality in systemic lupus erythematosus during a 5-year period. A multicenter prospective study of 1,000 patients. European Working Party on Systemic Lupus Erythematosus. Medicine (Baltimore). 1999;78(3):167–75.CrossRef
27.
go back to reference Symmons DP. Mortality in rheumatoid arthritis. Br J Rheumatol. 1988;27 Suppl 1:44–54.PubMed Symmons DP. Mortality in rheumatoid arthritis. Br J Rheumatol. 1988;27 Suppl 1:44–54.PubMed
28.
go back to reference Phillip R, Luqmani R. Mortality in systemic vasculitis: A systematic review. Clin Exp Rheumatol. 2008;26(5 Suppl 51):S94–104.PubMed Phillip R, Luqmani R. Mortality in systemic vasculitis: A systematic review. Clin Exp Rheumatol. 2008;26(5 Suppl 51):S94–104.PubMed
29.
go back to reference Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: Systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA. 2006;295(19):2275–85. doi:10.1001/jama.295.19.2275.PubMedCrossRef Bongartz T, Sutton AJ, Sweeting MJ, Buchan I, Matteson EL, Montori V. Anti-TNF antibody therapy in rheumatoid arthritis and the risk of serious infections and malignancies: Systematic review and meta-analysis of rare harmful effects in randomized controlled trials. JAMA. 2006;295(19):2275–85. doi:10.​1001/​jama.​295.​19.​2275.PubMedCrossRef
30.
go back to reference Doran MF, Crowson CS, Pond GR, O’Fallon WM, Gabriel SE. Frequency of infection in patients with rheumatoid arthritis compared with controls: A population-based study. Arthritis Rheum. 2002;46(9):2287–93. doi:10.1002/art.10524.PubMedCrossRef Doran MF, Crowson CS, Pond GR, O’Fallon WM, Gabriel SE. Frequency of infection in patients with rheumatoid arthritis compared with controls: A population-based study. Arthritis Rheum. 2002;46(9):2287–93. doi:10.​1002/​art.​10524.PubMedCrossRef
31.
go back to reference Crowe SR, Merrill JT, Vista ES, Dedeke AB, Thompson DM, Stewart S, Guthridge JM, Niewold TB, Franek BS, Air GM, Thompson LF, James JA. Influenza vaccination responses in human systemic lupus erythematosus: Impact of clinical and demographic features. Arthritis Rheum. 2011;63(8):2396–406. doi:10.1002/art.30388.PubMedCrossRef Crowe SR, Merrill JT, Vista ES, Dedeke AB, Thompson DM, Stewart S, Guthridge JM, Niewold TB, Franek BS, Air GM, Thompson LF, James JA. Influenza vaccination responses in human systemic lupus erythematosus: Impact of clinical and demographic features. Arthritis Rheum. 2011;63(8):2396–406. doi:10.​1002/​art.​30388.PubMedCrossRef
32.
go back to reference Del Porto F, Lagana B, Biselli R, Donatelli I, Campitelli L, Nisini R, Cardelli P, Rossi F, D’Amelio R. Influenza vaccine administration in patients with systemic lupus erythematosus and rheumatoid arthritis. Safety and immunogenicity. Vaccine. 2006;24(16):3217–23. doi:10.1016/j.vaccine.2006.01.028.PubMedCrossRef Del Porto F, Lagana B, Biselli R, Donatelli I, Campitelli L, Nisini R, Cardelli P, Rossi F, D’Amelio R. Influenza vaccine administration in patients with systemic lupus erythematosus and rheumatoid arthritis. Safety and immunogenicity. Vaccine. 2006;24(16):3217–23. doi:10.​1016/​j.​vaccine.​2006.​01.​028.PubMedCrossRef
33.
go back to reference Gabay C, Bel M, Combescure C, Ribi C, Meier S, Posfay-Barbe K, Grillet S, Seebach JD, Kaiser L, Wunderli W, Guerne PA, Siegrist CA. Impact of synthetic and biologic disease-modifying antirheumatic drugs on antibody responses to the AS03-adjuvanted pandemic influenza vaccine: a prospective, open-label, parallel-cohort, single-center study. Arthritis Rheum. 2011;63(6):1486–96. doi:10.1002/art.30325.PubMedCrossRef Gabay C, Bel M, Combescure C, Ribi C, Meier S, Posfay-Barbe K, Grillet S, Seebach JD, Kaiser L, Wunderli W, Guerne PA, Siegrist CA. Impact of synthetic and biologic disease-modifying antirheumatic drugs on antibody responses to the AS03-adjuvanted pandemic influenza vaccine: a prospective, open-label, parallel-cohort, single-center study. Arthritis Rheum. 2011;63(6):1486–96. doi:10.​1002/​art.​30325.PubMedCrossRef
34.
go back to reference Elkayam O, Amir S, Mendelson E, Schwaber M, Grotto I, Wollman J, Arad U, Brill A, Paran D, Levartovsky D, Wigler I, Caspi D, Mandelboim M. Efficacy and safety of vaccination against pandemic 2009 influenza A (H1N1) virus among patients with rheumatic diseases. Arthritis Care Res (Hoboken). 2011;63(7):1062–7. doi:10.1002/acr.20465.CrossRef Elkayam O, Amir S, Mendelson E, Schwaber M, Grotto I, Wollman J, Arad U, Brill A, Paran D, Levartovsky D, Wigler I, Caspi D, Mandelboim M. Efficacy and safety of vaccination against pandemic 2009 influenza A (H1N1) virus among patients with rheumatic diseases. Arthritis Care Res (Hoboken). 2011;63(7):1062–7. doi:10.​1002/​acr.​20465.CrossRef
35.
go back to reference Fomin I, Caspi D, Levy V, Varsano N, Shalev Y, Paran D, Levartovsky D, Litinsky I, Kaufman I, Wigler I, Mendelson E, Elkayam O. Vaccination against influenza in rheumatoid arthritis: The effect of disease modifying drugs, including TNF alpha blockers. Ann Rheum Dis. 2006;65(2):191–4. doi:10.1136/ard.2005.036434.PubMedCrossRef Fomin I, Caspi D, Levy V, Varsano N, Shalev Y, Paran D, Levartovsky D, Litinsky I, Kaufman I, Wigler I, Mendelson E, Elkayam O. Vaccination against influenza in rheumatoid arthritis: The effect of disease modifying drugs, including TNF alpha blockers. Ann Rheum Dis. 2006;65(2):191–4. doi:10.​1136/​ard.​2005.​036434.PubMedCrossRef
36.
go back to reference Oren S, Mandelboim M, Braun-Moscovici Y, Paran D, Ablin J, Litinsky I, Comaneshter D, Levartovsky D, Mendelson E, Azar R, Wigler I, Balbir-Gurman A, Caspi D, Elkayam O. Vaccination against influenza in patients with rheumatoid arthritis: The effect of rituximab on the humoral response. Ann Rheum Dis. 2008;67(7):937–41. doi:10.1136/ard.2007.077461.PubMedCrossRef Oren S, Mandelboim M, Braun-Moscovici Y, Paran D, Ablin J, Litinsky I, Comaneshter D, Levartovsky D, Mendelson E, Azar R, Wigler I, Balbir-Gurman A, Caspi D, Elkayam O. Vaccination against influenza in patients with rheumatoid arthritis: The effect of rituximab on the humoral response. Ann Rheum Dis. 2008;67(7):937–41. doi:10.​1136/​ard.​2007.​077461.PubMedCrossRef
37.
go back to reference Arad U, Tzadok S, Amir S, Mandelboim M, Mendelson E, Wigler I, Sarbagil-Maman H, Paran D, Caspi D, Elkayam O. The cellular immune response to influenza vaccination is preserved in rheumatoid arthritis patients treated with rituximab. Vaccine. 2011;29(8):1643–8. doi:10.1016/j.vaccine.2010.12.072.PubMedCrossRef Arad U, Tzadok S, Amir S, Mandelboim M, Mendelson E, Wigler I, Sarbagil-Maman H, Paran D, Caspi D, Elkayam O. The cellular immune response to influenza vaccination is preserved in rheumatoid arthritis patients treated with rituximab. Vaccine. 2011;29(8):1643–8. doi:10.​1016/​j.​vaccine.​2010.​12.​072.PubMedCrossRef
38.
go back to reference van Assen S, Holvast A, Benne CA, Posthumus MD, van Leeuwen MA, Voskuyl AE, Blom M, Risselada AP, de Haan A, Westra J, Kallenberg CG, Bijl M. Humoral responses after influenza vaccination are severely reduced in patients with rheumatoid arthritis treated with rituximab. Arthritis Rheum. 2010;62(1):75–81. doi:10.1002/art.25033.PubMedCrossRef van Assen S, Holvast A, Benne CA, Posthumus MD, van Leeuwen MA, Voskuyl AE, Blom M, Risselada AP, de Haan A, Westra J, Kallenberg CG, Bijl M. Humoral responses after influenza vaccination are severely reduced in patients with rheumatoid arthritis treated with rituximab. Arthritis Rheum. 2010;62(1):75–81. doi:10.​1002/​art.​25033.PubMedCrossRef
39.
go back to reference Bingham 3rd CO, Looney RJ, Deodhar A, Halsey N, Greenwald M, Codding C, Trzaskoma B, Martin F, Agarwal S, Kelman A. Immunization responses in rheumatoid arthritis patients treated with rituximab: Results from a controlled clinical trial. Arthritis Rheum. 2010;62(1):64–74. doi:10.1002/art.25034.PubMedCrossRef Bingham 3rd CO, Looney RJ, Deodhar A, Halsey N, Greenwald M, Codding C, Trzaskoma B, Martin F, Agarwal S, Kelman A. Immunization responses in rheumatoid arthritis patients treated with rituximab: Results from a controlled clinical trial. Arthritis Rheum. 2010;62(1):64–74. doi:10.​1002/​art.​25034.PubMedCrossRef
40.
go back to reference Pescovitz MD, Torgerson TR, Ochs HD, Ocheltree E, McGee P, Krause-Steinrauf H, Lachin JM, Canniff J, Greenbaum C, Herold KC, Skyler JS, Weinberg A. Effect of rituximab on human in vivo antibody immune responses. J Allergy Clin Immunol. 2011. doi:10.1016/j.jaci.2011.08.008. Pescovitz MD, Torgerson TR, Ochs HD, Ocheltree E, McGee P, Krause-Steinrauf H, Lachin JM, Canniff J, Greenbaum C, Herold KC, Skyler JS, Weinberg A. Effect of rituximab on human in vivo antibody immune responses. J Allergy Clin Immunol. 2011. doi:10.​1016/​j.​jaci.​2011.​08.​008.
41.
go back to reference Yri OE, Torfoss D, Hungnes O, Tierens A, Waalen K, Nordoy T, Dudman S, Kilander A, Wader KF, Ostenstad B, Ekanger R, Meyer P, Kolstad A. Rituximab blocks protective serologic response to influenza A (H1N1) 2009 vaccination in lymphoma patients during or within 6 months after treatment. Blood. 2011;118(26):6769–71. doi:10.1182/blood-2011-08-372649.PubMedCrossRef Yri OE, Torfoss D, Hungnes O, Tierens A, Waalen K, Nordoy T, Dudman S, Kilander A, Wader KF, Ostenstad B, Ekanger R, Meyer P, Kolstad A. Rituximab blocks protective serologic response to influenza A (H1N1) 2009 vaccination in lymphoma patients during or within 6 months after treatment. Blood. 2011;118(26):6769–71. doi:10.​1182/​blood-2011-08-372649.PubMedCrossRef
42.
go back to reference Sutter JA, Kwan-Morley J, Dunham J, Du YZ, Kamoun M, Albert D, Eisenberg RA, Luning Prak ET. A longitudinal analysis of SLE patients treated with rituximab (anti-CD20): Factors associated with B lymphocyte recovery. Clin Immunol. 2008;126(3):282–90. doi:10.1016/j.clim.2007.11.012.PubMedCrossRef Sutter JA, Kwan-Morley J, Dunham J, Du YZ, Kamoun M, Albert D, Eisenberg RA, Luning Prak ET. A longitudinal analysis of SLE patients treated with rituximab (anti-CD20): Factors associated with B lymphocyte recovery. Clin Immunol. 2008;126(3):282–90. doi:10.​1016/​j.​clim.​2007.​11.​012.PubMedCrossRef
43.
go back to reference Bedognetti D, Zoppoli G, Massucco C, Zanardi E, Zupo S, Bruzzone A, Sertoli MR, Balleari E, Racchi O, Messina M, Caltabiano G, Icardi G, Durando P, Marincola FM, Boccardo F, Ferrarini M, Ansaldi F, De Maria A. Impaired response to influenza vaccine associated with persistent memory B cell depletion in non-Hodgkin’s lymphoma patients treated with rituximab-containing regimens. J Immunol. 2011;186(10):6044–55. doi:10.4049/jimmunol.1004095.PubMedCrossRef Bedognetti D, Zoppoli G, Massucco C, Zanardi E, Zupo S, Bruzzone A, Sertoli MR, Balleari E, Racchi O, Messina M, Caltabiano G, Icardi G, Durando P, Marincola FM, Boccardo F, Ferrarini M, Ansaldi F, De Maria A. Impaired response to influenza vaccine associated with persistent memory B cell depletion in non-Hodgkin’s lymphoma patients treated with rituximab-containing regimens. J Immunol. 2011;186(10):6044–55. doi:10.​4049/​jimmunol.​1004095.PubMedCrossRef
44.
go back to reference Horwitz SM, Negrin RS, Blume KG, Breslin S, Stuart MJ, Stockerl-Goldstein KE, Johnston LJ, Wong RM, Shizuru JA, Horning SJ. Rituximab as adjuvant to high-dose therapy and autologous hematopoietic cell transplantation for aggressive non-Hodgkin lymphoma. Blood. 2004;103(3):777–83. doi:10.1182/blood-2003-04-1257.PubMedCrossRef Horwitz SM, Negrin RS, Blume KG, Breslin S, Stuart MJ, Stockerl-Goldstein KE, Johnston LJ, Wong RM, Shizuru JA, Horning SJ. Rituximab as adjuvant to high-dose therapy and autologous hematopoietic cell transplantation for aggressive non-Hodgkin lymphoma. Blood. 2004;103(3):777–83. doi:10.​1182/​blood-2003-04-1257.PubMedCrossRef
45.
go back to reference Jawad AF, Prak EL, Boyer J, McDonald-McGinn DM, Zackai E, McDonald K, Sullivan KE. A Prospective Study of Influenza Vaccination and a Comparison of Immunologic Parameters in Children and Adults with Chromosome 22q11.2 Deletion Syndrome (DiGeorge Syndrome/Velocardiofacial Syndrome). Journal of clinical immunology. 2011;31(6):927–35. doi:10.1007/s10875-011-9569-8.PubMedCrossRef Jawad AF, Prak EL, Boyer J, McDonald-McGinn DM, Zackai E, McDonald K, Sullivan KE. A Prospective Study of Influenza Vaccination and a Comparison of Immunologic Parameters in Children and Adults with Chromosome 22q11.2 Deletion Syndrome (DiGeorge Syndrome/Velocardiofacial Syndrome). Journal of clinical immunology. 2011;31(6):927–35. doi:10.​1007/​s10875-011-9569-8.PubMedCrossRef
46.
go back to reference Levin MJ, Song LY, Fenton T, Nachman S, Patterson J, Walker R, Kemble G, Allende M, Hultquist M, Yi T, Nowak B, Weinberg A. Shedding of live vaccine virus, comparative safety, and influenza-specific antibody responses after administration of live attenuated and inactivated trivalent influenza vaccines to HIV-infected children. Vaccine. 2008;26(33):4210–7. doi:10.1016/j.vaccine.2008.05.054.PubMedCrossRef Levin MJ, Song LY, Fenton T, Nachman S, Patterson J, Walker R, Kemble G, Allende M, Hultquist M, Yi T, Nowak B, Weinberg A. Shedding of live vaccine virus, comparative safety, and influenza-specific antibody responses after administration of live attenuated and inactivated trivalent influenza vaccines to HIV-infected children. Vaccine. 2008;26(33):4210–7. doi:10.​1016/​j.​vaccine.​2008.​05.​054.PubMedCrossRef
47.
go back to reference Albert D, Dunham J, Khan S, Stansberry J, Kolasinski S, Tsai D, Pullman-Mooar S, Barnack F, Striebich C, Looney RJ, Prak ET, Kimberly R, Zhang Y, Eisenberg R. Variability in the biological response to anti-CD20 B cell depletion in systemic lupus erythaematosus. Annals of the rheumatic diseases. 2008;67(12):1724–31. doi:10.1136/ard.2007.083162.PubMedCrossRef Albert D, Dunham J, Khan S, Stansberry J, Kolasinski S, Tsai D, Pullman-Mooar S, Barnack F, Striebich C, Looney RJ, Prak ET, Kimberly R, Zhang Y, Eisenberg R. Variability in the biological response to anti-CD20 B cell depletion in systemic lupus erythaematosus. Annals of the rheumatic diseases. 2008;67(12):1724–31. doi:10.​1136/​ard.​2007.​083162.PubMedCrossRef
48.
go back to reference Stevenson PG, Hawke S, Bangham CR. Protection against lethal influenza virus encephalitis by intranasally primed CD8+ memory T cells. J Immunol. 1996;157(7):3065–73.PubMed Stevenson PG, Hawke S, Bangham CR. Protection against lethal influenza virus encephalitis by intranasally primed CD8+ memory T cells. J Immunol. 1996;157(7):3065–73.PubMed
49.
go back to reference Kreijtz JH, Bodewes R, van Amerongen G, Kuiken T, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine. 2007;25(4):612–20. doi:10.1016/j.vaccine.2006.08.036.PubMedCrossRef Kreijtz JH, Bodewes R, van Amerongen G, Kuiken T, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine. 2007;25(4):612–20. doi:10.​1016/​j.​vaccine.​2006.​08.​036.PubMedCrossRef
50.
go back to reference Benton KA, Misplon JA, Lo CY, Brutkiewicz RR, Prasad SA, Epstein SL. Heterosubtypic immunity to influenza A virus in mice lacking IgA, all Ig, NKT cells, or gamma delta T cells. J Immunol. 2001;166(12):7437–45.PubMed Benton KA, Misplon JA, Lo CY, Brutkiewicz RR, Prasad SA, Epstein SL. Heterosubtypic immunity to influenza A virus in mice lacking IgA, all Ig, NKT cells, or gamma delta T cells. J Immunol. 2001;166(12):7437–45.PubMed
51.
go back to reference Doherty PC, Topham DJ, Tripp RA, Cardin RD, Brooks JW, Stevenson PG. Effector CD4+ and CD8+ T-cell mechanisms in the control of respiratory virus infections. Immunol Rev. 1997;159:105–17.PubMedCrossRef Doherty PC, Topham DJ, Tripp RA, Cardin RD, Brooks JW, Stevenson PG. Effector CD4+ and CD8+ T-cell mechanisms in the control of respiratory virus infections. Immunol Rev. 1997;159:105–17.PubMedCrossRef
52.
go back to reference Powell TJ, Strutt T, Reome J, Hollenbaugh JA, Roberts AD, Woodland DL, Swain SL, Dutton RW. Priming with cold-adapted influenza A does not prevent infection but elicits long-lived protection against supralethal challenge with heterosubtypic virus. J Immunol. 2007;178(2):1030–8.PubMed Powell TJ, Strutt T, Reome J, Hollenbaugh JA, Roberts AD, Woodland DL, Swain SL, Dutton RW. Priming with cold-adapted influenza A does not prevent infection but elicits long-lived protection against supralethal challenge with heterosubtypic virus. J Immunol. 2007;178(2):1030–8.PubMed
54.
go back to reference Rangel-Moreno J, Carragher DM, Misra RS, Kusser K, Hartson L, Moquin A, Lund FE, Randall TD. B cells promote resistance to heterosubtypic strains of influenza via multiple mechanisms. J Immunol. 2008;180(1):454–63.PubMed Rangel-Moreno J, Carragher DM, Misra RS, Kusser K, Hartson L, Moquin A, Lund FE, Randall TD. B cells promote resistance to heterosubtypic strains of influenza via multiple mechanisms. J Immunol. 2008;180(1):454–63.PubMed
55.
go back to reference Virelizier JL. Host defenses against influenza virus: The role of anti-hemagglutinin antibody. J Immunol. 1975;115(2):434–9.PubMed Virelizier JL. Host defenses against influenza virus: The role of anti-hemagglutinin antibody. J Immunol. 1975;115(2):434–9.PubMed
56.
go back to reference Doherty PC, Gerhard W. Breakdown of the blood–cerebrospinal fluid barrier to immunoglobulin in mice injected intracerebrally with a neurotropic influenza A virus. Post-exposure treatment with monoclonal antibody promotes recovery. J Neuroimmunol. 1981;1(3):227–37.PubMedCrossRef Doherty PC, Gerhard W. Breakdown of the blood–cerebrospinal fluid barrier to immunoglobulin in mice injected intracerebrally with a neurotropic influenza A virus. Post-exposure treatment with monoclonal antibody promotes recovery. J Neuroimmunol. 1981;1(3):227–37.PubMedCrossRef
57.
go back to reference Kris RM, Yetter RA, Cogliano R, Ramphal R, Small PA. Passive serum antibody causes temporary recovery from influenza virus infection of the nose, trachea and lung of nude mice. Immunology. 1988;63(3):349–53.PubMed Kris RM, Yetter RA, Cogliano R, Ramphal R, Small PA. Passive serum antibody causes temporary recovery from influenza virus infection of the nose, trachea and lung of nude mice. Immunology. 1988;63(3):349–53.PubMed
58.
go back to reference Querec TD, Akondy RS, Lee EK, Cao W, Nakaya HI, Teuwen D, Pirani A, Gernert K, Deng J, Marzolf B, Kennedy K, Wu H, Bennouna S, Oluoch H, Miller J, Vencio RZ, Mulligan M, Aderem A, Ahmed R, Pulendran B. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat Immunol. 2009;10(1):116–25. doi:10.1038/ni.1688.PubMedCrossRef Querec TD, Akondy RS, Lee EK, Cao W, Nakaya HI, Teuwen D, Pirani A, Gernert K, Deng J, Marzolf B, Kennedy K, Wu H, Bennouna S, Oluoch H, Miller J, Vencio RZ, Mulligan M, Aderem A, Ahmed R, Pulendran B. Systems biology approach predicts immunogenicity of the yellow fever vaccine in humans. Nat Immunol. 2009;10(1):116–25. doi:10.​1038/​ni.​1688.PubMedCrossRef
59.
go back to reference Forrest BD, Pride MW, Dunning AJ, Capeding MR, Chotpitayasunondh T, Tam JS, Rappaport R, Eldridge JH, Gruber WC. Correlation of cellular immune responses with protection against culture-confirmed influenza virus in young children. Clinical and vaccine immunology: CVI. 2008;15(7):1042–53. doi:10.1128/CVI.00397-07.PubMedCrossRef Forrest BD, Pride MW, Dunning AJ, Capeding MR, Chotpitayasunondh T, Tam JS, Rappaport R, Eldridge JH, Gruber WC. Correlation of cellular immune responses with protection against culture-confirmed influenza virus in young children. Clinical and vaccine immunology: CVI. 2008;15(7):1042–53. doi:10.​1128/​CVI.​00397-07.PubMedCrossRef
60.
go back to reference McElhaney JE, Xie D, Hager WD, Barry MB, Wang Y, Kleppinger A, Ewen C, Kane KP, Bleackley RC. T cell responses are better correlates of vaccine protection in the elderly. J Immunol. 2006;176(10):6333–9.PubMed McElhaney JE, Xie D, Hager WD, Barry MB, Wang Y, Kleppinger A, Ewen C, Kane KP, Bleackley RC. T cell responses are better correlates of vaccine protection in the elderly. J Immunol. 2006;176(10):6333–9.PubMed
Metadata
Title
Rituximab-Treated Patients Have a Poor Response to Influenza Vaccination
Authors
Robert A. Eisenberg
Abbas F. Jawad
Jean Boyer
Kelly Maurer
Kenyetta McDonald
Eline T. Luning Prak
Kathleen E Sullivan
Publication date
01-02-2013
Publisher
Springer US
Published in
Journal of Clinical Immunology / Issue 2/2013
Print ISSN: 0271-9142
Electronic ISSN: 1573-2592
DOI
https://doi.org/10.1007/s10875-012-9813-x

Other articles of this Issue 2/2013

Journal of Clinical Immunology 2/2013 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.