Differential influenza H1N1-specific humoral and cellular response kinetics in kidney transplant patients

Medical Microbiology and Immunology

Volumn 203, Issue 1, 2014, Pages 35-45

  Rambal, Vinay ^a   Müller, Karin ^a   Dang Heine, Chantip ^a   Sattler, Arne ^a   Dziubianau, Mikalai ^a   Weist, Benjamin ^a   Luu, Si Hong ^a   Stoyanova, Alexandra ^a   Nickel, Peter ^a   Thiel, Andreas ^a   Neumann, Avidan ^a   Schweiger, Brunhilde ^b   Reinke, Petra ^a   Babel, Nina ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b ROBERT KOCH INSTITUTE   (Germany)

Author keywords

H1N1; Influenza; Renal transplant recipients; Vaccination

Indexed keywords

ADULT; AGED; ANTIBODIES, VIRAL; CASE-CONTROL STUDIES; FEMALE; HUMANS; IMMUNITY, CELLULAR; IMMUNITY, HUMORAL; IMMUNIZATION, SECONDARY; IMMUNOCOMPROMISED HOST; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA VACCINES; INFLUENZA, HUMAN; KIDNEY TRANSPLANTATION; LEUKOCYTES, MONONUCLEAR; MALE; MIDDLE AGED; T-CELL ANTIGEN RECEPTOR SPECIFICITY; T-LYMPHOCYTES; VACCINATION; YOUNG ADULT;

EID: 84894229268     PISSN: 03008584     EISSN: 14321831     Source Type: Journal    
DOI: 10.1007/s00430-013-0312-3     Document Type: Article

References (57)

1. Ljungman P, Andersson J, Aschan J, Barkholt L, Ehrnst A, Johansson M, Weiland O (1993) Influenza A in immunocompromised patients. Clin Infect Dis 17(2):244-247
2. Vilchez RA, McCurry K, Dauber J, Lacono A, Griffith B, Fung J, Kusne S (2002) Influenza virus infection in adult solid organ transplant recipients. Am J Transplant 2(3):287-291
3. Kumar D, Michaels MG, Morris MI, Green M, Avery RK, Liu C, Danziger-Isakov L, Stosor V, Estabrook M, Gantt S, Marr KA, Martin S, Silveira FP, Razonable RR, Allen UD, Levi ME, Lyon GM, Bell LE, Huprikar S, Patel G, Gregg KS, Pursell K, Helmersen D, Julian KG, Shiley K, Bono B, Dharnidharka VR, Alavi G, Kalpoe JS, Shoham S, Reid GE, Humar A (2010) Outcomes from pandemic influenza A H1N1 infection in recipients of solid-organ transplants: a multicentre cohort study. Lancet Infect Dis 10(8):521-526
4. Fiore AE, Shay DK, Broder K, Iskander JK, Uyeki TM, Mootrey G, Bresee JS, Cox NJ (2009) Prevention and control of seasonal influenza with vaccines: recommendations of the advisory committee on immunization practices (ACIP). MMWR Recomm Rep 58(RR-8):1-52
5. Smith KG, Isbel NM, Catton MG, Leydon JA, Becker GJ, Walker RG (1998) Suppression of the humoral immune response by mycophenolate mofetil. Nephrol Dial Transplant 13(1):160-164
6. Sanchez-Fructuoso AI, Prats D, Naranjo P, Fernandez-Perez C, Gonzalez MJ, Mariano A, Gonzalez J, Figueredo MA, Martin JM, Paniagua V, Fereres J, Gomez de la Concha E, Barrientos A (2000) Influenza virus immunization effectivity in kidney transplant patients subjected to two different triple-drug therapy immunosuppression protocols: mycophenolate versus azathioprine. Transplantation 69(3):436-439
7. Wyzgal J, Brydak LB, Zygier D, Paczek L, Rowinski W, Grochowiecki T (2002) Study on efficacy of influenza vaccination in renal allograft recipients. Transplant Proc 34(2):572-575
8. Birdwell KA, Ikizler MR, Sannella EC, Wang L, Byrne DW, Ikizler TA, Wright PF (2009) Decreased antibody response to influenza vaccination in kidney transplant recipients: a prospective cohort study. Am J Kidney Dis 54(1):112-121
9. Carroll RN, Marsh SD, O'Donoghue EP, Breeze DC, Shackman R (1974) Response to influenza vaccine by renal transplant patients. Br Med J 2(5921):701-703
10. Scharpe J, Evenepoel P, Maes B, Bammens B, Claes K, Osterhaus AD, Vanrenterghem Y, Peetermans WE (2008) Influenza vaccination is efficacious and safe in renal transplant recipients. Am J Transplant 8(2):332-337
11. Candon S, Thervet E, Lebon P, Suberbielle C, Zuber J, Lima C, Charron D, Legendre C, Chatenoud L (2009) Humoral and cellular immune responses after influenza vaccination in kidney transplant recipients. Am J Transplant 9(10):2346-2354
12. Ridao-Cano N, Sanchez-Fructuoso AI, Rodriguez-Moreno A, Barrientos A (2009) H1N1 2009 influenza in kidney transplant patients. Transplantation 90(2):224-225
13. Camargo LF, de Sandes-Freitas TV, Silva CD, Bittante CD, Ono G, Correa L, Silva M Jr, Bellei NC, Goto JM, Medeiros EA, Gomes PS, Medina-Pestana JO (2012) Morbimortality of pandemic influenza A H1N1 infection in kidney transplant recipients requiring hospitalization: a comparative analysis with nonimmunocompromised patients. Transplantation 93(1):69-72
14. Keane WR, Helderman JH, Luby J, Gailiunas P, Hull AR, Kokko JP (1978) Epidemic renal transplant rejection associated with influenza A Victoria. Proc Clin Dial Transplant Forum 8:232-236
15. Kunisaki KM, Janoff EN (2009) Influenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses. Lancet Infect Dis 9(8):493-504
16. Danziger-Isakov L, Cherkassky L, Siegel H, McManamon M, Kramer K, Budev M, Sawinski D, Augustine JJ, Hricik DE, Fairchild R, Heeger PS, Poggio ED (2010) Effects of influenza immunization on humoral and cellular alloreactivity in humans. Transplantation 89(7):838-844
17. Poggio ED, Clemente M, Riley J, Roddy M, Greenspan NS, Dejelo C, Najafian N, Sayegh MH, Hricik DE, Heeger PS (2004) Alloreactivity in renal transplant recipients with and without chronic allograft nephropathy. J Am Soc Nephrol 15(7):1952-1960
18. Heeger PS (2003) T-cell allorecognition and transplant rejection: a summary and update. Am J Transplant 3(5):525-533
19. Matl I, Hribova P, Honsova E, Brabcova I, Viklicky O (2010) Potential predictive markers in protocol biopsies for premature renal graft loss. Kidney Blood Press Res 33(1):7-14
20. Matz M, Beyer J, Wunsch D, Mashreghi MF, Seiler M, Pratschke J, Babel N, Volk HD, Reinke P, Kotsch K (2006) Early post-transplant urinary IP-10 expression after kidney transplantation is predictive of short- and long-term graft function. Kidney Int 69(9):1683-1690
21. Hricik DE, Rodriguez V, Riley J, Bryan K, Tary-Lehmann M, Greenspan N, Dejelo C, Schulak JA, Heeger PS (2003) Enzyme linked immunosorbent spot (ELISPOT) assay for interferon-gamma independently predicts renal function in kidney transplant recipients. Am J Transplant 3(7):878-884
22. Meyer S, Adam M, Schweiger B, Ilchmann C, Eulenburg C, Sattinger E, Runte H, Schluter M, Deuse T, Reichenspurner H, Costard-Jackle A (2011) Antibody response after a single dose of an AS03-adjuvanted split-virion Influenza A(H1N1) vaccine in heart transplant recipients. Transplantation 91(9):1031-1035
23. Andree H, Nickel P, Nasiadko C, Hammer MH, Schonemann C, Pruss A, Volk HD, Reinke P (2006) Identification of dialysis patients with panel-reactive memory T cells before kidney transplantation using an allogeneic cell bank. J Am Soc Nephrol 17(2):573-580
24. Wrammert J, Koutsonanos D, Li GM, Edupuganti S, Sui J, Morrissey M, McCausland M, Skountzou I, Hornig M, Lipkin WI, Mehta A, Razavi B, Del Rio C, Zheng NY, Lee JH, Huang M, Ali Z, Kaur K, Andrews S, Amara RR, Wang Y, Das SR, O'Donnell CD, Yewdell JW, Subbarao K, Marasco WA, Mulligan MJ, Compans R, Ahmed R, Wilson PC (2011) Broadly cross-reactive antibodies dominate the human B cell response against 2009 pandemic H1N1 influenza virus infection. J Exp Med 208(1):181-193
25. Fairhead T, Hendren E, Tinckam K, Rose C, Sherlock CH, Shi L, Crowcroft NS, Gubbay JB, Landsberg D, Knoll G, Gill J, Kumar D (2012) Poor seroprotection but allosensitization after adjuvanted pandemic influenza H1N1 vaccine in kidney transplant recipients. Transpl Infect Dis 14(6):575-583
26. Ott U, Sauerbrei A, Lange J, Schafler A, Walther M, Wolf G, Wutzler P, Zell R, Krumbholz A (2012) Serological response to influenza A H1N1 vaccine (Pandemrix®) and seasonal influenza vaccine 2009/2010 in renal transplant recipients and in hemodialysis patients. Med Microbiol Immunol 201(3):297-302
27. Quintana LF, Serra N, De Molina-Llaurado P, Blasco M, Martinez M, Campos B, Bayas JM, Pumarola T, Campistol JM (2012) Influence of renal replacement therapy on immune response after one and two doses of the A(H1N1) pdm09 vaccine. Influenza Other Respi Viruses
28. Manuel O, Pascual M, Hoschler K, Giulieri S, Alves D, Ellefsen K, Bart PA, Venetz JP, Calandra T, Cavassini M (2011) Humoral response to the influenza A H1N1/09 monovalent AS03-adjuvanted vaccine in immunocompromised patients. Clin Infect Dis 52(2):248-256
29. Brakemeier S, Schweiger B, Lachmann N, Glander P, Schonemann C, Diekmann F, Neumayer HH, Budde K (2011) Immune response to an adjuvanted influenza A H1N1 vaccine (Pandemrix®) in renal transplant recipients. Nephrol Dial Transplant 27(1):423-428
30. Esposito S, Meregalli E, Daleno C, Ghio L, Tagliabue C, Valzano A, Serra D, Galeone C, Edefonti A, Principi N (2011) An open-label, randomized clinical trial assessing immunogenicity, safety and tolerability of pandemic influenza A/H1N1 MF59-adjuvanted vaccine administered sequentially or simultaneously with seasonal virosomal-adjuvanted influenza vaccine to paediatric kidney transplant recipients. Nephrol Dial Transplant 26(6):2018-2024
31. de Lavallade H, Garland P, Sekine T, Hoschler K, Marin D, Stringaris K, Loucaides E, Howe K, Szydlo R, Kanfer E, Macdonald D, Kelleher P, Cooper N, Khoder A, Gabriel IH, Milojkovic D, Pavlu J, Goldman JM, Apperley JF, Rezvani K (2011) Repeated vaccination is required to optimize seroprotection against H1N1 in the immunocompromised host. Haematologica 96(2):307-314
32. Muller K, Schachtner T, Sattler A, Meier S, Friedrich P, Trydzenskaya H, Hinrichs C, Trappe R, Thiel A, Reinke P, Babel N (2011) BK-VP3 as a new target of cellular immunity in BK virus infection. Transplantation 91(1):100-107
33. Bunde T, Kirchner A, Hoffmeister B, Habedank D, Hetzer R, Cherepnev G, Proesch S, Reinke P, Volk HD, Lehmkuhl H, Kern F (2005) Protection from cytomegalovirus after transplantation is correlated with immediate early 1-specific CD8 T cells. J Exp Med 201(7):1031-1036
34. Harari A, Petitpierre S, Vallelian F, Pantaleo G (2004) Skewed representation of functionally distinct populations of virus-specific CD4 T cells in HIV-1-infected subjects with progressive disease: changes after antiretroviral therapy. Blood 103(3):966-972
35. Kumar D, Campbell P, Humar A (2011) Donor-specific alloantibody upregulation after influenza vaccination in transplant recipients. Am J Transplant 11(11):2538
36. Lee VJ, Tay JK, Chen MI, Phoon MC, Xie ML, Wu Y, Lee CX, Yap J, Sakharkar KR, Sakharkar MK, Lin RT, Cui L, Kelly PM, Leo YS, Tan YJ, Chow VT (2010) Inactivated trivalent seasonal influenza vaccine induces limited cross-reactive neutralizing antibody responses against 2009 pandemic and 1934 PR8 H1N1 strains. Vaccine 28(42):6852-6857
37. Xing Z, Cardona CJ (2009) Preexisting immunity to pandemic (H1N1). Emerg Infect Dis 15(11):1847-1849
38. Duvvuri VR, Moghadas SM, Guo H, Duvvuri B, Heffernan JM, Fisman DN, Wu GE, Wu J (2010) Highly conserved cross-reactive CD4 + T-cell HA-epitopes of seasonal and the 2009 pandemic influenza viruses. Influenza Other Respi Viruses 4(5):249-258
39. Greenbaum JA, Kotturi MF, Kim Y, Oseroff C, Vaughan K, Salimi N, Vita R, Ponomarenko J, Scheuermann RH, Sette A, Peters B (2009) Pre-existing immunity against swine-origin H1N1 influenza viruses in the general human population. Proc Natl Acad Sci USA 106(48):20365-20370
40. Allwinn R, Geiler J, Berger A, Cinatl J, Doerr HW (2010) Determination of serum antibodies against swine-origin influenza A virus H1N1/09 by immunofluorescence, haemagglutination inhibition, and by neutralization tests: how is the prevalence rate of protecting antibodies in humans? Med Microbiol Immunol 199(2):117-121
41. Gueller S, Allwinn R, Mousset S, Martin H, Wieters I, Herrmann E, Serve H, Bickel M, Bug G (2011) Enhanced immune response after a second dose of an AS03-adjuvanted H1N1 influenza A vaccine in patients after hematopoietic stem cell transplantation. Biol Blood Marrow Transplant 17(10):1546-1550
42. Kamperschroer C, Dibble JP, Meents DL, Schwartzberg PL, Swain SL (2006) SAP is required for Th cell function and for immunity to influenza. J Immunol 177(8):5317-5327
43. Mozdzanowska K, Furchner M, Maiese K, Gerhard W (1997) CD4 + T cells are ineffective in clearing a pulmonary infection with influenza type A virus in the absence of B cells. Virology 239(1):217-225
44. van de Berg PJ, van Leeuwen EM, ten Berge IJ, van Lier R (2008) Cytotoxic human CD4(+) T cells. Curr Opin Immunol 20(3):339-343
45. Appay V (2004) The physiological role of cytotoxic CD4(+) T-cells: the holy grail? Clin Exp Immunol 138(1):10-13
46. Brown DM, Lee S, Garcia-Hernandez Mde L, Swain SL (2012) Multifunctional CD4 cells expressing gamma interferon and perforin mediate protection against lethal influenza virus infection. J Virol 86(12):6792-6803
47. Wilkinson TM, Li CK, Chui CS, Huang AK, Perkins M, Liebner JC, Lambkin-Williams R, Gilbert A, Oxford J, Nicholas B, Staples KJ, Dong T, Douek DC, McMichael AJ, Xu XN (2012) Preexisting influenza-specific CD4 + T cells correlate with disease protection against influenza challenge in humans. Nat Med 18(2):274-280
48. Ballet C, Roussey-Kesler G, Aubin JT, Brouard S, Giral M, Miqueu P, Louis S, van der Werf S, Soulillou JP (2006) Humoral and cellular responses to influenza vaccination in human recipients naturally tolerant to a kidney allograft. Am J Transplant 6(11):2796-2801
49. Ghendon Y (1990) The immune response to influenza vaccines. Acta Virol 34(3):295-304
50. Sant AJ, Chaves FA, Krafcik FR, Lazarski CA, Menges P, Richards K, Weaver JM (2007) Immunodominance in CD4 T-cell responses: implications for immune responses to influenza virus and for vaccine design. Expert Rev Vaccines 6(3):357-368
51. Teijaro JR, Verhoeven D, Page CA, Turner D, Farber DL (2010) Memory CD4 T cells direct protective responses to influenza virus in the lungs through helper-independent mechanisms. J Virol 84(18):9217-9226
52. Miesegaes G, Lute S, Brorson K (2010) Analysis of viral clearance unit operations for monoclonal antibodies. Biotechnol Bioeng 106(2):238-246
53. Neuzil KM, Jackson LA, Nelson J, Klimov A, Cox N, Bridges CB, Dunn J, DeStefano F, Shay D (2006) Immunogenicity and reactogenicity of 1 versus 2 doses of trivalent inactivated influenza vaccine in vaccine-naive 5-8-year-old children. J Infect Dis 194(8):1032-1039
54. Englund JA, Walter E, Black S, Blatter M, Nyberg J, Ruben FL, Decker MD (2010) Safety and immunogenicity of trivalent inactivated influenza vaccine in infants: a randomized double-blind placebo-controlled study. Pediatr Infect Dis J 29(2):105-110
55. Bickel M, Lassmann C, Wieters I, Doerr HW, Herrmann E, Wicker S, Brodt HR, Stephan C, Allwinn R, Jung O (2013) Immune response after a single dose of the 2010/11 Trivalent, seasonal influenza vaccine in HIV-1-infected patients and healthy controls. HIV Clin Trials 14(4):175-184
56. Walker WT, Faust SN (2010) Monovalent inactivated split-virion AS03-adjuvanted pandemic influenza A (H1N1) vaccine. Expert Rev Vaccines 9(12):1385-1398
57. Skowronski DM, Janjua NZ, De Serres G, Hottes TS, Dickinson JA, Crowcroft N, Kwindt TL, Tang P, Charest H, Fonseca K, Gubbay JB, Bastien N, Li Y, Petric M (2011) Effectiveness of AS03 adjuvanted pandemic H1N1 vaccine: case-control evaluation based on sentinel surveillance system in Canada, autumn 2009. BMJ 342:c7297