Impaired immune response to vaccination against infection with human respiratory syncytial virus at advanced age

Journal of Virology

Volumn 88, Issue 17, 2014, Pages 9744-9750

  Guichelaar, Teun ^a   Hoeboer, Jeroen ^a   Widjojoatmodjo, Myra N ^a,b   Reemers, Sylvia S N ^a,c   van Els, Cécile A C M ^a   Otten, Rob ^a   van Remmerden, Yvonne ^a   Boes, Jolande ^a,d   Luytjes, Willem ^a  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b CRUCELL HOLLAND BV   (Netherlands)

^c INTERVET INTERNATIONAL BV   (Netherlands)

^d Intravacc   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; NEUTRALIZING ANTIBODY; RESPIRATORY SYNCYTIAL VIRUS VACCINE; VIRUS ANTIBODY;

AGING; ANIMAL; BLOOD; DISEASE MODEL; HUMAN RESPIRATORY SYNCYTIAL VIRUS; IMMUNOLOGY; LUNG; PROCEDURES; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; SERUM; SIGMODONTINAE; VACCINATION;

AGING; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; DISEASE MODELS, ANIMAL; IMMUNOGLOBULIN A; IMMUNOGLOBULIN G; LUNG; RESPIRATORY SYNCYTIAL VIRUS INFECTIONS; RESPIRATORY SYNCYTIAL VIRUS VACCINES; RESPIRATORY SYNCYTIAL VIRUS, HUMAN; SERUM; SIGMODONTINAE; VACCINATION;

EID: 84921981186     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01101-14     Document Type: Article

References (45)

1. Jansen AG, Sanders EA, Hoes AW, van Loon AM, Hak E. 2007. Influenza-and respiratory syncytial virus-associated mortality and hospitalisations. Eur. Respir. J. 30:1158-1166. http://dx.doi.org/10.1183/09031936.00034407.
2. Falsey AR, Hennessey PA, Formica MA, Cox C, Walsh EE. 2005. Respiratory syncytial virus infection in elderly and high-risk adults. N. Engl. J. Med. 352:1749-1759. http://dx.doi.org/10.1056/NEJMoa043951.
3. Thompson WW, Shay DK, Weintraub E, Brammer L, Cox N, Anderson LJ, Fukuda K. 2003. Mortality associated with influenza and respiratory syncytial virus in the United States. JAMA 289:179-186. http://dx.doi.org/10.1001/jama.289.2.179.
4. Ademokun A, Wu YC, Martin V, Mitra R, Sack U, Baxendale H, Kipling D, Dunn-Walters DK. 2011. Vaccination-induced changes in human B-cell repertoire and pneumococcal IgM and IgA antibody at different ages. Aging Cell 10:922-930. http://dx.doi.org/10.1111/j.1474-9726.2011.00732.x.
5. Louie JK, Hacker JK, Gonzales R, Mark J, Maselli JH, Yagi S, Drew WL. 2005. Characterization of viral agents causing acute respiratory infection in a San Francisco University Medical Center Clinic during the influenza season. Clin. Infect. Dis. 41:822-828. http://dx.doi.org/10.1086/432800.
6. Zambon MC, Stockton JD, Clewley JP, Fleming DM. 2001. Contribution of influenza and respiratory syncytial virus to community cases of influenza-like illness: an observational study. Lancet 358:1410-1416. http://dx.doi.org/10.1016/S0140-6736(01)06528-X.
7. Fleming DM, Cross KW. 1993. Respiratory syncytial virus or influenza? Lancet 342:1507-1510. http://dx.doi.org/10.1016/S0140-6736(05)80082-0.
8. Walsh EE, Peterson DR, Falsey AR. 2007. Is clinical recognition of respiratory syncytial virus infection in hospitalized elderly and high-risk adults possible? J. Infect. Dis. 195:1046-1051. http://dx.doi.org/10.1086/511986.
9. Falsey AR, Walsh EE. 2000. Respiratory syncytial virus infection in adults. Clin. Microbiol. Rev. 13:371-384. http://dx.doi.org/10.1128/CMR.13.3.371-384.2000.
10. Niewiesk S, Prince G. 2002. Diversifying animal models: the use of hispid cotton rats (Sigmodon hispidus) in infectious diseases. Lab. Anim. 36: 357-372. http://dx.doi.org/10.1258/002367702320389026.
11. Boukhvalova MS, Prince GA, Blanco JC. 2009. The cotton rat model of respiratory viral infections. Biologicals 37:152-159. http://dx.doi.org/10.1016/j.biologicals.2009.02.017.
12. Prince GA, Jenson AB, Horswood RL, Camargo E, Chanock RM. 1978. The pathogenesis of respiratory syncytial virus infection in cotton rats. Am. J. Pathol. 93:771-791.
13. Ottolini MG, Blanco JC, Eichelberger MC, Porter DD, Pletneva L, Richardson JY, Prince GA. 2005. The cotton rat provides a useful smallanimal model for the study of influenza virus pathogenesis. J. Gen. Virol. 86:2823-2830. http://dx.doi.org/10.1099/vir.0.81145-0.
14. Dreizin RS, Vyshnevetskaia LO, Bagdamian EE, Iankevich OD, Tara-Sova LB. 1971. Experimental RS virus infection of cotton rats. A viral and immunofluorescent study. Vopr. ViRusol. 16:670-676. (In Russian.)
15. Prince GA, Horswood RL, Chanock RM. 1985. Quantitative aspects of passive immunity to respiratory syncytial virus infection in infant cotton rats. J. Virol. 55:517-520.
16. Murphy BR, Sotnikov AV, Lawrence LA, Banks SM, Prince GA. 1990. Enhanced pulmonary histopathology is observed in cotton rats immunized with formalin-inactivated respiratory syncytial virus (RSV) or purified F glycoprotein and challenged with RSV 3-6 months after immunization. Vaccine 8:497-502. http://dx.doi.org/10.1016/0264-410X(90)90253-I.
17. Widjojoatmodjo MN, Boes J, van Bers M, van Remmerden Y, Roholl PJ, Luytjes W. 2010. A highly attenuated recombinant human respiratory syncytial virus lacking the G protein induces long-lasting protection in cotton rats. Virol. J. 7:114. http://dx.doi.org/10.1186/1743-422X-7-114.
18. Curtis SJ, Ottolini MG, Porter DD, Prince GA. 2002. Age-dependent replication of respiratory syncytial virus in the cotton rat. Exp. Biol. Med. (Maywood) 227:799-802.
19. Boukhvalova MS, Yim KC, Kuhn KH, Hemming JP, Prince GA, Porter DD, Blanco JC. 2007. Age-related differences in pulmonary cytokine response to respiratory syncytial virus infection: modulation by antiinflammatory and antiviral treatment. J. Infect. Dis. 195:511-518. http://dx.doi.org/10.1086/510628.
20. Schuurhof A, Bont L, Pennings JL, Hodemaekers HM, Wester PW, Buisman A, de Rond LC, Widjojoatmodjo MN, Luytjes W, Kimpen JL, Janssen R. 2010. Gene expression differences in lungs of mice during secondary immune responses to respiratory syncytial virus infection. J. Virol. 84:9584-9594. http://dx.doi.org/10.1128/JVI.00302-10.
21. van Remmerden Y, Xu F, van Eldik M, Heldens JG, Huisman W, Widjojoatmodjo MN. 2012. An improved respiratory syncytial virus neutralization assay based on the detection of green fluorescent protein expression and automated plaque counting. Virol. J. 9:253. http://dx.doi.org/10.1186/1743-422X-9-253.
22. Sambhara S, McElhaney JE. 2009. Immunosenescence and influenza vaccine efficacy. Curr. Top. Microbiol. Immunol. 333:413-429. http://dx.doi.org/10.1007/978-3-540-92165-3_20.
23. Bukreyev A, Belyakov IM. 2002. Expression of immunomodulating molecules by recombinant viruses: can the immunogenicity of live virus vaccines be improved? Expert Rev. Vaccines 1:233-245. http://dx.doi.org/10.1586/14760584.1.2.233.
24. Liu WM, van der Zeijst BA, Boog CJ, Soethout EC. 2011. Aging and impaired immunity to influenza viruses: implications for vaccine development. Hum. Vaccin. 7:94-98. http://dx.doi.org/10.4161/hv.7.0.14568.
25. Falsey AR, Walsh EE. 1997. Safety and immunogenicity of a respiratory syncytial virus subunit vaccine (PFP-2) in the institutionalized elderly. Vaccine 15:1130-1132. http://dx.doi.org/10.1016/S0264-410X(97)00002-9.
26. Bouree P. 2003. Immunity and immunization in elderly. Pathol. Biol. (Paris) 51:581-585. http://dx.doi.org/10.1016/j.patbio.2003.09.004.
27. Beyer WE, Palache AM, Baljet M, Masurel N. 1989. Antibody induction by influenza vaccines in the elderly: a review of the literature. Vaccine 7:385-394. http://dx.doi.org/10.1016/0264-410X(89)90150-3.
28. Cusi MG, Martorelli B, Di Genova G, Terrosi C, Campoccia G, Correale P. 2010. Age related changes in T cell mediated immune response and effector memory to respiratory syncytial virus (RSV) in healthy subjects. Immun. Ageing 7:14. http://dx.doi.org/10.1186/1742-4933-7-14.
29. Rappuoli R, Mandl CW, Black S, De Gregorio E. 2011. Vaccines for the twenty-first century society. Nat. Rev. Immunol. 11:865-872. http://dx.doi.org/10.1038/nri3085.
30. van Bleek GM, Osterhaus AD, de Swart RL. 2011. RSV 2010: recent advances in research on respiratory syncytial virus and other pneumoviruses. Vaccine 29:7285-7291. http://dx.doi.org/10.1016/j.vaccine.2011.07.114.
31. Walsh EE, Peterson DR, Kalkanoglu AE, Lee FE, Falsey AR. 2013. Viral shedding and immune responses to respiratory syncytial virus infection in older adults. J. Infect. Dis. 207:1424-1432. http://dx.doi.org/10.1093/infdis/jit038.
32. Falsey AR, Walsh EE. 1998. Relationship of serum antibody to risk of respiratory syncytial virus infection in elderly adults. J. Infect. Dis. 177: 463-466. http://dx.doi.org/10.1086/517376.
33. Prince GA, Horswood RL, Camargo E, Koenig D, Chanock RM. 1983. Mechanisms of immunity to respiratory syncytial virus in cotton rats. Infect. Immun. 42:81-87.
34. Walsh EE, Peterson DR, Falsey AR. 2004. Risk factors for severe respiratory syncytial virus infection in elderly persons. J. Infect. Dis. 189:233-238. http://dx.doi.org/10.1086/380907.
35. Mills J, V, Van Kirk JE, Wright PF, Chanock RM. 1971. Experimental respiratory syncytial virus infection of adults. Possible mechanisms of resistance to infection and illness. J. Immunol. 107:123-130.
36. Downham MA, Scott R, Sims DG, Webb JK, Gardner PS. 1976. Breastfeeding protects against respiratory syncytial virus infections. Br. Med. J. ii:274-276. http://dx.doi.org/10.1136/bmj.2.6030.274.
37. Falsey AR, Singh HK, Walsh EE. 2006. Serum antibody decay in adults following natural respiratory syncytial virus infection. J. Med. Virol. 78: 1493-1497. http://dx.doi.org/10.1002/jmv.20724.
38. Terrosi C, Di Genova G, Martorelli B, Valentini M, Cusi MG. 2009. Humoral immunity to respiratory syncytial virus in young and elderly adults. Epidemiol. Infect. 137:1684-1686. http://dx.doi.org/10.1017/S0950268809002593.
39. Falsey AR, Walsh EE, Looney RJ, Kolassa JE, Formica MA, Criddle MC, Hall WJ. 1999. Comparison of respiratory syncytial virus humoral immunity and response to infection in young and elderly adults. J. Med. Virol. 59:221-226. http://dx.doi.org/10.1002/(SICI)1096-9071(199910)59:2+2 21::AID-JMV16+3.0.CO;2-H.
40. Hall CB, Hall WJ, Speers DM. 1979. Clinical and physiological manifestations of bronchiolitis and pneumonia. Outcome of respiratory syncytial virus. Am. J. Dis. Child. 133:798-802.
41. Gonzalez IM, Karron RA, Eichelberger M, Walsh EE, Delagarza VW, Bennett R, Chanock RM, Murphy BR, Clements-Mann ML, Falsey AR. 2000. Evaluation of the live attenuated cpts 248/404 RSV vaccine in combination with a subunit RSV vaccine (PFP-2) in healthy young and older adults. Vaccine 18:1763-1772. http://dx.doi.org/10.1016/S0264-410X(99)00527-7.
42. Sharma R, Woldehiwet Z. 1992. Class-specific antibodies to bovine respiratory syncytial virus in experimentally infected lambs. Epidemiol. Infect. 108:135-145. http://dx.doi.org/10.1017/S095026880004958X.
43. Welliver RC, Kaul TN, Putnam TI, Sun M, Riddlesberger K, Ogra PL. 1980. The antibody response to primary and secondary infection with respiratory syncytial virus: kinetics of class-specific responses. J. Pediatr. 96:808-813. http://dx.doi.org/10.1016/S0022-3476(80)80547-6.
44. Cherukuri A, Patton K, Gasser RA, Jr, Zuo F, Woo J, Esser MT, Tang RS. 2013. Adults 65 years old and older have reduced numbers of functional memory T cells to respiratory syncytial virus fusion protein. Clin. Vaccine Immunol. 20:239-247. http://dx.doi.org/10.1128/CVI.00580-12.
45. de Bree GJ, Heidema J, van Leeuwen EM, van Bleek GM, Jonkers RE, Jansen HM, van Lier RA, Out TA. 2005. Respiratory syncytial virusspecific CD8+ memory T cell responses in elderly persons. J. Infect. Dis. 191:1710-1718. http://dx.doi.org/10.1086/429695.