Vitamin D levels and influenza vaccine immunogenicity among HIV-infected and HIV-uninfected adults

Vaccine

Volumn 34, Issue 41, 2016, Pages 5040-5046

  Crum Cianflone, Nancy F ^a,b,c   Won, Seunghyun ^a,d   Lee, Rachel ^c   Lalani, Tahaniyat ^a,d,e   Ganesan, Anuradha ^a,d,f   Burgess, Timothy ^a   Agan, Brian K ^a,d  

^a Uniformed Services University of the Health Sciences   (United States)

^b SCRIPPS MERCY HOSPITAL   (United States)

^c NAVAL MEDICAL CENTER SAN DIEGO   (United States)

^d HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^e NAVAL MEDICAL CENTER PORTSMOUTH   (United States)

^f WALTER REED ARMY MEDICAL CENTER   (United States)

Author keywords

HIV infected persons; Immunogenicity; Influenza vaccine; Vitamin D level

Indexed keywords

25 HYDROXYVITAMIN D; INFLUENZA VACCINE; 25-HYDROXYVITAMIN D; VIRUS ANTIBODY; VITAMIN D;

ADULT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; CD4 LYMPHOCYTE COUNT; COHORT ANALYSIS; CONTROLLED STUDY; DISEASE SEVERITY; FEMALE; FOLLOW UP; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTED PATIENT; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNE RESPONSE; IMMUNOGENICITY; INFLUENZA A (H1N1); INFLUENZA VACCINATION; LIMIT OF DETECTION; MAJOR CLINICAL STUDY; MALE; OUTCOME ASSESSMENT; PRIORITY JOURNAL; PROSPECTIVE STUDY; SEROCONVERSION; VITAMIN BLOOD LEVEL; VITAMIN D DEFICIENCY; ANALOGS AND DERIVATIVES; ANTIBODY PRODUCTION; BLOOD; IMMUNOLOGY; MIDDLE AGED; VACCINE IMMUNOGENICITY; YOUNG ADULT;

ADULT; ANTIBODIES, VIRAL; ANTIBODY FORMATION; CD4 LYMPHOCYTE COUNT; FEMALE; HIV INFECTIONS; HUMANS; IMMUNOGENICITY, VACCINE; INFLUENZA VACCINES; MALE; MIDDLE AGED; PROSPECTIVE STUDIES; VITAMIN D; VITAMIN D DEFICIENCY; YOUNG ADULT;

EID: 84990028885     PISSN: 0264410X     EISSN: 18732518     Source Type: Journal    
DOI: 10.1016/j.vaccine.2016.06.019     Document Type: Article

References (61)

1. [1] Kim, D.K., Bridges, C.B., Harriman, K.H., on behalf of the Advisory Committee on Immunization Practices, Advisory committee on immunization practices recommended immunization schedule for adults aged 19 years or older: United States, 2016. Recommended adult immunization schedule: United States, 2016. Ann Intern Med 164 (2016), 184–194.
2. [2] Anema, A., Mills, E., Montaner, J., Brownstein, J.S., Cooper, C., Efficacy of influenza vaccination in HIV-positive patients: a systematic review and meta-analysis. HIV Med 9 (2008), 57–61.
3. [3] Atashili, J., Kalilani, L., Adimora, A., Efficacy and clinical effectiveness of influenza vaccines in HIV-infected individuals: a meta-analysis. BMC Infect Dis, 6, 2006, 138.
4. [4] Kunisaki, K., Janoff, E., Influenza in immunosuppressed populations: a review of infection frequency, morbidity, mortality, and vaccine responses. Lancet Infect Dis 9 (2009), 493–504.
5. [5] Tasker, S.A., Treanor, J.J., Paxton, W.B., Wallace, M.R., Efficacy of influenza vaccination in HIV-infected persons. A randomized, double-blind, placebo-controlled trial. Ann Int Med 131 (1999), 430–433.
6. [6] Kroon, F.P., van Dissel, J.T., de Jong, J.C., Zwinderman, K., van Furth, R., Antibody response after influenza vaccination in HIV-infected individuals: a consecutive 3-year study. Vaccine 18 (2000), 3040–3049.
7. [7] Bickel, M., Wieters, I., Khaykin, P., Nisius, G., Haberl, A., Stephan, C., et al. Low rate of seroconversion after vaccination with a split virion, adjuvanted pandemic H1N1 influenza vaccine in HIV-1-infected patients. AIDS 24 (2010), F31–F35.
8. [8] Tebas, P., Frank, I., Lewis, M., Quinn, J., Zifchak, L., Thomas, A., et al. Center for AIDS research and clinical trials unit of the University of Pennsylvania. Poor immunogenicity of the H1N1 2009 vaccine in well controlled HIV-infected individuals. AIDS 24 (2010), 2187–2192.
9. [9] Crum-Cianflone, N.F., Eberly, L.E., Duplessis, C., Maguire, J., Ganesan, A., Faix, D., et al. Immunogenicity of a monovalent 2009 influenza A (H1N1) vaccine in an immunocompromised population: a prospective study comparing HIV-infected adults with HIV-uninfected adults. Clin Infect Dis 52 (2011), 138–146.
10. [10] Neuzil, K.M., Reed, G.W., Mitchel, E.F. Jr, Griffin, M.R., Influenza-associated morbidity and mortality in young and middle-aged women. JAMA 281 (1999), 901–907.
11. [11] Lin, J.C., Nichol, K.L., Excess mortality due to pneumonia or influenza during influenza seasons among person with acquired immunodeficiency syndrome. Arch Int Med 161 (2001), 441–446.
12. [12] Safrin, S., Rush, J.D., Mills, J., Influenza in patients with human immunodeficiency virus infection. Chest 98 (1990), 33–37.
13. [13] Centers for disease control and prevention (CDC). Increase in pneumonia mortality among adults and the HIV epidemic in New York City, United States. MMWR Morb Mortal Wkly Rep 1988;37:593–6.
14. [14] McKittrick, N., Frank, I., Jacobson, J.M., White, C.J., Kim, D., Kappes, R., et al. Improved immunogenicity with high-dose seasonal influenza vaccine in HIV-infected persons: a single-center, parallel, randomized trial. Ann Int Med 158 (2013), 19–26.
15. [15] Nielsen, A.B., Nielsen, H.S., Nielsen, L., Thybo, S., Kronborg, G., Immune response after one or two doses of pandemic influenza A (H1N1) monovalent, AS03-adjuvanted vaccine in HIV infected adults. Vaccine 30 (2012), 7067–7071.
16. [16] Durier, C., Desaint, C., Lucht, F., Girard, P.M., Lévy, Y., May, T., et al. ANRS 151 study group and the REIVAC network. Long-term immunogenicity of two doses of 2009 A/H1N1v vaccine with and without AS03(A) adjuvant in HIV-1-infected adults. AIDS 2013:27 (2009), 87–93.
17. [17] Fabbiani, M., Di Giambenedetto, S., Sali, M., Farina, S., Sansonetti, P., Tamburrini, E., et al. Immune response to influenza A (H1N1)v monovalent MF59-adjuvanted vaccine in HIV-infected patients. Vaccine 29 (2011), 2836–2839.
18. [18] Aberg, J.A., Gallant, J.E., Ghanem, K.G., Emmanuel, P., Zingman, B.S., Horberg, M.A., Infectious Diseases Society of America. Primary care guidelines for the management of persons infected with HIV: 2013 update by the HIV Medicine Association of the Infectious Diseases Society of America. Clin Infect Dis 58 (2014), 1–10.
19. [19] Khoo, A.L., Chai, L., Koenen, H., Joosten, I., Netea, M., van der Ven, A., Translating the role of vitamin D3 in infectious diseases. Crit Rev Microbiol 38 (2012), 122–135.
20. [20] Liu, P.T., Stenger, S., Li, H., Wenzel, L., Tan, B.H., et al. Toll-like receptor triggering of a vitamin D-mediated human antimicrobial response. Science 311 (2006), 1770–1773.
21. [21] Boonstra, A., Barrat, F.J., Crain, C., Heath, V.L., Savelkoul, H.F., O'Garra, A., 1alpha,25-Dihydroxyvitamin d3 has a direct effect on naive CD4(+) T cells to enhance the development of Th2 cells. J Immunol 167 (2001), 4974–4980.
22. [22] Chen, S., Sims, G.P., Chen, X.X., Gu, Y.Y., Lipsky, P.E., Modulatory effects of 1,25-dihydroxyvitamin D3 on human B cell differentiation. J Immunol 179 (2007), 1634–1647.
23. [23] van Etten, E., Mathieu, C., Immunoregulation by 1,25-dihydroxyvitamin D3: basic concepts. J Steroid Biochem Mol Biol 97 (2005), 93–101.
24. [24] Lang, P.O., Aspinall, R., Can we translate vitamin D immunomodulating effect on innate and adaptive immunity to vaccine response?. Nutrients 7 (2015), 2044–2060.
25. [25] Lang, P.O., Samaras, N., Samaras, D., Aspinall, R., How important is vitamin D in preventing infections?. Osteoporos Int 24 (2013), 1537–1553.
26. [26] Chadha, M.K., Fakih, M., Muindi, J., Tian, L., Mashtare, T., Johson, C.S., et al. Effect of 25-hydroxyvitamin D status on serological response to influenza vaccine in prostate cancer patients. Prostate 71 (2011), 368–372.
27. [27] Science, M., Maguire, J.L., Russell, M.L., Smieja, M., Walter, S.D., Loeb, M., Serum 25-hydroxyvitamin d level and influenza vaccine immunogenicity in children and adolescents. PLoS ONE, 9, 2014, e83553.
28. [28] Sundaram, M.E., Talbot, H.K., Zhu, Y., Griffin, M.R., Spencer, S., Shay, D.K., et al. Vitamin D is not associated with serologic response to influenza vaccine in adults over 50 years old. Vaccine 31 (2013), 2057–2061.
29. [29] Bickel, M., Lassmann, C., Wieters, I., Doerr, H.W., Herrmann, E., Wicker, S., et al. 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 (2013), 175–181.
30. [30] Momplaisir, F., Frank, I., Meyer, W. 3rd, Kim, D., Kappes, R., Tebas, P., Vitamin D levels, natural H1N1 infection and response to H1N1 vaccine among HIV-infected individuals. J AIDS Clin Res, 3, 2012, 152.
31. [31] Cooper, C., Thorne, A., Canadian HIV trials network Ctn influenza vaccine research group. Vitamin D supplementation does not increase immunogenicity of seasonal influenza vaccine in HIV-infected adults. HIV Clin Trials 12 (2011), 275–276.
32. [32] Dao, C.N., Patel, P., Overton, E.T., Rhame, F., Pals, S.L., Johnson, C., Bush, T., Brooks, J.T., et al. Study to understand the natural history of HIV and AIDS in the Era of effective therapy (SUN) investigators. Low vitamin D among HIV-infected adults: prevalence of and risk factors for low vitamin D Levels in a cohort of HIV-infected adults and comparison to prevalence among adults in the US general population. Clin Infect Dis 52 (2011), 396–405.
33. [33] Oyedele, T., Adeyemi, O.M., High prevalence of vitamin D deficiency in HIV-infected adults: what are the future research questions?. Curr HIV/AIDS Rep 9 (2012), 1–4.
34. [34] Division of AIDS table for grading the severity of adult and pediatric adverse events (version 1.0); December 2004. [accessed 1 March 2016].
35. [35] Hobson, D., Curry, R.L., Beare, A.S., Ward-Gardner, A., The role of serum haemagglutination-inhibiting antibody in protection against challenge infection with influenza A2 and B viruses. J Hyg (Lond) 70 (1972), 767–777.
36. [36] Hannoun, C., Megas, F., Piercy, J., Immunogenicity and protective efficacy of influenza vaccination. Virus Res 103 (2004), 133–138.
37. [37] Crum-Cianflone, N.F., Iverson, E., Defang, G., Blair, P.J., Eberly, L.E., Maguire, J., et al. Durability of antibody responses after receipt of the monovalent 2009 pandemic influenza A (H1N1) vaccine among HIV-infected and HIV-uninfected adults. Vaccine 29 (2011), 3183–3191.
38. [38] Kendal, A.P., Pereira, M.S., Skehel, J.J., Concepts and procedures for laboratory-based influenza surveillance. 1982, World Health Organization, Geneva.
39. [39] Eagle Biosciences Vitamin 25 OH ELISA Package Insert. [accessed on March 23, 2016].
40. [40] DEQAS (Vitamin D External Quality Assessment Scheme). Endocrine Laboratory – Charing Cross Hospital – Fulham Palace Road – London W6 8RF – UK. [accessed on March 23, 2016].
41. [41] Holick, M.F., Vitamin D deficiency. N Engl J Med 357 (2007), 266–281.
42. [42] Holick, M.F., Chen, T.C., Vitamin D deficiency: a worldwide problem with health consequences. Am J Clin Nutr 87 (2008), 1080S–1086S.
43. [43] Sundaram, M.E., Coleman, L.A., Vitamin D and influenza. Adv Nutr 3 (2012), 517–525.
44. [44] Cannell, J.J., Vieth, R., Umhau, J.C., Holick, M.F., Grant, W.B., Madronich, S., et al. Epidemic influenza and vitamin D. Epidemiol Infect 134 (2006), 1129–1140.
45. [45] Sabetta, J.R., DePetrillo, P., Cipriani, R.J., Smardin, J., Burns, L.A., Landry, M.L., Serum 25-hydroxyvitamin D and the incidence of acute viral respiratory tract infections in healthy adults. PLoS ONE, 5, 2010, e11088.
46. [46] Science, M., Maguire, J.L., Russell, M.L., Smieja, M., Walter, S.D., Loeb, M., Low serum 25-hydroxyvitamin D level and risk of upper respiratory tract infection in children and adolescents. Clin Infect Dis 57 (2013), 392–397.
47. [47] Greiller, C.L., Martineau, A.R., Modulation of the immune response to respiratory viruses by vitamin D. Nutrients 7 (2015), 4240–4270.
48. [48] Pletz, M.W., Terkamp, C., Schumacher, U., Rohde, G., Schütte, H., Welte, T., Bals, R., CAPNETZ-study group. Vitamin D deficiency in community-acquired pneumonia: low levels of 1,25(OH)2 D are associated with disease severity. Respir Res, 15, 2014, 53.
49. [49] Watkins, R.R., Lemonovich, T.L., Salata, R.A., An update on the association of vitamin D deficiency with common infectious diseases. Can J Physiol Pharmacol 93 (2015), 363–368.
50. [50] Urashima, M., Segawa, T., Okazaki, M., Kurihara, M., Wada, Y., Ida, H., Randomized trial of vitamin D supplementation to prevent seasonal influenza A in schoolchildren. Am J Clin Nutr 91 (2010), 1255–1260.
51. [51] Bergman, P., Lindh, A.U., Björkhem-Bergman, L., Lindh, J.D., Vitamin D and respiratory tract infections: a systematic review and meta-analysis of randomized controlled trials. PLoS ONE, 8, 2013, e65835.
52. [52] Ivanov, A.P., Dragunsky, E.M., Chumakov, K.M., 1,25-Dihydroxyvitamin D3 enhances systemic and mucosal immune responses to inactivated poliovirus vaccine in mice. J Infect Dis 193 (2006), 598–600.
53. [53] Enioutina, E.Y., Visic, D., McGee, Z.A., Daynes, R.A., The induction of systemic and mucosal immune responses the subcutaneous immunization of mature adult mice: characterization of the antibodies in mucosal secretions of animals immunized with antigen formulations containing a vitamin D3 adjuvant. Vaccine 17 (1999), 3050–3064.
54. [54] Heine, G., Drozdenko, G., Lahl, A., Unterwalder, N., Mei, H., Volk, H.D., et al. Efficient tetanus toxoid immunization on vitamin D supplementation. Eur J Clin Nutr 65 (2011), 329–334.
55. [55] Zitt, E., Sprenger-Mahr, H., Knoll, F., Neyer, U., Lhotta, K., Vitamin D deficiency is associated with poor response to active hepatitis B immunization in patients with chronic kidney disease. Vaccine 30 (2012), 931–935.
56. [56] Osterholm, M.T., Kelley, N.S., Sommer, A., Belongia, E.A., Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect Dis 12 (2012), 36–44.
57. [57] Kriesel, J.D., Spruance, J., Calcitriol (1,25-dihydroxy-vitamin D3) coadministered with influenza vaccine does not enhance humoral immunity in human volunteers. Vaccine 17 (1999), 1883–1888.
58. [58] Principi, N., Marchisio, P., Terranova, L., Zampiero, A., Baggi, E., Daleno, C., et al. Impact of vitamin D administration on immunogenicity of trivalent inactivated influenza vaccine in previously unvaccinated children. Hum Vaccin Immunother 9 (2013), 969–974.
59. [59] Deeks, S.G., HIV infection, inflammation, immunosenescence, and aging. Annu Rev Med 62 (2011), 141–155.
60. [60] Dushoff, J., Plotkin, J.B., Viboud, C., Earn, D.J., Simonsen, L., Mortality due to influenza in the United States–an annualized regression approach using multiple-cause mortality data. Am J Epidemiol 163 (2006), 181–187.
61. [61] Klein, M.B., Lu, Y., DelBalso, L., Cote, S., Boivin, G., Influenza virus infection is a primary cause of febrile respiratory illness in HIV-infected adults, despite vaccination. Clin Infect Dis 45 (2007), 234–240.