Unravelling the nature of non-specific effects of vaccines—A challenge for innate immunologists

Seminars in Immunology

Volumn 28, Issue 4, 2016, Pages 377-383

  Jensen, Kristoffer Jarlov ^a,b   Benn, Christine Stabell ^a,c,d   van Crevel, Reinout ^e  

^a STATENS SERUM INSTITUT   (Denmark)

^b TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^c Studies of the Epidemiology of Epilepsy in Demographic Surveillance Systems   (Guinea-Bissau)

^d ODENSE UNIVERSITY HOSPITAL   (Denmark)

^e RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Epigenetic; Non specific effects; Trained immunity; Vaccination

Indexed keywords

BCG VACCINE; INACTIVATED VACCINE; LIVE VACCINE; MEASLES VACCINE; ORAL POLIOMYELITIS VACCINE; SMALLPOX VACCINE; VACCINE;

DRUG EFFECT; DRUG MECHANISM; EPIDEMIOLOGICAL DATA; HUMAN; IMMUNOLOGIST; INNATE IMMUNITY; NONHUMAN; OUTCOME ASSESSMENT; REVIEW; SEX DIFFERENCE; TREATMENT INDICATION; VACCINATION; ANIMAL; CELL DIFFERENTIATION; GENETIC EPIGENESIS; HETEROLOGOUS IMMUNITY; IMMUNOLOGICAL MEMORY; IMMUNOLOGY; LYMPHOCYTE; MYCOBACTERIUM BOVIS; PHYSIOLOGY;

ANIMALS; CELL DIFFERENTIATION; EPIGENESIS, GENETIC; HUMANS; IMMUNITY, HETEROLOGOUS; IMMUNITY, INNATE; IMMUNOLOGIC MEMORY; LYMPHOCYTES; MYCOBACTERIUM BOVIS; VACCINATION; VACCINES;

EID: 84977602153     PISSN: 10445323     EISSN: 10963618     Source Type: Journal    
DOI: 10.1016/j.smim.2016.05.005     Document Type: Review

References (74)

1. [1] Benn, C.S., Netea, M.G., Selin, L.K., Aaby, P., A small jab – a big effect: nonspecific immunomodulation by vaccines. Trends Immunol. 34 (2013), 431–439.
2. [2] Aaby, P., Roth, A., Ravn, H., Napirna, B.M., Rodrigues, A., Lisse, I.M., et al. Randomized trial of BCG vaccination at birth to low-birth-weight children: beneficial nonspecific effects in the neonatal period?. J. Infect. Dis., 2011, 245–252 2011/06/16.
3. [3] Biering-Sorensen, S., Aaby, P., Napirna, B.M., Roth, A., Ravn, H., Rodrigues, A., et al. Small randomized trial among low-birth-weight children receiving bacillus Calmette-Guerin vaccination at first health center contact. Pediatr. infect. dis. j., 2012, 306–308 2011/12/23.
4. [4] Aaby, P., Martins, C.L., Garly, M.L., Bale, C., Andersen, A., Rodrigues, A., et al. Non-specific effects of standard measles vaccine at 4.5 and 9 months of age on childhood mortality: randomised controlled trial. BMJ (Clin. Res. ed.), 2010, c6495 2010/12/02.
5. [5] Shann, F., Nonspecific effects of vaccines and the reduction of mortality in children. Clin. Ther. 35 (2013), 109–114.
6. [6] Aaby, P., Benn, C., Nielsen, J., Lisse, I.M., Rodrigues, A., Ravn, H., Testing the hypothesis that diphtheria-tetanus-pertussis vaccine has negative non-specific and sex-differential effects on child survival in high-mortality countries. BMJ Open, 2012 2012/05/24.
7. [7] WHO, Meeting of the Strategic advisory group of experts on immunization, april 2014-conclusions and recommendations. (2014), No. 21, 2014, 89, 221–236.
8. [8] Aaby, P., Jensen, H., Samb, B., Cisse, B., Sodemann, M., Jakobsen, M., et al. Differences in female-male mortality after high-titre measles vaccine and association with subsequent vaccination with diphtheria-tetanus-pertussis and inactivated poliovirus: reanalysis of West African studies. Lancet 361 (2003), 2183–2188.
9. [9] Netea, M.G., Quintin, J., van der Meer, J.W., Trained immunity: a memory for innate host defense. Cell Host Microbe 9 (2011), 355–361.
10. [10] Sorup, S., Benn, C.S., Poulsen, A., Krause, T.G., Aaby, P., Ravn, H., Live vaccine against measles, mumps, and rubella and the risk of hospital admissions for nontargeted infections. JAMA, 2014, 826–835 2014/02/27.
11. [11] Jensen, M.L., Dave, S., Schim van der, L.M., da, C.C., Vincent, T., Leligdowicz, A., et al. Vaccinia scars associated with improved survival among adults in rural Guinea-Bissau. PLoS One, 1, 2006, e101.
12. [12] Aaby, P., Gustafson, P., Roth, A., Rodrigues, A., Fernandes, M., Sodemann, M., et al. Vaccinia scars associated with better survival for adults. An observational study from Guinea-Bissau. Vaccine, 2006, 5718–5725 2006/05/25.
13. [13] Sorup, S., Villumsen, M., Ravn, H., Benn, C.S., Sorensen, T.I., Aaby, P., et al. Smallpox vaccination and all-cause infectious disease hospitalization: a Danish register-based cohort study. Int. J. Epidemiol., 2011, 955–963 2011/05/06.
14. [14] Lund, N., Andersen, A., Hansen, A.S., Jepsen, F.S., Barbosa, A., Biering-Sorensen, S., et al. The effect of oral polio vaccine at birth on infant mortality: a randomized trial. Clin. Infect. Dis. 61:November (10) (2015), 1504–1511.
15. [15] C. Naeslund, Vaccination Preventative de Tuberculose, Rapports et Documents, Resultats des experiences de vaccination par le BCG poursuivies dans le Norrbotten (Suède) (Septembre 1927–Décembre 1931) (Institut Pasteur, Paris). (1932).
16. [16] Roth, A., Garly, M.L., Jensen, H., Nielsen, J., Aaby, P., Bacillus Calmette-Guerin vaccination and infant mortality. Expert Rev. Vaccines, 2006, 277–293 2006/04/13.
17. [17] Roth, A., Jensen, H., Garly, M.L., Djana, Q., Martins, C.L., Sodemann, M., et al. Low birth weight infants and Calmette-Guerin bacillus vaccination at birth: community study from Guinea-Bissau. Pediatr. Infect. Dis. J. 23:June (6) (2004), 544–550.
18. [18] Shann, F., The non-specific effects of vaccines. Arch. Dis. Child. 95:September (9) (2010), 662–667.
19. [19] Rieckmann, A., Vaccinations against smallpox and tuberculosis are associated with better long-term survival: a Danish case-cohort study 1971–2010. Int. J. Epidemiol., 2016 (in press).
20. [20] Aaby, P., Martins, C.L., Garly, M.L., Rodrigues, A., Benn, C.S., Whittle, H., The optimal age of measles immunisation in low-income countries: a secondary analysis of the assumptions underlying the current policy. BMJ Open, 2(4), 2012.
21. [21] Higgins, J.P.T., Soares-Weiser, K., Reingold, A., Systematic review on the non-specific effects of BCG. DTP and Measles Containing Vaccines, 2014, WHO Sage.
22. [22] Contreras, G., Effect of the administration of oral poliovirus vaccine on infantile diarrhoea mortality. Vaccine 7:June (3) (1989), 211–212.
23. [23] Lund, N., Andersen, A., Monteiro, I., Aaby, P., Benn, C.S., No effect of oral polio vaccine administered at birth on mortality and immune response to BCG. A natural experiment. Vaccine 30 (2012), 6694–6699.
24. [24] Benn, C.S., Fisker, A.B., Rodrigues, A., Ravn, H., Sartono, E., Whittle, H., et al. Sex-differential effect on infant mortality of oral polio vaccine administered with BCG at birth in Guinea-Bissau. A natural experiment. PLoS One, 3, 2008, e4056.
25. [25] Seppala, E., Viskari, H., Hoppu, S., Honkanen, H., Huhtala, H., Simell, O., et al. Viral interference induced by live attenuated virus vaccine (OPV) can prevent otitis media. Vaccine 29 (2011), 8615–8618.
26. [26] Aaby, P., Rodrigues, A., Biai, S., Martins, C., Veirum, J.E., Benn, C.S., et al. Oral polio vaccination and low case fatality at the paediatric ward in Bissau, Guinea-Bissau. Vaccine 22 (2004), 3014–3017.
27. [27] Aaby, P., Hedegaard, K., Sodemann, M., Nhante, E., Veirum, J.E., Jakobsen, M., et al. Childhood mortality after oral polio immunisation campaign in Guinea-Bissau. Vaccine 23 (2005), 1746–1751.
28. [28] Sorup, S., Stensballe, L.G., Krause, T.G., Aaby, P., Benn, C.S., Ravn, H., Oral polio vaccination and hospital admissions with non-Polio infections in Denmark: nationwide retrospective cohort study. Open Forum Infect. Dis., 3(January (1)), 2016, ofv204.
29. [29] Mayr, A., Taking advantage of the positive side-effects of smallpox vaccination. J. Vet. Med. B Infect. Dis. Vet. Pub. Health 51:June (5) (2004), 199–201.
30. [30] Fisker, A.B., Ravn, H., Rodrigues, A., Ostergaard, M.D., Bale, C., Benn, C.S., et al. Co-administration of live measles and yellow fever vaccines and inactivated pentavalent vaccines is associated with increased mortality compared with measles and yellow fever vaccines only. An observational study from Guinea-Bissau. Vaccine 32:January (5) (2014), 598–605.
31. [31] Garly, M.L., Jensen, H., Martins, C.L., Bale, C., Balde, M.A., Lisse, I.M., et al. Hepatitis B vaccination associated with higher female than male mortality in Guinea-bissau: an observational study. Pediatr. Infect. Dis. J., 2004, 1086–1092 2005/01/01.
32. [32] Aaby, P., Garly, M.L., Nielsen, J., Ravn, H., Martins, C., Bale, C., et al. Increased female-male mortality ratio associated with inactivated polio and diphtheria-tetanus-pertussis vaccines: observations from vaccination trials in Guinea-Bissau. Pediatr. Infect. Dis. J., 2007, 247–252 2007/05/09.
33. [33] Fisker, A.B., Hornshoj, L., Rodrigues, A., Balde, I., Fernandes, M., Benn, C.S., et al. Effects of the introduction of new vaccines in Guinea-Bissau on vaccine coverage, vaccine timeliness, and child survival: an observational study. Lancet Glob Health 2:August (8) (2014), e478–e487.
34. [34] Aaby, P., Garly, M.L., Nielsen, J., Ravn, H., Martins, C., Bal, C., et al. Increased Female-Male Mortality Ratio Associated With Inactivated Polio and Diphtheria-Tetanus-Pertussis Vaccines: Observations from vaccination trials in Guinea-Bissau. Pediatr. Infect. Dis. J. 26 (2007), 247–252.
35. [35] Efficacy and safety, of RTS, S/AS01 malaria vaccine with or without a booster dose in infants and children in Africa: final results of a phase 3, individually randomised, controlled trial. Lancet 386:July (9988) (2015), 31–45.
36. [36] Aaby, P., Rodrigues, A., Kofoed, P.E., Benn, C.S., RTS,S/AS01 malaria vaccine and child mortality. Lancet 386:October (10005) (2015), 1735–1736.
37. [37] WHO, WHO Weekly epidemiological record, No. 3, (2016), 91, 21–32. 2016 Jan 22.
38. [38] Roth, A.E., Benn, C.S., Ravn, H., Rodrigues, A., Lisse, I.M., Yazdanbakhsh, M., et al. Effect of revaccination with BCG in early childhood on mortality: randomised trial in Guinea-Bissau. BMJ, 340, 2010, c671.
39. [39] Aaby, P., Jensen, H., Walraven, G., Age-specific changes in the female-male mortality ratio related to the pattern of vaccinations: an observational study from rural Gambia. Vaccine, 2006, 4701–4708 2006/04/20.
40. [40] Aaby, P., Biai, S., Veirum, J.E., Sodemann, M., Lisse, I., Garly, M.L., et al. DTP with or after measles vaccination is associated with increased in-hospital mortality in Guinea-Bissau. Vaccine, 2007, 1265–1269 2006/11/10.
41. [41] Stensballe, L.G., Nante, E., Jensen, I.P., Kofoed, P.E., Poulsen, A., Jensen, H., et al. Acute lower respiratory tract infections and respiratory syncytial virus in infants in Guinea-Bissau: a beneficial effect of BCG vaccination for girls community based case-control study. Vaccine, 2005, 1251–1257 2005/01/18.
42. [42] Aaby, P., Jensen, H., Rodrigues, A., Garly, M.L., Benn, C.S., Lisse, I.M., et al. Divergent female-male mortality ratios associated with different routine vaccinations among female-male twin pairs. Int. J. Epidemiol. 33 (2004), 367–373.
43. [43] Krishnan, A., Srivastava, R., Dwivedi, P., Ng, N., Byass, P., Pandav, C.S., Non-specific sex-differential effect of DTP vaccination may partially explain the excess girl child mortality in Ballabgarh. India Trop. Med. Int. Health 18:November (11) (2013), 1329–1337.
44. [44] Aaby, P., Martins, C.L., Garly, M.L., Andersen, A., Fisker, A.B., Claesson, M.H., et al. Measles vaccination in the presence or absence of maternal measles antibody: impact on child survival. Clin. Infect. Dis., 2014 2014/05/16.
45. [45] Wardhana, D., Datau, E.A., Sultana, A., Mandang, V.V., Jim, E., The efficacy of Bacillus Calmette-Guerin vaccinations for the prevention of acute upper respiratory tract infection in the elderly. Acta Med. Indones., 2011, 185–190 2011/10/08.
46. [46] Gil, A., Kenney, L.L., Mishra, R., Watkin, L.B., Aslan, N., Selin, L.K., Vaccination and heterologous immunity: educating the immune system. Trans. R. Soc. Trop. Med. Hyg. 109:January (1) (2015), 62–69.
47. [47] Alexandroff, A.B., Jackson, A.M., O'Donnell, M.A., James, K., BCG immunotherapy of bladder cancer: 20 years on. Lancet, 1999, 1689–1694 (1999/05/21).
48. [48] Kleinnijenhuis, J., Quintin, J., Preijers, F., Joosten, L.A., Ifrim, D.C., Saeed, S., et al. Bacille Calmette-Guerin induces NOD2-dependent nonspecific protection from reinfection via epigenetic reprogramming of monocytes. Proc. Natl. Acad. Sci. U. S. A., 2012, 17537–17542 2012/09/19.
49. [49] Kleinnijenhuis, J., Quintin, J., Preijers, F., Benn, C.S., Joosten, L.A., Jacobs, C., et al. Long-Lasting effects of BCG vaccination on both heterologous Th1/Th17 responses and innate trained immunity. J. Innate Immun., 2014, 152–158 (2013/11/07).
50. [50] Kleinnijenhuis, J., Quintin, J., Preijers, F., Joosten, L.A., Jacobs, C., Xavier, R.J., et al. BCG-induced trained immunity in NK cells: role for non-specific protection to infection. Clin. Immunol. 155:December (2) (2014), 213–219.
51. [51] Jensen, K.J., Larsen, N., Biering-Sorensen, S., Andersen, A., Eriksen, H.B., Monteiro, I., et al. Heterologous immunological effects of early BCG vaccination in low-birth weight infants in Guinea-Bissau: a randomized-controlled trial. J. Infect. Dis., 2014 2014/09/12.
52. [52] Parra, M., Liu, X., Derrick, S.C., Yang, A., Tian, J., Kolibab, K., et al. Molecular analysis of non-specific protection against murine malaria induced by BCG vaccination. PLoS One, 8, 2013, e66115.
53. [53] van ‘t Wout, J.W., Poell, R., van Furth, R., The role of BCG/PPD-activated macrophages in resistance against systemic candidiasis in mice. Scand. J. Immunol., 1992, 713–720 1992/11/01.
54. [54] Ritz, N., Mui, M., Balloch, A., Curtis, N., Non-specific effect of Bacille Calmette-Guerin vaccine on the immune response to routine immunisations. Vaccine 31 (2013), 3098–3103.
55. [55] Ota, M.O., Vekemans, J., Schlegel-Haueter, S.E., Fielding, K., Sanneh, M., Kidd, M., et al. Influence of Mycobacterium bovis bacillus Calmette-Guerin on antibody and cytokine responses to human neonatal vaccination. Journal of immunology (Baltimore, Md: 1950) 2002 (2002), 919–925 2002/01/05.
56. [56] Leentjens, J., Kox, M., Stokman, R., Gerretsen, J., Diavatopoulos, D.A., van, C.R., et al. BCG vaccination enhances the immunogenicity of subsequent influenza vaccination in healthy volunteers: a randomized, placebo-Controlled pilot study. J. Infect. Dis. 212:December (12) (2015), 1930–1938.
57. [57] Buffen, K., Oosting, M., Quintin, J., Ng, A., Kleinnijenhuis, J., Kumar, V., et al. Autophagy controls BCG-induced trained immunity and the response to intravesical BCG therapy for bladder cancer. PLoS Pathog., 10(October (10)), 2014, e1004485.
58. [58] Cheng, S.C., Quintin, J., Cramer, R.A., Shepardson, K.M., Saeed, S., Kumar, V., et al. mTOR- and HIF-1alpha-mediated aerobic glycolysis as metabolic basis for trained immunity. Science, 345(September (6204)), 2014, 1250684.
59. [59] Quintin, J., Saeed, S., Martens, J.H., Giamarellos-Bourboulis, E.J., Ifrim, D.C., Logie, C., et al. Candida albicans infection affords protection against reinfection via functional reprogramming of monocytes. Cell Host Microbe 12 (2012), 223–232.
60. [60] Scherer, C.A., Magness, C.L., Steiger, K.V., Poitinger, N.D., Caputo, C.M., Miner, D.G., et al. Distinct gene expression profiles in peripheral blood mononuclear cells from patients infected with vaccinia virus, yellow fever 17D virus, or upper respiratory infections. Vaccine 25:August (35) (2007), 6458–6473.
61. [61] Schleupner, C.J., Glasgow, L.A., Peritoneal macrophage activation indicated by enhanced chemiluminescence. Infect. Immun. 21:September (3) (1978), 886–895.
62. [62] Haralambieva, I.H., Ovsyannikova, I.G., Kennedy, R.B., Larrabee, B.R., Shane Pankratz, V., Poland, G.A., Race and sex-based differences in cytokine immune responses to smallpox vaccine in healthy individuals. Hum. Immunol. 74 (2013), 1263–1266.
63. [63] Jensen, K.J., Karkov, H.S., Lund, N., Andersen, A., Eriksen, H.B., Barbosa, A.G., et al. The immunological effects of oral polio vaccine provided with BCG vaccine at birth: a randomised trial. Vaccine, 2014 2014/09/17.
64. [64] Sartono, E., Lisse, I.M., Terveer, E.M., van de Sande, P.J., Whittle, H., Fisker, A.B., et al. Oral polio vaccine influences the immune response to BCG vaccination. A natural experiment. PLoS One, 2010, e10328 2010/05/27.
65. [65] Berkovich, S., Starr, S., Effects of live type 1 poliovirus vaccine and other viruses on the tuberculin test. N. Engl. J. Med., 1966, 67–72 1966/01/13.
66. [66] Alam, M.J., Rashid, M.M., Kabir, Y., Raqib, R., Ahmad, S.M., On birth single dose live attenuated OPV and BCG vaccination induces gut cathelicidin LL37 responses at 6 week of age: a natural experiment. Vaccine 33:January (1) (2015), 18–21.
67. [67] Hussey, G.D., Goddard, E.A., Hughes, J., Ryon, J.J., Kerran, M., Carelse, E., et al. The effect of Edmonston-Zagreb and Schwarz measles vaccines on immune response in infants. J. Infect. Dis. 173:June (6) (1996), 1320–1326.
68. [68] Ovsyannikova, I.G., Reid, K.C., Jacobson, R.M., Oberg, A.L., Klee, G.G., Poland, G.A., Cytokine production patterns and antibody response to measles vaccine. Vaccine, 2003, 3946–3953 2003/08/19.
69. [69] Ward, B.J., Griffin, D.E., Changes in cytokine production after measles virus vaccination: predominant production of IL-4 suggests induction of a Th2 response. Clin. Immunol. Immunopathol., 1993, 171–177 1993/05/01.
70. [70] Jensen, K.J., Sondergaard, M., Andersen, A., Sartono, E., Martins, C., Garly, M.L., et al. A randomized trial of an early measles vaccine at 4(1/2) months of age in Guinea-Bissau: sex-Differential immunological effects. PLoS One, 2014, e97536 2014/05/20.
71. [71] Umlauf, B.J., Haralambieva, I.H., Ovsyannikova, I.G., Kennedy, R.B., Pankratz, V.S., Jacobson, R.M., et al. Associations between demographic variables and multiple measles-specific innate and cell-mediated immune responses after measles vaccination. Viral Immunol. 25 (2012), 29–36.
72. [72] Kim, K.H., Lee, Y.T., Hwang, H.S., Kwon, Y.M., Jung, Y.J., Lee, Y., et al. Alum adjuvant enhances protection against respiratory syncytial virus but exacerbates pulmonary inflammation by modulating multiple innate and adaptive immune cells. PLoS One, 10(10), 2015, e0139916.
73. [73] Blander, J.M., Sander, L.E., Beyond pattern recognition: five immune checkpoints for scaling the microbial threat. Nat. Rev. Immunol. 12:March (3) (2012), 215–225.
74. [74] Arnold, A.P., Promoting the understanding of sex differences to enhance equity and excellence in biomedical science. Biol Sex Differ, 1(1), 2010, 1.