Immunization of preterm infants: current evidence and future strategies to individualized approaches

• Fortmann M.I.
• Dirks J.
• Goedicke-Fritz S.
• Liese J.
• Zemlin M.
• Morbach H.
• Christoph Hartel

Abstract

Preterm infants are at particularly high risk for infectious diseases. As this vulnerability extends beyond the neonatal period into childhood and adolescence, preterm infants benefit greatly from infection-preventive measures such as immunizations. However, there is an ongoing discussion about vaccine safety and efficacy due to preterm infants’ distinct immunological features. A significant proportion of infants remains un- or under-immunized when discharged from primary hospital stay. Educating health care professionals and parents, promoting maternal immunization and evaluating the potential of new vaccination tools are important means to reduce the overall burden from infectious diseases in preterm infants. In this narrative review, we summarize the current knowledge about vaccinations in premature infants. We discuss the specificities of early life immunity and memory function, including the role of polyreactive B cells, restricted B cell receptor diversity and heterologous immunity mediated by a cross-reactive T cell repertoire. Recently, mechanistic studies indicated that tissue-resident memory (Trm) cell populations including T cells, B cells and macrophages are already established in the fetus. Their role in human early life immunity, however, is not yet understood. Tissue-resident memory T cells, for example, are diminished in airway tissues in neonates as compared to older children or adults. Hence, the ability to make specific recall responses after secondary infectious stimulus is hampered, a phenomenon that is transcriptionally regulated by enhanced expression of T-bet. Furthermore, the microbiome establishment is a dominant factor to shape resident immunity at mucosal surfaces, but it is often disturbed in the context of preterm birth. The proposed function of Trm T cells to remember benign interactions with the microbiome might therefore be reduced which would contribute to an increased risk for sustained inflammation. An improved understanding of Trm interactions may determine novel targets of vaccination, e.g., modulation of T-bet responses and facilitate more individualized approaches to protect preterm babies in the future.

Keywords:preterm infants; immunization; vaccination; safety; mechanisms; resident memory T cells

Литература/References

1. Miller J.E., Hammond G.C., Strunk T., Moore H.C., Leonard H., Carter K.W., et al. Association of gestational age and growth measures at birth with infection-related admissions to hospital throughout childhood: a population-based, data-linkage study from Western Australia. Lancet Infect Dis. 2016; 16 (8): 952–61. DOI: https:// doi.org/10.1016/ S1473-3099(16) 00150-X

2. Crump C. An overview of adult health outcomes after preterm birth. Early Hum Dev. 2020; 150: 105187. DOI: https://doi. org/10.1016/j.earlh umdev.2020.105187

3. Humberg A., Fortmann I., Siller B., et al. Preterm birth and sustained inflammation: consequences for the neonate. Semin Immunopathol. 2020; 42 (4): 451–68. DOI: https://doi.org/10. 1007/s00281- 020- 00803-2

4. MacLennan C.A., Saul A. Vaccines against poverty. Proc Natl Acad Sci U S A. 2014; 111 (34): 12307–12. DOI: https://doi.org/10.1073/pnas.14004 73111

5. Gagneur A., Pinquier D., Quach C. Immunization of preterm infants. Hum Vaccin Immunother. 2015; 11 (11): 2556–63.

6. Angelidou A., Levy O. Vaccination of term and preterm infants. NeoReviews. 2020; 21 (12): e817–27.

7. Fortmann I., Dammann M.-T., Humberg A., Siller B., Stichtenoth G., Engels G., et al. Five year follow-up of extremely gestational age infants after timely or delayed administration of routine vaccinations. Vaccines. 2021; 9 (5): 493. DOI: https:// doi.org/10.3390/vacci nes90 50493

8. Levy O., Wynn J.L. A prime time for trained immunity: innate immune memory in newborns and infants. Neonatol. 2014; 105: 136–41.

9. MacKaness G.B. The immunological basis of acquired cellular resistance. J Exp Med. 1964; 120: 105–20.

10 Netea M.G., Joosten L.A., Latz E., Mills K.H., Natoli G., Stunnenberg H.G., et al. Trained immunity: a program of innate immune memory in health and disease. Sci. 2016; 352: aaf1098.

11. Holt P.G., Strickland D.H., Custovic A. Targeting maternal immune function during pregnancy for asthma prevention in offspring: harnessing the “farm effect”? J Allergy Clin Immunol. 2020; 146: 270–2.

12. Kollmann T.R., Marchant A., Way S.S. Vaccination strategies to enhance immunity in neonates. Sci. 2020; 368 (6491): 612–5.

13. Zimmermann P., Curtis N. Factors that influence the immune response to vaccination. Clin Microbiol Rev. 2019; 32: e0008418.

14. Vesikari T., Matson D.O., Dennehy P., Van Damme P., Santosham M., Rodriguez Z., et al. Study Team Safety and efficacy of a pentavalent human-bovine (WC3) reassortant rotavirus vaccine. N Engl J Med. 2006; 354 (1): 23–33. DOI: https://doi.org/10.1056/NEJMo a052664

15. Agarwal S., Mayer L. Diagnosis and treatment of gastrointestinal disorders in patients with primary immunodeficiency. Clin Gastroenterol Hepatol. 2013; 11 (9): 1050–63. DOI: https://doi.org/10.1016/j.cgh.2013.02.024

16. Hiramatsu H., Suzuki R., Nagatani A., et al. Rotavirus vaccination can be performed without viral dissemination in the neonatal intensive care unit. J Infect Dis. 2018; 217 (4): 589–96. DOI: https://doi.org/10.1093/infdis/jix590

17. Omenaca F, Sarlangue J, Szenborn L et al (2012) Safety, reactogenicity and immunogenicity of the human rotavirus vaccine in preterm European Infants: a randomized phase IIIb study. Pediatr Infect Dis J. 31 (5): 487–93. DOI: https://doi.org/10.1097/INF.0b013e3182 490a2c

18. Ellison V.J., Davis P.G., Doyle L.W. Adverse reactions to immunization with newer vaccines in the very preterm infant. J Paediatr Child Health. 2005; 41 (8): 441–3. DOI: https://doi.org/10.1111/j.1440-1754.2005.00663.x

19. Lee J., Robinson J.L., Spady D.W. Frequency of apnea, bradycardia, and desaturations following first diphtheria-tetanus-pertussis-inactivated polio-Haemophilus influenzae type B immunization in hospitalized preterm infants. BMC Pediatr. 2006; 6: 20. DOI: https://doi.org/10.1186/1471-2431-6-20

20. Zupancic J.A.F., Richardson D.K., Horbar J.D., Carpenter J.H., Lee S.K., Escobar G.J., Vermont Oxford Network SNAP Pilot Project Participants. Revalidation of the score for neonatal acute physiology in the Vermont Oxford Network. Pediatr. 2007; 119 (1): e156–63.

21. Carbone T., McEntire B., Kissin D., et al. Absence of an increase in cardiorespiratory events after diphtheria-tetanus-acellular pertussis immunization in preterm infants: a randomized, multicenter study. Pediatr. 2008; 121 (5): e1085–90. DOI: https://doi.org/10.1542/peds.2007-2059

22. Omenaca F., Garcia-Sicilia J., Garcia-Corbeira P., et al. Response of preterm newborns to immunization with a hexavalent diphtheria-tetanus-acellular pertussis-hepatitis B virus-inactivated polio and Haemophilus influenzae type b vaccine: first experiences and solutions to a serious and sensitive issue. Pediatr. 2005; 116 (6): 1292–8. DOI: https://doi.org/10.1542/peds.2004- 2336

23. Faldella G., Alessandroni R., Magini G.M., et al. The preterm infant’s antibody response to a combined diphtheria, tetanus, acellular pertussis and hepatitis B vaccine. Vaccine. 1998; 16 (17): 1646–9. DOI: https://doi.org/10.1016/s0264-410x(98)00060-7

24 Saari T.N. Immunization of preterm and low birth weight infants. American Academy of Pediatrics Committee on Infectious Diseases. Pediatr. 2003; 112 (1 Pt 1): 193–8. DOI: https://doi.org/10.1542/peds.112.1.193

25. Khalak R., Pichichero M.E., D’Angio C.T. Three-year follow-up of vaccine response in extremely preterm infants. Pediatrics. 1998; 101 (4 Pt 1): 597–603. DOI: https://doi.org/10.1542/peds.101.4.597

26. Kirmani K.I., Lofthus G., Pichichero M.E., Voloshen T., D’Angio C.T. Seven-year follow-up of vaccine response in extremely premature infants. Pediatrics. 2002; 109 (3): 498–504. DOI: https://doi.org/10.1542/peds.109.3.498

27. Baxter D., Ghebrehewet S., Welfare W., Ding D.C.D. Vaccinating premature infants in a Special Care Baby Unit in the UK: results of a prospective, non-inferiority based, pragmatic case series study. Hum Vaccin. 2010; 6 (6): 512–20. DOI: https:// doi. org/ 10.4161/ hv.6. 6. 11448

28. Rouers E.D.M., Bruijning-Verhagen P.C.J., van Gageldonk P.G.M., van Dongen J.A.P., Sanders E.A.M., Berbers G.A.M. Association of routine infant vaccinations with antibody levels among preterm infants. JAMA. 2020; 324 (11): 1068–77. DOI: https://doi.org/10.1001/jama.2020.12316

29. Kulkarni-Munje A., Malshe N., Palkar S., Amlekar A., Lalwani S., Mishra A.C., et al. Immune response of indian preterm infants to pentavalent vaccine varies with component antigens and gestational age. Front Immunol. 2021; 12: 592731. DOI: https://doi.org/10.3389/fimmu.2021.592731

30. Kent A., Ladhani S.N., Andrews N.J., et al. Schedules for pneumococcal vaccination of preterm infants: An RCT. Pediatr. 2016; 138 (3). DOI: https://doi. org/10.1542/ peds.2015-3945

31. Omenaca F., Merino J.M., Tejedor J.C., et al. Immunization of preterm infants with 10-valent pneumococcal conjugate vaccine. Pediatr. 2011; 128 (2): e290–8. DOI: https://doi.org/10.1542/ peds.2010-1184

32. D’Angio C.T., Heyne R.J., O’Shea T.M., et al. Heptavalent pneumococcal conjugate vaccine immunogenicity in very-lowbirth-weight, premature infants. Pediatr Infect Dis J. 2010; 29 (7): 600–6. DOI: https://doi.org/10.1097/INF.0b013e3181d264a6

33. Black S., Shinefield H. Safety and efficacy of the sevenvalent pneumococcal conjugate vaccine: evidence from Northern California. Eur J Pediatr. 2002; 161 (Suppl 2): S127–31. DOI: https://doi.org/10.1007/s00431-002-1064-z

34. Ruckinger S., van der Linden M., von Kries R. Effect of heptavalent pneumococcal conjugate vaccination on invasive pneumococcal disease in preterm born infants. BMC Infect Dis. 2010; 10: 12. DOI: https://doi.org/10.1186/1471-2334-10-12

35. Kent A., Beebeejaun K., Braccio S., et al. Safety of meningococcal group B vaccination in hospitalised premature infants. Arch Dis Child Fetal Neonatal Ed. 2019; 104 (2): F171–5. DOI: https://doi. org/10.1136/archdischild-2017-314152

36. Esposito S., Corbellini B., Bosis S., et al. Immunogenicity, safety and tolerability of meningococcal C CRM197 conjugate vaccine administered 3, 5 and 11 months post-natally to pre- and full-term infants. Vaccine. 2007; 25 (26): 4889–94. DOI: https://doi.org/10.1016/j.vaccine.2007.04.018

37. Colditz G.A., Berkey C.S., Mosteller F., Brewer T.F., Wilson M.E., Burdick E., et al. The efficacy of bacillus Calmette-Guerin vaccination of newborns and infants in the prevention of tuberculosis: meta-analyses of the published literature. Pediatrics. 1995; 96 (1 Pt 1): 29–35.

38. Saroha M., Faridi M.M.A., Batra P., Kaur I., Dewan D.K. Immunogenicity and safety of early vs delayed BCG vaccination in moderately preterm (31–33 weeks) infants. Hum Vaccines Immunother. 2015; 11 (12): 2864–71. DOI: https://doi.org/10.1080/21645515.2015.10743 61

39. Cirovic B., de Bree L.C.J., Groh L., et al. BCG Vaccination in humans elicits trained immunity via the hematopoietic progenitor compartment. Cell Host Microbe. 2020; 28 (2): 322–34.e5. DOI: https://doi.org/10.1016/j.chom.2020.05.014

40. Divangahi M., Aaby P., Khader S.A., Barreiro L.B., Bekkering S., Chavakis T., et al. Trained immunity, tolerance, priming and differentiation: distinct immunological processes. Nat Immunol. 2021; 22 (1): 2–6.

41. Goodridge H.S., Ahmed S.S., Curtis N., Kollmann T.R., Levy O., Netea M.G., et al. Harnessing the beneficial heterologous effects of vaccination. Nat Rev Immunol. 2016; 16 (6): 392–400. DOI: https://doi.org/10.1038/nri.2016.43

42. Biering-Sorensen S., Aaby P., Lund N., Monteiro I., Jensen K.J., Brander Eriksen H., et al. Early BCG-Denmark and neonatal mortality among infants weighing <2500 g: A randomized controlled trial. Clin Infect Dis. 2017; 65 (7): 1183–90.

43. Arts R.J.W., Moorlag S.J.C.F.M., Novakovic B., Li Y., Wang S.-Y., Oosting M., et al. BCG Vaccination Protects against Experimental Viral Infection in Humans through the Induction of Cytokines Associated with Trained Immunity. Cell Host Microbe. 2018; 23 (1): 89–100.e5. DOI: https://doi.org/10.1016/j.chom. 2017.12.010

44 Walk J., de Bree L.C.J., Graumans W., Stoter R., van Gemert G.-J., van de Vegte-Bolmer M., et al. Outcomes of controlled human malaria infection after BCG vaccination. Nat Commun. 2019; 10 (1): 874. DOI: https://doi.org/10.1038/s41467-019-08659-3

45. Jensen K.J., Larsen N., Biering-Sorensen S. et al Heterologous immunological effects of early BCG vaccination in lowbirth-weight infants in Guinea-Bissau: a randomized-controlled trial. J Infect Dis. 2015; 211 (6): 956–67. DOI: https://doi.org/10.1093/infdis/jiu508

46. Homaira N., Briggs N., Oei J.L., Hilder L., Bajuk B., Snelling T., Chambers G.M., et al. Impact of influenza on hospitalization rates in children with a range of chronic lung diseases. Influenza Other Respir Viruses. 2019; 13 (3): 233–9. DOI; https://doi.org/10.1111/irv.12633

47. Moriarty L.F., Omer S.B. Infants and the seasonal influenza vaccine: a global perspective on safety, effectiveness, and alternate forms of protection. Hum Vaccin Immunother. 2014; 10 (9): 2721–8.

48. D’Angio C.T., Wyman C.P., Misra R.S., et al. Plasma cell and serum antibody responses to influenza vaccine in preterm and full-term infants. Vaccine. 2017; 35 (38): 5163–71.

49. Hall C.B., Weinberg G.A., Iwane M.K., Blumkin A.K., Edwards K.M., Staat M.A., et al. The burden of respiratory syncytial virus infection in young children. N Engl J Med. 2009; 360 (6): 588–98. https://doi.org/10.1056/NEJMo a0804 877

50. Figueras-Aloy J., Manzoni P., Paes B., et al. Defining the risk and associated morbidity and mortality of severe respiratory syncytial virus infection among preterm infants without chronic lung disease or congenital heart disease. Infect Dis Ther. 2016; 5 (4): 417–52. DOI: https://doi.org/10.1007/s40121-016-0130-1

51. Palivizumab, a humanized respiratory syncytial virus monoclonal antibody, reduces hospitalization from respiratory syncytial virus infection in high-risk infants. The IMpact-RSV Study Group. Pediatrics. 1998; 102 (3 Pt 1): 531–7.

52. Griffin M.P., Yuan Y., Takas T., Domachowske J.B., Madhi S.A., Manzoni P., et al. Single-Dose Nirsevimab for Prevention of RSV in Preterm Infants. N Engl J Med. 2020; 383 (5): 415–25. DOI: https://doi.org/10.1056/NEJMoa1913556

53. Madhi S.A., Polack FP., Piedra P.A., Munoz F.M., Trenholme A.A., Simoes E.A.F., et al. Respiratory syncytial virus vaccination during pregnancy and effects in infants. N Engl J Med. 2020; 383 (5): 426–39. DOI: https://doi.org/10.1056/NEJMoa1908380

54. Crotty S. T follicular helper cell biology: A decade of discovery and diseases. Immunity. 2019; 50 (5): 1132–48.

55. McHeyzer-Williams M., et al Molecular programming of B cell memory. Nat Rev Immunol. 2011; 12 (1): 24–34.

56. Siegrist C.A., Aspinall R. B-cell responses to vaccination at the extremes of age. Nat Rev Immunol. 2009; 9 (3): 185–94.

57. Barrios C., et al. Neonatal and early life immune responses to various forms of vaccine antigens qualitatively differ from adult responses: predominance of a Th2-biased pattern which persists after adult boosting. Eur J Immunol. 1996; 26 (7): 1489–96.

58. Mastelic-Gavillet B., et al. Neonatal T follicular helper cells are lodged in a pre-t follicular helper stage favoring innate over adaptive germinal center responses. Front Immunol. 2019; 10: 1845.

59. Vergani S., Yuan J. Developmental changes in the rules for B cell selection. Immunol Rev. 2021; 300 (1): 194–202.

60. Davenport M.P., Smith N.L., Rudd B.D. Building a T cell compartment: how immune cell development shapes function. Nat Rev Immunol. 2020; 20 (8): 499–506.

61. Baumgarth N. A hard(y) look at B-1 cell development and function. J Immunol. 2017; 199 (10): 3387–94.

62. Hayakawa K., et al. The “Ly-1 B” cell subpopulation in normal immunodefective, and autoimmune mice. J Exp Med. 1983; 157 (1): 202–18.

63. Baumgarth N. The shaping of a B cell pool maximally responsive to infections. Annu Rev Immunol. 2021; 39: 103–29.

64. Girschick H.J., Lipsky P.E. The kappa gene repertoire of human neonatal B cells. Mol Immunol. 2002; 38 (15): 1113–27.

65. Rechavi E., Somech R. Survival of the fetus: fetal B and T cell receptor repertoire development. Semin Immunopathol. 2017; 39 (6): 577–83.

66. Richl P., et al. The lambda gene immunoglobulin repertoire of human neonatal B cells. Mol Immunol. 2008; 45 (2): 320–7.

67. Schelonka R.L. et al. The CDR-H3 repertoire from TdTdeficient adult bone marrow is a close, but not exact, homologue of the CDR-H3 repertoire from perinatal liver. J Immunol. 2010; 185 (10): 6075–84.

68. Schroeder H.W. Jr., Hillson J.L., Perlmutter R.M. Early restriction of the human antibody repertoire. Sci. 1987; 238 (4828): 791–3.

69. Souto-Carneiro M.M., et al. Developmental changes in the human heavy chain CDR3. J Immunol. 2005; 175 (11): 7425–36.

70. Zemlin M., et al. The diversity of rearranged immunoglobulin heavy chain variable region genes in peripheral blood B cells of preterm infants is restricted by short third complementaritydetermining regions but not by limited gene segment usage. Blood. 2001; 97(5): 1511–3.

71. Bauer K., et al. Diversification of Ig heavy chain genes in human preterm neonates prematurely exposed to environmental antigens. J Immunol. 2002; 169 (3): 1349–56.

72. Yuan J., et al. Lin28b reprograms adult bone marrow hematopoietic progenitors to mediate fetal-like lymphopoiesis. Sci. 2012; 335 (6073): 1195–200.

73. Zemlin M., et al. The postnatal maturation of the immunoglobulin heavy chain IgG repertoire in human preterm neonates is slower than in term neonates. J Immunol. 2007; 178 (2): 1180–8.

74. Meffre E. The establishment of early B cell tolerance in humans: lessons from primary immunodeficiency diseases. Ann N Y Acad Sci. 2011; 1246: 1–10.

75. Chen J.W., et al. Autoreactivity in naive human fetal B cells is associated with commensal bacteria recognition. Science. 2020; 369 (6501): 320–5.

76. Griffin D.O., Holodick N.E., Rothstein T.L. Human B1 cells in umbilical cord and adult peripheral blood express the novel phenotype CD20+ CD27+ CD43+ CD70. J Exp Med. 2011; 208 (1): 67–80.

77. Perez-Andres M., et al. The nature of circulating CD27+CD43+ B cells. J Exp Med. 2011; 208 (13): 2565–6.

78. Vanhee S., et al.) Lin28b controls a neonatal to adult switch in B cell positive selection. Sci Immunol. 2019; 4 (39).

79. Kreuk L.S., et al. B cell receptor and Toll-like receptor signaling coordinate to control distinct B-1 responses to both self and the microbiota. Elife. 2019; 8.

80. Steach H.R., et al. Cross-reactivity with self-antigen tunes the functional potential of naive B cells specific for foreign antigens. J Immunol. 2020; 204 (3): 498–509.

81. Tan C., et al. Self-reactivity on a spectrum: A sliding scale of peripheral B cell tolerance. Immunol Rev. 2019; 292 (1): 37–60.

82 New J.S., et al. Neonatal exposure to commensal-bacteria-derived antigens directs polysaccharide-specific B-1 B cell repertoire development. Immun. 2020; 53 (1): 172–86e6.

83. Vono M., et al. Maternal antibodies inhibit neonatal and infant responses to vaccination by shaping the early-life B cell repertoire within germinal centers. Cell Rep. 2019; 28 (7): 1773–84e5.

84 Meyer-Hermann M. Injection of antibodies against immunodominant epitopes tunes germinal centers to generate broadly neutralizing antibodies. Cell Rep. 2019; 29 (5): 1066–73e5.

85. Brophy-Williams S., et al. One vaccine for life: Lessons from immune ontogeny. J Paediatr Child Health. 2021; 57 (6): 782–5.

86. Bogue M., et al. A special repertoire of alpha:beta T cells in neonatal mice. EMBO J. 1991; 10 (12): 3647–54.

87. Feeney A.J. Junctional sequences of fetal T cell receptor beta chains have few N regions. J Exp Med. 1991; 174 (1): 115–24.

88. Gavin M.A., Bevan M.J. Increased peptide promiscuity provides a rationale for the lack of N regions in the neonatal T cell repertoire. Immunity. 1995; 3(6): 793–800.

89. Das A., et al Adaptive from Innate: Human IFN-gamma(+) CD4(+) T cells can arise directly from CXCL8-producing recent thymic emigrants in babies and adults. J Immunol. 2017; 199 (5): 1696–705.

90. Gibbons D., et al.) Interleukin-8 (CXCL8) production is a signatory T cell effector function of human newborn infants. Nat Med. 2014; 20 (10): 1206–10.

91. Pekalski M.L., et al. Neonatal and adult recent thymic emigrants produce IL-8 and express complement receptors CR1 and CR2. JCI Insight. 2017; 2 (16).

92. Sinnott B.D., et al. Direct TLR-2 costimulation unmasks the proinflammatory potential of neonatal CD4+ T Cells. J Immunol. 2016; 197 (1): 68–77.

93. Budeus B., et al. Human cord blood B cells differ from the adult counterpart by conserved Ig repertoires and accelerated response dynamics. J Immunol. 2021; 206 (12): 2839–51.

94. Twisselmann N., Pagel J., Kunstner A., Weckmann M., Hartz A., Glaser K., et al. Hyperoxia/hypoxia exposure primes a sustained pro-inflammatory profile of preterm infant macrophages upon LPS stimulation. Front Immunol. 2021; 12: 762789. DOI: https://doi.org/10.3389/fimmu.2021.762789

95. Laurens M.B. RTS, S/AS01 vaccine (Mosquirix™): an overview. Hum Vaccin Immunother. 2020; 16 (3): 480–9. DOI: https://doi.org/10.1080/21645515.2019.1669415

96. Van Haren S.D., Dowling D.J., Foppen W., Christensen D., Andersen P., Reed S.G., et al. Age-specific adjuvant synergy: Dual TLR7/8 and mincle activation of human newborn dendritic cells enables Th1 polarization. J Immunol. 2016; 197 (11): 4413–24. DOI: https://doi.org/10.4049/jimmunol.1600282

97. Borriello F., Pietrasanta C., Lai J.C.Y., Walsh L.M., Sharma P., O’Driscoll D.N., et al. Identification and characterization of stimulator of interferon genes as a robust adjuvant target for early life immunization. Front Immunol. 2017; 8: 1772. DOI: https://doi.org/10.3389/fimmu.2017.01772

98. Scheid A., Borriello F., Pietrasanta C., Christou H., Diray-Arce J., Pettengill M.A., et al. Adjuvant effect of bacille calmette-guerin on hepatitis B vaccine immunogenicity in the preterm and term newborn. Front Immunol. 2018; 9: 29. DOI: https://doi.org/10.3389/fimmu.2018.00029

99. Nanishi E., Dowling D.J., Levy O. Toward precision adjuvants: optimizing science and safety. Curr Opin Pediatr. 2020; 32 (1): 125–38. DOI: https://doi.org/10.1097/MOP.0000000000000868

100. Vygen-Bonnet S., Hellenbrand W., Garbe E., von Kries R., Bogdan C., Heininger U., et al. Safety and effectiveness of acellular pertussis vaccination during pregnancy: a systematic review. BMC Infect Dis. 2020; 20: 136. DOI: https://doi.org/10.1186/s12879-020-4824-3

101 Winter K., Nickell S., Powell M., Harriman K. Effectiveness of prenatal versus postpartum tetanus, diphtheria, and acellular pertussis vaccination in preventing infant pertussis. Clin Infect Dis. 2017; 64: 3–8. DOI: https://doi.org/10.1093/cid/ciw634

102. Skoff T.H., Blain A.E., Watt J., Scherzinger K., McMahon M., Zansky S.M., et al. Impact of the US maternal tetanus, diphtheria, and acellular pertussis vaccination program on preventing pertussis in infants <2 months of age: A case-control evaluation. Clin Infect Dis. 2017; 65: 1977–83. DOI: https://doi.org/10.1093/cid/cix724

103. Saul N., Wang K., Bag S., Baldwin H., Alexander K., Chandra M., et al. Effectiveness of maternal pertussis vaccination in preventing infection and disease in infants: The NSW Public Health Network case-control study. Vaccine. 2018; 36: 1887–92. DOI: https://doi.org/10.1016/j.vacci ne.2018.02.047

104. Mott K., Huybrechts K.F., Glynn R.J., Mogun H., Hernandez-Diaz S. Tetanus, diphtheria, acellular pertussis vaccination during pregnancy and risk of pertussis in the newborn in publicly and privately insured mother-infant Pairs in the United States. Pediatr Infect Dis J. 2021; 40 (7): 681–7. DOI: https://doi.org/10.1097/INF.0000000000003099

105. Linder N., Tallen-Gozani E., German B., Duvdevani P., Ferber A., Sirota L. Placental transfer of measles antibodies: effect of gestational age and maternal vaccination status. Vaccine. 2004; 22 (11–12): 1509–14. DOI: https://doi.org/10.1016/j.vaccine.2003.10.009

106. Voysey M., Kelly D.F., Fanshawe T.R., Sadarangani M., O’Brien K.L., Perera R., et al. The influence of maternally derived antibody and infant age at vaccination on infant vaccine responses: An individual participant meta-analysis. JAMA Pediatr. 2017; 171: 637–46. DOI: https://doi.org/10.1001/jamapediatrics.2017.0638

107. Hong M., Sandalova E., Low D., Gehring A.J., Fieni S., Amadei B., et al. Trained immunity in newborn infants of HBV-infected mothers. Nat Commun. 2015; 6: 6588. DOI: https://doi.org/10.1038/ncomms7588

108. Stelzer I.A., Urbschat C., Schepanski S., Thiele K., Triviai I., Wieczorek A., et al. Vertically transferred maternal immune cells promote neonatal immunity against early life infections. Nat Commun. 2021; 12 (1): 4706. DOI: https://doi.org/10.1038/s41467-021-24719-z

109. Stras S.F., Werner L., Toothaker J.M., Olaloye O.O., Oldham A.L., McCourt C.C., et al. Maturation of the human intestinal immune system occurs early in fetal development. Dev Cell. 2019; 51 (3): 357–73.e5. DOI: https://doi.org/10.1016/j.devcel. 2019.09.008

110. Feyaerts D., Urbschat C., Stelzer I.A. Establishment of tissue-resident immune populations in the fetus. Semin Immunopathol. 2022; 4: 1–20. DOI: https://doi.org/10.1007/s00281-022-0093

111. Chou C., Li M.O. Tissue-resident lymphocytes across innate and adaptive lineages. Front Immunol. 2018; 21 (9): 2104. DOI: https://doi.org/10.3389/fimmu.2018.02104; PMID: 30298 068.

112. Amezcua Vesely M.C., Pallis P., Bielecki P., Low J.S., Zhao J., Harman C.C.D., et al. Effector TH17 cells give rise to long-lived TRM cells that are essential for an immediate response against bacterial infection. Cell. 2019; 178 (5): 1176–88.e15

113. Lange J., Rivera-Ballesteros O., Buggert M. Human mucosal tissue-resident memory T cells in health and disease. Mucosal Immunol. 2021: 1–9. DOI: https://doi.org/10.1038/s41385-021-00467-7

114. Zens K.D., Chen J.K., Guyer R.S., Wu F.L., Cvetkovski F., Miron M., et al. Reduced generation of lung tissue-resident memory T cells during infancy. J Exp Med. 2017; 214 (10): 2915–32. DOI: https://doi.org/10.1084/jem.20170521

115. Connors T.J., Baird J.S., Yopes M.C., Zens K.D., Pethe K., Ravindranath T.M., et al. Developmental regulation of effector and resident memory T cell generation during pediatric viral respiratory tract infection. J Immunol. 2018; 201 (2): 432–9. DOI: https://doi.org/10.4049/jimmu nol.1800396

116. Varese A., Nakawesi J., Farias A., Kirsebom F.C.M., Paulsen M., Nuriev R., et al. Type I interferons and MAVS signaling are necessary for tissue resident memory CD8+ T cell responses to RSV infection. PLoS Pathog. 2022; 18 (2): e1010272.

117. De Jong C.S., Maurice N.J., McCartney S.A., Prlic M. Human tissue-resident memory T cells in the maternal-fetal interface. Lost soldiers or special forces? Cells. 2020; 9 (12): 2699. DOI: https://doi.org/10.3390/cells9122699

118. Morabito K.M., Ruckwardt T.R., Redwood A.J., Moin S.M., Price D.A., Graham B.S. Intranasal administration of RSV antigen-expressing MCMV elicits robust tissue-resident effector and effector memory CD8+ T cells in the lung. Mucosal Immunol. 2017; 10 (2): 545–54. DOI: https://doi.org/10.1038/mi.2016.48

119. Hassan A.O., Shrihari S., Gorman M.J., Ying B., Yaun D., Raju S., et al. An intranasal vaccine durably protects against SARS-CoV-2 variants in mice. Cell Rep. 2021; 36 (4): 109452. DOI: https://doi.org/10.1016/j.celrep.2021.109452

120. Wilk M.M., Mills K.H.G. CD4 T RM cells following infection and immunization: Implications for more effective vaccine design. Front Immunol. 2018; 9: 1860. DOI: https://doi.org/10.3389/fimmu.2018.01860

121. Overacre-Delgoffe A.E., Hand T. Regulation of tissueresident memory T cells by the microbiota. Mucosal Immunol. 2022; 15: 408–17.

122. Koch M.A., et al. Maternal IgG and IgA antibodies dampen mucosal T helper cell responses early life. Cell. 2016; 165: 827–41.

123. Brizić I., Šušak B., Arapović M., Huszthy P.C., Hiršl L., Kveštak D., et al. Brain-resident memory CD8 + T cells induced by congenital CMV infection prevent brain pathology and virus reactivation. Eur J Immunol. 2018; 48 (6): 950–64. DOI: https://doi.org/10.1002/eji. 201847526

124. De Jong E.N., Surette M.G., Bowdish D.M.E. The gut microbiota and unhealthy aging: Disentangling cause from consequence. Cell Host Microbe. 2020; 28 (2):180–9. DOI: https://doi.org/10.1016/j.chom.2020.07.013

125. Backhed F., Roswall J., Peng Y., Feng Q., Jia H., Kovatcheva-Datchary P., et al. Dynamics and stabilization of the human gut microbiome during the first year of life. Cell Host Microbe. 2015; 17 (5): 690–703. DOI: https://doi.org/10.1016/j.chom.2015.04.004

126. Li H., Limenitakis J.P., Greiff V., Yilmaz B., Scharen O., Urbaniak C., et al. Mucosal or systemic microbiota exposures shape the B cell repertoire. Nature. 2020; 584 (7820): 274–8. DOI: https://doi.org/10.1038/s41586-020-2564-6

127. Kim M., Qie Y., Park J., Kim C.H. Gut microbial metabolites fuel host antibody responses. Cell Host Microbe. 2016; 20 (2): 202–14. DOI: https://doi.org/10.1016/j.chom.2016.07.001

128. Oh J.Z., Ravindran R., Chassaing B., Carvalho F.A., Maddur M.S., Bower M., et al. TLR5-mediated sensing of gut microbiota is necessary for antibody responses to seasonal influenza vaccination. Immunity. 2014; 41 (3): 478–92. DOI: https://doi.org/10.1016/j.immuni.2014.08.009

129. Lynn M., Tumes D.J., Choo J.M., Sribnaia A., Blake S.J., Leong L.E.X., et al. Early-life antibiotic-driven dysbiosis leads to dysregulated vaccine immune responses in mice. Cell Host Microbe. 2018; 23 (5): 653–60.e5. DOI: https://doi.org/10.1016/j.chom.2018.04.009

130. Huda M.N., Lewis Z., Kalanetra K.M., Rashid M., Ahmad S.M., Raqib R., et al. Stool microbiota and vaccine responses of infants. Pediatrics. 2014; 134 (2): e362–72. DOI: https://doi.org/10.1542/peds.2013-3937

131. Huda M.N., Ahmad S.M., Alam M.J., Khanam A., Kalanetra K.M., Taft D.H., et al. Bifidobacterium abundance in early infancy and vaccine response at 2 years of age. Pediatrics. 2019; 143 (2): e20181489. DOI: https://doi.org/10.1542/peds.2018-1489

132. Lynn D.J., Benson S.C., Lynn M.A., Pulendran B. Modulation of immune responses to vaccination by the microbiota: implications and potential mechanisms. Nat Rev Immunol. 2022; 22 (1): 33–46. DOI: https://doi.org/10.1038/s41577-021-00554-7

133. Di Luccia B., Ahern P.P., Griffin N.W., Cheng J., Guruge J., Byrne A.E., et al. Combined prebiotic and microbial intervention improves oral cholera vaccination responses in a mouse model of childhood undernutrition. Cell Host Microbe. 2020; 27 (6): 899–908.e5. DOI: https://doi.org/10.1016/j.chom.2020.04.008

134. Zimmermann P., Curtis N. The influence of probiotics on vaccine responses – A systematic review. Vaccine. 2018; 36 (2): 207–13. DOI: https://doi.org/10.1016/j.vacci ne.2017.08.069

135. Sharif S., Meader N., Oddie S.J., Rojas-Reyes M.X., McGuire W. Probiotics to prevent necrotising enterocolitis in very preterm or very low birth weight infants. Cochrane Database Syst Rev. 2020; 10 (10): CD005496. DOI: https://doi.org/10.1002/14651858.CD005496.pub5

136. Chaudhary N., Weissman D., Whitehead K.A. Author correction: mRNA vaccines for infectious diseases: principles, delivery and clinical translation. Nat Rev Drug Discov. 2021; 20 (11): 880. DOI: https://doi.org/10.1038/s41573-021-00321-2

137. Willis E., Pardi N., Parkhouse K., Mui B.L., Tam Y.K., Weissman D., et al. Nucleoside-modified mRNA vaccination partially overcomes maternal antibody inhibition of de novo immune responses in mice. Sci Transl Med. 2020; 12 (525): eaav5701. DOI: https://doi.org/10.1126/scitranslmed.aav5701

138. Bartsch Y.C., St Denis K.J., Kaplonek P., Kang J., Lam E.C., Burns M.D., et al. Comprehensive antibody profiling of mRNA vaccination in children. bioRxiv. 2022; 2021.10.07.463592. DOI: https://doi.org/10.1101/2021.10.07.463592

139. Holtkamp S.J., Ince L.M., Barnoud C., Schmitt M.T., Sinturel F., Pilorz V., et al. Circadian clocks guide dendritic cells into skin lymphatics. Nat Immunol. 2021; 22 (11): 1375–81. DOI: https://doi.org/10.1038/s41590-021-01040-x

140. Lange T., Dimitrov S., Bollinger T., Diekelmann S., Born J. Sleep after vaccination boosts immunological memory. J Immunol. 2011; 187 (1): 283–90.

141. Gottlob S., Gille C., Poets C.F. Randomized controlled trial on the effects of morning versus evening primary vaccination on episodes of hypoxemia and bradycardia in very preterm infants. Neonatology. 2019; 116 (4): 315–20. DOI: https://doi.org/10.1159/000501338

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