Review article: Biomedical intelligence
Vol. 147 No. 4344 (2017)
Review of maternal immunisation during pregnancy: focus on pertussis and influenza
- Géraldine Blanchard-Rohner
- Christiane S. Eberhardt
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Cite this as:
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Swiss Med Wkly. 2017;147:w14526
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Published
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27.10.2017
Summary
Seasonal influenza and pertussis infections are known to be significant causes of morbidity and mortality in neonates and infants worldwide. Influenza has also been associated with severe complications in pregnant women and after delivery. The most efficient and safe strategy to protect mothers and their offspring is maternal immunisation during pregnancy. The maternal antibodies thus acquired are transferred to the fetus as of the second trimester and confer passive immunity until the first infant immunisations.
Therefore, it is strongly advised to administer booster doses of seasonal influenza and pertussis vaccines specifically during pregnancy. Influenza vaccines can be given at any time-point during pregnancy and pertussis vaccines after the first trimester. Both need a minimum interval of 14 days between immunisation and delivery and, especially for pertussis, early immunisation has been shown to increase neonatal antibody titres. Healthcare workers play a crucial role in vaccine uptake. This article aims to review the recommendations for maternal influenza and pertussis immunisation, and their physiological rationale, safety and benefit.
References
- Newell KW, Dueñas Lehmann A, LeBlanc DR, Garces Osorio N. The use of toxoid for the prevention of tetanus neonatorum. Final report of a double-blind controlled field trial. Bull World Health Organ. 1966;35(6):863–71.
- Thwaites CL, Beeching NJ, Newton CR. Maternal and neonatal tetanus. Lancet. 2015;385(9965):362–70. doi:.https://doi.org/10.1016/S0140-6736(14)60236-1
- Office Fédéral de la Santé Publique. Recommendations de vaccination contre la grippe saisonnière (2010-2011). Bull OFSP. 2010;25:624–7.
- Office Fédéral de la Santé Publique. Adaptation des recommandations de vaccination contre la coqueluche: pour les adolescents, les nourrissons fréquentant une structure d’accueil collectif et les femmes enceintes. Bull OFSP. 2013;9:118–23.
- Blanchard-Rohner G, Meier S, Ryser J, Schaller D, Combescure C, Yudin MH, et al. Acceptability of maternal immunization against influenza: the critical role of obstetricians. J Matern Fetal Neonatal Med. 2012;25(9):1800–9. doi:.https://doi.org/10.3109/14767058.2012.663835
- Schindler M, Blanchard-Rohner G, Meier S, Martinez de Tejada B, Siegrist CA, Burton-Jeangros C. Vaccination against seasonal flu in Switzerland: The indecision of pregnant women encouraged by healthcare professionals. Rev Epidemiol Sante Publique. 2012;60(6):447–53. doi:.https://doi.org/10.1016/j.respe.2012.03.008
- Zhao Y WaS. Cell Types of the Placenta. In: Vascular Biology of the Placenta. San Rafael (CA): Morgan & Claypool Life Sciences; 2010.
- Bright NA, Ockleford CD. Cytotrophoblast cells: a barrier to maternofetal transmission of passive immunity. J Histochem Cytochem. 1995;43(9):933–44. Published online September 01, 1995. doi:.https://doi.org/10.1177/43.9.7642966
- Malek A, Sager R, Kuhn P, Nicolaides KH, Schneider H. Evolution of maternofetal transport of immunoglobulins during human pregnancy. Am J Reprod Immunol. 1996;36(5):248–55. doi:.https://doi.org/10.1111/j.1600-0897.1996.tb00172.x
- Vidarsson G, Dekkers G, Rispens T. IgG subclasses and allotypes: from structure to effector functions. Front Immunol. 2014;5:520. doi:.https://doi.org/10.3389/fimmu.2014.00520
- Palmeira P, Quinello C, Silveira-Lessa AL, Zago CA, Carneiro-Sampaio M. IgG placental transfer in healthy and pathological pregnancies. Clin Dev Immunol. 2012;2012:985646. doi:.https://doi.org/10.1155/2012/985646
- Abu Raya B, Srugo I, Kessel A, Peterman M, Bader D, Peri R, et al. The induction of breast milk pertussis specific antibodies following gestational tetanus-diphtheria-acellular pertussis vaccination. Vaccine. 2014;32(43):5632–7. Published online August 26, 2014. doi:.https://doi.org/10.1016/j.vaccine.2014.08.006
- Munoz FM, Englund JA, Cheesman CC, Maccato ML, Pinell PM, Nahm MH, et al. Maternal immunization with pneumococcal polysaccharide vaccine in the third trimester of gestation. Vaccine. 2001;20(5-6):826–37. Published online December 12, 2001. doi:.https://doi.org/10.1016/S0264-410X(01)00397-8
- Schlaudecker EP, Steinhoff MC, Omer SB, McNeal MM, Roy E, Arifeen SE, et al. IgA and neutralizing antibodies to influenza a virus in human milk: a randomized trial of antenatal influenza immunization. PLoS One. 2013;8(8):e70867. doi:.https://doi.org/10.1371/journal.pone.0070867
- Kourtis AP, Read JS, Jamieson DJ. Pregnancy and infection. N Engl J Med. 2014;370(23):2211–8. doi:.https://doi.org/10.1056/NEJMra1213566
- Pazos M, Sperling RS, Moran TM, Kraus TA. The influence of pregnancy on systemic immunity. Immunol Res. 2012;54(1-3):254–61. doi:.https://doi.org/10.1007/s12026-012-8303-9
- Robinson DP, Klein SL. Pregnancy and pregnancy-associated hormones alter immune responses and disease pathogenesis. Horm Behav. 2012;62(3):263–71. doi:.https://doi.org/10.1016/j.yhbeh.2012.02.023
- Medina KL, Smithson G, Kincade PW. Suppression of B lymphopoiesis during normal pregnancy. J Exp Med. 1993;178(5):1507–15. doi:.https://doi.org/10.1084/jem.178.5.1507
- Mertz D, Geraci J, Winkup J, Gessner BD, Ortiz JR, Loeb M. Pregnancy as a risk factor for severe outcomes from influenza virus infection: A systematic review and meta-analysis of observational studies. Vaccine. 2017;35(4):521–8. doi:.https://doi.org/10.1016/j.vaccine.2016.12.012
- Schlaudecker EP, McNeal MM, Dodd CN, Ranz JB, Steinhoff MC. Pregnancy modifies the antibody response to trivalent influenza immunization. J Infect Dis. 2012;206(11):1670–3. Published online September 18, 2012. doi:.https://doi.org/10.1093/infdis/jis592
- Sperling RS, Engel SM, Wallenstein S, Kraus TA, Garrido J, Singh T, et al. Immunogenicity of trivalent inactivated influenza vaccination received during pregnancy or postpartum. Obstet Gynecol. 2012;119(3):631–9. doi:.https://doi.org/10.1097/AOG.0b013e318244ed20
- Kay AW, Bayless NL, Fukuyama J, Aziz N, Dekker CL, Mackey S, et al. Pregnancy Does Not Attenuate the Antibody or Plasmablast Response to Inactivated Influenza Vaccine. J Infect Dis. 2015;212(6):861–70. doi:.https://doi.org/10.1093/infdis/jiv138
- Jamieson DJ, Kissin DM, Bridges CB, Rasmussen SA. Benefits of influenza vaccination during pregnancy for pregnant women. Am J Obstet Gynecol. 2012;207(3, Suppl):S17–20. doi:.https://doi.org/10.1016/j.ajog.2012.06.070
- Halperin BA, Morris A, Mackinnon-Cameron D, Mutch J, Langley JM, McNeil SA, et al. Kinetics of the antibody response to tetanus-diphtheria-acellular pertussis vaccine in women of childbearing age and postpartum women. Clin Infect Dis. 2011;53(9):885–92. Published online September 29, 2011. doi:.https://doi.org/10.1093/cid/cir538
- Munoz FM. Respiratory syncytial virus in infants: is maternal vaccination a realistic strategy? Curr Opin Infect Dis. 2015;28(3):221–4. doi:.https://doi.org/10.1097/QCO.0000000000000161
- Van Savage J, Decker MD, Edwards KM, Sell SH, Karzon DT. Natural history of pertussis antibody in the infant and effect on vaccine response. J Infect Dis. 1990;161(3):487–92. Published online March 01, 1990. doi:.https://doi.org/10.1093/infdis/161.3.487
- Gaunt G, Ramin K. Immunological tolerance of the human fetus. Am J Perinatol. 2001;18(6):299–312. doi:.https://doi.org/10.1055/s-2001-17861
- Pierce M, Kurinczuk JJ, Spark P, Brocklehurst P, Knight M ; UKOSS. Perinatal outcomes after maternal 2009/H1N1 infection: national cohort study. BMJ. 2011;342(jun14 2):d3214. doi:.https://doi.org/10.1136/bmj.d3214
- Steinhoff MC, Omer SB. A review of fetal and infant protection associated with antenatal influenza immunization. Am J Obstet Gynecol. 2012;207(3, Suppl):S21–7. doi:.https://doi.org/10.1016/j.ajog.2012.06.071
- Poehling KA, Edwards KM, Weinberg GA, Szilagyi P, Staat MA, Iwane MK, et al.; New Vaccine Surveillance Network. The underrecognized burden of influenza in young children. N Engl J Med. 2006;355(1):31–40. doi:.https://doi.org/10.1056/NEJMoa054869
- Bhat N, Wright JG, Broder KR, Murray EL, Greenberg ME, Glover MJ, et al.; Influenza Special Investigations Team. Influenza-associated deaths among children in the United States, 2003-2004. N Engl J Med. 2005;353(24):2559–67. doi:.https://doi.org/10.1056/NEJMoa051721
- Puck JM, Glezen WP, Frank AL, Six HR. Protection of infants from infection with influenza A virus by transplacentally acquired antibody. J Infect Dis. 1980;142(6):844–9. doi:.https://doi.org/10.1093/infdis/142.6.844
- Blanchard-Rohner G, Meier S, Bel M, Combescure C, Othenin-Girard V, Swali RA, et al. Influenza vaccination given at least 2 weeks before delivery to pregnant women facilitates transmission of seroprotective influenza-specific antibodies to the newborn. Pediatr Infect Dis J. 2013;32(12):1374–80. Published online September 26, 2013. doi:.https://doi.org/10.1097/01.inf.0000437066.40840.c4
- Chu HY, Englund JA. Maternal immunization. Clin Infect Dis. 2014;59(4):560–8. doi:.https://doi.org/10.1093/cid/ciu327
- Tapia MD, Sow SO, Tamboura B, Tégueté I, Pasetti MF, Kodio M, et al. Maternal immunisation with trivalent inactivated influenza vaccine for prevention of influenza in infants in Mali: a prospective, active-controlled, observer-blind, randomised phase 4 trial. Lancet Infect Dis. 2016;16(9):1026–35. doi:.https://doi.org/10.1016/S1473-3099(16)30054-8
- Madhi SA, Cutland CL, Kuwanda L, Weinberg A, Hugo A, Jones S, et al.; Maternal Flu Trial (Matflu) Team. Influenza vaccination of pregnant women and protection of their infants. N Engl J Med. 2014;371(10):918–31. doi:.https://doi.org/10.1056/NEJMoa1401480
- Omer SB. Maternal Immunization. N Engl J Med. 2017;376(13):1256–67. doi:.https://doi.org/10.1056/NEJMra1509044
- Blanchard-Rohner G, Siegrist CA. Vaccination during pregnancy to protect infants against influenza: why and why not? Vaccine. 2011;29(43):7542–50. Published online August 09, 2011. doi:.https://doi.org/10.1016/j.vaccine.2011.08.013
- Hviid A, Svanström H, Mølgaard-Nielsen D, Lambach P. Association Between Pandemic Influenza A(H1N1) Vaccination in Pregnancy and Early Childhood Morbidity in Offspring. JAMA Pediatr. 2017;171(3):239–48. doi:.https://doi.org/10.1001/jamapediatrics.2016.4023
- Burney LE. Influenza immunization: Statement. Public Health Rep. 1960;75(10):944. doi:.https://doi.org/10.2307/4590965
- Harper SA, Fukuda K, Uyeki TM, Cox NJ, Bridges CB ; Centers for Disease Control and Prevention (CDC) Advisory Committee on Immunization Practices (ACIP). Prevention and control of influenza: recommendations of the Advisory Committee on Immunization Practices (ACIP). MMWR Recomm Rep. 2004;53(RR-6):1–40.
- No authors listed. Influenza vaccines. Wkly Epidemiol Rec. 2005;80(33):279–87.
- Office fédéral de la santé publique, Commission fédérale pour les vaccinations: Plan de vaccination suisse 2017 – Directives et recommandations. Berne: Office fédéral de la santé publique; 2017.
- Jakinovich A, Sood SK. Pertussis: still a cause of death, seven decades into vaccination. Curr Opin Pediatr. 2014;26(5):597–604. doi:.https://doi.org/10.1097/MOP.0000000000000139
- Castagnini LA, Munoz FM. Clinical characteristics and outcomes of neonatal pertussis: a comparative study. J Pediatr. 2010;156(3):498–500. Published online January 09, 2010. doi:.https://doi.org/10.1016/j.jpeds.2009.10.013
- RTS [Internet]. La coqueluche, une maladie qui tue encore en Suisse. Le rendez-vous santé. [Cited 20 January 2016]. Available from: https://www.rts.ch/info/sciences-tech/7425630-la-coqueluche-une-maladie-qui-tue-encore-en-suisse.html.
- Centers for Disease Control and Prevention (CDC). Fatal case of unsuspected pertussis diagnosed from a blood culture--Minnesota, 2003. MMWR Morb Mortal Wkly Rep. 2004;53(6):131–2. Published online February 26, 2004.
- Suryadevara M, Domachowske JB. Prevention of pertussis through adult vaccination. Hum Vaccin Immunother. 2015;11(7):1744–7. doi:.https://doi.org/10.1080/21645515.2015.1038442
- Cornia PB, Hersh AL, Lipsky BA, Newman TB, Gonzales R. Does this coughing adolescent or adult patient have pertussis? JAMA. 2010;304(8):890–6. Published online August 26, 2010. doi:.https://doi.org/10.1001/jama.2010.1181
- Eberhardt CS, Siegrist CA. What Is Wrong with Pertussis Vaccine Immunity? Inducing and Recalling Vaccine-Specific Immunity. Cold Spring Harb Perspect Biol. 2017:a029629. [Epub ahead of print]. doi:.https://doi.org/10.1101/cshperspect.a029629
- Warfel JM, Edwards KM. Pertussis vaccines and the challenge of inducing durable immunity. Curr Opin Immunol. 2015;35:48–54. doi:.https://doi.org/10.1016/j.coi.2015.05.008
- Belloni C, De Silvestri A, Tinelli C, Avanzini MA, Marconi M, Strano F, et al. Immunogenicity of a three-component acellular pertussis vaccine administered at birth. Pediatrics. 2003;111(5 Pt 1):1042–5. Published online May 03, 2003. doi:.https://doi.org/10.1542/peds.111.5.1042
- Halasa NB, O’Shea A, Shi JR, LaFleur BJ, Edwards KM. Poor immune responses to a birth dose of diphtheria, tetanus, and acellular pertussis vaccine. J Pediatr. 2008;153(3):327–32. Published online June 07, 2008. doi:.https://doi.org/10.1016/j.jpeds.2008.03.011
- Knuf M, Schmitt HJ, Wolter J, Schuerman L, Jacquet JM, Kieninger D, et al. Neonatal vaccination with an acellular pertussis vaccine accelerates the acquisition of pertussis antibodies in infants. J Pediatr. 2008;152(5):655–60.e1. doi:.https://doi.org/10.1016/j.jpeds.2007.09.034
- Carcione D, Regan AK, Tracey L, Mak DB, Gibbs R, Dowse GK, et al. The impact of parental postpartum pertussis vaccination on infection in infants: A population-based study of cocooning in Western Australia. Vaccine. 2015;33(42):5654–61. Published online September 01, 2015. doi:.https://doi.org/10.1016/j.vaccine.2015.08.066
- Zhang Q, Yin Z, Li Y, Luo H, Shao Z, Gao Y, et al. Prevalence of asymptomatic Bordetella pertussis and Bordetella parapertussis infections among school children in China as determined by pooled real-time PCR: a cross-sectional study. Scand J Infect Dis. 2014;46(4):280–7. Published online February 14, 2014. doi:.https://doi.org/10.3109/00365548.2013.878034
- De Schutter I, Malfroot A, Dab I, Hoebrekx N, Muyldermans G, Piérard D, et al. Molecular typing of Bordetella pertussis isolates recovered from Belgian children and their household members. Clin Infect Dis. 2003;36(11):1391–6. Published online May 27, 2003. doi:.https://doi.org/10.1086/375071
- Centers for Disease Control and Prevention (CDC). Updated recommendations for use of tetanus toxoid, reduced diphtheria toxoid and acellular pertussis vaccine (Tdap) in pregnant women and persons who have or anticipate having close contact with an infant aged <12 months --- Advisory Committee on Immunization Practices (ACIP), 2011. MMWR Morb Mortal Wkly Rep. 2011;60(41):1424–6. Published online October 21, 2011.
- Centers for Disease Control and Prevention (CDC). Updated recommendations for use of tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis vaccine (Tdap) in pregnant women--Advisory Committee on Immunization Practices (ACIP), 2012. MMWR Morb Mortal Wkly Rep. 2013;62(7):131–5. Published online February 22, 2013.
- Department of Health UK. Pregnant Women to be offered whooping cough vaccination. [updated 28.09.20121 November 2015]. Available from: http://www.dh.gov.uk/health/2012/09/whooping-cough/.
- Kharbanda EO, Vazquez-Benitez G, Lipkind HS, Klein NP, Cheetham TC, Naleway A, et al. Evaluation of the association of maternal pertussis vaccination with obstetric events and birth outcomes. JAMA. 2014;312(18):1897–904. doi:.https://doi.org/10.1001/jama.2014.14825
- Shakib JH, Korgenski K, Sheng X, Varner MW, Pavia AT, Byington CL. Tetanus, diphtheria, acellular pertussis vaccine during pregnancy: pregnancy and infant health outcomes. J Pediatr. 2013;163(5):1422–6.e1, 4. doi:.https://doi.org/10.1016/j.jpeds.2013.06.021
- Zheteyeva YA, Moro PL, Tepper NK, Rasmussen SA, Barash FE, Revzina NV, et al. Adverse event reports after tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis vaccines in pregnant women. Am J Obstet Gynecol. 2012;207(1):59.e1–7. doi:.https://doi.org/10.1016/j.ajog.2012.05.006
- Villarreal Pérez JZ, Ramírez Aranda JM, de la O Cavazos M, Zamudio Osuna MJ, Perales Dávila J, Ballesteros Elizondo MR, et al. Randomized clinical trial of the safety and immunogenicity of the Tdap vaccine in pregnant Mexican women. Hum Vaccin Immunother. 2017;13(1):128–35. doi:.https://doi.org/10.1080/21645515.2016.1232786
- Talbot EA, Brown KH, Kirkland KB, Baughman AL, Halperin SA, Broder KR. The safety of immunizing with tetanus-diphtheria-acellular pertussis vaccine (Tdap) less than 2 years following previous tetanus vaccination: Experience during a mass vaccination campaign of healthcare personnel during a respiratory illness outbreak. Vaccine. 2010;28(50):8001–7. Published online September 30, 2010. doi:.https://doi.org/10.1016/j.vaccine.2010.09.034
- Willhite CC, Karyakina NA, Yokel RA, Yenugadhati N, Wisniewski TM, Arnold IM, et al. Systematic review of potential health risks posed by pharmaceutical, occupational and consumer exposures to metallic and nanoscale aluminum, aluminum oxides, aluminum hydroxide and its soluble salts. Crit Rev Toxicol. 2014;44(sup4, Suppl 4):1–80. doi:.https://doi.org/10.3109/10408444.2014.934439
- Amirthalingam G, Campbell H, Ribeiro S, Fry NK, Ramsay M, Miller E, et al. Sustained Effectiveness of the Maternal Pertussis Immunization Program in England 3 Years Following Introduction. Clin Infect Dis. 2016;63(suppl 4):S236–43. doi:.https://doi.org/10.1093/cid/ciw559
- Dabrera G, Amirthalingam G, Andrews N, Campbell H, Ribeiro S, Kara E, et al. A case-control study to estimate the effectiveness of maternal pertussis vaccination in protecting newborn infants in England and Wales, 2012-2013. Clin Infect Dis. 2015;60(3):333–7. doi:.https://doi.org/10.1093/cid/ciu821
- 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(1):3–8. doi:.https://doi.org/10.1093/cid/ciw634
- Eberhardt CS, Blanchard-Rohner G, Lemaître B, Boukrid M, Combescure C, Othenin-Girard V, et al. Maternal Immunization Earlier in Pregnancy Maximizes Antibody Transfer and Expected Infant Seropositivity Against Pertussis. Clin Infect Dis. 2016;62(7):829–36. doi:.https://doi.org/10.1093/cid/ciw027
- Eberhardt CS, Blanchard-Rohner G, Lemaître B, Combescure C, Othenin-Girard V, Chilin A, et al. Pertussis Antibody Transfer to Preterm Neonates After Second- Versus Third-Trimester Maternal Immunization. Clin Infect Dis. 2017;64(8):1129–32. doi:.https://doi.org/10.1093/cid/cix046
- Munoz FM, Bond NH, Maccato M, Pinell P, Hammill HA, Swamy GK, et al. Safety and immunogenicity of tetanus diphtheria and acellular pertussis (Tdap) immunization during pregnancy in mothers and infants: a randomized clinical trial. JAMA. 2014;311(17):1760–9. doi:.https://doi.org/10.1001/jama.2014.3633
- Maertens K, Caboré RN, Huygen K, Vermeiren S, Hens N, Van Damme P, et al. Pertussis vaccination during pregnancy in Belgium: Follow-up of infants until 1 month after the fourth infant pertussis vaccination at 15 months of age. Vaccine. 2016;34(31):3613–9. doi:.https://doi.org/10.1016/j.vaccine.2016.04.066
- Maertens K, Hoang TT, Nguyen TD, Caboré RN, Duong TH, Huygen K, et al. The Effect of Maternal Pertussis Immunization on Infant Vaccine Responses to a Booster Pertussis-Containing Vaccine in Vietnam. Clin Infect Dis. 2016;63(suppl 4):S197–204. doi:.https://doi.org/10.1093/cid/ciw551
- Hardy-Fairbanks AJ, Pan SJ, Decker MD, Johnson DR, Greenberg DP, Kirkland KB, et al. Immune responses in infants whose mothers received Tdap vaccine during pregnancy. Pediatr Infect Dis J. 2013;32(11):1257–60. doi:.https://doi.org/10.1097/INF.0b013e3182a09b6a