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Meta-Analysis
. 2018 Feb 1;2(2):CD001269.
doi: 10.1002/14651858.CD001269.pub6.

Vaccines for preventing influenza in healthy adults

Vittorio Demicheli  1 , Tom Jefferson, Eliana Ferroni, Alessandro Rivetti, Carlo Di Pietrantonj
Affiliations
Meta-Analysis

Vaccines for preventing influenza in healthy adults

Vittorio Demicheli et al. Cochrane Database Syst Rev. .

Abstract

Background: The consequences of influenza in adults are mainly time off work. Vaccination of pregnant women is recommended internationally. This is an update of a review published in 2014. Future updates of this review will be made only when new trials or vaccines become available. Observational data included in previous versions of the review have been retained for historical reasons but have not been updated due to their lack of influence on the review conclusions.

Objectives: To assess the effects (efficacy, effectiveness, and harm) of vaccines against influenza in healthy adults, including pregnant women.

Search methods: We searched the Cochrane Central Register of Controlled Trials (CENTRAL; 2016, Issue 12), MEDLINE (January 1966 to 31 December 2016), Embase (1990 to 31 December 2016), the WHO International Clinical Trials Registry Platform (ICTRP; 1 July 2017), and ClinicalTrials.gov (1 July 2017), as well as checking the bibliographies of retrieved articles.

Selection criteria: Randomised controlled trials (RCTs) or quasi-RCTs comparing influenza vaccines with placebo or no intervention in naturally occurring influenza in healthy individuals aged 16 to 65 years. Previous versions of this review included observational comparative studies assessing serious and rare harms cohort and case-control studies. Due to the uncertain quality of observational (i.e. non-randomised) studies and their lack of influence on the review conclusions, we decided to update only randomised evidence. The searches for observational comparative studies are no longer updated.

Data collection and analysis: Two review authors independently assessed trial quality and extracted data. We rated certainty of evidence for key outcomes (influenza, influenza-like illness (ILI), hospitalisation, and adverse effects) using GRADE.

Main results: We included 52 clinical trials of over 80,000 people assessing the safety and effectiveness of influenza vaccines. We have presented findings from 25 studies comparing inactivated parenteral influenza vaccine against placebo or do-nothing control groups as the most relevant to decision-making. The studies were conducted over single influenza seasons in North America, South America, and Europe between 1969 and 2009. We did not consider studies at high risk of bias to influence the results of our outcomes except for hospitalisation.Inactivated influenza vaccines probably reduce influenza in healthy adults from 2.3% without vaccination to 0.9% (risk ratio (RR) 0.41, 95% confidence interval (CI) 0.36 to 0.47; 71,221 participants; moderate-certainty evidence), and they probably reduce ILI from 21.5% to 18.1% (RR 0.84, 95% CI 0.75 to 0.95; 25,795 participants; moderate-certainty evidence; 71 healthy adults need to be vaccinated to prevent one of them experiencing influenza, and 29 healthy adults need to be vaccinated to prevent one of them experiencing an ILI). The difference between the two number needed to vaccinate (NNV) values depends on the different incidence of ILI and confirmed influenza among the study populations. Vaccination may lead to a small reduction in the risk of hospitalisation in healthy adults, from 14.7% to 14.1%, but the CI is wide and does not rule out a large benefit (RR 0.96, 95% CI 0.85 to 1.08; 11,924 participants; low-certainty evidence). Vaccines may lead to little or no small reduction in days off work (-0.04 days, 95% CI -0.14 days to 0.06; low-certainty evidence). Inactivated vaccines cause an increase in fever from 1.5% to 2.3%.We identified one RCT and one controlled clinical trial assessing the effects of vaccination in pregnant women. The efficacy of inactivated vaccine containing pH1N1 against influenza was 50% (95% CI 14% to 71%) in mothers (NNV 55), and 49% (95% CI 12% to 70%) in infants up to 24 weeks (NNV 56). No data were available on efficacy against seasonal influenza during pregnancy. Evidence from observational studies showed effectiveness of influenza vaccines against ILI in pregnant women to be 24% (95% CI 11% to 36%, NNV 94), and against influenza in newborns from vaccinated women to be 41% (95% CI 6% to 63%, NNV 27).Live aerosol vaccines have an overall effectiveness corresponding to an NNV of 46. The performance of one- or two-dose whole-virion 1968 to 1969 pandemic vaccines was higher (NNV 16) against ILI and (NNV 35) against influenza. There was limited impact on hospitalisations in the 1968 to 1969 pandemic (NNV 94). The administration of both seasonal and 2009 pandemic vaccines during pregnancy had no significant effect on abortion or neonatal death, but this was based on observational data sets.

Authors' conclusions: Healthy adults who receive inactivated parenteral influenza vaccine rather than no vaccine probably experience less influenza, from just over 2% to just under 1% (moderate-certainty evidence). They also probably experience less ILI following vaccination, but the degree of benefit when expressed in absolute terms varied across different settings. Variation in protection against ILI may be due in part to inconsistent symptom classification. Certainty of evidence for the small reductions in hospitalisations and time off work is low. Protection against influenza and ILI in mothers and newborns was smaller than the effects seen in other populations considered in this review.Vaccines increase the risk of a number of adverse events, including a small increase in fever, but rates of nausea and vomiting are uncertain. The protective effect of vaccination in pregnant women and newborns is also very modest. We did not find any evidence of an association between influenza vaccination and serious adverse events in the comparative studies considered in this review. Fifteen included RCTs were industry funded (29%).

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Conflict of interest statement

Vittorio Demicheli: none known

Tom Jefferson (TJ) was a co‐recipient of a UK National Institute for Health Research grant (HTA – 10/80/01 Update and amalgamation of two Cochrane Reviews: neuraminidase inhibitors for preventing and treating influenza in healthy adults and children (www.nets.nihr.ac.uk/projects/hta/108001)). TJ receives royalties from his books published by Blackwells and Il Pensiero Scientifico Editore, Rome. TJ is occasionally interviewed by market research companies for anonymous interviews about phase I or II pharmaceutical products. In 2011 to 2013, TJ acted as an expert witness in a litigation case related to oseltamivir phosphate (Tamiflu; Roche) and in a labour case on influenza vaccines in healthcare workers in Canada. TJ acted as a consultant for Roche (1997‐99), GSK (2001‐2), and Sanofi‐Synthelabo (2003) for the antirhinoviral pleconaril, which was not approved by the US Food and Drug Administration. TJ was a consultant for IMS Health in 2013, and in 2014 he was retained as a scientific adviser to a legal team acting on the drug oseltamivir (Tamiflu; Roche). In 2014 to 2015, TJ was a member of two advisory boards for Boerhinger and is in receipt of a Cochrane Methods Innovations Fund grant to develop guidance on the use of regulatory data in Cochrane Reviews. TJ has a potential financial conflict of interest in the investigation of the drug oseltamivir. TJ acted as an expert witness in a legal case involving the drug oseltamivir (Roche) and the vaccine Pandemrix (GSK). TJ was a member of an Independent Data Monitoring Committee for a Sanofi Pasteur clinical trial.

Eliana Ferroni: none known

Alessandro Rivetti: none known

Carlo Di Pietrantonj: none known

Figures

1
1
Study flow diagram.
2
2
'Risk of bias' graph: review authors' judgements about each risk of bias item presented as percentages across all included studies.
3
3
'Risk of bias' summary: review authors' judgements about each risk of bias item for each included study.
1.1
1.1. Analysis
Comparison 1 Inactivated parenteral influenza vaccine versus placebo or 'do nothing', Outcome 1 Influenza.
1.2
1.2. Analysis
Comparison 1 Inactivated parenteral influenza vaccine versus placebo or 'do nothing', Outcome 2 Influenza‐like illness.
1.3
1.3. Analysis
Comparison 1 Inactivated parenteral influenza vaccine versus placebo or 'do nothing', Outcome 3 Physician visits.
1.4
1.4. Analysis
Comparison 1 Inactivated parenteral influenza vaccine versus placebo or 'do nothing', Outcome 4 Days ill.
1.5
1.5. Analysis
Comparison 1 Inactivated parenteral influenza vaccine versus placebo or 'do nothing', Outcome 5 Times any drugs were prescribed.
1.6
1.6. Analysis
Comparison 1 Inactivated parenteral influenza vaccine versus placebo or 'do nothing', Outcome 6 Times antibiotic was prescribed.
1.7
1.7. Analysis
Comparison 1 Inactivated parenteral influenza vaccine versus placebo or 'do nothing', Outcome 7 Working days lost.
1.8
1.8. Analysis
Comparison 1 Inactivated parenteral influenza vaccine versus placebo or 'do nothing', Outcome 8 Hospitalisations.
1.9
1.9. Analysis
Comparison 1 Inactivated parenteral influenza vaccine versus placebo or 'do nothing', Outcome 9 Clinical cases (clinically defined without clear definition).
1.10
1.10. Analysis
Comparison 1 Inactivated parenteral influenza vaccine versus placebo or 'do nothing', Outcome 10 Local harms.
1.11
1.11. Analysis
Comparison 1 Inactivated parenteral influenza vaccine versus placebo or 'do nothing', Outcome 11 Systemic harms.
2.1
2.1. Analysis
Comparison 2 Live aerosol influenza vaccine versus placebo or 'do nothing', Outcome 1 Influenza.
2.2
2.2. Analysis
Comparison 2 Live aerosol influenza vaccine versus placebo or 'do nothing', Outcome 2 Influenza‐like illness.
2.3
2.3. Analysis
Comparison 2 Live aerosol influenza vaccine versus placebo or 'do nothing', Outcome 3 Influenza cases (clinically defined without clear definition).
2.4
2.4. Analysis
Comparison 2 Live aerosol influenza vaccine versus placebo or 'do nothing', Outcome 4 Local harms.
2.5
2.5. Analysis
Comparison 2 Live aerosol influenza vaccine versus placebo or 'do nothing', Outcome 5 Systemic harms.
3.1
3.1. Analysis
Comparison 3 Inactivated aerosol influenza vaccine versus placebo or 'do nothing', Outcome 1 Influenza.
3.2
3.2. Analysis
Comparison 3 Inactivated aerosol influenza vaccine versus placebo or 'do nothing', Outcome 2 Local harms.
3.3
3.3. Analysis
Comparison 3 Inactivated aerosol influenza vaccine versus placebo or 'do nothing', Outcome 3 Systemic harms.
4.1
4.1. Analysis
Comparison 4 Inactivated parenteral influenza vaccine versus placebo or 'do nothing' administered during pregnancy, Outcome 1 Influenza in mothers.
4.2
4.2. Analysis
Comparison 4 Inactivated parenteral influenza vaccine versus placebo or 'do nothing' administered during pregnancy, Outcome 2 Influenza‐like illness in mothers.
4.3
4.3. Analysis
Comparison 4 Inactivated parenteral influenza vaccine versus placebo or 'do nothing' administered during pregnancy, Outcome 3 Influenza in newborn.
4.4
4.4. Analysis
Comparison 4 Inactivated parenteral influenza vaccine versus placebo or 'do nothing' administered during pregnancy, Outcome 4 Influenza‐like illness in newborn.
5.1
5.1. Analysis
Comparison 5 Inactivated parenteral influenza vaccine versus placebo ‐ cohort studies, Outcome 1 Seasonal inactivated vaccine effectiveness in mothers ‐ pregnant women.
5.2
5.2. Analysis
Comparison 5 Inactivated parenteral influenza vaccine versus placebo ‐ cohort studies, Outcome 2 Seasonal inactivated vaccine effectiveness in newborns ‐ pregnant women.
5.3
5.3. Analysis
Comparison 5 Inactivated parenteral influenza vaccine versus placebo ‐ cohort studies, Outcome 3 Seasonal inactivated vaccine effectiveness in newborns ‐ pregnant women.
5.4
5.4. Analysis
Comparison 5 Inactivated parenteral influenza vaccine versus placebo ‐ cohort studies, Outcome 4 H1N1 vaccine ‐ safety ‐ pregnancy‐related outcomes ‐ pregnant women.
5.5
5.5. Analysis
Comparison 5 Inactivated parenteral influenza vaccine versus placebo ‐ cohort studies, Outcome 5 Seasonal vaccine ‐ safety ‐ pregnancy‐related outcomes ‐ pregnant women.
5.6
5.6. Analysis
Comparison 5 Inactivated parenteral influenza vaccine versus placebo ‐ cohort studies, Outcome 6 Seasonal vaccine containing H1N1.
6.1
6.1. Analysis
Comparison 6 Inactivated parenteral influenza vaccine versus placebo ‐ case‐control studies, Outcome 1 Effectiveness in newborns ‐ pregnant women (adjusted data).
6.2
6.2. Analysis
Comparison 6 Inactivated parenteral influenza vaccine versus placebo ‐ case‐control studies, Outcome 2 Seasonal vaccine safety ‐ pregnancy‐related outcomes (adjusted data).
7.1
7.1. Analysis
Comparison 7 Serious adverse events: Guillain‐Barré syndrome ‐ cohort studies, Outcome 1 Seasonal influenza vaccination and Guillain‐Barré syndrome.
8.1
8.1. Analysis
Comparison 8 Serious adverse events: Guillain‐Barré syndrome ‐ case‐control studies, Outcome 1 2009 to 2010 A/H1N1 ‐ general population (unadjusted data).
8.2
8.2. Analysis
Comparison 8 Serious adverse events: Guillain‐Barré syndrome ‐ case‐control studies, Outcome 2 2009 to 2010 A/H1N1 ‐ general population (adjusted data).
8.3
8.3. Analysis
Comparison 8 Serious adverse events: Guillain‐Barré syndrome ‐ case‐control studies, Outcome 3 Seasonal influenza vaccination general population (adjusted data).
9.1
9.1. Analysis
Comparison 9 Serious adverse events: demyelinating diseases (multiple sclerosis, optic neuritis) ‐ cohort studies, Outcome 1 Influenza vaccination (seasonal) ‐ demyelinating diseases (unadjusted data).
9.2
9.2. Analysis
Comparison 9 Serious adverse events: demyelinating diseases (multiple sclerosis, optic neuritis) ‐ cohort studies, Outcome 2 Influenza vaccination (H1N1) ‐ demyelinating diseases (unadjusted).
10.1
10.1. Analysis
Comparison 10 Serious adverse events: demyelinating diseases (multiple sclerosis, optic neuritis) ‐ case‐control studies, Outcome 1 Influenza vaccination (seasonal) ‐ general population ‐ demyelinating diseases (unadjusted data).
10.2
10.2. Analysis
Comparison 10 Serious adverse events: demyelinating diseases (multiple sclerosis, optic neuritis) ‐ case‐control studies, Outcome 2 Influenza vaccination (seasonal) ‐ general population ‐ multiple sclerosis (adjusted data).
10.3
10.3. Analysis
Comparison 10 Serious adverse events: demyelinating diseases (multiple sclerosis, optic neuritis) ‐ case‐control studies, Outcome 3 Influenza vaccination (seasonal) ‐ general population ‐ optic neuritis (adjusted data).
11.1
11.1. Analysis
Comparison 11 Serious adverse events: immune thrombocytopenic purpura ‐ cohort studies, Outcome 1 Seasonal influenza vaccine ‐ HR (adjusted data).
11.2
11.2. Analysis
Comparison 11 Serious adverse events: immune thrombocytopenic purpura ‐ cohort studies, Outcome 2 Seasonal influenza vaccine (unadjusted data).
12.1
12.1. Analysis
Comparison 12 Serious adverse events: immune thrombocytopenic purpura ‐ case‐control studies, Outcome 1 Seasonal influenza vaccine ‐ general population (adjusted data).
12.2
12.2. Analysis
Comparison 12 Serious adverse events: immune thrombocytopenic purpura ‐ case‐control studies, Outcome 2 Seasonal influenza vaccine ‐ general population (unadjusted data).
13.1
13.1. Analysis
Comparison 13 1968 to 1969 pandemic: inactivated polyvalent parenteral influenza vaccine versus placebo, Outcome 1 Influenza‐like illness.
13.2
13.2. Analysis
Comparison 13 1968 to 1969 pandemic: inactivated polyvalent parenteral influenza vaccine versus placebo, Outcome 2 Influenza.
13.3
13.3. Analysis
Comparison 13 1968 to 1969 pandemic: inactivated polyvalent parenteral influenza vaccine versus placebo, Outcome 3 Hospitalisations.
13.4
13.4. Analysis
Comparison 13 1968 to 1969 pandemic: inactivated polyvalent parenteral influenza vaccine versus placebo, Outcome 4 Pneumonia.
14.1
14.1. Analysis
Comparison 14 1968 to 1969 pandemic: inactivated monovalent parenteral influenza vaccine versus placebo, Outcome 1 Influenza‐like illness.
14.2
14.2. Analysis
Comparison 14 1968 to 1969 pandemic: inactivated monovalent parenteral influenza vaccine versus placebo, Outcome 2 Influenza.
14.3
14.3. Analysis
Comparison 14 1968 to 1969 pandemic: inactivated monovalent parenteral influenza vaccine versus placebo, Outcome 3 Hospitalisations.
14.4
14.4. Analysis
Comparison 14 1968 to 1969 pandemic: inactivated monovalent parenteral influenza vaccine versus placebo, Outcome 4 Pneumonia.
14.5
14.5. Analysis
Comparison 14 1968 to 1969 pandemic: inactivated monovalent parenteral influenza vaccine versus placebo, Outcome 5 Working days lost.
14.6
14.6. Analysis
Comparison 14 1968 to 1969 pandemic: inactivated monovalent parenteral influenza vaccine versus placebo, Outcome 6 Days ill.
15.1
15.1. Analysis
Comparison 15 1968 to 1969 pandemic: inactivated polyvalent aerosol influenza vaccine versus placebo, Outcome 1 Influenza‐like illness.
16.1
16.1. Analysis
Comparison 16 1968 to 1969 pandemic: inactivated monovalent aerosol influenza vaccine versus placebo, Outcome 1 Influenza‐like illness.
17.1
17.1. Analysis
Comparison 17 1968 to 1969 pandemic: live aerosol influenza vaccine versus placebo, Outcome 1 Influenza cases (clinically defined without clear definition).
17.2
17.2. Analysis
Comparison 17 1968 to 1969 pandemic: live aerosol influenza vaccine versus placebo, Outcome 2 Complications (bronchitis, otitis, pneumonia).
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References

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aa Waldman 1972b {published data only}
    1. Waldman RH, Coggins WJ. Influenza immunization: field trial on a university campus. Journal of Infectious Diseases 1972;126(3):242‐8. - PubMed
aa Waldman 1972c {published data only}
    1. Waldman RH, Coggins WJ. Influenza immunization: field trial on a university campus. Journal of Infectious Diseases 1972;126(3):242‐8. - PubMed
aa Waldman 1972d {published data only}
    1. Waldman RH, Coggins WJ. Influenza immunization: field trial on a university campus. Journal of Infectious Diseases 1972;126(3):242‐8. - PubMed
aa Weingarten 1988 {published data only}
    1. Weingarten S, Staniloff H, Ault M, Miles P, Bamberger M, Meyer RD. Do hospital employees benefit from the influenza vaccine?. Journal of General Internal Medicine 1988;3(1):32‐7. - PubMed
aa Zhilova 1986a {published data only}
    1. Zhilova GP, Ignat'eva GS, Orlov VA, Malikova EV, Maksakova VL. Results of a study of the effectiveness of simultaneous immunization against influenza with live and inactivated vaccines (1980 ‐ 1983). Voprosy Virusologii 1986;31(1):40‐4. - PubMed
aa Zhilova 1986b {published data only}
    1. Zhilova GP, Ignat'eva GS, Orlov VA, Malikova EV, Maksakova VL. Results of a study of the effectiveness of simultaneous immunization against influenza with live and inactivated vaccines (1980 ‐ 1983). Voprosy Virusologii 1986;31(1):40‐4. - PubMed
ab Atmar 1990 {published data only}
    1. Atmar RL, Bloom K, Keitel W, Couch RB, Greenberg SB. Effect of live attenuated, cold recombinant (CR) influenza virus vaccines on pulmonary function in healthy and asthmatic adults. Vaccine 1990;8(3):217‐24. - PubMed
ab Betts 1977a {published data only}
    1. Betts RF, Douglas RG Jr, Roth FK, Little JW 3rd. Efficacy of live attenuated influenza A/Scotland/74 (H3N2) virus vaccine against challenge with influenza A/Victoria/3/75 (H3N2) virus. Journal of Infectious Diseases 1977;136(6):746‐53. - PubMed
ab Boyce 2000 {published data only}
    1. Boyce TG, Hsu HH, Sannella EC, Coleman‐Dockery SD, Baylis E, Zhu Y, et al. Safety and immunogenicity of adjuvanted and unadjuvanted subunit influenza vaccines administered intranasally to healthy adults. Vaccine 2000;19(2‐3):217‐26. - PubMed
ab Caplan 1977 {published data only}
    1. Caplan ES, Hughes TP, O'Donnel S, Levine MM, Hornick RB. Reactogenicity and immunogenicity of parenteral monovalent influenza A/Victoria/3/75 (H3N2) virus vaccine in healthy adults. Journal of Infectious Diseases 1977;136(Suppl):484‐90. - PubMed
ab El'shina 1996 {published data only}
    1. El'shina GA, Masalin IM, Shervali VI, Gorbunov MA, Lonskaia NI, Agafonova LV, et al. The trivalent polymer‐subunit influenza vaccine Grippol studied in a controlled epidemiological trial. Voenno‐Meditsinskii Zhurnal 1996;317(8):57‐60. - PubMed
ab Evans 1976 {published data only}
    1. Evans AE, Letley E, Ferris RD, Freestone DS. WRL 105 strain live attenuated influenza vaccine; comparison of one and two dose schedules. Journal of Hygiene 1976;77(3):327‐32. - PMC - PubMed
ab Forsyth 1967 {published data only}
    1. Forsyth JR. An assessment of oil adjuvant and aqueous influenza vaccines. I. Reactions to the vaccines. Journal of Hygiene 1967;65(4):485‐95. - PMC - PubMed
ab Goodeve 1983 {published data only}
    1. Goodeve A, Potter CW, Clark A, Jennings R, Schild GC, Yetts R. A graded‐dose study of inactivated, surface antigen influenza B vaccine in volunteers: reactogenicity, antibody response and protection to challenge virus infection. Journal of Hygiene 1983;90(1):107‐15. - PMC - PubMed
ab Hrabar 1977 {published data only}
    1. Hrabar A, Vodopija I, Andre FE, Mitchell JR, Maassab HF, Hennessy AV, et al. A placebo‐controlled dose‐response study of the reactogenicity and immunogenicity of a cold‐adapted recombinant A/Victoria/3/75 (H3N2) live influenza virus candidate vaccine in healthy volunteers. Developments in Biological Standardization 1977;39:53‐60. - PubMed
ab Keitel 1993a {published data only}
    1. Keitel WA, Couch RB, Quarles JM, Cate TR, Baxter B, Maassab HF. Trivalent attenuated cold‐adapted influenza virus vaccine: reduced viral shedding and serum antibody responses in susceptible adults. Journal of Infectious Diseases 1993;167(2):305‐11. - PubMed
ab Keitel 1993b {published data only}
    1. Keitel WA, Couch RB, Quarles JM, Cate TR, Baxter B, Maassab HF. Trivalent attenuated cold‐adapted influenza virus vaccine: reduced viral shedding and serum antibody responses in susceptible adults. Journal of Infectious Diseases 1993;167(2):305‐11. - PubMed
ab Langley 2005 {published data only}
    1. Langley JM, Halperin SA, McNeil S, Smith B, Jones T, Burt D, et al. Safety and immunogenicity of a Proteosome‐trivalent inactivated influenza vaccine, given nasally to healthy adults. Vaccine 2005;24(10):1601‐8. - PubMed
ab Lauteria 1974 {published data only}
    1. Lauteria SF, Kantzler GB, High PC, Lee JD, Waldman RH. An attenuated influenza virus vaccine: reactogenicity, transmissibility, immunogenicity, and protective efficacy. Journal of Infectious Diseases 1974;130(4):380‐3. - PubMed
ab Miller 1977 {published data only}
    1. Miller LW, Togo Y, Hornick RB. Clinical and serologic effects of live attenuated serum inhibitor‐resistant influenza B vaccine in seronegative adults. Journal of Medical Virology 1977;1(3):193‐9. - PubMed
ab Pyrhönen 1981 {published data only}
    1. Pyrhönen S, Suni J, Romo M. Clinical trial of a subunit influenza vaccine. Scandinavian Journal of Infectious Diseases 1981;13:95‐9. - PubMed
ab Reeve 1982 {published data only}
    1. Reeve P, Pibermann M, Bachmayer H, Liehl E, Moritz A, Ganzinger U, et al. Studies in man with a cold‐recombinant live influenza B virus vaccine. Journal of Medical Virology 1982;9(1):1‐9. - PubMed
ab Rocchi 1979a {published data only}
    1. Rocchi G, Ragona G, Piga C, Pelosio A, Volpi A, Vella S, et al. Influenza vaccination with live‐attenuated and inactivated virus‐vaccines during an outbreak of disease. Journal of Hygiene 1979;83(3):383‐90. - PMC - PubMed
ab Rocchi 1979b {published data only}
    1. Rocchi G, Ragona G, Piga C, Pelosio A, Volpi A, Vella S, et al. Influenza vaccination with live‐attenuated and inactivated virus‐vaccines during an outbreak of disease. Journal of Hygiene 1979;83(3):383‐90. - PMC - PubMed
ab Saxen 1999 {published data only}
    1. Saxen H, Virtanen M. Randomized, placebo‐controlled double blind study on the efficacy of influenza immunization on absenteeism of health care workers. Pediatric Infectious Disease Journal 1999;18(9):779‐83. - PubMed
ab Scheifele 2003 {published data only}
    1. Scheifele DW, Duval B, Russell ML, Warrington R, DeSerres G, Skowronski DM, et al. Ocular and respiratory symptoms attributable to inactivated split influenza vaccine: evidence from a controlled trial involving adults. Clinical Infectious Diseases 2003;36(7):850‐7. - PubMed
ab Spencer 1977 {published data only}
    1. Spencer MJ, Cherry JD, Powell KR. Clinical trial with "R‐75" strain live, attenuated, serum inhibitor‐resistant intranasal influenza B vaccine. Journal of Clinical Microbiology 1977;5(6):584‐7. - PMC - PubMed
bb Dauvilliers 2013 {published data only}
    1. Dauvilliers Y, Arnulf I, Lecendreux M, Monaca Charley C, Franco P, Drouot X, et al. Increased risk of narcolepsy in children and adults after pandemic H1N1 vaccination in France. Brain 2013;139(Pt 8):2486‐96. - PubMed
bb DeStefano 2003 {published data only}
    1. DeStefano F, Verstraeten T, Jackson LA, Okoro CA, Benson P, Black SB, et al. Vaccinations and risk of central nervous system demyelinating diseases in adults. Archives of Neurology 2003;60(4):504‐9. - PubMed
bb Dieleman 2011a {published data only}
    1. Dieleman J, Romio S, Johansen K, Weibel D, Bonhoeffer J, Sturkenboom M, et al. Guillain‐Barré syndrome and adjuvanted pandemic influenza A (H1N1) 2009 vaccine: multinational case‐control study in Europe. BMJ 2012;343:d3908. - PMC - PubMed
bb Dieleman 2011b {published data only}
    1. Dieleman J, Romio S, Johansen K, Weibel D, Bonhoeffer J, Sturkenboom M, et al. Guillain‐Barré syndrome and adjuvanted pandemic influenza A (H1N1) 2009 vaccine: multinational case‐control study in Europe. BMJ 2012;343:d3908. - PMC - PubMed
bb Dieleman 2011c {published data only}
    1. Dieleman J, Romio S, Johansen K, Weibel D, Bonhoeffer J, Sturkenboom M, et al. Guillain‐Barré syndrome and adjuvanted pandemic influenza A (H1N1) 2009 vaccine: multinational case‐control study in Europe. BMJ 2012;343:d3908. - PMC - PubMed
bb Dieleman 2011d {published data only}
    1. Dieleman J, Romio S, Johansen K, Weibel D, Bonhoeffer J, Sturkenboom M, et al. Guillain‐Barré syndrome and adjuvanted pandemic influenza A (H1N1) 2009 vaccine: multinational case‐control study in Europe. BMJ 2012;343:d3908. - PMC - PubMed
bb Dieleman 2011e {published data only}
    1. Dieleman J, Romio S, Johansen K, Weibel D, Bonhoeffer J, Sturkenboom M, et al. Guillain‐Barré syndrome and adjuvanted pandemic influenza A (H1N1) 2009 vaccine: multinational case‐control study in Europe. BMJ 2012;343:d3908. - PMC - PubMed
bb Galeotti 2013 {published data only}
    1. Galeotti F, Massari M, D'Alessandro R, Beghi E, Chiò A, Logroscino G, et al. Risk of Guillain‐Barré syndrome after 2010‐2011 influenza vaccination. European Journal of Epidemiology 2013;28(5):433‐44. - PMC - PubMed
bb Garbe 2012 {published data only}
    1. Garbe E, Andersohn F, Bronder E, Klimpel A, Thomae M, Kurtal H. Association between drug use and acute immune thrombocytopenia in adults: results from the Berlin case‐control surveillance study. Pharmacoepidemiology and Drug Safety 2011;20:S147.
    1. Garbe E, Andersohn F, Bronder E, Salama A, Klimpel A, Thomae M, et al. Drug‐induced immune thrombocytopaenia: results from the Berlin Case‐Control Surveillance Study. European Journal of Clinical Pharmacology 2012;68(5):821‐32. - PubMed
bb Grimaldi‐Bensouda 2011 {published data only}
    1. Grimaldi‐Bensouda L, Alpérovitch A, Besson G, Vial C, Cuisset JM, Papeix C, et al. Guillain‐Barre syndrome, influenzalike illnesses, and influenza vaccination during seasons with and without circulating A/H1N1 viruses. American Journal of Epidemiology 2011;174(3):326‐35. - PubMed
bb Grimaldi‐Bensouda 2012 {published data only}
    1. Grimaldi‐Bensouda L, Michel M, Aubrun E, Leighton P, Viallard JF, Adoue D, et al. A case‐control study to assess the risk of immune thrombocytopenia associated with vaccines. Blood 2012;120(25):4938‐44. - PubMed
    1. Grimaldi‐Bensouda L, Michel M, Viallard J‐F, Adoue D, Magy‐Bertrand N, Khellaf M, et al. A multicenter case‐control prospective study to assess the risk of immune thrombocytopenia (ITP) associated with vaccines in adults using the PGRx‐ITP registry. Blood 2011;118(21):1169.
bb Hernan 2004 {published data only}
    1. Hernan MA, Jick SS, Olek MJ, Jick H. Recombinant hepatitis B vaccine and the risk of multiple sclerosis: a prospective study. Neurology 2004;63(5):838‐42. - PubMed
bb MacIntyre 2013 {published data only}
    1. MacIntyre CR, Heywood AE, Kovoor P, Ridda I, Seale H, Tan T, et al. Ischaemic heart disease, influenza and influenza vaccination: a prospective case control study. Heart 2013;99(24):1843‐8. - PMC - PubMed
bb Mastrangelo 2000 {published data only}
    1. Mastrangelo G, Rossi CR, Pfahlberg A, Marzia V, Barba A, Baldo M, et al. Is there a relationship between influenza vaccinations and risk of melanoma? A population‐based case‐control study. European Journal of Epidemiology 2000;16(9):777‐82. - PubMed
bb Mutsch 2004 {published data only}
    1. Mutsch M, Zhou W, Rhodes P, Bopp M, Chen RT, Linder T, et al. Use of the inactivated intranasal influenza vaccine and the risk of Bell's palsy in Switzerland. New England Journal of Medicine 2004;350(9):896‐903. - PubMed
bb Payne 2006 {published data only}
    1. Payne DC, Rose CE Jr, Kerrison J, Aranas A, Duderstadt S, McNeil MM. Anthrax vaccination and risk of optic neuritis in the United States military, 1998‐2003. Archives of Neurology 2006;63(6):871‐5. - PubMed
bb Ray 2011 {published data only}
    1. Ray P, Black S, Shinefield H, Dillon A, Carpenter D, Lewis E, et al. Vaccine Safety Datalink Team. Risk of rheumatoid arthritis following vaccination with tetanus, influenza and hepatitis B vaccines among persons 15‐59 years of age. Vaccine 2011;29(38):6592‐7. - PubMed
bb Rouleau 2014 {published data only}
    1. Rouleau I, Serres G, Skowronski DM, Drolet JP, Lemire C, Toth E, et al. Risk factors associated with anaphylaxis and other allergic‐like events following receipt of 2009 monovalent AS03‐adjuvanted pandemic influenza vaccine in Quebec, Canada. Vaccine 2014;32(28):3480‐7. - PubMed
bb Siscovick 2000 {published data only}
    1. Siscovick DS, Raghunathan TE, Lin D, Weinmann S, Arbogast P, Lemaitre RN, et al. Influenza vaccination and the risk of primary cardiac arrest. American Journal of Epidemiology 2000;152(7):674‐7. - PubMed
bb Zorzon 2003 {published data only}
    1. Zorzon M, Zivadinov R, Nasuelli D, Dolfini P, Bosco A, Bratina A, et al. Risk factors of multiple sclerosis: a case‐control study. Neurological Sciences 2003;24(4):242‐7. - PubMed
cb Bardage 2011 {published data only}
    1. Bardage C, Persson I, Ortqvist A, Bergman U, Ludvigsson JF, Granath F. Neurological and autoimmune disorders after vaccination against pandemic influenza A (H1N1) with a monovalent adjuvanted vaccine: population based cohort study in Stockholm, Sweden. BMJ 2011;343:d5956. - PMC - PubMed
cb Baxter 2012 {published data only}
    1. Baxter R, Toback SL, Sifakis F, Hansen J, Bartlett J, Aukes L, et al. A postmarketing evaluation of the safety of Ann Arbor strain live attenuated influenza vaccine in adults 18‐49 years of age. Vaccine 2012;30(20):3053‐60. - PubMed
cb Kaplan 1982 {published data only}
    1. Kaplan JE, Katona P, Hurwitz ES, Schonberger LB. Guillain‐Barre syndrome in the United States, 1979‐1980 and 1980‐1981. Lack of an association with influenza vaccination. JAMA 1982;248(6):698‐700. - PubMed
cb Lasky 1998 {published data only}
    1. Lasky T, Terracciano GJ, Magder L, Koski CL, Ballesteros M, Nash D, et al. The Guillain‐Barre syndrome and the 1992‐1993 and 1993‐1994 influenza vaccines. New England Journal of Medicine 1998;339(25):1797‐802. - PubMed
cb Moro 2013 {published data only}
    1. Moro ML, Nobilio L, Voci C, Mario S, Candela S, Magrini N. A population based cohort study to assess the safety of pandemic influenza vaccine Focetria in Emilia‐Romagna region, Italy ‐ part two. Vaccine 2013;31(10):1438‐46. - PubMed
cb O'Flanagan 2014 {published data only}
    1. O'Flanagan D, Barret AS, Foley M, Cotter S, Bonner C, Crowe C, et al. Investigation of an association between onset of narcolepsy and vaccination with pandemic influenza vaccine, Ireland April 2009‐December 2010. Eurosurveillance 2014;19(17):15‐25. - PubMed
cb Persson 2014 {published data only}
    1. Persson I, Granath F, Askling J, Ludvigsson JF, Olsson T, Feltelius N. Risks of neurological and immune‐related diseases, including narcolepsy, after vaccination with Pandemrix: a population‐ and registry‐based cohort study with over 2 years of follow‐up. Journal of Internal Medicine 2014;275(2):172‐90. - PubMed
cb Ray 2011 {published data only}
    1. Ray P, Black S, Shinefield H, Dillon A, Carpenter D, Lewis E, et al. Risk of rheumatoid arthritis following vaccination with tetanus, influenza and hepatitis B vaccines among persons 15‐59 years of age. Vaccine 2011;29(38):6592‐7. - PubMed
cb Shonberger 1979 {published data only}
    1. Schonberger LB, Bregman DJ, Sullivan‐Bolyai JZ, Keenlyside RA, Ziegler DW, Retailliau HF, et al. Guillain‐Barre syndrome following vaccination in the National Influenza Immunization Program, United States, 1976 ‐ 1977. American Journal of Epidemiology 1979;110(2):105‐23. - PubMed
paa Ma 2014 {published data only}
    1. Ma F, Zhang L, Jiang R, Zhang J, Wang H, Gao X, et al. Prospective cohort study of the safety of an influenza A (H1N1) vaccine in pregnant Chinese women. Clinical and Vaccine Immunology 2014;21(9):1282‐7. - PMC - PubMed
paa Madhi 2014 {published data only}
    1. Madhi SA, Cutland CL, Kuwanda L, Weinberg A, Hugo A, Jones S, et al. Influenza vaccination of pregnant women and protection of their infants. New England Journal of Medicine 2014;371(10):918‐31. - PubMed
pba Benowitz 2010 {published data only}
    1. Benowitz I, Esposito DB, Gracey KD, Shapiro ED, Vázquez M. Influenza vaccine given to pregnant women reduces hospitalization due to influenza in their infants. Clinical Infectious Diseases 2010;51(12):1355‐61. - PMC - PubMed
pba Poehling 2011 {published data only}
    1. Poehling KA, Szilagyi PG, Staat MA, Snively BM, Payne DC, Bridges CB, et al. Impact of maternal immunization on influenza hospitalizations in infants. American Journal of Obstetrics and Gynecology 2001;204(Suppl 6):141‐8. - PMC - PubMed
pbb Irving 2013 {published data only}
    1. Irving SA, Kieke BA, Donahue JG, Mascola MA, Baggs J, Destefano F, et al. Trivalent inactivated influenza vaccine and spontaneous abortion. Obstetrics and Gynecology 2013;121(1):159‐65. - PubMed
pca Ahrens 2014 {published data only}
    1. Ahrens KA, Louik C, Kerr S, Mitchell AA, Werler MM. Seasonal influenza vaccination during pregnancy and the risks of preterm delivery and small for gestational age birth. Paediatric and Perinatal Epidemiology 2014;28(6):498‐509. - PMC - PubMed
pca Black 2004 {published data only}
    1. Black SB, Shinefield HR, France EK, Fireman BH, Blatt ST, Shay D. Effectiveness of influenza vaccine during pregnancy in preventing hospitalizations and outpatient visits for respiratory illness in pregnant women and their infants. American Journal of Perinatology 2004;21(6):333‐9. - PubMed
pca Eick 2011 {published data only}
    1. Eick AA, Uyeki TM, Klimov A, Hall H, Reid R, Santosham M, et al. Maternal influenza vaccination and effect on influenza virus infection in young infants. Archives of Pediatrics and Adolescent Medicine 2011;165(2):104‐11. - PubMed
pca France 2006 {published data only}
    1. France EK, Smith‐Ray R, McClure D, Hambidge S, Xu S, Yamasaki K, et al. Impact of maternal influenza vaccination during pregnancy on the incidence of acute respiratory illness visits among infants. Archives of Pediatrics and Adolescent Medicine 2006;160(12):1277‐83. - PubMed
pca Hulka 1964 {published data only}
    1. Hulka JF. Effectiveness of polyvalent influenza vaccine in pregnancy. Report of a controlled study during an outbreak of Asian influenza. Obstetrics and Gynecology 1964;23:830‐7. - PubMed
pca Munoz 2005 {published data only}
    1. Munoz FM, Greisinger AJ, Wehmanen OA, Mouzoon ME, Hoyle JC, Smith FA, et al. Safety of influenza vaccination during pregnancy. American Journal of Obstetrics and Gynecology 2005;192(4):1098‐106. - PubMed
pca Yamada 2012 {published data only}
    1. Yamada T, Yamada T, Morikawa M, Cho K, Endo T, Sato SS, et al. Pandemic (H1N1) 2009 in pregnant Japanese women in Hokkaido. Journal of Obstetrics and Gynaecology Research 2012;38(1):130‐6. - PubMed
pcb Beau 2014 {published data only}
    1. Beau AB, Hurault‐Delarue C, Vidal S, Guitard C, Vayssiere C, Petiot D. Pandemic A/H1N1 influenza vaccination during pregnancy: a comparative study using the EFEMERIS database. Vaccine 2014;32(11):1254‐8. - PubMed
pcb Cantu 2013 {published data only}
    1. Cantu J, Biggio J, Jauk V, Wetta L, Andrews W, Tita A. Selective uptake of influenza vaccine and pregnancy outcomes. Journal of Maternal‐Fetal and Neonatal Medicine 2013;26(12):1207‐11. - PubMed
pcb Chambers 2013 {published data only}
    1. Chambers CD, Johnson D, Xu R, Luo Y, Louik C, Mitchell AA, et al. Risks and safety of pandemic H1N1 influenza vaccine in pregnancy: birth defects, spontaneous abortion, preterm delivery, and small for gestational age infants. Vaccine 2013;31(44):5026‐32. - PubMed
pcb Cleary 2014 {published data only}
    1. Cleary BJ, Rice U, Eogan M, Metwally N, McAuliffe F. 2009 A/H1N1 influenza vaccination in pregnancy: uptake and pregnancy outcomes ‐ a historical cohort study. European Journal of Obstetrics & Gynecology and Reproductive Biology 2014;178:163‐8. - PubMed
pcb Deinard 1981 {published data only}
    1. Deinard AS, Ogburn P Jr. A/NJ/8/76 influenza vaccination program: effects on maternal health and pregnancy outcome. American Journal of Obstetrics and Gynecology 1981;140(3):240‐5. - PubMed
pcb Dodds 2012 {published data only}
    1. Dodds L, Macdonald N, Scott J, Spencer A, Allen VM, McNeil S. The association between influenza vaccine in pregnancy and adverse neonatal outcomes. Journal of Obstetrics and Gynaecology Canada 2012;34(8):714‐20. - PubMed
pcb Fell 2012 {published data only}
    1. Fell DB, Sprague AE, Liu N, Yasseen AS 3rd, Wen SW, Smith G, et al. Better Outcomes Registry & Network (BORN) Ontario. H1N1 influenza vaccination during pregnancy and fetal and neonatal outcomes. American Journal of Public Health 2012;102(6):e33‐40. - PMC - PubMed
pcb Håberg 2013 {published data only}
    1. Håberg SE, Trogstad L, Gunnes N, Wilcox AJ, Gjessing HK, Samuelsen SO, et al. Risk of fetal death after pandemic influenza virus infection or vaccination. New England Journal of Medicine 2013;368(4):333‐40. - PMC - PubMed
    1. Håberg SE, Trogstad L, Gunnes N, Wilcox AJ, Gjessing HK, Samuelsen SO, et al. Risk of fetal death after pandemic influenza virus infection or vaccination. Obstetrical and Gynecological Survey 2013;68(5):348‐9. - PMC - PubMed
pcb Heikkinen 2012 {published data only}
    1. Heikkinen T, Young J, Beek E, Franke H, Verstraeten T, Weil JG, et al. Safety of MF59‐adjuvanted A/H1N1 influenza vaccine in pregnancy: a comparative cohort study. American Journal of Obstetrics & Gynecology 2012;207(3):177.e1‐8. - PubMed
pcb Källén 2012 {published data only}
    1. Källén B, Olausson PO. Vaccination against H1N1 influenza with Pandemrix during pregnancy and delivery outcome: a Swedish register study. British Journal of Obstetrics and Gynaecology 2012;119(13):1583‐90. - PubMed
pcb Launay 2012 {published data only}
    1. Launay O, Krivine A, Charlier C, Truster V, Tsatsaris V, Lepercq J, et al. Low rate of pandemic A/H1N1 2009 influenza infection and lack of severe complication of vaccination in pregnant women: a prospective cohort study. PLoS ONE 2012;7(12):e52303. - PMC - PubMed
pcb Lin 2012 {published data only}
    1. Lin TH, Lin SY, Lin CH, Lin RI, Lin HC, Chiu TH, et al. AdimFlu‐S influenza A (H1N1) vaccine during pregnancy: the Taiwanese Pharmacovigilance Survey. Vaccine 2012;30(16):2671‐5. - PubMed
pcb Louik 2013 {published data only}
    1. Louik C, Ahrens K, Kerr S, Pyo J, Chambers C, Jones KL, et al. Risks and safety of pandemic H1N1 influenza vaccine in pregnancy: exposure prevalence, preterm delivery, and specific birth defects. Vaccine 2013;31(44):5033‐40. - PubMed
pcb Ludvigsson 2013 {published data only}
    1. Ludvigsson JF, Zugna D, Cnattingius S, Richiardi L, Ekbom A, Ortqvist A, et al. Influenza H1N1 vaccination and adverse pregnancy outcome. European Journal of Epidemiology 2013;28(7):579‐88. - PubMed
pcb Nordin 2013 {published data only}
    1. Nordin JD, Kharbanda EO, Benitez GV, Nichol K, Lipkind H, Naleway A, et al. Maternal safety of trivalent inactivated influenza vaccine in pregnant women. Obstetrics and Gynecology 2013;121(3):519‐25. - PubMed
pcb Nordin 2014 {published data only}
    1. Nordin JD, Kharbanda EO, Vazquez Benitez G, Lipkind H, Vellozzi C, Destefano F. Maternal influenza vaccine and risks for preterm or small for gestational age birth. Journal of Pediatrics 2014;164(5):1051‐7.e2. - PubMed
pcb Omer 2011 {published data only}
    1. Omer SB, Goodman D, Steinhoff MC, Rochat R, Klugman KP, Stoll BJ, et al. Maternal influenza immunization and reduced likelihood of prematurity and small for gestational age births: a retrospective cohort study. PLoS Medicine 2011;8(5):e1000441. - PMC - PubMed
pcb Oppermann 2012 {published data only}
    1. Oppermann M, Fritzsche J, Weber‐Schoendorfer C, Keller‐Stanislawski B, Allignol A, Meister R, et al. A(H1N1)v2009: a controlled observational prospective cohort study on vaccine safety in pregnancy. Vaccine 2012;30(30):4445‐52. - PubMed
pcb Pasternak 2012 {published data only}
    1. Pasternak B, Svanström H, Mølgaard‐Nielsen D, Krause TG, Emborg HD, Melbye M, et al. Risk of adverse fetal outcomes following administration of a pandemic influenza A (H1N1) vaccine during pregnancy. JAMA 2012;308(2):165‐74. - PubMed
pcb Richards 2013 {published data only}
    1. Richards JL, Hansen C, Bredfeldt C, Bednarczyk RA, Steinhoff MC, Adjaye‐Gbewonyo D, et al. Neonatal outcomes after antenatal influenza immunization during the 2009 H1N1 influenza pandemic: impact on preterm birth, birth weight, and small for gestational age birth. Clinical Infectious Diseases 2013;56(9):1216‐22. - PMC - PubMed
pcb Rubinstein 2013 {published data only}
    1. Rubinstein F, Micone P, Bonotti A, Wainer V, Schwarcz A, Augustovski F. Influenza A/H1N1 MF59 adjuvanted vaccine in pregnant women and adverse perinatal outcomes: multicentre study. BMJ Online 2013;346(7896):f393. - PMC - PubMed
pcb Sheffield 2012 {published data only}
    1. Sheffield JS, Greer LG, Rogers VL, Roberts SW, Lytle H, McIntire DD, et al. Effect of influenza vaccination in the first trimester of pregnancy. Obstetrics and Gynecology 2012;120(3):532‐7. - PubMed
pcb Toback 2012 {published data only}
    1. Toback SL, Beigi R, Tennis P, Sifakis F, Calingaert B, Ambrose CS. Maternal outcomes among pregnant women receiving live attenuated influenza vaccine. Influenza and Other Respiratory Viruses 2012;6(1):44‐51. - PMC - PubMed
pcb Trotta 2014 {published data only}
    1. Trotta F, Cas R, Spila Alegiani S, Gramegna M, Venegoni M, Zocchetti C, et al. Evaluation of safety of A/H1N1 pandemic vaccination during pregnancy: cohort study. BMJ 2014;348:g3361. - PMC - PubMed

References to studies excluded from this review

ab López‐Macías 2011a {published data only}
    1. López‐Macías C, Ferat‐Osorio E, Tenorio‐Calvo A, Isibasi A, Talavera J, Arteaga‐Ruiz O, et al. Safety and immunogenicity of a virus‐like particle pandemic influenza A (H1N1) 2009 vaccine in a blinded, randomised, placebo‐controlled trial of adults in Mexico. Vaccine 2011;29(44):7826‐34. - PMC - PubMed
ab López‐Macías 2011b {published data only}
    1. López‐Macías C, Ferat‐Osorio E, Tenorio‐Calvo A, Isibasi A, Talavera J, Arteaga‐Ruiz O, et al. Safety and immunogenicity of a virus‐like particle pandemic influenza A (H1N1) 2009 vaccine in a blinded, randomised, placebo‐controlled trial of adults in Mexico. Vaccine 2011;29(44):7826‐34. - PMC - PubMed
ab Mallory 2010 {published data only}
    1. Mallory RM, Malkin E, Ambrose CS, Bellamy T, Shi L, Yi T, et al. Safety and immunogenicity following administration of a live, attenuated monovalent 2009 H1N1 influenza vaccine to children and adults in two randomised controlled trials. PLoS ONE 2010;5(10):e13755. - PMC - PubMed
ab Plennevaux 2010 {published data only}
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ab Precioso 2011 {published data only}
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