John Treanor

University of Rochester, Rochester, New York, United States

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Publications (103)942.84 Total impact

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    ABSTRACT: Background: We evaluated a candidate A/Anhui/2013(H7N9) pandemic live attenuated influenza vaccine (pLAIV) in healthy adults, and assessed the ability of 1 or 2 doses to induce immune memory. Methods: Healthy subjects in 2 age groups (18-49 years and 50-70 years) with undetectable hemagglutination-inhibiting (HAI) antibody to H7N9 were enrolled. Younger subjects received either 1 or 2 intranasal doses of 10(7.0) fluorescent focus units of A/Anhui/1/2013 pLAIV, while older subjects received a single dose. All subjects received a single 30-µg dose of unadjuvanted, antigenically matched A/Shanghai2/2013(H7N9) pandemic inactivated influenza vaccine (pIIV) 12 weeks after their first dose of pLAIV. Results: Both vaccines were well tolerated. Serum HAI antibody responses were detected in 0 of 32 younger subjects and 1 of 17 older subjects after 1 dose of pLAIV and in 2 of 16 younger subjects after a second dose. Strong serum antibody responses were detected after a single subsequent dose of pIIV that was broadly reactive against H7 influenza viruses. Conclusions: An A(H7N9) pLAIV candidate was safe in both age groups. Priming with pLAIV resulted in responses to subsequent pIIV that exceeded those seen in naive subjects in previous reports. The A(H7N9) pLAIV induces strong immune memory that can be demonstrated by exposure to subsequent antigenic challenge. Clinical trial registration: NCT01995695 and NCT02274545.
    No preview · Article · Dec 2015 · The Journal of Infectious Diseases
  • John Treanor

    No preview · Article · Nov 2015 · Clinical Infectious Diseases
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    ABSTRACT: Background: Based on the success of vaccination with pneumococcal conjugate vaccines (PCVs) in children, recent studies have focused on PCVs in adults. Data from a randomized, double-blind study comparing the immunogenicity, tolerability, and safety of the 13-valent PCV (PCV13) and the 23-valent pneumococcal polysaccharide vaccine (PPSV23) in PPSV23-naive adults 60-64 years of age have been published. The same study also included a cohort of adults aged 18-49 years that received open-label PCV13. The purpose of this cohort was to examine the immunogenicity, safety, and tolerability of PCV13 in adult subjects 18-49 years of age compared with adults 60-64 years of age for whom PCV13 is approved. Methods: Adults naive to PPSV23 were grouped by age into 2 cohorts: 18-49 years (n=899; further stratified by age into 3 subgroups 18-29, 30-39, and 40-49 years) and 60-64 years (n=417). All subjects received 1 dose of PCV13. In both age groups, immunogenicity was assessed by antipneumococcal opsonophagocytic activity (OPA) geometric mean titers (GMT) and IgG geometric mean concentrations (GMCs) 1 month after vaccination. Safety and tolerability were evaluated. Results: In adults aged 18-49 years, OPA GMTs and IgG GMCs were noninferior for all 13 serotypes and statistically significantly higher for all except 1 serotype (OPA GMT) and 5 serotypes (IgG GMCs) compared with adults 60-64 years. Immune responses were highest in the youngest age subgroup (18-29 years). Local reactions and systemic events were more common in adults 18-49 years compared with 60-64 years and were self-limited. Conclusion: Immune responses to PCV13 are robust in adults ≥18 years of age, with highest responses observed in the youngest subgroup. Based on its safety and immunologic profile, PCV13 may serve an important therapeutic role in younger adults, particularly those with underlying medical conditions who have an increased risk of serious pneumococcal infections.
    Full-text · Article · Sep 2015 · Vaccine
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    ABSTRACT: Background H7 influenza viruses have emerged as potential pandemic threat. We evaluated the safety and immunogenicity of two candidate H7 pandemic live attenuated influenza vaccines (pLAIV) and their ability to prime for responses to an unadjuvanted H7 pandemic inactivated influenza vaccine (pIIV). Methods Healthy seronegative adults received two doses of A/Netherlands/219/03 (H7N7) or one dose of A/chicken/British Columbia/CN-6/04 (H7N3) pLAIV all given as 107.5 50% tissue culture infective doses (TCID50) intranasally. A subset of subjects received one 45 μg dose of H7N7 pIIV containing the A/Mallard/Netherlands/12/2000 HA intramuscularly 18–24 months after pLAIV. Viral shedding was assessed by culture and real-time polymerase chain reaction (rRT-PCR), B cell responses following pLAIV were evaluated by ELISPOT and flow cytometry. Serum antibody was assessed by hemagglutination-inhibition (HAI), microneutralization (MN) and ELISA assays after each vaccine. Results Serum HAI or MN responses were not detected in any subject following one or two doses of either H7 pLAIV, although some subjects had detectable H7 specific B cells after vaccination. However, 10/13 subjects primed with two doses of H7N7 pLAIV responded to a subsequent dose of the homologous H7N7 pIIV with high titer HAI and MN antibody that cross-reacted with both North American and Eurasian lineage H7 viruses, including H7N9. In contrast, naïve subjects and recipients of a single dose of the mismatched H7N3 pLAIV did not develop HAI or MN antibody after pIIV. Conclusions While pLAIVs did not elicit detectable serum MN or HAI antibody, strain-specific pLAIV priming established long term immune memory that was cross-reactive with other H7 influenza strains. Understanding the mechanisms underlying priming by pLAIV may aid in pandemic vaccine development.
    No preview · Article · Nov 2014 · Vaccine
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    ABSTRACT: Introduction: Observational studies of influenza vaccine effectiveness often study persons seeking medical care for acute respiratory infection (ARI). We conducted a pilot study to determine if vaccine effectiveness could be estimated in the general population with a novel rolling cross-sectional survey sampling design and laboratory confirmation of influenza. Methods: Cross-sectional samples were selected weekly from defined populations in Marshfield, Wisconsin and Monroe County, New York from January through April, 2011 (12 weeks). Persons were telephoned and asked about the occurrence of ARI in the past week. Nasal and throat swabs were obtained from consenting individuals with ARI and tested by real-time reverse transcription polymerase chain reaction (RT-PCR). Vaccine effectiveness (VE) was defined as (100×[1-OR]) for vaccination in a logistic regression model that adjusted for age, calendar week, and site. The comparison group included all study participants without RT-PCR confirmed influenza, including those who were not ill. Results: Study personnel contacted 9537 (62%) of 15,303 persons sampled; the primary analysis included 5678 subjects. Of these, 193 (3%) reported an ARI and agreed to be tested for influenza; 13 (7%) were influenza positive. The adjusted effectiveness of the influenza vaccine was 1% (95% confidence limits -239-70%). Conclusions: The rolling cross-sectional design is methodologically feasible and may be useful as a complement to clinic-based VE studies. This pilot study did not have sufficient power to detect significant vaccine effectiveness during a mild influenza season, but this approach may facilitate rapid estimation of VE in a pandemic setting when normal patterns of health care utilization are disrupted.
    No preview · Article · Oct 2014 · Vaccine
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    Full-text · Article · Sep 2014 · Journal of Virological Methods
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    ABSTRACT: Background: As compared with a standard-dose vaccine, a high-dose, trivalent, inactivated influenza vaccine (IIV3-HD) improves antibody responses to influenza among adults 65 years of age or older. This study evaluated whether IIV3-HD also improves protection against laboratory-confirmed influenza illness. Methods: We conducted a phase IIIb-IV, multicenter, randomized, double-blind, active-controlled trial to compare IIV3-HD (60 μg of hemagglutinin per strain) with standard-dose trivalent, inactivated influenza vaccine (IIV3-SD [15 μg of hemagglutinin per strain]) in adults 65 years of age or older. Assessments of relative efficacy, effectiveness, safety (serious adverse events), and immunogenicity (hemagglutination-inhibition [HAI] titers) were performed during the 2011-2012 (year 1) and the 2012-2013 (year 2) northern-hemisphere influenza seasons. Results: A total of 31,989 participants were enrolled from 126 research centers in the United States and Canada (15,991 were randomly assigned to receive IIV3-HD, and 15,998 to receive IIV3-SD). In the intention-to-treat analysis, 228 participants in the IIV3-HD group (1.4%) and 301 participants in the IIV3-SD group (1.9%) had laboratory-confirmed influenza caused by any viral type or subtype associated with a protocol-defined influenza-like illness (relative efficacy, 24.2%; 95% confidence interval [CI], 9.7 to 36.5). At least one serious adverse event during the safety surveillance period was reported by 1323 (8.3%) of the participants in the IIV3-HD group, as compared with 1442 (9.0%) of the participants in the IIV3-SD group (relative risk, 0.92; 95% CI, 0.85 to 0.99). After vaccination, HAI titers and seroprotection rates (the percentage of participants with HAI titers ≥ 1:40) were significantly higher in the IIV3-HD group. Conclusions: Among persons 65 years of age or older, IIV3-HD induced significantly higher antibody responses and provided better protection against laboratory-confirmed influenza illness than did IIV3-SD. (Funded by Sanofi Pasteur; ClinicalTrials.gov number, NCT01427309.).
    Preview · Article · Aug 2014 · New England Journal of Medicine
  • R. Dolin · J.J. Treanor

    No preview · Article · Jan 2014
  • R. Dolin · J.J. Treanor

    No preview · Article · Jan 2014
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    ABSTRACT: The estimation of the effectiveness of vaccination against seasonal influenza is guided by the comparison of antigenicities between influenza virus isolates from clinical breakthrough cases with strains included in the vaccine. This study examined whether the prediction of antigenicity using sequence analysis of the hemagglutinin (HA) gene-encoded HA1-domain could be a simpler alternative to using the conventional hemagglutination inhibition (HI) assay, which requires influenza virus culturing. Specimens were taken from breakthrough cases that occurred in a trivalent influenza vaccine efficacy trial involving over 43000 participants during the 2008-2009 season. A total of 498 influenza viruses were successfully subtyped as A(H3N2) (380), A(H1N1) (29), B(Yamagata) (23) and B(Victoria) (66), from 603 PCR- or culture-confirmed specimens. Unlike the B-strain, most A(H3N2) (377) and all A(H1N1) viruses were designated as homologous to the respective vaccine strains based on the HA1-domain nucleic acid sequence. HI titers relative to the respective vaccine strains and PCR subtyping were determined for 48% (182/380) of A(H3N2) and 86% (25/29) of A(H1N1) viruses. Eighty-four percent of the A(H3N2) and A(H1N1) viruses designated as homologous by sequence were matched to the respective vaccine strains by HI testing. However, these homologous A(H3N2) and A(H1N1) viruses displayed a wide range of relative HI titers. Therefore, although PCR was a sensitive diagnostic method to confirm influenza cases, HA1 sequence analysis appeared to be of limited value in accurately predicting antigenicity and hence may be inappropriate to classify clinical specimens as homologous or heterologous to the vaccine-strain for estimating vaccine efficacy in a prospective clinical trial.
    Full-text · Article · Dec 2013 · Clinical and vaccine Immunology: CVI
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    ABSTRACT: Bacteriophage lambda capsids provide a flexible molecular scaffold that can be engineered to display a wide range of exogenous proteins, including full-length viral glycoproteins produced in eukaryotic cells. One application for such particles lies in the detection of virus-specific antibodies, since they may obviate the need to work with infectious stocks of highly pathogenic or emerging viruses that can pose significant biosafety and biocontainment challenges. Bacteriophage lambda capsids were produced that displayed an insect-cell derived, recombinant H5 influenza virus hemagglutinin (HA) on their surface. The particles agglutinated red blood cells efficiently, in a manner that could be blocked using H5 HA-specific monoclonal antibodies. The particles were then used to develop a modified hemagglutinination-inhibition (HAI) assay, which successfully identified human sera with H5 HA-specific HAI activity. These results demonstrate the utility of HA-displaying bacteriophage capsids for the detection of influenza virus-specific HAI antibodies.
    No preview · Article · Dec 2013 · Journal of virological methods
  • Wendy A. Keitel · Kathleen M. Neuzil · John Treanor
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    ABSTRACT: Immunization against influenza serves as the primary approach for control of influenza in persons and populations. Parenterally administered killed or inactivated vaccines and intranasally administered live attenuated vaccines are approved for use worldwide. Currently licensed inactivated vaccines predominantly target the hemagglutinin surface antigen. Influenza vaccines are unique in that they are reformulated on an annual or semi-annual basis. The immunogenicity, safety, and effectiveness profiles differ by vaccine formulation and by population group. Newer influenza vaccines formulated with oil-in-water adjuvant show promise for enhancing immunogenicity and efficacy of inactivated vaccines in specific age and risk groups. To assess the impact of influenza vaccines on disease reduction, relative efficacy must be considered in the context of the burden of influenza illness in any given population.
    No preview · Chapter · Aug 2013
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    ABSTRACT: Background: Unlike free polysaccharide vaccines, pneumococcal polysaccharide conjugate vaccines (PCVs) induce a T cell-dependent immune response and have the potential to provide an extended duration of protection with repeated vaccinations. Methods: This was an extension of a previous study in pneumococcal vaccine-naïve adults aged 50-64 years in which adults 60-64 years of age were given 13-valent PCV (PCV13) or 23-valent pneumococcal polysaccharide vaccine (PPSV23) and adults aged 50-59 were given PCV13. In this follow up study conducted about 4 years later, the 60-64 year olds initially given PCV13 received PCV13 or PPSV23, and those initially given PPSV23 received another PPSV23. All adults aged 50-59 years were re-vaccinated with PCV13. Anti-pneumococcal opsonophagocytic activity (OPA) titers were measured before and 1 month after vaccination. Results: A second PCV13 given about 4 years after a first vaccination induced OPA titers that were significantly higher than those following the initial vaccination for 7 of 13 serotypes in the older group, and 6 of 13 serotypes in the younger group, and responses to the remaining serotypes were largely non-inferior. In contrast, OPA titers following revaccination with PPSV23 were statistically significantly lower for 9 of the 13 serotypes, and non-inferior for the remaining serotypes, when compared to the responses to the first PPSV23. OPA titers in the older adults who received PPSV23 after initial PCV13 were significantly higher than those following a first PPSV23 for 10 of the 13 serotypes. Conclusion: In adults 50 to 64 years of age, initial vaccination with PCV13 establishes an immune state that results in recall anti-pneumococcal responses upon subsequent vaccination with either conjugated or free polysaccharide vaccine. In contrast, initial vaccination with PPSV23 results in an immune state in which subsequent PPSV23 administration yields generally lower responses compared with the initial responses.
    Full-text · Article · May 2013 · Vaccine
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    ABSTRACT: The immune response of patients who have cancer, who may be receiving immunosuppressive therapy, is generally considered to be decreased. This study aimed to evaluate the immune response of cancer patients to the 2009 influenza A (H1N1) vaccine. We conducted a prospective single site study comparing the immune response after H1N1 vaccination of healthy controls (group A), patients who had solid tumors and were taking myelosuppressive chemotherapy (group B), patients who had solid tumors and were taking nonmyelosuppressive or no treatment (group C), and patients who had hematologic malignancies (group D). At 2-6 weeks after vaccination, seroconversion was observed in 80.0% of group A (95% confidence interval [CI], 65.0%-89.7%), 72.2% of group B (95% CI, 55.9%-84.3%), 87.0% of group C (95% CI, 72.2%-94.7%), and 75.0% of group D (95% CI, 52.8%-89.2%) (p = NS). The geometric mean titer ratio, that is, geometric mean factor increase in antibody titer after vaccination, was 12.6 (95% CI, 7.9-19.9), 12.7 (95% CI, 7.3-22.1), 23.0 (95% CI, 13.9-38.2), and 12.1 (95% CI, 5.3-27.9) (p = NS), and the seroprotection rates were 95.5% (95% CI, 84.0%-99.6%), 79.0% (95% CI, 63.4%-89.2%), 90.5% (95% CI, 77.4%-96.8%), and 90.0% (95% CI, 71%-98.7%) in the corresponding groups (p = NS). Immune responses were robust regardless of malignancy, or time intervals between the use of myelosuppressive or immunosuppressive medications and vaccination. No participants developed clinical H1N1 infection. Cancer patients, whether taking myelosuppressive chemotherapy or not, are able to generate an immune response to the H1N1 vaccine similar to that of healthy controls.
    Full-text · Article · Jan 2012 · The Oncologist
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    ABSTRACT: The aim of the study was to determine whether reduced doses of trivalent inactivated influenza vaccine (TIV) administered by the intradermal (ID) route generated similar immune responses to standard TIV given intramuscularly (IM) with comparable safety profiles. Recent changes in immunization recommendations have increased the number of people for whom influenza vaccination is recommended. Thus, given this increased need and intermittent vaccine shortages, means to rapidly expand the vaccine supply are needed. Previously healthy subjects 18-64 years of age were randomly assigned to one of four TIV vaccine groups: standard 15 μg HA/strain TIV IM, either 9 μg or 6 μg HA/strain of TIV ID given using a new microinjection system (BD Soluvia™ Microinjection System), or 3 μg HA/strain of TIV ID given by Mantoux technique. All vaccines contained A/New Caledonia (H1N1), A/Wyoming (H3N2) and B/Jiangsu strains of influenza. Sera were obtained 21 days after vaccination and hemagglutination inhibition (HAI) assays were performed and geometric mean titers (GMT) were compared among the groups. Participants were queried immediately following vaccination regarding injection pain and quality of the experience. Local and systemic reactions were collected for 7 days following vaccination and compared. Ten study sites enrolled 1592 subjects stratified by age; 18-49 years [N=814] and 50-64 years [N=778]. Among all subjects, for each of the three vaccine strains, the GMTs at 21 days post-vaccination for both the 9 μg and the 6 μg doses of each strain given ID were non inferior to GMTs generated after standard 15 μg doses/strain IM. However, for the 3 μg ID dose, only the A/Wyoming antigen produced a GMT that was non-inferior to the standard IM dose. Additionally, in the subgroup of subjects 50-64 years of age, the 6μg dose given ID induced GMTs that were inferior to the standard IM TIV for the A/H1N1 and B strains. No ID dose produced a GMT superior to that seen after standard IM TIV. Local erythema and swelling were significantly more common in the ID groups but the reactions were mild to moderate and short-lived. No significant safety issues related to intradermal administration were identified. Participants given TIV ID provided favorable responses to questions about their experiences with ID administration. In conclusion, for the aggregated cohorts of adults 18-64 years of age, reduced doses (6 μg and 9 μg) of TIV delivered ID using a novel microinjection system stimulated comparable HAI antibody responses to standard TIV given IM. The reduced 3 μg dose administered ID by needle and syringe, as well as the 6 μg ID for subjects aged 50-64 years of age generated poorer immune responses as compared to the 15 μg IM dose.
    Full-text · Article · Jun 2011 · Vaccine
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    ABSTRACT: Upon vaccination, B cells differentiate into antibody secreting cells (ASCs) that migrate via the circulation to tissues. The kinetics of this response and the relationship of circulating ASCs to protective antibody titers have not been completely explored. Influenza-specific and total-IgG ASCs were enumerated by Elispot and flow cytometry daily in the blood in 6 healthy adults after trivalent influenza vaccination (TIV). Peak H1-specific IgG ASC frequencies occurred variably from day 5 to 8 and correlated with the fold-rise rise in hemagglutination inhibition (HAI titers); r=0.91, p=0.006. H3-specific IgG ASC frequencies correlated less well, perhaps due to a mismatch of the H3 protein in the vaccine and that used in the Elispot assay. Peak frequencies of vaccine-specific and total-IgG ASCs were 0.3% and 0.8%, respectively, of peripheral blood mononuclear cells (PBMC). Peak TIV-, H1-, H3-, and total-IgG ASC frequencies were 1736+/-1133, 626+/-520, 592+/-463, and 4091+/-2019 spots/10(6) PBMC, respectively. Peak TIV-, H1-, and H3-specific IgG ASC of total-IgG ASC frequencies constituted 63%+/-21, 26%+/-10, 22%+/-17, respectively. After immunization with inactivated influenza vaccine the peak in influenza-specific ASC frequencies is variable but correlates well with the magnitude of protective HAI responses.
    Full-text · Article · Mar 2010 · Vaccine
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    ABSTRACT: B cell responses after immunization with a drifted H5 influenza/A/Vietnam/1203/04 vaccine were characterized in the peripheral blood of human subjects primed with experimental recombinant H5 influenza A/Hong Kong/156/97 vaccine. Antibody secreting cells were assayed by ELISPOT against a panel of recombinant hemagglutinin and control proteins. Increased frequencies of H5 HA-specific antibody secreting and memory B cells could be observed within 7 days of re-vaccination. Furthermore, these responses were cross-reactive to both H5 HA variants, but not H3 or avian H6 HA strains. These observations suggest prior vaccination against H5 influenza HA induces cellular immune responses that cross-react among drifted variants, without precluding a response to new, or existing HA strains.
    Full-text · Article · Nov 2009 · Vaccine
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    ABSTRACT: We conducted a population-based pharmacokinetic study to assess blood levels and elimination of mercury after vaccination of premature infants born at > or =32 and <37 weeks of gestation and with birth weight > or =2000 but <3000 g. Blood, stool, and urine samples were obtained before vaccination and 12 hours to 30 days after vaccination from 72 premature newborn infants. Total mercury levels were measured by atomic absorption. The mean +/- standard deviation (SD) birth weight was 2.4 +/- 0.3 kg for the study population. Maximal mean +/- SD blood mercury level was 3.6 +/- 2.1 ng/mL, occurring at 1 day after vaccination; maximal mean +/- SD stool mercury level was 35.4 +/- 38.0 ng/g, occurring on day 5 after vaccination; and urine mercury levels were mostly nondetectable. The blood mercury half-life was calculated to be 6.3 (95% CI, 3.85 to 8.77) days, and mercury levels returned to prevaccination levels by day 30. The blood half-life of intramuscular ethyl mercury from thimerosal in vaccines given to premature infants is substantially shorter than that of oral methyl mercury in adults. Because of the differing pharmacokinetics, exposure guidelines based on oral methyl mercury in adults may not be accurate for children who receive thimerosal-containing vaccines.
    Full-text · Article · Jun 2009 · The Journal of pediatrics
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    ABSTRACT: The cellular immune response to primary influenza virus infection is complex, involving multiple cell types and anatomical compartments, and is difficult to measure directly. Here we develop a two-compartment model that quantifies the interplay between viral replication and adaptive immunity. The fidelity of the model is demonstrated by accurately confirming the role of CD4 help for antibody persistence and the consequences of immune depletion experiments. The model predicts that drugs to limit viral infection and/or production must be administered within 2 days of infection, with a benefit of combination therapy when administered early, and cytotoxic CD8 T cells in the lung are as effective for viral clearance as neutralizing antibodies when present at the time of challenge. The model can be used to investigate explicit biological scenarios and generate experimentally testable hypotheses. For example, when the adaptive response depends on cellular immune cell priming, regulation of antigen presentation has greater influence on the kinetics of viral clearance than the efficiency of virus neutralization or cellular cytotoxicity. These findings suggest that the modulation of antigen presentation or the number of lung resident cytotoxic cells and the combination drug intervention are strategies to combat highly virulent influenza viruses. We further compared alternative model structures, for example, B-cell activation directly by the virus versus that through professional antigen-presenting cells or dendritic cell licensing of CD8 T cells.
    Full-text · Article · Jun 2009 · Journal of Virology
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    John Treanor
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    ABSTRACT: Both purified expressed proteins and virus-like particles generated in insect cells by recombinant baculoviruses are being explored as potential vaccines for seasonal and pandemic influenza. Clinical trials have suggested that recombinant hemagglutinin vaccines are well tolerated in healthy and elderly adults, that they induce a functional antibody response, and that they provide protection against seasonal influenza in adults. In one trial, a pandemic formulation of H5 vaccine (rH5) induced neutralizing antibody in adults at rates roughly similar to that seen with egg-derived subvirion H5N1 vaccine. Preliminary data suggest that vaccination with the rH5 can also prime for booster responses on revaccination with drifted strains of H5. Recombinant approaches may be extremely valuable in combating future pandemics and further studies of recombinant pandemic vaccines in humans are needed.
    Preview · Article · Jan 2009 · Current topics in microbiology and immunology

Publication Stats

6k Citations
942.84 Total Impact Points

Institutions

  • 1988-2015
    • University of Rochester
      • • Division of Infectious Diseases
      • • Department of Environmental Medicine
      • • Department of Medicine
      • • Division of Hospital Medicine
      Rochester, New York, United States
  • 2009
    • IBMS
      Londinium, England, United Kingdom
  • 1986-2007
    • United States Army Medical Research Institute for Infectious Diseases
      Фредерик, Maryland, United States
  • 2005
    • Dalhousie University
      • Department of Pediatrics
      Halifax, Nova Scotia, Canada
  • 1990-2004
    • University Center Rochester
      • • Department of Medicine
      • • Elmwood Pediatric Group
      • • Infectious Diseases Unit
      Рочестер, Minnesota, United States
  • 1997
    • National Institutes of Health
      • Laboratory of Infectious Diseases
      베서스다, Maryland, United States
  • 1995
    • Children's Hospital of the King's Daughters
      Norfolk, Virginia, United States
  • 1994
    • University of Pittsburgh
      • Department of Medicine
      Pittsburgh, Pennsylvania, United States