RSV Vaccines in Clinical Trials. Ruth A. Karron 30 Jan 2013

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RSV Vaccines in Clinical Trials Ruth A. Karron 30 Jan 2013

Disclosures Funding from LID, NIAID intramural program Consultant on RSV Vaccine Development: GenVec GSK Novartis Novavax

RSV Vaccine Technology Landscape 2003 PRECLINICAL PHASE I PHASE II PHASE III MARKET APPROVED Live- Attenuated Whole- Inactivated Subunit RSV LID/NIAID/NIH RSV ΔNS2 Wyeth Δ1313 Medi-RSV Wyeth ΔM2-2 Medi-559, RSV Wyeth NanoBio MERCK University of Pittsburgh LID/NIAID/NIH LID/NIAID/NIH Particle- Based VLP Peptide microparticle Mucosis Virosome Virosome VLP BLP VLP University of Saskatchewan Subunit RSV F protein RSV F-based antigen RSV F protein Ghent University SH protein RSV F protein Nucleic Acid RNA DNA Gene- Based Vectors Alphavirus Sendai virus BAVARIAN NORDIC Adenovirus Adenovirus/MVA Alphavirus Medi-534, RSV/PIV3 MVA Sendai virus

RSV Vaccine Technology Landscape 2013 PRECLINICAL PHASE I PHASE II PHASE III MARKET APPROVED Live- Attenuated LID/NIAID/NIH RSV ΔNS2 Δ1313 RSV cps2 LID/NIAID/NIH LID/NIAID/NIH Medi-RSV ΔM2-2 LID/NIAID/NIH Medi-559, RSV Whole- Inactivated RSV NanoBio MERCK University of Pittsburgh Particle- Based VLP Peptide microparticle Mucosis Virosome Virosome VLP BLP VLP University of Saskatchewan Subunit RSV F protein RSV F-based antigen RSV F protein Ghent University SH protein RSV F protein Nucleic Acid RNA DNA Gene- Based Vectors Alphavirus Sendai virus BAVARIAN NORDIC MVA Vector prime/ subunit boost Adenovirus Adenovirus/MVA Sendai virus Alphavirus Medi-534, RSV/PIV3 h.p://sites.path.org/vaccinedevelopment/files/2012/12/ RSV_vaccine_landscape_snapshot.pdf Updated: 10/11/12

Devising RSV Vaccines: What Do We Know? What are the Obstacles? Immunity Natural infection provides durable protection against lower respiratory tract illness (LRI), but not against repeated infections or mild illness Neutralizing antibody protects against LRI Maternal antibody may suppress antibody response in early infancy Epidemiology Heterogeneous at-risk population (infants, children <5, elderly) Safety Enhanced disease must be avoided.

Enhanced RSV Disease Formalin-inactivated RSV (FI-RSV) developed in the early 1960s Vaccine administered to RSV seropositive toddlers and RSV naive infants The vaccine did not harm the toddlers, but when the infants later encountered wild-type (live) RSV, they experienced severe (enhanced) disease. Two (ages 14 and 16 months) died. Kapikian et al. Am J Epidemiol 1969;89:1699 Kim et al. Am J Epidemiol 1969;89:422-434

100 Potentiation of RSV LRI following formalin inactivated vaccine % of subjects enrolled at CHC 80 60 40 20 % RSV infected % hospitalized 0 vaccinees controls Adapted from Kim et al., Am J Epidemiol 89:422-434, 1969

Possible Mechanisms of Enhanced RSV Disease Humoral: induction of non-neutralizing antibodies 1, impaired affinity maturation of antibodies 2, deposition of immune complexes 3 Cellular: Overstimulation of Th2 CD4+ T cells, poor induction of IFNγ-producing Th1 cells, NK cells and CD8 T cells 4,5 1. Murphy BR et al J Clin Micro 1986; 24(2) 197-202. 2. Polack FP et al, Nature Medicine 2009;15, 34-41 3. Polack FP et al, J Exp Med 2002; 196, 859-865. 4. Openshaw et al. Vaccine 2001; 20: S27-31 5. Johnson TR et al.. J Virol 2002 May; 76(9):4294-303..

Implications of Enhanced RSV Disease for Vaccine Development Animal models are imperfect. Preclinical studies cannot provide a complete assessment of the risk of enhanced disease from administration of non-replicating vaccines to RSV-naïve children. Replicating (live) RSV vaccines Safest alternatives for active immunization of RSV-naïve populations Live-attenuated RSV candidate vaccines have been administered to hundreds of RSV-naïve children and have never been associated with enhanced disease. 1 Non-replicating (subunit) RSV vaccines For passive immunization of infants and children via maternal immunization For immunization of non-naïve populations (older children, pregnant women, elderly) 1. Wright PF. Vaccine. 2007 Oct 16;25(42):7372-8.

Active Immunization of Infants & Young Children: Live Attenuated Vaccines Paramyxovirus vectors Chimeric B/HPIV3: MEDI 534 (Sendai-virus vectored RSV F) Live-attenuated native RSV Empirically derived attenuating mutations MEDI 559 and the codon-stabilized version, cps2 Rational vaccine design RSV MEDI ΔM2-2 (RSV ΔNS2Δ1313/1314L)

Vectored RSV Vaccine: MEDI-534 (rb/hpiv3/rsv F) RSV F 3 N P/C M hpiv3 F F hpiv3 HN L Well- tolerated in infants and young children (n=49) 5 Immune response to HPIV3 (100%) exceeded immune response to RSV (50%) 1 Sequence analysis revealed changes in RSV F noncoding region and ORF yielding decreased RSV F expression 2 Rela[onship between RSV F instability and immune response being analyzed 1. Bernstein DI et al. Pediatr Infect Dis J. 2012 Feb;31(2):109-14 2. Tang RS et al. RSV 2012 Abstract #38, Santa Fe, NM

ra2cp248/404/1030/δsh: RSV with Attenuating Point and Deletion Mutations cold passage (cp), temperature sensitive (ts), and gene deletions 3' 5' NS 1 NS 2 N P M S H G F M2 L cp cp cp 404 cp 248 1030 cp -

Initial clinical experience with ra2cp248/404/1030/δsh Well tolerated in RSV-naïve infants and children; highly restricted in replication Neut Ab responses in children >6 months Neut Ab responses limited in infants, but replication of 2 nd vaccine dose restricted (marker of immune response) Genetic instability in 30% of isolates: 4 of 5 attenuating elements detected in all recovered virus No increased illness in vaccinees Karron R. J Infect Dis. 2005 Apr 1;191(7):1093-104.

Current status of ra2cp248/404/1030/δsh MEDI-559 (MedImmune) Phase I/II study in RSV-naïve infants and children <23 months completed (NCT00767416); analysis underway cps2 (MedImmune/LID, NIAID) genetically stabilized version (positions 248 (831L[TTG]), 1030 (Y1321K) 1, and 1313) 1 clinical trials to begin Q2 2013 1. Luongo C. J Virol. 2012 Oct;86(19):10792-804.

RSV MEDI ΔM2-2: novel rrsv deletion mutant (MedImmune/ LID, NIAID) M2-2 is an RNA regulatory factor Deletion of M2-2 results in: decreased RNA replication increased transcription and antigen expression 1 (more Ag/ infectious virion) RSV MEDI ΔM2-2 is currently being evaluated in RSVnaïve infants and children (NCT 01459198) 3' 5' NS 1 NS 2 N P M S H G F M2 L 1. Bermingham A Proc Natl Acad Sci U S A. 1999 Sep 28;96(20):11259-64.

Maternal RSV Immunization: Subunit RSV Vaccines

RSV fusion (F) glycoprotein is the primary target for subunit vaccines Most neutralizing antibodies directed against RSV F Little antigenic variation in RSV F (unlike RSV G) Previously RSV F vaccine candidates (PFP-1,2,3; RSV F/G/M) did not induce high titers of neutralizing antibodies and/or were difficult to manufacture F

Recent advances in understanding RSV F structure have guided vaccine development RSV F exists in a prefusion and postfusion state Prefusion F is not naturally stable Recent data from Novartis and NIAID,NIH indicate that postfusion RSV F contains certain neutralizing epitopes, including the palivizumab epitope 1,2 Other studies indicate that most of the neutralizing antibody found in human sera (RSVIg) is directed toward prefusion RSV F 3 1. McLellan J S et al. J. Virol. 2011;85:7788-7796 2. Swanson KA. Proc Natl Acad Sci U S A. 2011 Jun 7;108(23):9619-24. 3. Magro M. Proc Natl Acad Sci U S A. 2012 Feb 21;109(8):3089-94.

RSV F Nanoparticle Vaccine is Currently Being Evaluated in Clinical Trials Developed by Novavax Engineered RSV postfusion F expressed in baculovirus forms nanoparticles Preclinical studies in cotton rats showed protection against RSV challenge Phase I studies in healthy adults completed Phase II studies in women of childbearing age initiated Glenn GM Vaccine 2013 31: 524-532 h.p://www.novavax.com/download/file/presenta[ons/rsv- F- Phase- 1- Poster- 2012_gs.pdf 19 2009, Johns Hopkins University. All rights reserved.

Novartis postfusion RSV F vaccine protective in preclinical trials Cotton rats immunized with postfusion RSV F trimer developed high titers of RSV neutralizing antibody and were protected against viral challenge Similar RSV F subunit vaccine is being developed for clinical trials Swanson KA. Proc Natl Acad Sci U S A. 2011 Jun 7;108(23):9619-24.

Summary: RSV F subunit vaccines New RSV postfusion F subunit vaccines are in clinical trials or about to be tested in clinical trials Clinical trials will determine: Magnitude of antibody response Duration of antibody response Ability of RSV postfusion F subunit vaccines to induce neutralizing as well as non-neutralizing RSV F antibodies

Immunization Strategies for Pathogens of. Infancy and Early Childhood Tetanus: Maternal and infant immunization Pertussis: Maternal and infant immunization Influenza: Maternal and infant immunization RSV:???

RSV Vaccines: Global implementation questions Will the protection observed in wealthy countries also be observed in resource limited settings, where RSV exposure and disease may be influenced by Crowding Limited access to water Indoor air pollution For maternal immunization, how will maternal illnesses affect transplacental transmission of antibody? HIV Placental malaria 23 2009, Johns Hopkins University. All rights reserved.

Evalua[on of live- a.enuated vaccines for Acknowledgementsl illness in pediatric popula[ons LID,NIAID,NIH Novavax P. Collins G. Glenn U. Buchholz G. Smith PATH NovarBs D. Higgins P Dormitzer K. Neuzil