Pulmonary delivery of influenza vaccine formulations in cotton rats: site of deposition plays a minor role in the protective efficacy against clinical isolate of H1N1pdm virus

References

• Amorij JP, Saluja V, Petersen AH, et al. (2007). Pulmonary delivery of an inulin-stabilized influenza subunit vaccine prepared by spray-freeze drying induces systemic, mucosal humoral as well as cell-mediated immune responses in BALB/c mice. Vaccine 25:8707–17.
   PubMed Web of Science ®Google Scholar
• Audouy SAL, van der Schaaf G, Hinrichs WLJ, et al. (2011). Development of a dried influenza whole inactivated virus vaccine for pulmonary immunization. Vaccine 29:4345–52.
   PubMed Web of Science ®Google Scholar
• Blanco JC, Boukhvalova MS, Perez DR, et al. (2014). Modeling human respiratory viral infections in the cotton rat (Sigmodon hispidus). J Antivir Antiretrovir 6:40–2.
   PubMedGoogle Scholar
• Blanco JC, Pletneva LM, Wan H, et al. (2013). Receptor characterization and susceptibility of cotton rats to avian and 2009 pandemic influenza virus strains. J Virol 87:2036–45.
   PubMed Web of Science ®Google Scholar
• de Boer AH, Hagedoorn P, Westerman EM, et al. (2006). Design and in vitro performance testing of multiple air classifier technology in a new disposable inhaler concept (Twincer) for high powder doses. Eur J Pharm Sci 28:171–8.
   PubMed Web of Science ®Google Scholar
• Bouvier NM, Lowen AC. (2010). Animal models for influenza virus pathogenesis and transmission. Viruses 2:1530–63.
   PubMed Web of Science ®Google Scholar
• Brandtzaeg P. (2007). Induction of secretory immunity and memory at mucosal surfaces. Vaccine 25:5467–84.
   PubMed Web of Science ®Google Scholar
• Budimir N, Huckriede A, Meijerhof T, et al. (2012). Induction of heterosubtypic cross-protection against influenza by a whole inactivated virus vaccine: the role of viral membrane fusion activity. PLoS One 7:e30898.
   PubMed Web of Science ®Google Scholar
• Cheng YS. (2014). Mechanisms of pharmaceutical aerosol deposition in the respiratory tract. AAPS PharmSciTech 15:630–40.
   PubMed Web of Science ®Google Scholar
• Cox RJ, Brokstad KA, Ogra P. (2004). Influenza virus: immunity and vaccination strategies. Comparison of the immune response to inactivated and live, attenuated influenza vaccines. Scand J Immunol 59:1–15.
   PubMed Web of Science ®Google Scholar
• Crosby CM, Matchett WE, Anguiano-zarate SS, et al. (2017). Replicating single-cycle adenovirus vectors generate amplified influenza vaccine responses. J Virol 91:1–12.
   Web of Science ®Google Scholar
• Eichelberger MC, Prince GA, Ottolini MG. (2004). Influenza-induced tachypnea is prevented in immune cotton rats, but cannot be treated with an anti-inflammatory steroid or a neuraminidase inhibitor. Virology 322:300–7.
   PubMed Web of Science ®Google Scholar
• Flood A, Estrada M, McAdams D, et al. (2016). Development of a freeze-dried, heat-stable influenza subunit vaccine formulation. PLoS One 11:18.
   Web of Science ®Google Scholar
• Geeraedts F, Saluja V, ter Veer W, et al. (2010). Preservation of the immunogenicity of dry-powder influenza H5N1 whole inactivated virus vaccine at elevated storage temperatures. AAPS J 12:215–22.
   PubMed Web of Science ®Google Scholar
• Haigh W, Howell RW. (1973). The efficacy of the a2/aichi/68 strain in inhaled influenza immunisation against the a/England/42/72 variant. Occup Med 23:125–7.
   Google Scholar
• Holt PG, Schon-Hegrad MA, Oliver J. (1988). MHC class II antigen-bearing dendritic cells in pulmonary tissues of the rat. Regulation of antigen presentation activity by endogenous macrophage populations. J Exp Med167:262–74.
   PubMed Web of Science ®Google Scholar
• Hoppentocht M, Hoste C, Hagedoorn P, et al. (2014). In vitro evaluation of the DP-4M PennCentury TM insufflator. Eur J Pharm Biopharm 88:153–9.
   PubMed Web of Science ®Google Scholar
• Kim SH, Jang YS. (2017). The development of mucosal vaccines for both mucosal and systemic immune induction and the roles played by adjuvants. Clin Exp Vaccine Res 6:15–21.
   PubMed Web of Science ®Google Scholar
• Kondrich JRM. (2017). Influenza in children. Curr Opin Pediatr 29:297–302.
   PubMed Web of Science ®Google Scholar
• Lambrecht BN, Hammad H. (2012). Lung dendritic cells in respiratory viral infection and asthma: from protection to immunopathology. Annu Rev Immunol 30:243–70.
   PubMed Web of Science ®Google Scholar
• Liu H, Patil HP, de Vries-Idema J, et al. (2012). Enhancement of the immunogenicity and protective efficacy of a mucosal influenza subunit vaccine by the saponin adjuvant GPI-0100. PLoS One 7:e52135.
   PubMed Web of Science ®Google Scholar
• Lovalenti PM, Anderl J, Yee L, et al. (2016). Stabilization of live attenuated influenza vaccines by freeze drying, spray drying, and foam drying. Pharm Res 33:1144–60.
   PubMed Web of Science ®Google Scholar
• McDermott MR, Bienenstock J. (1979). Evidence for a common mucosal immunologic system. I. Migration of B immunoblasts into intestinal, respiratory, and genital tissues. J Immunol 122:1892–8.
   PubMed Web of Science ®Google Scholar
• Minne A, Louahed J, Mehauden S, et al. (2007). The delivery site of a monovalent influenza vaccine within the respiratory tract impacts on the immune response. Immunology 122:316–25.
   PubMed Web of Science ®Google Scholar
• Murugappan S, Patil HP, Kanojia G, et al. (2013). Physical and immunogenic stability of spray freeze-dried influenza vaccine powder for pulmonary delivery: comparison of inulin, dextran, or a mixture of dextran and trehalose as protectants. Eur J Pharm Biopharm 85:716–25.
   PubMed Web of Science ®Google Scholar
• Neutra MR, Pringault E, Kraehenbuhl JP. (1996). Antigen sampling across epithelial barriers and induction of mucosal immune responses. Annu Rev Immunol 14:275–300.
   PubMed Web of Science ®Google Scholar
• Neyt K, Lambrecht BN. (2013). The role of lung dendritic cell subsets in immunity to respiratory viruses. Immunol Rev 255:57–67.
   PubMed Web of Science ®Google Scholar
• Novakova-jiresova A, van Luijk P, van Goor H, et al. (2005). Pulmonary radiation injury: identification of risk factors associated with regional hypersensitivity. Cancer Res 65:3568–76.
   PubMed Web of Science ®Google Scholar
• Onodera T, Takahashi Y, Yokoi Y, et al. (2012). Memory B cells in the lung participate in protective humoral immune responses to pulmonary influenza virus reinfection. Proc Natl Acad Sci USA 109:2485–90.
   PubMed Web of Science ®Google Scholar
• Ottolini MG, Blanco JCG, Eichelberger MC, et al. (2005). The cotton rat provides a useful small-animal model for the study of influenza virus pathogenesis. J Gen Virol 86:2823–30.
   PubMed Web of Science ®Google Scholar
• Patil H, Herrera Rodriguez J, de Vries-Idema J, et al. (2017). Adjuvantation of pulmonary-administered influenza vaccine with GPI-0100 primarily stimulates antibody production and memory B cell proliferation. Vaccines 5:19.
   Web of Science ®Google Scholar
• Patil HP, Murugappan S, Ter Veer W, et al. (2014). Evaluation of monophosphoryl lipid A as adjuvant for pulmonary delivered influenza vaccine. J Control Release 174:51–62.
   PubMed Web of Science ®Google Scholar
• Peeters B, Tonnis WF, Murugappan S, et al. (2014). Pulmonary immunization of chickens using non-adjuvanted spray-freeze dried whole inactivated virus vaccine completely protects against highly pathogenic H5N1 avian influenza virus. Vaccine 32:6445–50.
   PubMed Web of Science ®Google Scholar
• Saluja V, Amorij JP, Kapteyn JC, et al. (2010). A comparison between spray drying and spray freeze drying to produce an influenza subunit vaccine powder for inhalation. J Control Release 144:127–33.
   PubMed Web of Science ®Google Scholar
• Sertl K, Takemura T, Tschachler E, et al. (1986). Dendritic cells with antigen-presenting capability reside in airway epithelium, lung parenchyma, and visceral pleura. J Exp Med 163:436–51.
   PubMed Web of Science ®Google Scholar
• Sheth P, Stein SW, Myrdal PB. (2015). Factors influencing aerodynamic particle size distribution of suspension pressurized metered dose inhalers. AAPS PharmSciTech 16:192–201.
   PubMed Web of Science ®Google Scholar
• Sou T, Morton DAV, Williamson M, et al. (2015). Spray-dried influenza antigen with trehalose and leucine produces an aerosolizable powder vaccine formulation that induces strong systemic and mucosal immunity after pulmonary administration. J Aerosol Med Pulm Drug Deliv 28:361–71.
   PubMed Web of Science ®Google Scholar
• Southam DS, Dolovich M, O’Byrne PM, Inman MD. (2002). Distribution of intranasal instillations in mice: effects of volume, time, body position, and anesthesia. Am J Physiol Lung Cell Mol Physiol 282:L833–9.
   PubMed Web of Science ®Google Scholar
• Srivastava A, Gowda DV, Madhunapantula SV, et al. (2015). Mucosal vaccines: a paradigm shift in the development of mucosal adjuvants and delivery vehicles. APMIS 123:275–88.
   PubMed Web of Science ®Google Scholar
• Straight TM, Ottolini MG, Prince GA, Eichelberger MC. (2006). Evidence of a cross-protective immune response to influenza A in the cotton rat model. Vaccine 24:6264–71.
   PubMed Web of Science ®Google Scholar
• Straight TM, Ottolini MG, Prince GA, Eichelberger MC. (2008). Antibody contributes to heterosubtypic protection against influenza A-induced tachypnea in cotton rats. Virol J 5:44.
   PubMed Web of Science ®Google Scholar
• Todoroff J, Ucakar B, Inglese M, et al. (2013). Targeting the deep lungs, Poloxamer 407 and a CpG oligonucleotide optimize immune responses to Mycobacterium tuberculosis antigen 85A following pulmonary delivery. Eur J Pharm Biopharm 84:40–8.
   PubMed Web of Science ®Google Scholar
• Tomar J, Born PA, Frijlink HW, Hinrichs WLJ. (2016). Dry influenza vaccines: towards a stable, effective and convenient alternative to conventional parenteral influenza vaccination. Expert Rev Vaccines 15:1431–47.
   PubMed Web of Science ®Google Scholar
• Tonnis WF, Lexmond AJ, Frijlink HW, et al. (2013). Devices and formulations for pulmonary vaccination. Expert Opin Drug Deliv 10:1383–97.
   PubMed Web of Science ®Google Scholar
• Trias EL, Hassantoufighi A, Prince GA, Eichelberger MC. (2009). Comparison of airway measurements during influenza-induced tachypnea in infant and adult cotton rats. BMC Pulm Med 9:28.
   PubMedGoogle Scholar
• Tschernig T, Debertin AS, Paulsen F, et al. (2001). Dendritic cells in the mucosa of the human trachea are not regularly found in the first year of life. Thorax 56:427–31.
   PubMed Web of Science ®Google Scholar
• Tschernig T, de Vries VC, Debertin AS, et al. (2006). Density of dendritic cells in the human tracheal mucosa is age dependent and site specific. Thorax 61:986–91.
   PubMed Web of Science ®Google Scholar
• van Riet E, Ainai A, Suzuki T, Hasegawa H. (2012). Mucosal IgA responses in influenza virus infections; thoughts for vaccine design. Vaccine 30:5893–900.
   PubMed Web of Science ®Google Scholar
• Vareille M, Kieninger E, Edwards MR, Regamey N. (2011). The airway epithelium: soldier in the fight against respiratory viruses. Clin Microbiol Rev 24:210–29.
   PubMed Web of Science ®Google Scholar
• Waldman RH, Bond JO, Levitt LP, et al. (1969a). An evaluation of influenza immunization: influence of route of administration and vaccine strain. Bull World Health Organ 41:543–8.
   PubMed Web of Science ®Google Scholar
• Waldman RH, Mann J, Small PA. (1969b). Immunization against influenza, prevention of illness in man by aerosolized inactivated vaccine. JAMA 207:520–4.
   PubMed Web of Science ®Google Scholar
• Wee JLK, Scheerlinck JPY, Snibson KJ, et al. (2008). Pulmonary delivery of ISCOMATRIX influenza vaccine induces both systemic and mucosal immunity with antigen dose sparing. Mucosal Immunol 1:489–96.
   PubMed Web of Science ®Google Scholar
• WHO. (2016). WHO report: influenza (seasonal) fact sheet. Geneva, Switzerland: World Health Organization.
   Google Scholar